Biochemical characterization of oxidative stress in the compatible interaction between Pepper golden mosaic virus and habanero pepper plants

Cristina Aguilar-Sánchez, Yereni Minero-García, Cecilia Hernández-Zepeda, Oscar Alberto Moreno-Valenzuela

Abstract


In this work, the role of Pepper golden mosaic virus-mosaic strain (PepGMV-Mo) infection on hydrogen peroxide (H2O2), salicylic acid (SA), and the antioxidant enzymes catalase (CAT) and peroxidase (POX) were analyzed in vitro during the compatible interaction between PepGMV-Mo and Capsicum chinense plants. Endogenous H2O2, SA, CAT and POX were monitored over time, and the levels of all four were increased in the PepGMV-Mo-Mo inoculated plants compared to the mock-inoculated (cloning vector) and healthy plants. Three peaks of H2O2 were observed in the inoculated plants during the time course experiment. The first increase was observed at the beginning of the time course experiment, at 30 minutes post inoculation (mpi), and the last at the end of the experiment, at 24 days pos-inoculation (dpi). The SA concentration increased 12 hours post-inoculation (hpi) in inoculated plants relative to mock-inoculated and healthy plants. Due to PepGMV-Mo infection, CAT and POX activity increased. An increase in CAT activity was observed 4 hpi in PepGMV-Mo-infected plants, and a decrease in CAT activity correlated with the increase in SA concentration at 12 hpi in the infected plants. POX activity was higher in the infected plants than in the mock-inoculated and healthy plants for the duration of the time course experiment. Taken together, the findings suggest that oxidative stress is involved in the compatible interaction between PepGMV-Mo-Mo and C. chinense; however, this burst was not sufficient to confer resistance or tolerance to habanero pepper against the virus based on symptom phenotype observed.


Keywords


in vitro plants; hydrogen peroxide; salicylic acid; peroxidase; catalase

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Baebler S, Witek K, Petek M, Stare K, Tusek-Znidaric M, Pompe-Novak M, Renaut J, Szajko K, Strzelczyk-?yta D, Marczewski W, Morgiewicz K, Gruden K and Hennig J. 2014. Salicylic acid is an indispensable component of the Ny-1 resistance-gene-mediated response against Potato virus Y infection in potato. Journal of Experimental Botany 65 (4): 1095-1109. https://doi.org/10.1093/jxb/ert447.

Barboza N, Blanco-Meneses M, Esker P, Moriones E and Inoue-Nagata AK. 2018. Distribution and diversity of begomoviruses in tomato and sweet pepper plants in Costa Rica. Annals of Applied Biology 172 (1): 20-32. https://doi.org/10.1111/aab.12398.

Berg BM and Huystee RB. 1984. Rapid isolation of plant peroxidase. Purification of peroxidase from petunia. Physiologia Plantarum 60 (3): 299-304. https://doi.org/10.1111/j.1399-3054.1984.tb06066.x.

Bestwick CS, Brown IR, Bennett MH and Mansfield JW. 1997. Localization of hydrogen peroxide accumulation during the hypersensitive reaction of lettuce cells to Pseudomonas syringae pv. phaseolicola. Plant Cell 9 (2): 209-221. https://doi.org/10.1105/tpc.9.2.209.

Bolwell GP, Butt VS, Davies DR and Zimmerlin A. 1995. The origin of the oxidative burst in plants. Free Radical Research 23:517-532. https://doi.org/10.3109/10715769509065273.

Brown JK, Idris AM, Ostrow KM, Goldberg N, French R and Stenger DC. 2005. Genetic and phenotypic variation of the Pepper golden mosaic virus complex. Phytopathology 95 (10):1217-1224. https://doi.org/10.1094/PHYTO-95-1217.

Carrillo-Tripp J, Lozoya-Gloria E and Rivera-Bustamante RF. 2007. Symptom remission and specific resistance of pepper plants after infection by Pepper golden mosaic virus. Phytopathology 97 (1): 51-59. https://doi.org/10.1094/PHYTO-97-0051.

Clark D, Durner J, Navarre D and Klessig D. 2007. Nitric Oxide inhibition of tobacco Catalase and Ascorbate Peroxidase. Molecular Plant-Microbe Interaction 13 (12): 1380–1384. https://doi.org/10.1094/MPMI.2000.13.12.1380.

Clarke SF, Guya PL, Burritta DJ and Jameson PE. 2002. Changes in the activities of antioxidant enzymes in response to virus infection and hormone treatment. Physiologia Plantarum 114 (2): 157-164. https://doi.org/10.1034/j.1399-3054.2002.1140201.x.

Cheeseman J. 2006. Hydrogen peroxide concentrations in leaves under natural conditions. Journal of Experimental Botany 57 (10): 2435-2444. https://doi.org/10.1093/jxb/erl004.

Chen Z, Silva H and Klessig DF. 1993. Active oxygen species in the induction of plant systemic acquired resistance by salicylic acid. Science 262 (5141): 1883-1886. http://doi.org/10.1126/science.8266079.

Chivasa S, Murphy AM, Naylor M and Carr JP. 1997. Salicylic acid interferes with Tobacco mosaic virus replication via a novel Salicylhidroxamic acid-sensitive mechanism. Plant Cell 9 (4): 547-557. https://doi.org/10.1105/tpc.9.4.547.

Dempsey DA and Klessig DF. 1995. Signals in plant disease resistance. Bulletin de l'Institut Pasteur 93 (3): 167-186. https://doi.org/10.1016/0020-2452(96)81488-6.

Echevarría-Machado I, Sánchez-Cach LA, Hernández-Zepeda C, Rivera-Madrid R and Moreno-Valenzuela OA. 2005. A simple and efficient method for isolation of DNA in high mucilaginous plant tissue. Molecular Biotechnology 31 (2): 129-136. https://doi.org/10.1385/MB:31:2:129.

Elstner EF and Heupel A. 1976. Formation of hydrogen peroxide by isolated cell walls from horseradish (Armoracia lapathifolia Gilib.). Planta 130 (1): 175-180. https://doi.org/10.1007/BF00384416.

Gaffney T, Friedrich L, Vernooij B, Negrotto D, Nye G, Uknes S, Ward E, Kessmann H and Ryals J. 1993. Requirement of salicylic acid for the induction of systemic acquired resistance. Science 261 (5122): 754–756. http://doi.org/10.1126/science.261.5122.754.

García-Neria MA and Rivera-Bustamante RF. 2011. Characterization of Geminivirus resistance in an accession of Capsicum chinense Jacq. Molecular Plant-Microbe Interactions 24 (2): 172-182. https://doi.org/10.1094/MPMI-06-10-0126.

Hernández-Espinal LA, Enríquez-Verdugo I, Melgoza-Villagómez CM, Retes-Manjarrez JE, Velarde-Félix S, Linares-Flores PJ y Garzón-Tiznado JA. 2018. Análisis filogenético y distribución de begomovirus en el cultivo del chile (Capsicum annuum L.) en Sinaloa, México. Fitotecnia Mexicana 41(2): 149-157. https://doi.org/10.35196/rfm.2018.2.149-157.

Hernández JA, Corpas FJ, Gómez M, del Río LA and Sevilla F. 1993. Salt-induced oxidative stress mediated by activated oxygen species in pea leaf mitochondria. Physiologia Plantarum 89 (1): 103-110. https://doi.org/10.1111/j.1399-3054.1993.tb01792.x.

Hernández JA, Díaz-Vivancos P, Rubio M, Olmos E, Ros-Barceló A and Martínez-Gómez P. 2006. Long-term Plum pox virus infection produces an oxidative stress in a susceptible apricot Prunus armeniaca, cultivar but not in a resistant cultivar. Physiologia Plantarum 126 (1): 140-152. https://doi.org/10.1111/j.1399-3054.2005.00581.x.

Hernández-Zepeda C, Idris AM, Carnevali G, Brown JK and Moreno-Valenzuela OA. 2007a. Molecular characterization and experimental host range of Euphorbia mosaic virus-Yucatan Peninsula, a begomovirus species in the Squash leaf curl virus clade. Plant Pathology 56 (5): 763-770. https://doi.org/10.1111/j.1365-3059.2007.01652.x.

Hernández-Zepeda C, Idris AM, Carnevali G, Brown JK and Moreno-Valenzuela OA. 2007b. Preliminary identification and coat protein gene phylogenetic relationships of begomoviruses associated with native flora and cultivated plants from the Yucatan Peninsula of Mexico. Virus Genes 35 (3): 825-833. https://doi.org/10.1007/s11262-007-0149-1.

Huang ZL, Yeakley JM, García EW, Holdridge JD, Fan JB and Whitham SA. 2005. Salicylic acid-dependent expression of host genes in compatible Arabidopsis-virus interactions. Plant Physiology 137 (3): 1147-1159. https://doi.org/10.1104/pp.104.056028.

Idris AM, Smith SE and Brown JK. 2001. Ingestion, transmission and persistance of Chino del Tomate virus (CdTV), a New World begomovirus, by Old and New World biotypes of the whitefly vector Bemisia tabaci. Annals of Applied Biology 139 (1): 145-154. https://doi.org/10.1111/j.1744-7348.2001.tb00139.x.

Inamine GS and Baker JE. 1989. A catalase from tomato fruit. Phytochemistry 28 (2): 345-348. https://doi.org/10.1016/0031-9422(89)80010-X.

Quan LJ, Zhang B, Shi WW and Li HY. 2008. Hydrogen peroxide in plants: a versatile molecule of the reactive oxygen species network. Journal of Integrated Plant Biology 50 (1): 2-18. https://doi.org/10.1111/j.1744-7909.2007.00599.x.

Klessig DF, Choi HW and Dempsey DA. 2018. Systemic acquired resistance and salicylic acid: past, present, and future. Molecular Plant Microbe Interaction 31 (9):871-888.

Kozlowska M, Fryder K and Wolko B. 2001. Peroxidase involvement in the defense response of red raspberry to Dymellia applanata (Niessl/Sacc.). Acta Physiologiae Plantarum 23 (3): 303-310. https://doi.org/10.1007/s11738-001-0037-6.

Laird J, Armengaud P, Giuntini P, Laval V and Milner JJ. 2004. Inappropriate annotation of a key defense marker in Arabidopsis: will the real PR-1 please stand up? Planta 219 (6): 1089-1092. https://doi.org/10.1007/s00425-004-1355-x.

Lukan T, Baebler S, Pompe-Novak M ,Gu?ek K, Zagorš?ak M, Coll A and Gruden K. 2018. Cell death is not sufficient for the restriction of Potato virus Y spread in hypersensitive response-conferred resistance in potato. Frontiers in Plant Science 9:1-12 https://doi.org/10.3389/fpls.2018.00168.

Mandal S, Kumar Das R and Mishra S. 2011. Differential occurrence of oxidative burst and antioxidative mechanism in compatible and incompatible interactions of Solanum lycopersicum and Ralstonia solanacearum. Plant Physiology and Biochemistry 49 (2): 117-223. https://doi.org/10.1016/j.plaphy.2010.10.006.

Mayers CN, Lee KC, Moore CA, Wong SM and Carr JP. 2005. Salicylic acid induced resistance to Cucumber mosaic virus in Squash and Arabidopsis thaliana: Contrasting mechanisms of induction and antiviral action. Molecular Plant-Microbe Interaction 18 (5): 428-434. https://doi.org/10.1094/MPMI-18-0428.

Mejía-Teniente L, Durán-Flores BA, Torres-Pacheco I, González-Chavira MM. Rivera-Bustamante RF, Feregrino-Pérez AA, Pérez-Ramírez I, Rocha-Guzmán NE, Reynoso-Camacho R and Guevara-González RG. 2019. Hydrogen peroxide protects pepper (Capsicum annuum L.) against Pepper golden mosaic geminivirus (PepGMV) infections. Physiological and Molecular Plant Pathology 106: 23-29. https://doi.org/10.1016/j.pmpp.2018.11.008.

Méndez-Lozano J, Rivera-Bustamante RF, Fauquet CM and De la Torre-Almaráz R. 2001. Pepper huasteco virus and Pepper golden mosaic virus are Geminiviruses affecting tomatillo (Physalis ixocarpa) crops in Mexico. Plant Disease 85 (12): 1291. https://doi.org/10.1094/PDIS.2001.85.12.1291A.

Miguel E, Poza-Carrión C, López-Solanilla E, Aguilar I, Llama-Palacios A, García-Olmedo F and Rodríguez-Palenzuela P. 2000. Evidence against a direct antimicrobial role of H2O2 in the infection of plants by Erwinia chrysanthemi. Molecular Plant-Microbe Interaction 13 (4): 421-429. https://doi.org/10.1094/MPMI.2000.13.4.421.

Milavec M, Gruden K, Ravnikar M and Kova? M. 2008. Peroxidases in the early responses of different potato cultivars to infection by Potato virus Y. Plant Pathology 57 (5): 861-869. https://doi.org/10.1111/j.1365-3059.2008.01833.x.

Milavec M, Ravnikar M and Kovac M. 2001. Peroxidases and photosynthetic pigments in susceptible potato infected with Potato virus YNTN. Plant Physiology and Biochemistry 39 (10): 891?898. https://doi.org/10.1016/S0981-9428(01)01303-1.

Murphy AM and Carr JP. 2002. Salicylic acid has cell-specific effects on Tobacco mosaic virus replication and cell-to-cell movement. Plant Physiology 128 (2): 552-563. https://doi.org/10.1104/pp.010688.

Murphy AM, Chivasa S, Singh DP and Carr JP. 1999. Salicylic acid-induced resistance to viruses and other pathogens: a parting of the ways? Trends in Plant Science 4 (4): 155-160. https://doi.org/10.1016/S1360-1385(99)01390-4.

Nakhla MK, Sorensen A, Mejía L, Ramírez P, Karkashian JP and Maxwell DP. 2005. Molecular characterization of tomato infecting Begomoviruses in Central America and development of DNA-based detection methods. Acta Horticulture 695 (31): 277-288. https://doi.org/10.17660/Acta Hortic.2005.695.31.

NCBI. 2021. National Center for Biotechnology Information. www.ncbi.nlm.nih.gov/blast/.

Neuenschwander U, Verooij L, Friedich S, Uknes H and Kessmann Ryals J. 1995. Is hydrogen peroxide a second messenger of salicylic acid in systemic acquired resistance? Plant Journal 8 (2): 227-233. https://doi.org/10.1046/j.1365-313X.1995.08020227.x.

Olson PD and Varner JE 1993. Hydrogen peroxide and lignifications. Plant Journal 4 (5): 887-892. https://doi.org/10.1046/j.1365-313X.1993.04050887.x.

Park SW, Kaimoyo E, Kumar D, Mosher S and Klessig D. 2007. Methyl Salicylate is a critical mobile signal for plant systemic acquired resistance. Science 318 (5847): 113-116. http://doi.org/10.1126/science.1147113.

Peterson G. 1977. A simplification of the protein assay method of Lowry et al, which is more generally applicable. Analytical Biochemistry 83 (2): 346-356. https://doi.org/10.1016/0003-2697(77)90043-4.

Riedle-Bauer M. 1998. Activities of antioxidant enzymes in cucumber plants infected with Cucumber mosaic virus. Phyton 38 (1): 149–157. https://www.zobodat.at/pdf/PHY_38_1_0149-0157.pdf.

Riedle-Bauer M. 2000. Role of reactive oxygen species and antioxidant enzymes in systemic virus infections of plants. Journal of Phytopathology 148 (5): 297-302. https://doi.org/10.1046/j.1439-0434.2000.00503.x.

Rodrigues-Alencar MS, Da Silva-Solino AJ, Batista-Oliveira JS, Pascholati SJ and Freitas-Schwan-Estrada KR. 2020. Induction of defense mechanisms in tomato plants by saprobic fungi filtrates against early blight disease. Revista Caatinga 33 (3): 671– 678. https://doi.org/10.1590/1983-21252020v33n310rc.

Rodríguez-Negrete EA, Carrillo-Tripp J and Rivera-Bustamante RF. 2009. RNA Silencing against Geminivirus: complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery. Journal of Virology 83 (3): 1332-1340. https://doi.org/10.1128/JVI.01474-08.

Takahashi H, Miller J, Nozaki Y, Takeda M, Shah J, Hase S, Ikegami M, Ehara Y and Dinesh-Kumar SP. 2002. RCY1, an Arabidopsis thaliana RPP8/HRT family resistance gene, conferring resistance to Cucumber mosaic virus requires salicylic acid, ethylene and a novel signal transduction mechanism. Plant Journal 32 (5): 655–667. https://doi.org/10.1046/j.1365-313X.2002.01453.x.

Uknes S, Winter AM, Delaney T, Vernooij B, Morse A, Friedrich L, Nye G, Potter S, Ward E and Ryals J. 1993. Biological induction of systemic acquired resistance in Arabidopsis. Molecular Plant-Microbe Interactions 6 (6): 692-698. https://www.apsnet.org/publications/mpmi/BackIssues/Documents/1993Articles/Microbe06_692.pdf.

Van Camp W, Van Montagu M and Inzé D. 1998. H2O2 and NO: redox signals in disease resistance. Trends in Plant Science 3 (9): 330-334. https://doi.org/10.1016/S1360-1385(98)01297-7.

Wohlgemuth H, Mittelstrass K, Kschieschan S, Bender J, Weigel HJ, Overmyer K, Kangasjärvi J, Sandermann H and Langebartels C. 2002. Activation of an oxidative burst is a general feature of sensitive plants exposed to the air pollutant ozone. Plant Cell and Environment 25 (6): 717-726. https://doi.org/10.1046/j.1365-3040.2002.00859.x.

Wojtaszek P. 1997. Mechanisms for the generation of reactive oxygen species in plant defense response. Acta Physiologiae Plantarum 19 (4): 581-589. https://link.springer.com/content/pdf/10.1007/s11738-997-0057-y.pdf.




DOI: http://dx.doi.org/10.18781/R.MEX.FIT.2111-1

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