rmfi Revista mexicana de fitopatología Rev. mex. fitopatol 0185-3309 2007-8080 Sociedad Mexicana de Fitopatología A.C. 10.18781/R.MEX.FIT.2302-2 Revisión Aspergillus oryzae: Una oportunidad para la agricultura García-Conde Karen Berenice 1 Cerna-Chávez Ernesto 1 Ochoa-Fuentes Yisa María 1 Velázquez-Guerrero Jazmín Janet 2 Universidad Autónoma Agraria Antonio Narro. Calzada Antonio Narro Núm. 1923, Col. Buenavista, Saltillo, Coahuila, México. CP. 25315; Universidad Autónoma Agraria Antonio Narro Universidad Autónoma Agraria Antonio Narro Coahuila 25315 Mexico Departamento de I+D, CULTA SA de CV. Boulevard Luis Echeverría Álvarez 1700, Col. Altavista, El Mante, Tamaulipas, México.. CULTA SA de CV , CULTA SA de CV. Tamaulipas Mexico Autor de correspondencia: Yisa María Ochoa-Fuentes yisa8a@yahoo.com 04 10 2024 Jan-Apr 2024 42 1 RMEXFIT23022 02 09 2023 10 10 2023 Este es un artículo publicado en acceso abierto bajo una licencia Creative Commons Resumen

Aspergillus oryzae es un hongo filamentoso, capaz de degradar diversas sustancias empleando enzimas, por lo que es ampliamente utilizado en la industria biotecnológica, productos farmacéuticos, enzimas para uso industrial, agentes blanqueadores y tratamientos textiles anticontaminación. Sin embargo, son pocos los trabajos centrados en las aplicaciones de campo de este microorganismo. El presente manuscrito revisa las posibles aplicaciones con potencial benéfico de A. oryzae y algunos subproductos en la agricultura como control biológico, inductor de crecimiento y biorremediador de suelos contaminados con metales pesados.

 Palabras clave: Biorremediación nematicida insecticida microorganismos metabolitos no toxígeno. Introducción

Los hongos del género Aspergillus spp. se consideran un grupo complejo de ascomicetos que comprende 350 especies aceptadas (Kocsubé et al., 2016). Son descritos como hongos filamentosos, capaces de secretar una amplia gama de metabolitos secundarios y enzimas, cuya función es degradar y reciclar biopolímeros de tejidos vegetales (El-Enshasy, 2007). El género Aspergillus spp., por lo general se encuentran en semillas almacenadas, vegetación en descomposición y suelo, donde se desarrollan como saprófitos (Mousavi et al., 2016).

Aunque los hongos del género Aspergillus spp. no se consideran fuentes importantes de enfermedades fitosanitarias, son responsables de alteraciones en plantas y productos almacenados, al ser mohos oportunistas prosperan en condiciones de almacén (Awuchi et al., 2021). Además es un género reconocido por su producción de micotoxinas identificando alrededor de 300 y 400, como las aflatoxinas, ácidos secalónicos, ácido ciclopíazonico, aflatrem, citrinina, estregmatocistina, glicotoxina, ocratoxina A (OTA), y terreína (Navale et al., 2021), con potencial riesgo a la salud humana como de animales, a la par también afectan el medio ambiente e influyen negativamente en la economía mundial (Bueno et al., 2015). Un ejemplo importante de este tipo de metabolitos secundarios tóxicos son las aflatoxinas, las cuales suponen un riesgo para los productos en postcosecha y son considerados como indicadores de degradación biológica de suelo (Marshall et al., 2020). Generan cambios cualitativos nutricionales y sensoriales en los productos de origen vegetal, ya que la infección puede provocar sabores u olores desagradables, podredumbre y decoloración (Kozakiewic, 1989).

Algunos hongos del género Aspergillus spp., como A. flavus, A. nidulans, A. nomius y A. parasiticus, tienen importancia agronómica, debido a que son productores de aflatoxinas (AF) (Hesseltine et al., 1970; Gomi, 2014), principalmente B1, B2, G1 y G2, han demostrado ser fuertes biotoxinas cancerígenas, citotóxicas y potencialmente mortales para el ser humano y el ganado (Ráduly et al., 2019).

A. flavus se ha reportado como causante de contaminación por aflatoxinas AFB1 en cualquier etapa de la cadena de suministro de maní (importadores, fabricantes y minoristas), en países como Malasia, donde las condiciones de clima tropical son favorables para el crecimiento de este hongo (Norlia et al., 2018, 2019). En México el maíz se ha visto afectado por la contaminación con aflatoxinas, de igual manera granos como arroz, cebada, frijol, sorgo, trigo, algunas oleaginosas y frutos secos son susceptibles a estas biotoxinas, producidas por A. flavus (AFB1 y AFB2), A. parasiticus y A. nomius (AFG1 y AFG2) (Anguiano-Ruvalcaba et al., 2005; Escobar et al., 2023).

Es importante destacar, la existencia de cepas no toxigénicas, dentro de Aspergillus spp., las cuales no generan aflatoxinas y pueden aplicarse en el área de cultivo, llegándose a instalar, competir y desplazar a las cepas toxigénicas, resultando en la reducción de aflatoxinas (Marshall et al., 2020; Senghor et al., 2020). Cepas no toxigénicas de A. niger, A. sojae y A. oryzae, no producen compuestos que contengan en esencia un anillo de furano unido al núcleo de cumarina, importantes en la ruta de biosíntesis de aflatoxinas, y no generan ácido ciclopiazónico en conjunto con aflatoxinas como A. flavus (Dorner et al., 2000; Padrón et al., 2013).

Cepas de Aspergillus spp. que no producen aflatoxinas pueden ser utilizadas como agentes de biocontrol fúngico en la prevención de contaminación por biotoxinas (Barberis et al., 2019). Las cepas A. westerdijkiae 107, A. fumigatos C143, A. tamarii C122 y A. niger C187 han demostrado en términos de inhibición y producción de OTA tener resultados favorables, siendo la cepa A. niger C187 la que obtuvo un 100% de inhibición de la producción de OTA y del crecimiento de A. ochraceus, A. westerdijkiae, A. carbonarius y A. niger en granos de café (de Almeida et al., 2019). De igual manera suelen utilizarse en la industria farmacéutica, y en procesos industriales como la fermentación de alimentos, debido a que son fuentes abundantes de enzimas como proteasas, amilasas y amiloglucosidasas entre otras (Schuster et al., 2002; Olempska-Beer et al., 2006; Samson et al., 2014; Gómez et al., 2016). La producción de poligalacturonasa (Exo-PGs), un consorcio de enzimas necesarias para la hidrólisis de pectina, se encuentra dentro de las aplicaciones de la cepa A. sojae ATCC 20235, útil en la despectinización y clarificación de jugos de frutas, extracción de aceites de cascaras de vegetales y cítricos, y tratamiento de aguas residuales pésicas (Tari et al., 2008).

Por lo tanto, al ser un hongo que cuenta con cepas no toxigénicas, A. oryzae figura como una de las especies más importantes debido a su potencial uso como herramienta biotecnológica, en procesos metabólicos degradativos de diversos almidones y proteínas; en el metabolismo de aminoácidos, y transportadores de absorción de aminoácidos y azúcares (Machida et al., 2005, 2008; Watarai et al., 2019; Daba et al., 2021). A. oryzae es considerado por la FDA como “generalmente reconocido como seguro” (GRAS), esto hace referencia a cualquier sustancia agregada intencionalmente a alimentos, la cual debe estar sujeta a revisión y aprobación previa antes de su comercialización, a menos que la sustancia sea generalmente reconocida, entre los expertos calificados (Gad, 2005; FDA, 2019). Por lo tanto, la OMS avala la seguridad ante el uso de A. oryzae (He et al., 2019). Siendo de este microorganismo apto para su aplicación en la industria alimenticia como la fermentación de alimentos, producción de alcohol y vinagre, en la industria farmacéutica y cosmética mediante la formulación de fármacos y agentes despigmentantes, dichas aplicaciones se deben a la producción de enzimas y metabolitos secundarios como lipasas, celulasas, pectinasas, β-galactosidasa, amilasas, ácido kójico, ácido málico, ácido fumárico y ácido felurico entre otros (Daba et al., 2021).

Por lo tanto, el presente estudio se enfoca en revisar trabajos de investigación y literatura sobre los diversos productos derivados de A. oryzae, sus aportaciones y aplicaciones en el área agrícola como biorremediadores, inductores de crecimiento y agentes de control biológico. Es necesario destacar, que, si bien el estudio de A. oryzae ha tenido un enfoque en mayor parte para el área industrial, en el presente trabajo solo se consideraron aquellos trabajos e investigaciones en los que su aplicación va dirigida a la parte agronómica. Se pone principal atención en el ácido kójico y cepas de A. oryzae involucradas en su producción, debido a que el proceso fermentativo presenta características sustentables, y sus aplicaciones son novedosas para el área agrícola.

El objetivo principal de esta revisión es dar a conocer el potencial de A. oryzae en áreas poco estudiadas de importancia agrícola. Si bien A. oryzae ha sido estudiado en gran medida en áreas industriales, alimenticias y médicas, los estudios de su potencial agronómico son pocos y en México su estudio es prácticamente nulo, de tal manera que parte de esta revisión busca el desarrollo en un futuro de trabajos científicos referentes a A. oryzae encaminados al sector agrícola, aportando al desarrollo y cuidado del campo mexicano.

<bold>Morfología y descripción de <italic>Aspergillus oryzae</italic>; origen, aislamiento y desarrollo</bold>

Aspergillus spp. presenta hifas septadas hialinas, con ramificación dicotómica de 45° (Cuervo-Maldonado et al., 2010), el crecimiento forma micelios extendidos que cubren toda la superficie de los medios de cultivo (Gomi, 2014) (Figura 1). La

Morfología de <italic>A. oryzae</italic>; A) Partes y estructura del hongo (Adaptado de “Structure of <italic>Aspergillus</italic> spp.”, 2023), B) <italic>A. oryzae</italic> cultivado en medio PDA, y C) Crecimiento de <italic>A. oryzae</italic> en arroz al vapor (köji).

vesícula en forma de globo mide de 100 a 200 µm de diámetro con una estructura formada por conidios de forma ovalada de 5 a 8 µm de largo que contiene cuatro núcleos de textura suave y ligeramente rugosa. Las fiálides se encuentran en la vesícula y pueden ser esterigmas uniseriados o biseriados. Los tallos son incoloros y de 1 a 5 mm de largo con textura áspera (Moubasher, 1993; Powell et al., 1994). Ahlburg (1876) aisló por primera vez a A. oryzae del köji, el material fermentado por el moho de A. oryzae cultivado en un medio sólido de arroz al vapor (Machida et al., 2008). Dicho hongo pertenece a la Clase Erotiómycetes; Orden: Eurotiales; Familia: Trichocomaceae (Daba et al., 2021). El uso de A. oryzae en la producción de sake (bebida alcohólica fermentada de arroz), vinagre, miso (pasta de soja), y salsa de soja, se ha reportado durante al menos dos milenios (Furukawa, 2012; Chang et al., 2014), en general se considera seguro, y no se conoce ninguna cepa que produzca aflatoxinas (Machida et al., 2005).

Los genes que codifican la vía enzimática para la biosíntesis de aflatoxinas están agrupados en una región del ADN de 75 Kb en A. flavus, este grupo se encuentra en A. oryzae, pero no parece ser funcional (Yu et al., 2004). A. oryzae y A. flavus son morfológicamente similares, varios estudios sugieren que son ecotipos, refiriéndose a una misma especie que en ambientes diferentes tienen una expresión diferente por la interacción de los genes con el medio donde se encuentran (Kurtzman et al., 2018). Dando a entender que A. oryzae fue el resultado de la domesticación de A. flavus después de siglos de cultivo (Payne et al., 2006).

Aspergillus oryzae ser reportado como microorganismo domesticado, no se puede encontrar en la naturaleza. Sin embargo, existen algunos reportes donde se habla del aislamiento de A. oryzae de alimentos, plantas y suelo, presentándose con menor frecuencia (Klich, 2002). Un archivo historio describía que A. oryzae debía aislarse de una espiga de arroz, dando a entender que puede haber existido en la naturaleza antes de la domesticación (Murakami, 1980).

Dicho hongo crece en varios medios, incluidos agar dextrosa de papa, donde crece particularmente rápido en 7 días a 25 °C (Moubasher, 1993), su etapa de esporulación comienza a los 7 días, cuando el crecimiento alcanza de 7 a 8 cm comienza a formarse un contorno amarillo, que gradualmente se torna verde (Daba et al., 2021). Las condiciones ideales para el desarrollo de A. oryzae incluyen pH ligeramente ácido entre 5 y 6, a la par la temperatura debe oscilar entre 32 a 36 °C (±1 °C), variaciones en la temperatura superiores a 44 °C inhiben su crecimiento. Estos hongos muestran un desarrollo eficiente en medios con actividad de agua superior a 0.8 y rara vez crecen por debajo de este rango (Gomi, 2014).

 <bold>Aplicaciones de <italic>Aspergillus oryzae</italic> y su posible implementación en la agricultura</bold>

La versatilidad de A. oryzae, se ve reflejada en el amplio espectro de áreas donde se puede llevar acabo su aplicación (Figura 2), ya que es altamente efectivos en la

Áreas de aplicación de Aspergillus oryzae.

fabricación de productos biotecnológicos principalmente por su diversidad metabólica y enzimática (El-Enshasy, 2007).

Lee y colaboradores (2016), proporcionaron un perfil metabólico obtenido durante la fermentación de köji con A. oryzae, el cual comprende los metabolitos secundarios secretados en el proceso fermentativo, clasificándolos en; a) azucares ( xilosa, fructosa y glucosa); b) polioles ( glicerol, eritriol, xilitol, sorbitol y myoinositol); c) ácidos orgánicos (ácido succínico, ácido glicérico, ácido fumárico, ácido málico, ácido kójico, ácido cítrico y ácido glucónico); d) ácidos fenólicos ( ácido 4-hidroxybenzoico y ácido ferúlico); e) aminoácidos (alanina, prolina, glicina, serina, treonina, aspartato y GABA); f) ácidos grasos (ácido palmítico, ácido linoleico, ácido oleico y ácido pinélico); y g) vitaminas (vitamina B3). Cada uno de estos compuestos tiene diferentes propiedades antimicrobianas, antioxidantes, anticancerígenas, antivirales, compuestos hormonales y quelantes de metales (Frisvad et al., 2018; Daba et al., 2021).

La aplicación de A. oryzae y en la producción de ácido málico y ácido fumárico (Xu et al., 2012; Brown et al., 2013), propone la posibilidad de la creación de un proceso de biorrefinería para la producción de ácidos orgánicos y enzimas, sustituyendo los polímeros derivados del petróleo actualmente utilizados (Brink et al., 2023). El proceso de biorrefinería puede ser potencializado al implementar de subproductos agrícolas, sustratos baratos y no alimenticios, reduciendo costos de producción y siendo una opción libre de productos químicos (Jiménez-Quero et al., 2020).

Las enzimas microbianas empleadas en la industria han demostrado ser mejores en su aplicación, económicas y respetuosas con el medio ambiente en comparación con productos químicos (Whiteley y Lee, 2006). Cuentan con ventajas técnicoeconómicas implicando menores tiempos de producción, mejor espacio por unidad de enzima producida y potencial ilimitado en cuanto a disponibilidad de nuevas enzimas (Scriban, 1985).

Se ha reportado la aplicación de A. oryzae en el proceso de fermentación de orujo de uva, mediante la producción de enzimas (celulasa, pectinasa y tanasa) las cuales facilitan la extracción acuosa de polifenoles (ácido gálico, ácido sinápico y ácido ferúlico), con propiedades antioxidantes y prebióticas, como aditivos alimenticios, en donde A. oryzae tiene una mayor producción y selectividad de tanasa en condiciones húmedas, teniendo un efecto positivo sobre la actividad antioxidante, el cual puede verse influido por la producción de ácido gálico (Meini et al., 2021). Por otro lado, A. oryzae tiene la capacidad de estimular la fermentación ruminal al mejorar el consumo y digestión del alimento y materia seca en ganado vacuno, mediante su aplicación como aditivo microbiano en el alimento del ganado (Sosa et al., 2022), a la par se ha demostrado la eficiencia en el aumento de ácidos grasos volátiles, haciendo de A. oryzae un elemento de mejora para potencializar las dietas de los rumiantes de manera diferente, además influye en el suministro de enzimas en ensilaje de maíz, heno de avena y heno de alfalfa (Kong et al., 2021).

El progreso tecnológico ha aprovechado el potencial de A. oryzae (Matsunaga et al., 2002) para uso industrial en el desarrollo de detergentes, pigmentos, antioxidantes, (Christensen et al., 1988; Machida et al., 2008; Panchanawaporn et al., 2022). De igual forma su aplicación en la fermentación de alimentos (Machida et al., 2008; Yasui et al., 2020) y la implementación de la producción de metabolitos como ácidos orgánicos y reguladores de crecimiento vegetal son áreas importantes de estudio (El-Enshasy, 2007; Siddiqui, 2016). Además puede ser útil en actividades biológicas como en el área de la veterinaria como probióticos para aves de corral y digestivo de pienso de ganado (Lee et al., 2006; Murphy, 2021; Podversich et al., 2023).

 A. oryzae como biorremediador de suelos, promotor de crecimiento y control biológico

A. oryzae puede ser una alternativa para el desarrollo de una agricultura sustentable y ecológicamente amigable, en específico en México donde sus aplicaciones en campo no son tema de estudio. La siguiente información describe algunas áreas de oportunidad donde se puede aplicar este microorganismo en la agricultura, con la finalidad de dar pie a posibles estudios científicos dirigidos al campo mexicano. Los hongos endófitos vegetales, son aquellos que habitan en los tejidos de plan tas y no causan ningún daño evidente. Debido a esto en algunas ocasiones se identifica una relación mutualista (endófito-hospedero) desencadenando la producción de sustancias bioactivas (metabolitos secundarios, enzimas etc.) las cuales influyen en la promoción del crecimiento, la supervivencia del hospedero bajo diversas condiciones ambientales, disminuir la susceptibilidad a enfermedades y ayudar en el control de insectos plaga y agentes fitopatógenos (El-hawary et al., 2020; Murali et

al., 2012; Sharma and Singh, 2021).

Si bien A. oryzae no se reporta comúnmente como endófito natural, se ha proporcionado información sobre su aislamiento en raíces de Ginkgo biloba en China (Machida et al., 2005).Sun y colaboradores (2018), mediante el estudio de la inoculación de semillas de Raphanus sativus con la cepa A. oryzae BNCC341706, lo establecieron como un hongo con propiedades endófitas, al no afectar la germinación de la semilla inoculada, y promover el crecimiento del cultivo de R. sativus con alturas de 116 mm en comparación con el testigo con una altura de 99.6 mm. Otro efecto del uso de A. oryzae, se vio reflejado en la salud de su principal insecto plaga Plutella xylostella, afectando los parámetros de consumo, peso de larvas y pupas. Lo cual, abre la posibilidad al tratamiento de semilla de crucíferas, y el control de insectos plaga mediante A. oryzae.

De igual manera como agentes biorremediadores los hongos endófitos, ha demostrado ser eficaces en la degradación de contaminantes sin dejar rastros de subproductos tóxicos (Skinder et al., 2022), representando una ventaja debido a sus características de biomasa, largo ciclo de vida y su red de hifas (Sun et al., 2012), a la par la capacidad de degradar sustancias químicamente tóxicas mediante modificación o actuando sobre su biodisponibilidad química (Bornyasz et al., 2005). En el caso de A. oryzae como agente biorremediador, el estudio in vitro de las cepas A. oryzae AM1 y AM2, demostró la capacidad de degradar atrazina (90%), endosulfán (56 y 76%) y clorpirifós (50 y 73%), y a la par logra obtener un buen desarrollo bajo concentraciones altas de pesticidas, lo que genera la posibilidad de degradar este tipo de productos químicos (Barberis et al., 2019).

La OTA, es una micotoxina que afecta la salud humana y productos agrícolas, por lo cual se buscan medidas de control, por lo tanto, la biodegradación se plantea como un método prometedor. La cepa A. oryzae M30011, es capaz de degradar hasta en un 94% la OTA en un periodo de 72 h, en condiciones de pH de 8, temperatura de 30 °C y concentración del inoculo de 104 UFC mL-1. Por otra parte, el reducir los niveles de aflatoxinas, es un tema de importancia, debido a que son una amenaza a la seguridad alimentaria mundial (Xiong et al., 2021). Se ha demostrado, que la cepa A. oryzae M2040, es capaz de inhibir en un 87% la producción de AFB1, y la proliferación de A. flavus, en condiciones in vitro, y en maní al desplazar al hongo productor de aflatoxinas con éxito, mediante la secreción de compuestos antimicóticos, los cuales no han sido reportados (Alshannaq et al., 2018). Estos estudios respaldan el potencial de A. oryzae en la industria agrícola y alimentaria.

El potencial que tiene el uso de A. oryzae, se ha enfatizado en el desarrollado de trabajos de investigación como promotor de crecimiento y agente de control biológico, presentes en el Cuadro 1.

Uso de A. oryzae como promotor de crecimiento, agente de control de plagas y biorremediador de suelos contaminados.
Application Strain Crop / Pest Results Reference
Arsenic biorremediator and growth enhancer FNBR_L35 Oat (Avena sativa), Calendula (Calendula officinalis), Ashwagandha (Withania somifera) Effects of bioaccumulation and biovolatilization of arsenic in concentrations of 100 to 10,000 ppm in a period of 21 days and enhancement of plant growth Singh et al., 2015
Entomopathogen XJ-1 Locusta migratoria Mortality in third instar of the insect Zhang et al., 2015
Growth enhancer and control agent BNCC341706 Radish seeds (Raphanus stativus), Puntella xylostella Greatest plant height. Inhibition of feeding and low weight of larvae and pupae Sun et al., 2018
Removal of glyphosate AM1 and AM2 In vitro Degradation of 50% in glyphosate concentrations, long periods of incubation and permanence of the fungus Carranza et al., 2019
Entomopathogen USMN05 USMM03 NRRL2097 Spodoptera litura Mortality of 20% and inability to produce aflatoxins Fitriana et al., 2021

La facultad de A. oryzae en la secreción de enzimas, es una alternativa para el desarrollo de compuestos de origen microbiológico, debido a que desempe ñan actividades biológicas que pueden ser adaptadas en el área agronómica. Un ejemplo, es la actividad antifúngica de la xilanasa producida por la cepa A. oryzae MN894021, la cual presenta una reducción en un 75, 90 y 100% de la incidencia de Botrytis cinerea, Fusarium solani, F. chlamydosporum, F. incranatum, Macrophomina phaseolina, Rhizotocnia solani y Sclerotinia sclerotiorum, en semillas de haba recubiertas con xilanasa, brindando una protección contra la invasión de estos hongos fitopatógenos (Atalla et al., 2020). Los resultados obtenidos de la xilanasa producida por la cepa A. oryzae MN894021, coinciden la actividad de la xilanasa de Trichoderma harzianum kj831197 contra Corynespora cassiicola, Alternaria spp.,F. oxysporum y Botrytis fabae (Ellatif et al., 2022).

El control de hongos fitopatógenos es un desafío importante para la agricultura. El desarrollo procesos de control sostenibles, ecológicos, fáciles y respetuosas con la naturaleza, es constante en la investigación actual, una opción es la síntesis biogénica de nanopartículas (Zhang et al., 2020). La cepa A. oryzae MTCC3107 ha sido implementada en la formulación de nanopartículas de plata (AgNP), cuyo potencial antimicrobiano contra Sclerotinia sclerotium, reflejó inhibición del 100% a una concentración de 100 µL mL-1. El papel de A. oryzae en la formulación, se debe a la secreción de amilasa, la cual cataliza el proceso de producción de las AgNP, haciéndolo un proceso de síntesis verde (Gupta y Saxena, 2023).

El estudio y publicación de información relacionada con el potencial de A. oryzae, sirven de respaldo para futuras investigaciones en el área de la fitopatología, ya que ha sido relativamente poco estudiada. Si bien A. oryzae cuenta con un amplio margen de sustancias bioactivas producidas, son pocos los aplicados en esta área. Algunas actividades y metabolitos se presentan en el Cuadro 2.

2. Actividad de sustancias bioactivas producidas por <italic>A. oryzae</italic> contra fitopatógenos.
Bioactive substances Strains Application Result Reference
Kojic acid NRRL 447, 552, 552, 1730 Y30038 (S-03) Prevention of contamination by toxins in agricultural products Reduction of aflatoxins in peanut Dorner et al., 1998
Kojic acid * Insecticide: Glyphodes pyloalis Inhibition of phenyloxidase activity Sharifi et al., 2013
Oryzaeins A-D KM999948 Antiviral: TMV Rates of inhibition of 22.4 - 30.6% Zhou et al., 2016
Xylanase MN894021 antifungal: Alternaria alternata, Fusarium oxysporum, Phoma destructor, Rhizotocnia solani and Sclerotium rolfsii Reduction of the live growth Reduction in percentages of incidence of root rotting Atalla et al., 2020
Kojic acid * Antifungal activity: Sclerotinia slerotiorum Inhibiyion of chitin and melanin synthesis Reduction of oxalic acid of the virulence factor Zhu et al., 2022

*Strain not provided by the author.

 Ácido kójico metabolito secundario de A. oryzae; alternativa de control contra los fitopatógenos

Dentro de los principales metabolitos secundarios producidos por A. oryzae, el ácido kójico es de los más relevantes (Figura 3) (Yamada et al., 2014), su aplicación dentro el control de agentes fitopatógenos e insectos plaga es un tema relativamente nuevo; sin embargo, los informes de investigación muestran que esta aplicación puede ser una alternativa factible para el control de plagas en cultivos.

A. oryzae cuenta con propiedades bactericidas, fungicidas e insecticidas (Mohamad et al., 2010), su modo de acción está relacionado con la inhibición de enzimas oxidativas tanto de plantas como de artrópodos. Estudios han demostrado que el ácido kójico inhibe de manera eficaz la tasa de formación de productos pigmentados y de absorción de oxígeno cuando compuestos como las catecolaminas (DL-DOPA, dopamina y norepinefrina), al ser oxidados por la enzima la tirosinasa (Kahn, 1995; Kahn y Ben-Shalom, 1997).

Características y generalidades del Ácido kójico basado en los informes de <xref ref-type="bibr" rid="B62">Phasha et al. (2022</xref>) y <xref ref-type="bibr" rid="B72">Siddiquee (2018</xref>).

Mahmoud y colaboradores (2023), analizaron la actividad insecticida del ácido kójico producido por la cepa A. oryzae ASU44 (OL314732), contra Aphis gossypii, vector del virus del enanismo de la hoja del algodón (Cotton leafroll dwarf virus-CLRDV) (Mahas et al., 2022). Evaluaron la diferencia entre el ácido kójico extraído de la cepa A. oryzae ASU44 (OL314732) y el ácido kójico sintético, indicando que el ácido kójico producido por A. oryzae ASU44 (OL314732), era más eficaz contra Aphis gossypii, con concentración letal media (CL50) de 11.2 ppm, concentración letal (CL90) de 50.3 ppm, y tiempo letal (LT90) de 7 días, ya que los resultados son menores que los del ácido kójico sintético, destacando su aplicación como un modelo de evaluación in vitro eficaz y económico (Mahmoud et al., 2023). De igual manera, la actividad antifungica del ácido kójico, se ha evaluado con A. terrus, A. flavus, A. parasiticus, A. fumigatus, Penicilium y Sclerotinia sclerotiorum (Kim et al., 2012; Kim y Chan, 2014; Zhu et al., 2022). En el caso de S. sclerotiorum, el ácido kójico inhibe la biosíntesis de melanina, lo que afecta el desarrollo de esclerocios, y la biosíntesis de quitina y β-1,3-glucanos, lo que altera la pared celular y el crecimiento del micelio, rediciendo en su totalidad, los síntomas de S. sclerotiorum, en las vainas de soya con 50 mM de ácido kójico. Tiene la capacidad de prevenir como inhibir los síntomas de S. sclerotiorum, a la par cuenta mayor eficiencia que fungicidas comerciales (carbendazim y procloraz) (Zhu et al., 2022). Con mayor frecuencia se ha señalado a los nematodos fitoparásitos como la causa de pérdidas económicas importantes en diversos cultivos oscilan alrededor de $77 mil millones de dólares a nivel mundial, lo cual genera preocupación en la agricultura, horticultura y silvicultura (Yadav, 2017; Seo et al., 2019). Por ejemplo, Meloidogyne spp. nematodo agallador, es responsable de pérdidas anuales, las cuales se elevan a $100 mil millones de dólares. Kim y colaboradores (2016) establecieron un método de control de estos nematodos mediante el uso de ácido kójico como ingrediente activo, el cual fue producido por la cepa A. oryzae EML-DML3PNa1 obtenida de plantas de cornejo (Cornus alba). Durante sus experimentos, se demostró un efecto inhibidor de la eclosión de huevos y el desarrollo de larvas y se sugirió la implementación del ácido kójico en conjunto con un agente dispersante, penetrante o tensioactivo, con la finalidad de mejorar la absorción y el efecto del producto en el cultivo (Kim et al., 2016). La acción nematicida del ácido kójico reportó un 87.6% de mortalidad en juveniles de Meloidogyne incognita bajo condiciones del 20% de un filtrado de caldo fermentativo. Presentó inhibición en la incubación del nematodo y una mortalidad dependiente de la dosis, con valores de concentración efectiva media (CE50) de 195.2 µg mL-1 y 238.3 µg mL-1, respectivamente, a las 72 h posteriores a la exposición, lo cual sugiere que tiene un potencial como agente de control biológico (Kim et al., 2016).

El interés por productos agrícolas seguros para la salud y libres de contaminación va en aumento, esto debido la conciencia sobre la toxicidad residual ocasionada por el uso de pesticidas. La implementación de microorganismos que tienen actividad nematicida se recomienda por ser respetuosos con el medio ambiente al ser obtenidos a partir de productos naturales, como lo es el caso del ácido kójico, por lo cual su implementación en la agronomía abre una puerta para el desarrollo de productos sustentablemente económicos, amigables con el medio ambiente y sobre todo que no generen daños a la salud de quien los aplica.

 Conclusiones

El presente estudio destaca el potencial de las cepas de A. oryzae y sus derivados (enzimas y metabolitos secundarios), considerando la capacidad de competir con productos químicos comerciales como plaguicidas, ya que, presenta características insecticidas, fungicidas y nematicidas, las cuales representan una alternativa económica y sustentable, debido a que su manera de producción deja de lado el uso de productos de elevados costos. Desarrollar nuevos trabajos de investigación y optar por la aplicación de productos procedentes de A. oryzae a nivel invernadero, es necesario para comprobar su adaptabilidad en condiciones externas al laboratorio, y verificar si los beneficios de A. oryzae se mantienen o disminuyen de tal manera que puedan llegar a ser empleados en campo. Finalmente, el estudio de A. oryzae y sus productos derivados es poco estudiado en México, por lo cual, lo convierte en un tema debatible para ser explotado para el beneficio del desarrollo del campo en México, ya que abre una nueva vertiente de estudio, en el desarrollo de productos benéficos para cultivos, y para el control de agentes fitopatógenos.

 Acknowledgement

Se agradece a la Universidad Autónoma Agraria Antonio Narro (UAAAN), al programa de Doctorado de Parasitología Agrícola y al Consejo Nacional de Humanidades, Ciencias y Tecnologías (CONAHCYT).

 Literatura Citada AlshannaqAF, GibbonsJG, LeeMK, HanKH, HongSB y YuJH. 2018. Controlling aflatoxin contamination and propagation of Aspergillus flavus by a soy-fermenting Aspergillus oryzae strain. Scientific Reports 8(1): 16871. https://doi.org/10.1038/s41598-018-35246-1 Alshannaq AF Gibbons JG Lee MK Han KH Hong SB Yu JH 2018 Controlling aflatoxin contamination and propagation of Aspergillus flavus by a soy-fermenting Aspergillus oryzae strain Scientific Reports 8 1 16871 16871 10.1038/s41598-018-35246-1 Anguiano-RuvalcabaGL, Vargas-CortinaAV y Guzmán-De PeñaD. 2005. Inactivación de aflatoxina B1 y aflatoxicol por nixtamalización tradicional del maíz y su regeneración por acidificación de la masa. Salud Pública de México 47(5): 369-375. http://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S0036-36342005000500007&lng=es&nrm=iso&tlng=es Anguiano-Ruvalcaba GL Vargas-Cortina AV Guzmán-De Peña D 2005 Inactivación de aflatoxina B1 y aflatoxicol por nixtamalización tradicional del maíz y su regeneración por acidificación de la masa Salud Pública de México 47 5 369 375 http://www.scielo.org.mx/scielo.php?script=sci_arttext&pid=S0036-36342005000500007&lng=es&nrm=iso&tlng=es AtallaSMM, AhmedNE, AwadHM, El GamalNG y El-ShamyAR. 2020. Statistical optimization of xylanase production, using different agricultural wastes by Aspergillus oryzae MN894021, as a biological control of faba bean root diseases. Egyptian Journal of Biological Pest Control 30(1): 125. https://doi.org/10.1186/s41938-020-00323-z Atalla SMM Ahmed NE Awad HM El Gamal NG El-Shamy AR 2020 Statistical optimization of xylanase production, using different agricultural wastes by Aspergillus oryzae MN894021, as a biological control of faba bean root diseases Egyptian Journal of Biological Pest Control 30 1 125 125 10.1186/s41938-020-00323-z AwuchiCG, OndariEN, OgbonnaCU, UpadhyayAK, BaranK, OkpalaCOR, KorzeniowskaM y GuinéRPF. 2021. Mycotoxins affecting animals, foods, humans, and plants: Types, occurrence, toxicities, action mechanisms, prevention, and detoxification strategies—a revisit. Foods 10(6). https://doi.org/10.3390/foods10061279 Awuchi CG Ondari EN Ogbonna CU Upadhyay AK Baran K Okpala COR Korzeniowska M Guiné RPF 2021 Mycotoxins affecting animals, foods, humans, and plants: Types, occurrence, toxicities, action mechanisms, prevention, and detoxification strategies—a revisit Foods 10 6 10.3390/foods10061279 BarberisCL, CarranzaCS, MagnoliK, BenitoN y MagnoliCE. 2019. Development and removal ability of non-toxnic Aspergillus section Flavi in presence of atrazine, chlorpyrifos and endosulfan. Revista Argentina de Microbiología 51(1): 3-11. https://doi.org/10.1016/J.RAM.2018.03.002 Barberis CL Carranza CS Magnoli K Benito N Magnoli CE 2019 Development and removal ability of non-toxnic Aspergillus section Flavi in presence of atrazine, chlorpyrifos and endosulfan Revista Argentina de Microbiología 51 1 3 11 10.1016/J.RAM.2018.03.002 BornyaszMA, GrahamRC y AllenMF. 2005. Ectomycorrhizae in a soil-weathered granitic bedrock regolith: Linking matrix resources to plants. Geoderma 126(1-2): 141-160. https://doi.org/10.1016/J.GEODERMA.2004.11.023 Bornyasz MA Graham RC Allen MF 2005 Ectomycorrhizae in a soil-weathered granitic bedrock regolith: Linking matrix resources to plants Geoderma 126 1-2 141 160 10.1016/J.GEODERMA.2004.11.023 BrinkHG, Geyer-JohnsonM, SwartRM y NicolW. 2023. Malic acid production by Aspergillus oryzae: the immobilized fungal fermentation route. Biofuels, Bioproducts and Biorefining 17(2): 363-379. https://doi.org/10.1002/BBB.2440 Brink HG Geyer-Johnson M Swart RM Nicol W 2023 Malic acid production by Aspergillus oryzae: the immobilized fungal fermentation route Biofuels, Bioproducts and Biorefining 17 2 363 379 10.1002/BBB.2440 BrownSH, BashkirovaL, BerkaR, ChandlerT, DotyT, McCallK, McCullochM, McFarlandS, ThompsonS, YaverD y BerryA. 2013. Metabolic engineering of Aspergillus oryzae NRRL 3488 for increased production of L-malic acid. Applied Microbiology and Biotechnology 97(20): 8903-8912. https://doi.org/10.1007/s00253-013-5132-2 Brown SH Bashkirova L Berka R Chandler T Doty T McCall K McCulloch M McFarland S Thompson S Yaver D Berry A 2013 Metabolic engineering of Aspergillus oryzae NRRL 3488 for increased production of L-malic acid Applied Microbiology and Biotechnology 97 20 8903 8912 10.1007/s00253-013-5132-2 BuenoD, IstamboulieG, MuñozR y MartyJL. 2015. Determination of mycotoxins in food: A review of bioanalytical to analytical methods. Applied Spectroscopy Reviews 50(9): 728-774. https://doi.org/10.1080/05704928.2015.1072092 Bueno D Istamboulie G Muñoz R Marty JL 2015 Determination of mycotoxins in food: A review of bioanalytical to analytical methods Applied Spectroscopy Reviews 50 9 728 774 10.1080/05704928.2015.1072092 CarranzaCS, RegñicoliJP, AluffiME, BenitoN, ChiacchieraSM, BarberisCL y MagnoliCE. 2019. Glyphosate in vitro removal and tolerance by Aspergillus oryzae in soil microcosms. International Journal of Environmental Science and Technology 16(12): 7673-7682. https://doi.org/10.1007/s13762-019-02347-x Carranza CS Regñicoli JP Aluffi ME Benito N Chiacchiera SM Barberis CL Magnoli CE 2019 Glyphosate in vitro removal and tolerance by Aspergillus oryzae in soil microcosms International Journal of Environmental Science and Technology 16 12 7673 7682 10.1007/s13762-019-02347-x ChangPK, BhatnagarD y ClevelandTE. 2014. Aspergillus Introduction. Encyclopedia of Food Microbiology 1: 77-82. https://doi.org/10.1016/B978-0-12-384730-0.00010-0 Chang PK Bhatnagar D Cleveland TE 2014 Aspergillus Introduction Encyclopedia of Food Microbiology 1 77 82 10.1016/B978-0-12-384730-0.00010-0 ChristensenT, WoeldikeH, BoelE, MortensenSB, HjortshoejK, ThimL y HansenMT. 1988. High level expression of recombinant genes in Aspergillus oryzae. Applied Microbiology and Biotechnology 6(12): 1419-1422. https://doi.org/10.1038/NBT1288-1419 Christensen T Woeldike H Boel E Mortensen SB Hjortshoej K Thim L Hansen MT 1988 High level expression of recombinant genes in Aspergillus oryzae Applied Microbiology and Biotechnology 6 12 1419 1422 10.1038/NBT1288-1419 Cuervo-MaldonadoSI, Gómez-RincónJC, RivasP y Orlando GuevaraF. 2010. Actualización en Aspergilosis con énfasis en Aspergilosis invasora. Infectio 14: 131-144. https://doi.org/10.1016/S0123-9392(10)70131-4 Cuervo-Maldonado SI Gómez-Rincón JC Rivas P Orlando Guevara F 2010 Actualización en Aspergilosis con énfasis en Aspergilosis invasora Infectio 14 131 144 10.1016/S0123-9392(10)70131-4 DabaGM, MostafaFA y ElkhateebWA. 2021. The ancient koji mold (Aspergillus oryzae) as a modern biotechnological tool. Bioresources and Bioprocessing 8(1): 1-17. https://doi.org/10.1186/S40643-021-00408-Z Daba GM Mostafa FA Elkhateeb WA 2021 The ancient koji mold (Aspergillus oryzae) as a modern biotechnological tool Bioresources and Bioprocessing 8 1 1 17 10.1186/S40643-021-00408-Z de AlmeidaÁB, CorrêaIP, FuruieJL, de Farias PiresT, do Rocio DalzotoP y PimentelIC. 2019. Inhibition of growth and Ochratoxin A production in Aspergillus species by fungi isolated from coffee beans. Brazilian Journal of Microbiology 50(4): 1091-1098. https://doi.org/10.1007/s42770-019-00152-9 de Almeida ÁB Corrêa IP Furuie JL de Farias Pires T do Rocio Dalzoto P Pimentel IC 2019 Inhibition of growth and Ochratoxin A production in Aspergillus species by fungi isolated from coffee beans Brazilian Journal of Microbiology 50 4 1091 1098 10.1007/s42770-019-00152-9 DornerJW, HornBW y ColeRJ. 2000. Non-toxicogenic strain of Aspergillus oryzae and Aspergillus sojae for biocontrol of toxicogenic fungi. United States Patent. (Patent No. 6027724). https://patentimages.storage.googleapis.com/84/e6/5f/65765dbc491a4f/US5347263.pdf Dorner JW Horn BW Cole RJ 2000 Non-toxicogenic strain of Aspergillus oryzae and Aspergillus sojae for biocontrol of toxicogenic fungi United States Patent. (Patent No. 6027724) https://patentimages.storage.googleapis.com/84/e6/5f/65765dbc491a4f/US5347263.pdf El-EnshasyHA. 2007. Filamentous fungal cultures - process characteristics, products, and applications. En: YangS-T (ed.). Bioprocessing for Value-Added Products from Renewable Resources, n.1 (p.225-261). 670p. El-Enshasy HA 2007 Filamentous fungal cultures - process characteristics, products, and applications Yang S-T Bioprocessing for Value-Added Products from Renewable Resources 670p El-hawarySS, Moawa-dAS, BahrHS, AbdelmohsenUR y MohammedA. 2020. Natural product diversity from the endophytic fungi of the genus Aspergillus. RSC Advances 10(37): 22058-22079. https://doi.org/10.1039/D0RA04290K El-hawary SS Moawa-d AS Bahr HS Abdelmohsen UR Mohammed A 2020 Natural product diversity from the endophytic fungi of the genus Aspergillus RSC Advances 10 37 22058 22079 10.1039/D0RA04290K El-ShafieAK. 1996. Soil fungi in Qatar and other Arab countries. Economic Botany 50: 242. El-Shafie AK 1996 Soil fungi in Qatar and other Arab countries Economic Botany 50 242 242 EllatifSA, Abdel RazikES, Al-SurhaneeAA, Al-SarrajF, DaighamGE y MahfouzAY. 2022. Enhanced production, cloning, and expression of a xylanase gene from endophytic fungal strain Trichoderma harzianum KJ831197.1: Unveiling the in vitro antifungal activity against phytopathogenic fungi. Journal of Fungi (Basel, Switzerland) 8(5). https://doi.org/10.3390/jof8050447 Ellatif SA Abdel Razik ES Al-Surhanee AA Al-Sarraj F Daigham GE Mahfouz AY 2022 Enhanced production, cloning, and expression of a xylanase gene from endophytic fungal strain Trichoderma harzianum KJ831197.1: Unveiling the in vitro antifungal activity against phytopathogenic fungi Journal of Fungi (Basel, Switzerland) 8 5 10.3390/jof8050447 EscobarKV, RamónP, CárdenasFR y MonroyBLD. 2023. Detección de micotoxinas (aflatoxinas) en alimentos primarios y procesados para humanos y animales de granja, en Riobamba-Ecuador. Siembra 10(1): 1-7. https://doi.org/10.29166/SIEMBRA.V10I1.4126 Escobar KV Ramón P Cárdenas FR Monroy BLD 2023 Detección de micotoxinas (aflatoxinas) en alimentos primarios y procesados para humanos y animales de granja, en Riobamba-Ecuador Siembra 10 1 1 7 10.29166/SIEMBRA.V10I1.4126 FitrianaY, SuharjoR, SwibawaIG, SemengukB, PasaribuLT, HartamanM, RwandiniRA, IndriyatiI, PurnomoP y SolikhinS. 2021. Aspergillus oryzae and Beauveria bassiana as entomopathogenic fungi of Spodoptera litura Fabricius (Lepidoptera: Noctuidae) infesting corn in Lampung, Indonesia. Egyptian Journal of Biological Pest Control 31(1): 1-12. https://doi.org/10.1186/S41938-021-00473-8/FIGURES/7 Fitriana Y Suharjo R Swibawa IG Semenguk B Pasaribu LT Hartaman M Rwandini RA Indriyati I Purnomo P Solikhin S 2021 Aspergillus oryzae and Beauveria bassiana as entomopathogenic fungi of Spodoptera litura Fabricius (Lepidoptera: Noctuidae) infesting corn in Lampung, Indonesia Egyptian Journal of Biological Pest Control 31 1 1 12 10.1186/S41938-021-00473-8/FIGURES/7 FrisvadJC, MøllerLLH, LarsenTO, KumarR y ArnauJ. 2018. Safety of the fungal workhorses of industrial biotechnology: update on the mycotoxin and secondary metabolite potential of Aspergillus niger, Aspergillus oryzae, and Trichoderma reesei. Applied Microbiology and Biotechnology 102(22): 9481-9515. https://doi.org/10.1007/s00253-018-9354-1 Frisvad JC Møller LLH Larsen TO Kumar R Arnau J 2018 Safety of the fungal workhorses of industrial biotechnology: update on the mycotoxin and secondary metabolite potential of Aspergillus niger, Aspergillus oryzae, and Trichoderma reesei Applied Microbiology and Biotechnology 102 22 9481 9515 10.1007/s00253-018-9354-1 FurukawaS. 2012. Sake: quality characteristics, flavour chemistry and sensory analysis. En: PiggottJ (ed.). Alcoholic Beverages, n.1 (p.180-195). Woodhead Publishing. 461p.. https://doi.org/10.1533/9780857095176.2.180 Furukawa S 2012 Sake: quality characteristics, flavour chemistry and sensory analysis Piggott J Alcoholic Beverages Woodhead Publishing. 461p. 10.1533/9780857095176.2.180 GadSE. 2005. Generally recognized as safe (GRAS). En: WexlerP (ed.). Encyclopedia of Toxicology, Vol 2. (p.417-420). Gad Consulting Services, Inc.. Gad SE 2005 Generally recognized as safe (GRAS) Wexler P Encyclopedia of Toxicology Gad Consulting Services, Inc. GómezS, FernándezFJ y VegaMC. 2016. Heterologous expression of proteins in Aspergillus. En: GuptaVK (ed.). New and Future Developments in Microbial Biotechnology and Bioengineering, n.1 (p.55-68). Spanish National Science Council (CIB-CSIC). https://doi.org/10.1016/B978-0-444-63505-1.00004-X Gómez S Fernández FJ Vega MC 2016 Heterologous expression of proteins in Aspergillus Gupta VK New and Future Developments in Microbial Biotechnology and Bioengineering Spanish National Science Council (CIB-CSIC) 10.1016/B978-0-444-63505-1.00004-X GomiK. 2014. Aspergillus | Aspergillus oryzae. En: ElsieverInc (ed.). Encyclopedia of Food Microbiology, Vol 2. (p.92-96). https://doi.org/10.1016/B978-0-12-384730-0.00011-2 Gomi K 2014 Aspergillus | Aspergillus oryzae Elsiever Inc Encyclopedia of Food Microbiology 10.1016/B978-0-12-384730-0.00011-2 GuptaT y SaxenaJ. 2023. Biogenic synthesis of silver nanoparticles from Aspergillus oryzae MTCC 3107 against plant pathogenic fungi Sclerotinia sclerotiorum MTCC 8785. Journal of Microbiology, Biotechnology and Food Sciences 12(4): 1-4. https://doi.org/10.55251/JMBFS.9387 Gupta T Saxena J 2023 Biogenic synthesis of silver nanoparticles from Aspergillus oryzae MTCC 3107 against plant pathogenic fungi Sclerotinia sclerotiorum MTCC 8785 Journal of Microbiology, Biotechnology and Food Sciences 12 4 1 4 10.55251/JMBFS.9387 HeB, TuY, JiangC, ZhangZ, LiY y ZengB. 2019. Functional genomics of Aspergillus oryzae: Strategies and progress. Microorganisms 7(4): 103. https://doi.org/10.3390/MICROORGANISMS7040103 He B Tu Y Jiang C Zhang Z Li Y Zeng B 2019 Functional genomics of Aspergillus oryzae: Strategies and progress Microorganisms 7 4 103 103 10.3390/MICROORGANISMS7040103 HesseltineCW, SorensonWG y SmithM. 1970. Taxonomic studies of the aflatoxin-producing strains in the Aspergillus flavus group. Mycologia 62(1): 123-132. Hesseltine CW Sorenson WG Smith M 1970 Taxonomic studies of the aflatoxin-producing strains in the Aspergillus flavus group Mycologia 62 1 123 132 Jiménez-QueroA, PolletE, AvérousL y PhalipV. 2020. Optimized bioproduction of itaconic and fumaric acids based on solid-state fermentation of lignocellulosic biomass. Molecules (Basel, Switzerland) 25(5). https://doi.org/10.3390/molecules25051070 Jiménez-Quero A Pollet E Avérous L Phalip V 2020 Optimized bioproduction of itaconic and fumaric acids based on solid-state fermentation of lignocellulosic biomass Molecules (Basel, Switzerland) 25 5 10.3390/molecules25051070 KahnV. 1995. Effect of kojic acid on the oxidation of DL-DOPA, norepinephrine, and dopamine by mushroom tyrosinase. Pigment Cell Research 8(5): 234-240. https://doi.org/10.1111/J.1600-0749.1995.TB00669.X Kahn V 1995 Effect of kojic acid on the oxidation of DL-DOPA, norepinephrine, and dopamine by mushroom tyrosinase Pigment Cell Research 8 5 234 240 10.1111/J.1600-0749.1995.TB00669.X KahnV y Ben-ShalomN. 1997. Effect of maltol on the oxidation of DL-DOPA, Dopamine, N-Acetyldopamine (NADA), and Norepinephrine by mushroom tyrosinase. Pigment Cell Research 10(3): 139-149. https://doi.org/10.1111/j.1600-0749.1997.tb00475.x Kahn V Ben-Shalom N 1997 Effect of maltol on the oxidation of DL-DOPA, Dopamine, N-Acetyldopamine (NADA), and Norepinephrine by mushroom tyrosinase Pigment Cell Research 10 3 139 149 10.1111/j.1600-0749.1997.tb00475.x KimJH, ChanKL. 2014. Augmenting the antifungal activity of an oxidizing agent with kojic acid: control of Penicillium strains infecting crops. Molecules (Basel, Switzerland) 19(11): 18448-18464. https://doi.org/10.3390/molecules191118448 Kim JH Chan KL 2014 Augmenting the antifungal activity of an oxidizing agent with kojic acid: control of Penicillium strains infecting crops Molecules (Basel, Switzerland) 19 11 18448 18464 10.3390/molecules191118448 KimJH, ChangPK, ChanKL, FariaNCG, MahoneyN, KimYK, MartinsM de L y CampbellBC. 2012. Enhancement of commercial antifungal agents by kojic acid. International Journal of Molecular Sciences 13(11): 13867-13880. https://doi.org/10.3390/ijms131113867 Kim JH Chang PK Chan KL Faria NCG Mahoney N Kim YK Martins M de L Campbell BC 2012 Enhancement of commercial antifungal agents by kojic acid International Journal of Molecular Sciences 13 11 13867 13880 10.3390/ijms131113867 KimT, YeongJJ, JeongJS, LeeH, BaeCH, YeoJ, LeeH, KimI, ParkH y KimJC. 2016. Nematicidal activity of kojic acid produced by Aspergillus oryzae against Meloidogyne incognita. Journal of Microbiology and Biotechnology 26(8): 1383-1391. https://doi.org/10.4014/jmb.1603.03040 Kim T Yeong JJ Jeong JS Lee H Bae CH Yeo J Lee H Kim I Park H Kim JC 2016 Nematicidal activity of kojic acid produced by Aspergillus oryzae against Meloidogyne incognita Journal of Microbiology and Biotechnology 26 8 1383 1391 10.4014/jmb.1603.03040 KlichMA. 2002. Biogeography of Aspergillus species in soil and litter. Mycologia 94(1): 21-27. Klich MA 2002 Biogeography of Aspergillus species in soil and litter Mycologia 94 1 21 27 KocsubéS, PerroneG, MagistàD, HoubrakenJ, VargaJ, SzigetiG, HubkaV, HongSB, FrisvadJC y SamsonRA. 2016. Aspergillus is monophyletic: Evidence from multiple gene phylogenies and extrolites profiles. Studies in Mycology 85: 199-213. https://doi.org/10.1016/J.SIMYCO.2016.11.006 Kocsubé S Perrone G Magistà D Houbraken J Varga J Szigeti G Hubka V Hong SB Frisvad JC Samson RA 2016 Aspergillus is monophyletic: Evidence from multiple gene phylogenies and extrolites profiles Studies in Mycology 85 199 213 10.1016/J.SIMYCO.2016.11.006 KongF, LuN, LiuY, ZhangS, JiangH, WangH, WangW y LiS. 2021. Aspergillus oryzae and Aspergillus niger co-cultivation extract affects in vitro degradation, fermentation characteristics, and bacterial composition in a diet-specific manner. Animals : An Open Access Journal from MDPI 11(5). https://doi.org/10.3390/ani11051248 Kong F Lu N Liu Y Zhang S Jiang H Wang H Wang W Li S 2021 Aspergillus oryzae and Aspergillus niger co-cultivation extract affects in vitro degradation, fermentation characteristics, and bacterial composition in a diet-specific manner Animals : An Open Access Journal from MDPI 11 5 10.3390/ani11051248 KozakiewicZ. 1989. Aspergillus species on stored products. Mycological Papers 161: 188. Kozakiewic Z 1989 Aspergillus species on stored products Mycological Papers 161 188 188 KurtzmanCP, SmileyMJ, RobnettCJ y WicklowDT. 2018. DNA relatedness among wild and domesticated species in the Aspergillus flavus group. Mycologia 78(6): 955-959. https://doi.org/10.1080/00275514.1986.12025355 Kurtzman CP Smiley MJ Robnett CJ Wicklow DT 2018 DNA relatedness among wild and domesticated species in the Aspergillus flavus group Mycologia 78 6 955 959 10.1080/00275514.1986.12025355 LeeDE, LeeS, JangES, ShinHW, MoonBS y LeeCH. 2016. Metabolomic profiles of Aspergillus oryzae and Bacillus amyloliquefaciens during rice koji fermentation. Molecules 21(6). https://doi.org/10.3390/molecules21060773 Lee DE Lee S Jang ES Shin HW Moon BS Lee CH 2016 Metabolomic profiles of Aspergillus oryzae and Bacillus amyloliquefaciens during rice koji fermentation Molecules 21 6 10.3390/molecules21060773 LeeK, LeeSK y LeeBD. 2006. Aspergillus oryzae as probiotic in poultry—A review. International Journal of Poultry Science 5(1): 1-3. 10.3923/ijps.2006.1.3 Lee K Lee SK Lee BD 2006 Aspergillus oryzae as probiotic in poultry—A review International Journal of Poultry Science 5 1 1 3 10.3923/ijps.2006.1.3 MachidaM, AsaiK, SanoM, TanakaT, KumagaiT, TeraiG, KusumotoKI, ArimaT, AkitaO, KashiwagiY, AbeK, GomiK, HoriuchiH, KitamotoK, KobayashiT, TakeuchiM, DenningDW, GalaganJE, NiermanWC y KikuchiH. 2005. Genome sequencing and analysis of Aspergillus oryzae. Nature 438(7071): 1157-1161. https://doi.org/10.1038/NATURE04300 Machida M Asai K Sano M Tanaka T Kumagai T Terai G Kusumoto KI Arima T Akita O Kashiwagi Y Abe K Gomi K Horiuchi H Kitamoto K Kobayashi T Takeuchi M Denning DW Galagan JE Nierman WC Kikuchi H 2005 Genome sequencing and analysis of Aspergillus oryzae Nature 438 7071 1157 1161 10.1038/NATURE04300 MachidaM, YamadaO y GomiK. 2008. Genomics of Aspergillus oryzae: Learning from the history of koji mold and exploration of its future. DNA Research: An International Journal for Rapid Publication of Reports on Genes and Genomes 15(4): 173-183. https://doi.org/10.1093/DNARES/DSN020 Machida M Yamada O Gomi K 2008 Genomics of Aspergillus oryzae: Learning from the history of koji mold and exploration of its future DNA Research: An International Journal for Rapid Publication of Reports on Genes and Genomes 15 4 173 183 10.1093/DNARES/DSN020 MahasJW, HamiltonFB, RobertsPM, RayCH, MillerGL, SharmanM, ConnerK, BagS, BlytheEK, ToewsMD y JacobsonAL. 2022. Investigating the effects of planting date and Aphis gossypii management on reducing the final incidence of cotton leafroll dwarf virus. Crop Protection 158: 106005. https://doi.org/https://doi.org/10.1016/j.cropro.2022.106005 Mahas JW Hamilton FB Roberts PM Ray CH Miller GL Sharman M Conner K Bag S Blythe EK Toews MD Jacobson AL 2022 Investigating the effects of planting date and Aphis gossypii management on reducing the final incidence of cotton leafroll dwarf virus Crop Protection 158 106005 106005 https://doi.org/10.1016/j.cropro.2022.106005 MahmoudGA, ZohriANA, Kamal-EldinNA y AbdelhamidNMR. 2023. Application of Aspergillus oryzae ASU44 (OL314732) and their kojic acid as pesticides against cotton aphid, Aphis gossypii. Bulletin of Pharmaceutical Sciences. Assiut 46(1): 63-82. https://doi.org/10.21608/bfsa.2023.300763 Mahmoud GA Zohri ANA Kamal-Eldin NA Abdelhamid NMR 2023 Application of Aspergillus oryzae ASU44 (OL314732) and their kojic acid as pesticides against cotton aphid, Aphis gossypii Bulletin of Pharmaceutical Sciences. Assiut 46 1 63 82 10.21608/bfsa.2023.300763 MarshallH, MeneelyJP, QuinnB, ZhaoY, BourkeP, GilmoreBF, ZhangG y ElliottCT. 2020. Novel decontamination approaches and their potential application for post-harvest aflatoxin control. Trends in Food Science & Technology 106: 489-496. https://doi.org/https://doi.org/10.1016/j.tifs.2020.11.001 Marshall H Meneely JP Quinn B Zhao Y Bourke P Gilmore BF Zhang G Elliott CT 2020 Novel decontamination approaches and their potential application for post-harvest aflatoxin control Trends in Food Science & Technology 106 489 496 https://doi.org/10.1016/j.tifs.2020.11.001 MatsunagaK, FurukawaK y HaraS. 2002. Effects of enzyme activity on the mycelial penetration of rice koji. Journal of the Brewing Society of Japan 97(10): 721-726. https://doi.org/10.6013/JBREWSOCJAPAN1988.97.721 Matsunaga K Furukawa K Hara S 2002 Effects of enzyme activity on the mycelial penetration of rice koji Journal of the Brewing Society of Japan 97 10 721 726 10.6013/JBREWSOCJAPAN1988.97.721 MeiniMR, CabezudoI, GalettoCS y RomaniniD. 2021. Production of grape pomace extracts with enhanced antioxidant and prebiotic activities through solid-state fermentation by Aspergillus niger and Aspergillus oryzae. Food Bioscience 42: 101168. https://doi.org/https://doi.org/10.1016/j.fbio.2021.101168 Meini MR Cabezudo I Galetto CS Romanini D 2021 Production of grape pomace extracts with enhanced antioxidant and prebiotic activities through solid-state fermentation by Aspergillus niger and Aspergillus oryzae Food Bioscience 42 101168 101168 https://doi.org/10.1016/j.fbio.2021.101168 MohamadR, MohamedM, SuhailiN, SallehMM y AriffA. 2010. Kojic acid: applications and development of fermentation process for production. Biotechnology and Molecular Biology Reviews 5(2): 24-37. Mohamad R Mohamed M Suhaili N Salleh MM Ariff A 2010 Kojic acid: applications and development of fermentation process for production Biotechnology and Molecular Biology Reviews 5 2 24 37 MousaviB, HedayatiM, HedayatiN, IlkitM y SyedmousaviS. 2016. Aspergillus species in indoor environments and their possible occupational and public health hazards. Current Medical Mycology 2(1): 36-47. https://doi.org/10.18869/ACADPUB.CMM.2.1.36 Mousavi B Hedayati M Hedayati N Ilkit M Syedmousavi S 2016 Aspergillus species in indoor environments and their possible occupational and public health hazards Current Medical Mycology 2 1 36 47 10.18869/ACADPUB.CMM.2.1.36 MuraliM, AmrutheshKN, SudishaJ, NiranjanaSR y ShettyHS. 2012. Screening for plant growth promoting fungi and their ability for growth promotion and induction of resistance in pearl millet against downy mildew disease. Journal of Phytology 4(5): 30-36. Murali M Amruthesh KN Sudisha J Niranjana SR Shetty HS 2012 Screening for plant growth promoting fungi and their ability for growth promotion and induction of resistance in pearl millet against downy mildew disease Journal of Phytology 4 5 30 36 MurphyMM. 2021. Effect of Aspergillus niger and oryzae on the intake and digestibility of Coastal Bermudagrass and Teff hay in horses. Journal of Equine Veterinary Science 100(103516). https://doi.org/10.1016/j.jevs.2021.103516 Murphy MM 2021 Effect of Aspergillus niger and oryzae on the intake and digestibility of Coastal Bermudagrass and Teff hay in horses Journal of Equine Veterinary Science 100 103516 10.1016/j.jevs.2021.103516 NavaleV, VamkudothKR, AjmeraS y DhuriV. 2021. Aspergillus-derived mycotoxins in food and the environment: Prevalence, detection, and toxicity. Toxicology Reports 8: 1008-1030. https://doi.org/10.1016/j.toxrep.2021.04.013 Navale V Vamkudoth KR Ajmera S Dhuri V 2021 Aspergillus-derived mycotoxins in food and the environment: Prevalence, detection, and toxicity Toxicology Reports 8 1008 1030 10.1016/j.toxrep.2021.04.013 NorliaM, JinapS, Nor-KhaizuraMAR, RaduS, SamsudinNIP y AzriFA. 2019. Aspergillus section Flavi and aflatoxins: occurrence, detection, and identification in raw peanuts and peanut-based products along the supply chain. Frontiers in Microbiology 10: 2602. https://doi.org/10.3389/fmicb.2019.02602 Norlia M Jinap S Nor-Khaizura MAR Radu S Samsudin NIP Azri FA 2019 Aspergillus section Flavi and aflatoxins: occurrence, detection, and identification in raw peanuts and peanut-based products along the supply chain Frontiers in Microbiology 10 2602 2602 10.3389/fmicb.2019.02602 NorliaM, Nor-KhaizuraMAR, SelamatJ, Abu BakarF, RaduS y ChinCK. 2018. Evaluation of aflatoxin and Aspergillus sp. contamination in raw peanuts and peanut-based products along this supply chain in Malaysia. Food Additives and Contaminants. Part A, Chemistry, Analysis, Control, Exposure and Risk Assessment 35(9): 1787-1802. https://doi.org/10.1080/19440049.2018.1488276 Norlia M Nor-Khaizura MAR Selamat J Abu Bakar F Radu S Chin CK 2018 Evaluation of aflatoxin and Aspergillus sp. contamination in raw peanuts and peanut-based products along this supply chain in Malaysia Food Additives and Contaminants. Part A, Chemistry, Analysis, Control, Exposure and Risk Assessment 35 9 1787 1802 10.1080/19440049.2018.1488276 Olempska-BeerZS, MerkerRI, DittoMD y DiNoviMJ. 2006. Food-processing enzymes from recombinant microorganisms—a review. Regulatory Toxicology and Pharmacology 45(2): 144-158. https://doi.org/10.1016/J.YRTPH.2006.05.001 Olempska-Beer ZS Merker RI Ditto MD DiNovi MJ 2006 Food-processing enzymes from recombinant microorganisms—a review Regulatory Toxicology and Pharmacology 45 2 144 158 10.1016/J.YRTPH.2006.05.001 PadrónMHY, DelgadoHS, ReyesMCA y VázquezCG. 2013. The genus Aspergillus and their mycotoxins in maize in Mexico: Problems and perspectives. Revista Mexicana de Fitopatología 31(19): 126-146. Padrón MHY Delgado HS Reyes MCA Vázquez CG 2013 The genus Aspergillus and their mycotoxins in maize in Mexico: Problems and perspectives Revista Mexicana de Fitopatología 31 19 126 146 PanchanawapornS, ChutrakulC, JeennorS, AnantayanonJ, RattanaphanN y LaotengK. 2022. Potential of Aspergillus oryzae as a biosynthetic platform for indigoidine, a non-ribosomal peptide pigment with antioxidant activity. PLoS ONE 17(6). https://doi.org/10.1371/JOURNAL.PONE.0270359 Panchanawaporn S Chutrakul C Jeennor S Anantayanon J Rattanaphan N Laoteng K 2022 Potential of Aspergillus oryzae as a biosynthetic platform for indigoidine, a non-ribosomal peptide pigment with antioxidant activity PLoS ONE 17 6 10.1371/JOURNAL.PONE.0270359 PayneGA, NiermanWC, WortmanJR, PritchardBL, BrownD, DeanRA, BhatnagarD, ClevelandTE, MachidaM y YuJ. 2006. Whole genome comparison of Aspergillus flavus and A. oryzae. Medical Mycology 44: 9-11. https://doi.org/10.1080/13693780600835716 Payne GA Nierman WC Wortman JR Pritchard BL Brown D Dean RA Bhatnagar D Cleveland TE Machida M Yu J 2006 Whole genome comparison of Aspergillus flavus and A. oryzae Medical Mycology 44 9 11 10.1080/13693780600835716 PhashaV, SenabeJ, NdzotoyiP, OkoleB, FoucheG y ChuturgoonA. 2022. Review on the use of kojic Acid—a skin-lightening ingredient. Cosmetics 9(3): 64. https://doi.org/10.3390/COSMETICS9030064 Phasha V Senabe J Ndzotoyi P Okole B Fouche G Chuturgoon A 2022 Review on the use of kojic Acid—a skin-lightening ingredient Cosmetics 9 3 64 64 10.3390/COSMETICS9030064 PodversichF, TarnonskyF, BollattiJM, SilvaGM, SchulmeisterTM, MartinezJJV, HerediaD, IpharraguerreIR, BargoF, GonellaDiazaA, DubeuxJCB, FerrarettoLF y DiLorenzoN. 2023. Effects of Aspergillus oryzae prebiotic on animal performance, nutrients digestibility, and feeding behavior of backgrounding beef heifers fed with either a sorghum silageor a byproductsbased diet. Journal of Animal Science 101. https://doi.org/10.1093/jas/skac312 Podversich F Tarnonsky F Bollatti JM Silva GM Schulmeister TM Martinez JJV Heredia D Ipharraguerre IR Bargo F GonellaDiaza A Dubeux JCB Ferraretto LF DiLorenzo N 2023 Effects of Aspergillus oryzae prebiotic on animal performance, nutrients digestibility, and feeding behavior of backgrounding beef heifers fed with either a sorghum silageor a byproductsbased diet Journal of Animal Science 101 10.1093/jas/skac312 PowellKA, RenwickA, PeberdyJF y Federation of European Microbiological Societies . 1994. The Genus Aspergillus: from taxonomy and genetics to industrial application. Plenum Press, New York USA. 380p. Powell KA Renwick A Peberdy JF Federation of European Microbiological Societies 1994 The Genus Aspergillus: from taxonomy and genetics to industrial application Plenum Press New York USA 380p 380p RádulyZ, SzabóL, MadarA, PócsiI y CsernochL. 2019. Toxicological and medical aspects of Aspergillus-derived mycotoxins entering the feed and food chain. Frontiers in Microbiology 10(2908): 1-23. https://doi.org/10.3389/fmicb.2019.02908 Ráduly Z Szabó L Madar A Pócsi I Csernoch L 2019 Toxicological and medical aspects of Aspergillus-derived mycotoxins entering the feed and food chain Frontiers in Microbiology 10 2908 1 23 10.3389/fmicb.2019.02908 Samson, R.A. , Visagie, C.M. , Houbraken, J. , Hong, S.B. , Hubka, V. , Klaassen, C.H.W. , Perrone, G. , Seifert, K.A. , Susca, A. , Tanney, J.B. , Varga, J. , Kocsub, S. , Szigeti, G. , Yaguchi, T. , Frisvad, J.C. (2014). Phylogeny, identification and nomenclature of the genus Aspergillus. Studies in Mycology, 78, 141-173. https://doi.org/10.1016/j.simyco.2014.07.004 Samson R.A. Visagie C.M. Houbraken J. Hong S.B. Hubka V. Klaassen C.H.W. Perrone G. Seifert K.A. Susca A. Tanney J.B. Varga J. Kocsub S. Szigeti G. Yaguchi T. Frisvad J.C. 2014 Phylogeny, identification and nomenclature of the genus Aspergillus Studies in Mycology 78 141 173 10.1016/j.simyco.2014.07.004 Schuster, E. , Dunn-Coleman, N. , Frisvad, J.C. , Van Dijck, P.W.M. (2002). On the safety of Aspergillus niger—a review. Applied Microbiology and Biotechnology, 59 (4-5), 426-435. https://doi.org/10.1007/s00253-002-1032-6 Schuster E. Dunn-Coleman N. Frisvad J.C. Van Dijck P.W.M. 2002 On the safety of Aspergillus niger—a review Applied Microbiology and Biotechnology 59 4-5 426 435 10.1007/s00253-002-1032-6 Senghor, L.A. , Ortega-Beltran, A. , Atehnkeng, J. , Callicott, K.A. , Cotty, P.J. , Bandyopadhyay, R. (2020). The atoxigenic biocontrol product Aflasafe SN01 is a valuable tool to mitigate aflatoxin contamination of both maize and groundnut cultivated in Senegal. Plant Disease, 104 (2), 510-520. Senghor L.A. Ortega-Beltran A. Atehnkeng J. Callicott K.A. Cotty P.J. Bandyopadhyay R. 2020 The atoxigenic biocontrol product Aflasafe SN01 is a valuable tool to mitigate aflatoxin contamination of both maize and groundnut cultivated in Senegal Plant Disease 104 2 510 520 Seo, H.J. , Park, A.R. , Kim, S. , Yeon, J. , Yu, N.H. , Ha, S. , Chang, J.Y. , Park, H.W. , Kim, J.C. (2019). Biological control of root-knot nematodes by organic acid-producing Lactobacillus brevis WIKIM0069 isolated from kimchi. Plant Pathology Journal, 35 (6), 662-673. https://doi.org/10.5423/PPJ.OA.08.2019.0225 Seo H.J. Park A.R. Kim S. Yeon J. Yu N.H. Ha S. Chang J.Y. Park H.W. Kim J.C. 2019 Biological control of root-knot nematodes by organic acid-producing Lactobacillus brevis WIKIM0069 isolated from kimchi Plant Pathology Journal 35 6 662 673 10.5423/PPJ.OA.08.2019.0225 Sharifi, M. , Ghadamyari, M. , Sajedi, R.H. , Zavareh, M. , Sheikhnejad, H. (2013). Insecticidal effects of 4-hexylresorcinol on the lesser mulberry snout moth, Glyphodes pyloalis Walker. Archives of Phytopathology and Plant Protection, 46 (4), 423-435. https://doi.org/10.1080/03235408.2012.743387 Sharifi M. Ghadamyari M. Sajedi R.H. Zavareh M. Sheikhnejad H. 2013 Insecticidal effects of 4-hexylresorcinol on the lesser mulberry snout moth, Glyphodes pyloalis Walker Archives of Phytopathology and Plant Protection 46 4 423 435 10.1080/03235408.2012.743387 Sharma, P. , Singh, S.P. (2021). Role of the endogenous fungal metabolites in the plant growth improvement and stress tolerance. In: Fungi Bio-Prospects in Sustainable Agriculture, Environment and Nano-Technology , Volume 3. 381-401. https://doi.org/10.1016/B978-0-12-821734-4.00002-2 Sharma P. Singh S.P. 2021 Role of the endogenous fungal metabolites in the plant growth improvement and stress tolerance Fungi Bio-Prospects in Sustainable Agriculture, Environment and Nano-Technology Volume 3 381 401 10.1016/B978-0-12-821734-4.00002-2 Siddiquee, S. (2018). Recent advancements on the role of biologically active secondary metabolites from Aspergillus. In: Gupta, V.K. , Rodriguez-Couto, S. (eds.). New and Future Developments in Microbial Biotechnology and Bioengineering: Penicillium System Properties and Applications, 69-94. Siddiquee S. 2018 Recent advancements on the role of biologically active secondary metabolites from Aspergillus Gupta V.K. Rodriguez-Couto S. New and Future Developments in Microbial Biotechnology and Bioengineering: Penicillium System Properties and Applications 69 94 Siddiqui, S. (2016). Protein production: Quality control and secretion stress response. In: Gupta, V.K. (eds.). New and Future Developments in Microbial Biotechnology and Bioengineering: Aspergillus System Properties and Applications, 257-266. Siddiqui S. 2016 Protein production: Quality control and secretion stress response Gupta V.K. New and Future Developments in Microbial Biotechnology and Bioengineering: Aspergillus System Properties and Applications 257 266 Singh, M. , Srivastava, P.K. , Verma, P.C. , Kharwar, R.N. , Singh, N. , Tripathi, R.D. (2015). Soil fungi for mycoremediation of arsenic pollution in agriculture soils. Journal of Applied Microbiology, 119 (5), 1278-1290. https://doi.org/10.1111/JAM.12948 Singh M. Srivastava P.K. Verma P.C. Kharwar R.N. Singh N. Tripathi R.D. 2015 Soil fungi for mycoremediation of arsenic pollution in agriculture soils Journal of Applied Microbiology 119 5 1278 1290 10.1111/JAM.12948 Skinder, B.M. , Nabi, M. , Gojree, B.A.S. , Dar, G.H. , Ganai, B.A. (2022). Endophytic Microbes: Bioremediation of soil contaminants. In: Dar, G.H. , Bhat, R.A. , Qadri, H. , Hakeem, K.R. (eds.). Microbial Consortium and Biotransformation for Pollution Decontamination, 243-258. Skinder B.M. Nabi M. Gojree B.A.S. Dar G.H. Ganai B.A. 2022 Endophytic Microbes: Bioremediation of soil contaminants Dar G.H. Bhat R.A. Qadri H. Hakeem K.R. Microbial Consortium and Biotransformation for Pollution Decontamination 243 258 Sosa, A. , Marrero, Y. , González, N. , Albelo, N. , Moreira, O.B. , Cairo, J. , Galindo, J. (2022). Effect of Aspergillus oryzae on ruminal fermentation, feed intake and dry matter digestibility in cows fed forage-based diets. Animal Biotechnology, 33 (7), 1519-1524. https://doi.org/10.1080/10495398.2021.1914069 Sosa A. Marrero Y. González N. Albelo N. Moreira O.B. Cairo J. Galindo J. 2022 Effect of Aspergillus oryzae on ruminal fermentation, feed intake and dry matter digestibility in cows fed forage-based diets Animal Biotechnology 33 7 1519 1524 10.1080/10495398.2021.1914069 Sun, B.T. , Akutse, K.S. , Xia, X.F. , Chen, J.H. , Ai, X. , Tang, Y. , Wang, Q. , Feng, B.W. , Goettel, M.S. , You, M.S. (2018). Endophytic effects of Aspergillus oryzae on radish (Raphanus sativus) and its herbivore, Plutella xylostella. Planta, 248 (3), 705-714. https://doi.org/10.1007/s00425-018-2928-4 Sun B.T. Akutse K.S. Xia X.F. Chen J.H. Ai X. Tang Y. Wang Q. Feng B.W. Goettel M.S. You M.S. 2018 Endophytic effects of Aspergillus oryzae on radish (Raphanus sativus) and its herbivore, Plutella xylostella Planta 248 3 705 714 10.1007/s00425-018-2928-4 Sun, J. , Zou, X. , Ning, Z. , Sun, M. , Peng, J. , Xiao, T. (2012). Culturable microbial groups and thallium-tolerant fungi in soils with high thallium contamination. The Science of the Total Environment, 441, 258-264. https://doi.org/10.1016/J.SCITOTENV.2012.09.053 Sun J. Zou X. Ning Z. Sun M. Peng J. Xiao T. 2012 Culturable microbial groups and thallium-tolerant fungi in soils with high thallium contamination The Science of the Total Environment 441 258 264 10.1016/J.SCITOTENV.2012.09.053 Tari, C. , Dogan, N. , Gogus, N. (2008). Biochemical and thermal characterization of crude exo-polygalacturonase produced by Aspergillus sojae. Food Chemistry, 111 (4), 824-829. https://doi.org/10.1016/j.foodchem.2008.04.056 Tari C. Dogan N. Gogus N. 2008 Biochemical and thermal characterization of crude exo-polygalacturonase produced by Aspergillus sojae Food Chemistry 111 4 824 829 10.1016/j.foodchem.2008.04.056 U.S. Food and Drug Administration (2019). Generally Recognized Safe (GRAS) | FDA. https://www.fda.gov/food/food-ingredients-packaging/generally-recognized-safe-gras (consulta, noviembre 2022). U.S. Food and Drug Administration 2019 Generally Recognized Safe (GRAS) | FDA https://www.fda.gov/food/food-ingredients-packaging/generally-recognized-safe-gras Watarai, N. , Yamamoto, N. , Sawada, K. , Yamada, T. (2019). Evolution of Aspergillus oryzae before and after domestication inferred by large-scale comparative genomic analysis. DNA Research, 26 (6), 465-472. https://doi.org/10.1093/DNARES/DSZ024 Watarai N. Yamamoto N. Sawada K. Yamada T. 2019 Evolution of Aspergillus oryzae before and after domestication inferred by large-scale comparative genomic analysis DNA Research 26 6 465 472 10.1093/DNARES/DSZ024 Xiong, K. , Zhi, H.W. , Liu, J.Y. , Wang, X.Y. , Zhao, Z.Y. , Pei, P.G. , Deng, L. , Xiong, S.Y. (2021). Detoxification of Ochratoxin A by a novel Aspergillus oryzae strain and optimization of its biodegradation. Revista Argentina de Microbiología, 53 (1), 48-58. https://doi.org/10.1016/j.ram.2020.06.001 Xiong K. Zhi H.W. Liu J.Y. Wang X.Y. Zhao Z.Y. Pei P.G. Deng L. Xiong S.Y. 2021 Detoxification of Ochratoxin A by a novel Aspergillus oryzae strain and optimization of its biodegradation Revista Argentina de Microbiología 53 1 48 58 10.1016/j.ram.2020.06.001 Xu, Q. , Li, S. , Huang, H. , Wen, J. (2012). Key technologies for the industrial production of fumaric acid by fermentation. Biotechnology Advances, 30 (6), 1685-1696. https://doi.org/10.1016/j.biotechadv.2012.08.007 Xu Q. Li S. Huang H. Wen J. 2012 Key technologies for the industrial production of fumaric acid by fermentation Biotechnology Advances 30 6 1685 1696 10.1016/j.biotechadv.2012.08.007 Yadav, U. (2017). Recent trends in nematode management practices: the Indian context. International Research Journal of Engineering and Technology, 10 (12), 483-489. Yadav U. 2017 Recent trends in nematode management practices: the Indian context International Research Journal of Engineering and Technology 10 12 483 489 Yamada, R. , Yoshie, T. , Wakai, S. , Asai-Nakashima, N. , Okazaki, F. , Ogino, C. , Hisada, H. , Tsutsumi, H. , Hata, Y. , Kondo, A. (2014). Aspergillus oryzae-based cell factory for direct kojic acid production from cellulose. Microbial Cell Factories, 13 (1), 1-8. https://doi.org/10.1186/1475-2859-13-71 Yamada R. Yoshie T. Wakai S. Asai-Nakashima N. Okazaki F. Ogino C. Hisada H. Tsutsumi H. Hata Y. Kondo A. 2014 Aspergillus oryzae-based cell factory for direct kojic acid production from cellulose Microbial Cell Factories 13 1 1 8 10.1186/1475-2859-13-71 Yasui, M. , Oda, K. , Masuo, S. , Hosoda, S. , Katayama, T. , Maruyama, J.I. , Takaya, N. , Takeshita, N. (2020). Invasive growth of Aspergillus oryzae in rice koji and increase of nuclear number. Fungal Biology and Biotechnology, 7 (1), 1-15. https://doi.org/10.1186/S40694-020-00099-9 Yasui M. Oda K. Masuo S. Hosoda S. Katayama T. Maruyama J.I. Takaya N. Takeshita N. 2020 Invasive growth of Aspergillus oryzae in rice koji and increase of nuclear number Fungal Biology and Biotechnology 7 1 1 15 10.1186/S40694-020-00099-9 Yu, J. , Chang, P.K. , Ehrlich, K.C. , Cary, J.W. , Bhatnagar, D. , Cleveland, T.E. , Payne, G.A. , Linz, J.E. , Woloshuk, C.P. , Bennett, J.W. (2004). Clustered pathway genes in aflatoxin biosynthesis. Applied and Environmental Microbiology, 70 (3), 1253-1262. Yu J. Chang P.K. Ehrlich K.C. Cary J.W. Bhatnagar D. Cleveland T.E. Payne G.A. Linz J.E. Woloshuk C.P. Bennett J.W. 2004 Clustered pathway genes in aflatoxin biosynthesis Applied and Environmental Microbiology 70 3 1253 1262 Zhang, D. , Ma, X. , Gu, Y. , Huang, H. , Zhang, G. (2020). Green synthesis of metallic nanoparticles and their potential applications to treat cancer. Frontiers in Chemistry, 8 (799), 1-18. https://doi.org/10.3389/fchem.2020.00799 Zhang D. Ma X. Gu Y. Huang H. Zhang G. 2020 Green synthesis of metallic nanoparticles and their potential applications to treat cancer Frontiers in Chemistry 8 799 1 18 10.3389/fchem.2020.00799 Zhang, P. , You, Y. , Song, Y. , Wang, Y. , Zhang, L. (2015). First record of Aspergillus oryzae (Eurotiales: Trichocomaceae) as an entomopathogenic fungus of the locust, Locusta migratoria (Orthoptera: Acrididae). Biocontrol Science and Technology, 25 (11), 1285-1298. https://doi.org/10.1080/09583157.2015.1049977 Zhang P. You Y. Song Y. Wang Y. Zhang L. 2015 First record of Aspergillus oryzae (Eurotiales: Trichocomaceae) as an entomopathogenic fungus of the locust, Locusta migratoria (Orthoptera: Acrididae) Biocontrol Science and Technology 25 11 1285 1298 10.1080/09583157.2015.1049977 Zhou, M. , Zhou, K. , He, P. , Wang, K.M. , Zhu, R.Z. , Wang, Y.D. , Dong, W. , Li, G.P. , Yang, H.Y. , Ye, Y.Q. , Du, G. , Li, X.M. , Hu, Q.F. (2016). Antiviral and cytotoxic isocoumarin derivatives from an endophytic fungus Aspergillus oryzae. Planta Medica, 82 (5), 414-417. https://doi.org/10.1055/s-0035-1558331 Zhou M. Zhou K. He P. Wang K.M. Zhu R.Z. Wang Y.D. Dong W. Li G.P. Yang H.Y. Ye Y.Q. Du G. Li X.M. Hu Q.F. 2016 Antiviral and cytotoxic isocoumarin derivatives from an endophytic fungus Aspergillus oryzae Planta Medica 82 5 414 417 10.1055/s-0035-1558331 Zhu, G.Y. , Shi, X.C. , Wang, S.Y. , Wang, B. , Laborda, P. (2022). Antifungal mechanism and efficacy of kojic acid for the control of Sclerotinia sclerotiorum in soybean. Frontiers in Plant Science, 13 (845698), 1-11. https://doi.org/10.3389/fpls.2022.845698 Zhu G.Y. Shi X.C. Wang S.Y. Wang B. Laborda P. 2022 Antifungal mechanism and efficacy of kojic acid for the control of Sclerotinia sclerotiorum in soybean Frontiers in Plant Science 13 845698 1 11 10.3389/fpls.2022.845698 Review Aspergillus oryzae: An opportunity for agriculture Abstract

Aspergillus oryzae is a filamentous fungus capable of degrading various substances employing enzymes, which is why it is widely used in the biotechnological industry, pharmaceutical products, enzymes for industrial use, bleaching agents, anti- pollution textile treatments. However, few works focus on these microorganism’s field applications. This manuscript reviews the potentially beneficial applications of A. oryzae and some by-products in agriculture as biological control, growth inducer, and bioremediation for soils contaminated with heavy metals.

 Keywords: Bioremediation nematicide insecticide microorganisms metabolites non-toxigenic. Introduction

The fungi of the Aspergillus spp. genus are considered a complex group of ascomycetes that compose 350 accepted species (Kocsubé et al., 2016). They are described as filamentous fungi, able to secrete a wide range of secondary metabolites and enzymes, whose function is to degrade and recycle biopolymers from plant tissues (El-Enshasy, 2007). The Aspergillus spp. genus is generally found in stored seeds, plants in decomposition and soil, where they develop as saprophytes (Mousavi et al., 2016).

Although fungi from the Aspergillus spp. genus are not considered important sources of phytosanitary diseases, they are responsible for alterations in plants and stored products; since they are opportunist molds, they prosper under storage conditions (Awuchi et al., 2021). This genus is also recognized for its production of mycotoxins, with around 300 and 400 identified, such as aflatoxins, secalonic acids, cyclopiazonic acid, aflatrem, citrinin, stregmatocystin, glycytoxin, ochratoxin A (OTA) and terrein (Navale et al., 2021), with a potential health risk for humans and animals, as well as affecting the environment and having a negative effect on the world’s economy (Bueno et al., 2015). An important example of this type of toxic secondary metabolites are aflatoxins, which represent a hazard for farmers in postharvest and are considered indicators of biological soil degradation (Marshall et al., 2020). They bring about qualitative nutritional and sensory changes in plant- based products, since the infection can produce unpleasant flavors or odors, rotting and discoloration (Kozakiewic, 1989).

Some fungi of the Aspergillus spp. genus, such as A. flavus, A. nidulans, A. nomius and A. parasiticus, are agronomically important, since they produce aflatoxins (AF) (Hesseltine et al., 1970; Gomi, 2014). Mainly B1, B2, G1 and G2 have proven to be strong carcinogenic, cytotoxic and potentially mortal biotoxins for humans and cattle (Ráduly et al., 2019). A. flavus has been reported as the cause of contamination with aflatoxins AFB1 in any stage of the peanut supply chain (imports, manufacturing and retail) in countries such as Malaysia, where the tropical climate conditions are favorable for the growth of this fungus (Norlia et al., 2018, 2019). In Mexico, maize has been affected by contamination with aflatoxins, in the same way as grains such as rice, barley, bean, sorghum, wheat, some oleaginous plants and dried fruits are susceptible to these biotoxins, produced by A. flavus (AFB1 and AFB2), A. parasiticus and A. nomius (AFG1 and AFG2) (Anguiano-Ruvalcaba et al., 2005; Escobar et al., 2023).

It is worth highlighting the existence of non-toxicogenic strains within Aspergillus spp., which do not produce aflatoxins and which can be applied in the planting area, to then be installed, compete and displace the toxigenic strains, resulting in the reduction of aflatoxins (Marshall et al., 2020; Senghor et al., 2020). Non-toxicogenic A. niger, A. sojae and A. oryzae strains do not produce compounds that contain, essentially, a furan ring attached to the coumarin nucleus, important in the biosynthesis path of aflatoxins, and do not produce cyclopiazonic acid jointly with aflatoxins such as A. flavus (Dorner et al., 2000; Padrón et al., 2013).

Aspergillus spp. strains that do not produce aflatoxins can be used as fungal biocontrol agents in the prevention of contamination with biotoxins (Barberis et al., 2019). Strains A. westerdijkiae 107, A. fumigatos C143, A. tamarii C122 and A. niger C187 have proven, in terms of inhibition and production of OTA, to have favorable results, with the strain A. niger C187 displaying an inhibition of 100% in the production of OTA and in the growth of A. ochraceus, A. westerdijkiae, A. carbonarius and A. niger in coffee grains (de Almeida et al., 2019). Likewise, they are used in the pharmaceutical industry and in industrial processes such as the fermentation of foods, since they are abundant sources of enzymes such as proteases, amylases and amylglucosidases, and others (Schuster et al., 2002; Olempska- Beer et al., 2006; Samson et al., 2014; Gómez et al., 2016). The production of polygalacturonase (Exo-PGs), a consortium of enzymes required for the hydrolysis of pectin, is one of the applications of the strain A. sojae ATCC 20235, useful in the depectinization and clarification of fruit juices, the extraction of oils from the skins of vegetables and citrus fruits, and treating wastewater (Tari et al., 2008).

Therefore, because A. oryzae has non-toxigenic strains, it figures as one of the most important species, due to its potential use as a biotechnological tool in degrading metabolic processes of diverse starches and proteins; in the metabolism of amino acids and amino acid and sugar absorption transporters (Machida et al., 2005, 2008; Watarai et al., 2019; Daba et al., 2021). A. oryzae is considered by the FDA as “generally recognized as safe” (GRAS), which refers to any substance intentionally added to foods, which must be subjected to revision and approval before its commercialization, unless the substance is generally recognized among qualified experts (Gad, 2005; FDA, 2019). Therefore, the WHO endorses the security in the use of A. oryzae (He et al., 2019), considering this microorganism adequate for its application in the food industry, such as the fermentation of foods, the production of alcohol and vinegar, in the pharmaceutical and cosmetics industries via the formulation of drugs and depigmenting agents. These applications are due to the production of enzymes and secondary metabolites such as lipases, cellulases, pectinases, β-galactosidase, amylases, kojic acid, malic acid, fumaric acid, pheluric acid and others (Daba et al., 2021).

Therefore, this study focuses on reviewing investigation and literature studies on the diverse products derived from A. oryzae, their contributions and applications in the agricultural areas, such as bioremediators, growth enhancers and biological control agents. It is worth highlighting that, although the study of A. oryzae has focused mostly in the industrial area, this study only considered those studies and investigations in which their application is directed to the agronomic part. It focuses primarily on kojic acid and A. oryzae strains involved in its production, since the fermentation process presents sustainable characteristics, and its applications are novel for the agricultural area.

The main objective of this revision is to publish the potential of A. oryzae in scarcely studied areas of agricultural importance. Although A. oryzae has been studied on a large scale in industrial, food and medical areas, studies on its agronomic potential are few, and in Mexico its study is practically inexistent, hence part of this revision seeks the development in the future of scientific studies on A. oryzae aimed at the agricultural sector, contributing to the development and care of the Mexican countryside.

<bold>Morphology and description of <italic>Aspergillus oryzae;</italic> origin, isolation and development</bold>

Aspergillus spp. presents hyaline septate hyphae, with a 45° dichotomic ramification (Cuervo-Maldonado et al., 2010). Growth forms extended mycelia that cover the entire surface of the culture media (Gomi, 2014) (Figure 1). The balloon-shaped vesicle has a diameter between 100 and 200 µm with a structure formed by oval-shaped conidia, 5 to 8 µm in length that contains four soft and slightly coarse nuclei. The phialides are found in the vesicle and may be uniseriate or biseriate sterigmata. The shoots are colorless and 1 to 5 mm in length, with a rugged texture (Moubasher, 1993; Powell et al., 1994).

Ahlburg (1876) first isolated A. oryzae from köji, the material fermented by the mold of A. oryzae planted in a steamed rice solid medium (Machida et al.,

Morphology of <italic>A. oryzae</italic>; A) Parts and structures of the fungus (Adapted from “Structure of <italic>Aspergillus</italic> spp.”, 2023), B) <italic>A. oryzae</italic> planted in a PDA medium and C) Growth of <italic>A. oryzae</italic> in steamed rice (köji).

2008). This fungus belongs to the Erotyomicetes class; Order: Eurotiales; Family: Trichocomaceae (Daba et al., 2021). The use of A. oryzae in the production of sake (fermented rice alcoholic beverage), vinegar, miso (soybean paste) and soy sauce, has been reported for at least two millennia (Furukawa, 2012; Chang et al., 2014). In general terms, it is considered safe and no strains that produce aflatoxins are known (Machida et al., 2005).

The genes that codify the enzymatic pathway for the biosynthesis of aflatoxins are grouped in a 74 Kb region of the DNA in A. flavus. This group is found in A. oryzae, but it does not seem to be functional (Yu et al., 2004). A. oryzae and A. flavus are morphologically similar. Several studies suggest they are ecotypes, which refers to a same species which have a different expression in different environments, due to the interaction of their genes with the environment in which they are found (Kurtzman et al., 2018). This indicates that A. oryzae was the result of the domestication of A. flavus after centuries of planting it (Payne et al., 2006).

Because Aspergillus oryzae was reported as a domesticated microorganism, it cannot be found in nature. However, there are some reports that mention the isolation of A. oryzae from foods, plants and soils, appearing less frequently (Klich, 2002). A historical file described that A. oryzae should be isolated from a spike of rice, indicating that it could have existed in nature before its domestication (Murakami, 1980).

This fungus grows in several media, including potato dextrose agar, where it grows particularly fast in 7 days at 25 °C (Moubasher, 1993). Its stage of sporulation begins on day 7; when growth reaches 7 to 8 cm, yellow ring begins to form, and which will gradually turn green (Daba et al., 2021). The ideal conditions for the development of A. oryzae include a slightly acidic pH between 5 and 6, its temperature must range between 32 and 36 °C (±1 °C), and variations in temperature above 44 °C inhibit its growth. These fungi show an efficient development in media with water activity above 0.8 and they rarely grow below this range (Gomi, 2014).

 <bold>Applications of <italic>Aspergillus oryzae</italic> and its possible implementation in agriculture</bold>

The versatility of A. oryzae is reflected in the wide variety of areas in which it can be applied (Figure 2), since it is highly effective in the manufacturing of biotechnological products, due mainly to its metabolic and enzymatic diversity (El- Enshasy, 2007).

Lee and collaborators (2016) provided a metabolic profile obtained during the fermentation of köji with A. oryzae, which comprises the secondary metabolites secreted in the fermentation process, classifying them into; a) sugars (xylose, fructose and glucose); b) polyols (glycerol, erythritol, xylitol, sorbitol y myo- inositol); c) organic acids (succinic acid, glyceric acid, fumaric acid, malic acid,

Areas of application of <italic>Aspergillus oryzae.</italic>

kojic acid, citric acid and gluconic acid); d) phenolic acids (4-hydroxybenzoic acid and ferulic acid); e) amino acids (alanine, proline, glycine, serine, threonine, aspartate and GABA); f) fatty acids (palmitic acid, linoleic acid, oleic acid and pinellic acid); and g) vitamins (vitamin B3). Each one of these compounds has different antimicrobial, antioxidant, anticarcinogenic and antiviral properties, as well as hormonal compounds and metal chelators (Frisvad et al., 2018; Daba et al., 2021).

The application of A. oryzae in the production of malic acid and fumaric acid (Xu et al., 2012; Brown et al., 2013) proposes the possibility of the creation of a biorefining process for the production of organic acids and enzymes, replacing the currently used polymers derived from crude oil (Brink et al., 2023). The biorefining process can be enhanced by incorporating agricultural by-products, inexpensive non-food substrates, reducing production costs and providing an option free of any chemical products (Jiménez-Quero et al., 2020).

The microbial enzymes used in the industry have proven to be better in their application, as well as inexpensive and respectful to the environment in comparison with chemical products (Whiteley and Lee, 2006). They have technical-economic advantages, meaning shorter production times, better space per enzyme unit produced and unlimited potential in terms of availability of new enzymes (Scriban, 1985).

There are reports on the application of A. oryzae in the process of fermentation of grape pomace with the production of enzymes (cellulase, pectinase and tannase), which facilitate the aqueous extraction of polyphenols (gallic acid, sinapic acid and ferulic acid) with antioxidant and prebiotic properties, such as food additives, where A. oryzae has a greater production and selectivity of tannase under humid conditions, having a positive effect on the antioxidant activity, which can be influenced by the production of galic acid (Meini et al., 2021). On the other hand, A. oryzae can stimulate ruminal fermentation by improving the consumption and digestion of the food and dry matter in cattle, by applying it as a microbial additive in the cattle feed (Sosa et al., 2022). At the same time, the efficiency in the increase of volatile fatty acids has been proven, making A. oryzae an element of improvement to potentialize the diets of ruminants in a different way. It also exerts an influence on the supply of enzymes in maize, oat hay and alfalfa hay silage (Kong et al., 2021).

Technological progress has taken advantage of the potential of A. oryzae (Matsunaga et al., 2002) for industrial use in the development of detergents, pigments and antioxidants, (Christensen et al., 1988; Machida et al., 2008; Panchanawaporn et al., 2022). Likewise, its application in the fermenting of foods (Machida et al., 2008; Yasui et al., 2020) and the implementation in the production of metabolites such as organic acids and plant growth regulators are important areas of study (El- Enshasy, 2007; Siddiqui, 2016). It can also be useful in biological activities such as in veterinary science as probiotics for poultry and livestock feed digestive (Lee et al., 2006; Murphy, 2021; Podversich et al., 2023).

 <bold> <italic>A.oryzae</italic> as a soil bioremediator, growth enhancer and biological control</bold>

A. oryzae can be an alternative for the development of a sustainable and eco- friendly agriculture, specifically in Mexico, where their applications on the field are not a topic of study. The following information describes some areas of opportunity where this microorganism can be applied on the field, in order to pave the way for possible scientific studies aimed at the Mexican countryside.

Endophytic plant fungi are those which live on plant tissues and cause no visible harm. Due to this, a mutualistic relationship (endophyte-host) is occasionally identified, which unleashes the production of bioactive substances (secondary metabolites, enzymes etc.) which exert an influence on growth enhancement, the survival of the host under diverse environmental conditions, the reduction of susceptibility to diseases, and helping control pest insects and plant pathogen agents (El-hawary et al., 2020; Murali et al., 2012; Sharma and Singh, 2021).

Although A. oryzae is not commonly reported as a natural endophyte, information has been provided on its isolation in Ginkgo biloba roots in China (Machida et al., 2005).Sun and collaborators (2018), in the study of the inoculation of Raphanus sativus seeds with the strain A. oryzae BNCC341706, established it as a fungus with endophytic properties, since it did not affect the germination of the inoculated seed and instead promoted the growth of the R. sativus culture, which reached a height of 116 mm in comparison with the control, which had a height of 99.6 mm. Another effect of the use of A. oryzae was reflected on the health of its main pest insect Plutella xylostella, affecting its consumption parameters, weight of larvae and pupae, which opens the possibility of treating cruciferous seeds and the control of pest insects using A. oryzae.

Likewise, as bioremediating agents, endophytic fungi have proven to be efficient in the degradation of contaminants, leaving no traces of toxic by-products (Skinder et al., 2022), which is advantageous, due to its biomass, long life cycle and network of hyphae (Sun et al., 2012), along with its ability to degrade chemically toxic substances by modification or acting upon its chemical bioavailability (Bornyasz et al., 2005). In the case of A. oryzae as a bioremediating agent, the in vitro study of the A. oryzae strains AM1 and AM2 displayed the ability to degrade atrazine (90%), endosulfan (56 and 76%) and chlorpyrifos (50 and 73%), while also obtaining an adequate development under high concentration of pesticides, which generates the possibility of degrading this type of chemical products (Barberis et al., 2019).

The OTA is a microtoxin that affects human health and agricultural products, which has led to a search for control measures, therefore, biodegradation has been proposed as a promising method. The strain A. oryzae M30011 is able to degrade OTA by up to 94% in 72 h, at a pH of 8, a temperature of 30 °C and a concentration of the inoculant of 104 UFC mL-1. On the other hand, a reduction in the levels of aflatoxins is an important matter, since they are a threat to worldwide food security (Xiong et al., 2021). The strain A. oryzae M2040 has been proven capable of inhibiting the production of AFB1 by 87%, and the proliferation of A. flavus, under in vitro conditions, and in peanuts by successfully displacing the aflatoxin- producing fungus by secreting antimycotic compounds, which have not been reported (Alshannaq et al., 2018). These studies back the potential of A. oryzae in the agricultural and food industry.

The potential of the use of A. oryzae has been emphasized in the development of research work as a growth enhancer and a biological control agent, shown in Table 1.

The ability of A. oryzae to secrete enzymes is an alternative for the development of microbiological compounds, since biological activities are carried out which can be adapted in the area of agronomy. An example of this is the antifungal activity of xylanase produced by the strain A. oryzae MN894021, which displayed a reduction

Use of <italic>A. oryzae</italic> as a growth enhancer, pest control agent and bioremediator od contaminated soils.
Application Strain Crop / Pest Results Reference
Arsenic biorremediator and growth enhancer FNBR_L35 Oat (Avena sativa), Calendula (Calendula officinalis), Ashwagandha (Withania somifera) Effects of bioaccumulation and biovolatilization of arsenic in concentrations of 100 to 10,000 ppm in a period of 21 days andenhancement of plant growth Singh et al.,2015
Entomopathogen XJ-1 Locusta migratoria Mortality in third instar of the insect Zhang et al.,2015
Growth enhancer and control agent BNCC341706 Radish seeds (Raphanus stativus), Puntella xylostella Greatest plant height. Inhibition of feeding and low weight of larvae and pupae Sun et al., 2018
Removal of glyphosate AM1 and AM2 In vitro Degradation of 50% in glyphosate concentrations, long periods of incubation and permanence of the fungus Carranza et al.,2019
Entomopathogen USMN05 USMM03 NRRL2097 Spodoptera litura Mortality of 20% and inability to produce aflatoxins Fitriana et al.,2021

of 75, 90 and 100% in the incidence of Botrytis cinerea, Fusarium solani, F. chlamydosporum, F. incranatum, Macrophomina phaseolina, Rhizotocnia solani and Sclerotinia sclerotiorum in broad bean seeds covered with xylanase, providing protection against the invasion of these phytopathogenic fungi (Atalla et al., 2020). The results obtained from the xylanase produced by the strain A. oryzae MN894021 coincide with the activity of the xylanase from Trichoderma harzianum kj831197 against Corynespora cassiicola, Alternaria spp., F. oxysporum and Botrytis fabae (Ellatif et al., 2022).

The control of phytopathogens is an important challenge for agriculture. The development of sustainable, environmental, easy and eco-friendly control processes is constant in current research; an option is the biogenic synthesis of bioparticles (Zhang et al., 2020). The strain A. oryzae MTCC3107 has been implemented in the formulation of silver nanoparticles (AgNP), whose antimicrobial potential against Sclerotinia sclerotium reflected an inhibition of 100% at a concentration of 100 µL mL-1. The role of A. oryzae in the formulation is due to the secretion of amylase, which catalyzed the AgNP production process, making it a green synthesis process (Gupta and Saxena, 2023).

The study and publication of information related to the potential of A. oryzae serve as a support for future investigations in the area of phytopathology, since it has been relatively scarcely studied. Despite A. oryzae having a wide margin of produced bioactive substances, those applied in this area are few. Some activities and metabolites are presented in Table 2.

Activity of bioactive substances produced by <italic>A. oryzae</italic> against plant pathogens.
Bioactive substances Strains Application Result Reference
Kojic acid NRRL 447, 552, 552, 1730 Y30038 (S-03) Prevention of contamination by toxins in agricultural products Reduction of aflatoxins in peanut Dorner et al., 1998
Kojic acid * Insecticide: Glyphodes pyloalis Inhibition of phenyloxidase activity Sharifi et al., 2013
Oryzaeins A-D KM999948 Antiviral: TMV Rates of inhibition of 22.4 - 30.6% Zhou et al., 2016
Xylanase MN894021 antifungal: Alternaria alternata, Fusarium oxysporum, Phoma destructor, Rhizotocnia solani and Sclerotium rolfsii Reduction of the live growth Reduction in percentages of incidence of root rotting Atalla et al., 2020
Kojic acid * Antifungal activity: Sclerotinia slerotiorum Inhibiyion of chitin and melanin synthesis Reduction of oxalic acid of the virulence factor Zhu et al., 2022

*Strain not provided by the author.

 <bold>Kojic acid, secondary <italic>A.</italic> oryzae metabolite; alternative for the control of plant pathogens</bold>

Within the main secondary metabolites produced by A. oryzae, kojic acid is one of the most relevant (Figure 3) (Yamada et al., 2014). Its application in the control of phytopathogenic agents and pest insects is a relatively new topic; however, the investigation reports show that this application may be a feasible alternative for the control of pests in crops.

A. oryzae has bactericidal, fungicidal and insecticidal effects (Mohamad et al., 2010). It acts in relation with the inhibition of oxidative enzymes in both plants and arthropods. Studies have shown that kojic acid efficiently inhibits the rate of formation of pigmented products and absorption of oxygen when compounds such as catecholamines (DL-DOPA, dopamine and norepinephrine), are oxidized by the enzyme tyrosinase (Kahn, 1995; Kahn and Ben-Shalom, 1997).

Mahmoud and collaborators (2023) analyzed the insecticidal activity of kojic acid produced by the strain A. oryzae ASU44 (OL314732), against Aphis

Characteristics and basics of kojic acid based on reports by <xref ref-type="bibr" rid="B62">Phasha <italic>et al</italic>. (2022</xref>) and <xref ref-type="bibr" rid="B72">Siddiquee (2018</xref>).

gossypii, vector of the Cotton leafroll dwarf virus (CLRDV) (Mahas et al., 2022).

They evaluated the difference between the kojic acid extracted from the strain A. oryzae ASU44 (OL314732) and synthetic kojic acid, and indicated that the kojic acid produced by A. oryzae ASU44 (OL314732) was more efficient against Aphis gossypii, with a medium lethal concentration (CL50) of 11.2 ppm, a lethal concentration (CL90) of 50.3 ppm, and a lethal time of (LT90) of 7 days, since the results are lower than those for synthetic kojic acid, highlighting their application as an efficient and inexpensive in vitro evaluation model (Mahmoud et al., 2023). Likewise, the antifungal activity of kojic acid has been evaluated with A. terrus, A. flavus, A. parasiticus, A. fumigatus, Penicilium and Sclerotinia sclerotiorum (Kim et al., 2012; Kim and Chan, 2014; Zhu et al., 2022). In the case of S. sclerotiorum, kojic acid inhibits the biosynthesis of melanin, which affects the development of sclerotia and the biosynthesis of chitin and β-1,3-glucanos, which alters the cell walls and the growth of the mycelium, reducing in its entirety the symptoms of S. sclerotiorum in soybean pods with 50 mM de ácido kójico. It has the ability to prevent and inhibit symptoms of S. sclerotiorum. In turn, it is more effective than commercial fungicides (carbendazim and prochloraz) (Zhu et al., 2022).

More frequently, phytoparasitic nematodes have been pointed out as the cause of important economic losses in several crops, fluctuating around $77 billion dollars worldwide, which raises concerns in agriculture, horticulture and forestry (Yadav, 2017; Seo et al., 2019). For example, Meloidogyne spp., the gall-forming nematodes, is responsible for annual losses of up to $100 billion dollars. Kim and collaborators (2016) established a method to control these nematodes using kojic acid as the active ingredient, which was produced by the strain A. oryzae EML- DML3PNa1 obtained from white dogwood (Cornus alba). During their experiments, an inhibiting effect was displayed on the hatching of eggs and the development of larvae, and the use of kojic acid was suggested along with a dispersing, penetrating or surfactant agent, in order to improve absorption and the effect of the product on the crop (Kim et al., 2016). The nematicidal action of the kojic acid reported a mortality of 87.6% in juvenile Meloidogyne incognita under conditions of 20% of a filtrate of a fermentation broth. It displayed inhibition in the incubation of the nematode and a mortality dependent on the dose, with mean effective concentration values (CE ) of 195.2 µg mL-1 and 238.3 µg mL-1, respectively, 72 h after exposure, which suggests that is has potential as a biological control agent (Kim et al., 2016).

Interest in safe agricultural products for human health and free of contaminants is on the rise, due to awareness on residual toxicity caused by the use of pesticides. The implementation of microorganisms with nematocidal activity is recommended, since they are respectful with the environment because they are obtained from natural products, as in the case of kojic acid, therefore its implementation in agronomy opens a door for the development of sustainably inexpensive, environmentally friendly products that, above all, do not harm the health of people who apply them.

 Conclusions

This study highlights the potential of the A. oryzae strains and its derivatives (enzymes and secondary metabolites), considering the ability to compete with commercial chemical products as pesticides, since it presents insecticidal, fungicidal and nematocidal characteristics, which represent an inexpensive and sustainable alternative, since the way in which it is produced excludes the use of costly products. Developing new investigation work and opting for the application of products based on A. oryzae at a greenhouse level is required to confirm its adaptability in conditions outside the laboratory and verify if the benefits of A. oryzae are maintained or reduced in such a way that they can be used in the field. Finally, the study of A. oryzae and its by-products is scarcely studied in Mexico, making it a debatable topic to be exploited for the benefit of the Mexican countryside, since it opens a new aspect of study for the development of products that benefit crops and for the control of phytopathogenic agents.

 <p>Acknowledgement</p> <p> </p> <p>Our thanks to the Antonio Narro Autonomous Agrarian University (Universidad Autónoma Agraria Antonio Narro - UAAAN), to the PhD Agricultural Parasitology Program, as well as to the National Council of Humanities, Sciences and Technolo- gies (Consejo Nacional de Humanidades, Ciencias y Tecnologías- CONAHCYT)</p> </ack> </back> </sub-article> </article>