Vol. 61 No. 1 (2022)
Articles

Candidate marker genes and enzymes for selection of potato with resistance to early blight, caused by Alternaria alternata

Neda Peymani
Department of Agronomy and Plant Breeding, College of Agriculture, Isfahan (Khorasgan) Branch, Islamic Azad University, Isfahan
Ahmad Reza Golparvar
Department of Agronomy and Plant Breeding, College of Agriculture, Isfahan (Khorasgan) Branch, Islamic Azad University, Isfahan
Mehdi Nasresfahani
Plant Protection Research Department, Isfahan Agriculture and Natural Resource Research and Education Center (AREEO), Isfahan
Esmaeeil Mahmoudi
Department of Agronomy and Plant Breeding, College of Agriculture, Isfahan (Khorasgan) Branch, Islamic Azad University, Isfahan
Majid Shams
Department of Agronomy and Plant Breeding, College of Agriculture, Isfahan (Khorasgan) Branch, Islamic Azad University, Isfahan

Published 2022-03-25

Keywords

  • Antioxidant enzymes,
  • biomass,
  • defense mechanism,
  • Solanum tuberosum

How to Cite

[1]
N. Peymani, A. R. Golparvar, M. Nasresfahani, E. Mahmoudi, and M. Shams, “Candidate marker genes and enzymes for selection of potato with resistance to early blight, caused by Alternaria alternata”, Phytopathol. Mediterr., vol. 61, no. 1, pp. 11–26, Mar. 2022.

Abstract

Early blight, caused by Alternaria alternata (Fr.) Keissler is a serious disease of potato and other cultivated Solanum species. The molecular components defining defense responses to A. alternata in potato are limited. Host transcript accumulation after A. alternata inoculation of six potato genotypes (10/33/R1, 3/33/R2 and 21/33/R2, resistant to the pathogen, and 8707/106, 8703/804 and 8707/112, susceptible) was examined to develop understanding of mechanisms of their responses to A. alternata genotypes. The marker genes PR-2, ChtA, PR-5, PR1-b, PIN2, ERF3, PAL and LOX, activity of catalase (CAT), superoxide dismutase (SOD), peroxidase (POX), polyphenol oxidase (PPOs) and phenylalanine ammonia-lyase (PAL), as well as biomass growth parameters, were analysed. Expression of PR-2, ChtA, PR-5, PR1-b and PAL genes was greatly increased in the inoculated resistant genotypes compared to the susceptible genotypes and un-inoculated controls. Transcription levels of PIN2, ERF3 and LOX genes were decreased in resistant inoculated plants. Simultaneously, activities of POX, SOD and PPOs were greatly increased in the inoculated resistant host genotypes, compared to the susceptible and non-inoculated controls. CAT activity in genotype 21/33/R2 and PAL activity in resistant genotypes 21/33/R2 and 10/33/R1 increased in the susceptible and non-inoculated. Host growth parameters of inoculated plants decreased compared to un-inoculated controls. Knowledge of changes in gene expression levels and enzyme production in defense processes in infected potato plants can inform future studies to identify the defense mechanisms, and assist generation of potato cultivars resistant to early blight.

Downloads

Download data is not yet available.

Metrics

Metrics Loading ...

References

References
Ab Rahman S.F.S., Singh, E., Pieterse C.M., Schenk P.M., 2018. Emerging microbial biocontrol strategies for plant pathogens. Plant Sci 267, 102-111.
Ali S., Ganai B.A., Kamili A.N., Bhat A.A., Mir Z.A., Bhat J.A., Tyagi A., Islam S.T., Mushtaq M., Yadav P., 2018. Pathogenesis-related proteins and peptides as promising tools for engineering plants with multiple stress tolerance. Microbiol Res 212: 29-37.
Arseneault T., Goyer C., Filion M., 2015. Pseudomonas fluorescens LBUM223 increases potato yield and reduces common scab symptoms in the field. Phytopathology 105: 1311-1317.
Arseneault T., Pieterse C.M., Gérin-Ouellet M., Goyer C., Filion M., 2014. Long-term induction of defense gene expression in potato by Pseudomonas sp. LBUM223 and Streptomyces scabies. Phytopathology 104: 926-932.
Bagheri L.M., Nasr-Esfahani M, Abdossi V, Naderi D., 2020. Analysis of candidate genes expression associated with defense responses to root and collar rot disease caused by Phytophthora capsici in peppers Capsicum annuum. Genomics 112: 2309-2317.
Beaudoin-Eagan L.D., Thorpe T.A., 1985. Tyrosine and phenylalanine ammonia lyase activities during shoot initiation in tobacco callus cultures. Plant Physiol 78: 438-441.
Bektas Y., Eulgem T., 2015. Synthetic plant defense elicitors. Front Plant Sci 5: 804.
Bradford M.M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254.
Brouwer S.M., Odilbekov F., Burra D.D. et al. 2020. Intact salicylic acid signalling is required for potato defence against the necrotrophic fungus Alternaria solani. Plant Mol Biol 104: 1–19.
Chen G., Hu Z., Grierson D., 2008. Differential regulation of tomato ethylene responsive factor LeERF3b, a putative repressor, and the activator Pti4 in ripening mutants and in response to environmental stresses. J Plant Physiol 165: 662-670.
Collinge D.B., 2018. Transgenic crops and beyond: how can biotechnology contribute to the sustainable control of plant diseases? Eur J Plant Pathol 152: 977-986.
Dazy M., Masfaraud J.-F., Férard J.-F., 2009. Induction of oxidative stress biomarkers associated with heavy metal stress in Fontinalis antipyretica Hedw. Chemosphere 75: 297-302.
Debbarma J., Sarki Y.N., Saikia B., Boruah H.P.D., Singha D.L., Chikkaputtaiah C., 2019. Ethylene response factor (ERF) family proteins in abiotic stresses and CRISPR–Cas9 genome editing of ERFs for multiple abiotic stress tolerance in crop plants: a review. Mol Biotechnol 61: 153-172.
Derksen H., Badawi M., Henriquez M.A., Yao Z., El‐Bebany A.F., Daayf F., 2013. Differential expression of potato defence genes associated with the salicylic acid defence signalling pathway in response to weakly and highly aggressive isolates of Verticillium dahliae. J Phytopathol 161: 142-153.
Ding S., 2018. An integrated study of potato early blight and brown spot in Wisconsin. The University of Wisconsin-Madison.
Ding S., Meinholz K., Cleveland K., Jordan S.A., Gevens A.J., 2019. Diversity and virulence of Alternaria spp. causing potato early blight and Brown spot in Wisconsin. Phytopathology 109: 436-445.
Esfahani M.N., 2018a. Analysis of virulence and genetic variability of Alternaria alternata associated with leaf spot disease in potato plants in Iran. Acta Mycologica 53: 1−9.
Esfahani M.N., 2018b. Identification of Ulocladium atrum causing potato leaf blight in Iran. Phytopathol Mediterr 57: 112-114.
Gallou A., Mosquera H.P.L., Cranenbrouck S., Suárez J.P., Declerck S., 2011. Mycorrhiza induced resistance in potato plantlets challenged by Phytophthora infestans. Physiol Mol Plant Pathol 76 20-26.
Gangadhar B. H., Sajeesh K., Venkatesh J. et al. 2016. Enhanced Tolerance of Transgenic Potato Plants Over-Expressing Non-specific Lipid Transfer Protein-1 (StnsLTP1) against Multiple Abiotic Stresses. Frontiers in plant science: 1228.
Ghasemi A.R., Golparvar A.R., Nasr Esfahani M., 2014. Analysis of genetic diversity of sugar beet genotypes using random amplified polymorphic DNA marker. Genetika 46: 975-984.
Giannopolitis C.N., Ries S.K., 1977. Superoxide dismutases: II. Purification and quantitative relationship with water-soluble protein in seedlings. Plant Physiol 59: 315-318.
Hamza R., Pérez-Hedo M., Urbaneja A., Rambla J.L., Granell A., Gaddour K., Beltrán J.P., Cañas L.A., 2018. Expression of two barley proteinase inhibitors in tomato promotes endogenous defensive response and enhances resistance to Tuta absoluta. BMC Plant Biol 18: 24.
Hashemi L., Golparvar A. R., Nasr Esfahani M., Golabadi M. (2019). Correlation between cucumber genotype and resistance to damping-off disease caused by Phytophthora melonis. Biotechnology & Biotechnological Equipment 33 1: 1494-1504,
Hashemi L., Golparvar A.R., Nasr-Esfahani M., Golabadi M., 2020. Expression analysis of defense-related genes in cucumber (Cucumis sativus L.) against Phytophthora melonis. Mol Biol Rep 45: 1-12.
Hellmann E., Helariutta Y., 2019. Plant Genetics: Advances in Regeneration Pathways. Curr Biol 29, R702-R704.
Heyman J., Canher B., Bisht A., Christiaens F., De Veylder L., 2018. Emerging role of the plant ERF transcription factors in coordinating wound defense responses and repair. J Cell Sci 131: 208215.
Hoegen E., Strömberg A., Pihlgren U., Kombrink E., 2002. Primary structure and tissue‐specific expression of the pathogenesis‐related protein PR‐1b in potato. Mol Plant Pathol 3: 329-345.
Hou Y., Ban Q., Meng K., He Y., Han, S., Jin M., Rao J., 2018. Overexpression of persimmon 9-lipoxygenase DkLOX3 confers resistance to Pseudomonas syringae pv. tomato DC3000 and Botrytis cinerea in Arabidopsis. Plant Growth Reg 84: 179-189.
Hu T., Hu Z., Zeng H., Qv X., Chen G., 2015. Tomato lipoxygenase D involved in the biosynthesis of jasmonic acid and tolerance to abiotic and biotic stress in tomato. Plant Biotechnol Rep 9: 37-45.
Hu Z., Zhang H., Shi K., 2018. Plant peptides in plant defense responses. Plant signaling & behavior 13: 1475175.
Huang K., Zhong, Y., Li Y., Zheng, D., Cheng Z.-M., 2016. Genome-wide identification and expression analysis of the apple ASR gene family in response to Alternaria alternata f. sp. mali. Genome 59: 866-878.
Hussain T., 2016. Potatoes: ensuring food for the future. Adv Plants Agr Res 3: 00117.
Isah T., 2019. Stress and defense responses in plant secondary metabolites production. Biol Res 52: 39. doi.org /10.1186/s40659-019-0246-3.
Jiang D., Chen F. X., Zhou H., Lu Y. Y., Tan H., Yu S. J., et al., 2020. Bioenergetic crosstalk between mesenchymal stem cells and various ocular cells through the intercellular trafficking of mitochondria. Theranostics 10: 7260.
Kawar P.G., 2016. Enriched potato for mitigating hidden hunger, Biofort Food Crops. Springer, pp. 433-457.
Kgatle M., Flett B., Truter M., Aveling T., 2020. Control of Alternaria leaf blight caused by Alternaria alternata on sunflower using fungicides and Bacillus amyloliquefaciens. Crop Pro: 105146.
Khan A., Nasir I.A., Tabassum B., Aaliya K., Tariq M., Rao A.Q., 2017. Expression studies of chitinase gene in transgenic potato against Alternaria solani. Plant Cell, Tissue and Organ Culture (PCTOC) 128: 563-576.
Kim Y.-H., Jeong J.C., Park S., Lee H.-S., Kwak S.-S., 2012. Molecular characterization of two ethylene response factor genes in sweetpotato that respond to stress and activate the expression of defense genes in tobacco leaves. J Plant Physiol 169: 1112-1120.
Kolomiets M.V., Chen H., Gladon R.J., Braun E., Hannapel D.J., 2000. A leaf lipoxygenase of potato induced specifically by pathogen infection. Plant Physiol 124: 1121-1130.
Kumari, M., Kumar M., Solankey S.S., 2018. Breeding Potato for Quality Improvement. Potato: From Incas to All Over the World IntechOpen: 37-59.
Lekota M., Muzhinji N., Van der Waals J.E., 2019. Identification of differentially expressed genes in tolerant and susceptible potato cultivars in response to Spongospora subterranea f. sp. subterranea tuber infection. Plant Pathol 68: 1196-1206.
Li C., Ren Y., Jiang S., Zhou S., Zhao J., Wang R., Li Y., 2018. Effects of dietary supplementation of four strains of lactic acid bacteria on growth, immune-related response and genes expression of the juvenile sea cucumber Apostichopus japonicus Selenka. Fish & Shellfish Immunol 74: 69-75.
Li H., Dong Q., Zhao Q., Shi S., Ran K., 2020. Isolation, sequencing, and expression analysis of 30 AP2/ERF transcription factors in apple. PeerJ 8: e8391.
Liu Y., Xin J., Liu L., Song A., Guan Z., Fang W., Chen F., 2020. A temporal gene expression map of Chrysanthemum leaves infected with Alternaria alternata reveals different stages of defense mechanisms. Horti Res 7: 1-14.
Liu L., Li J., Yue F., Yan X., Wang F., Bloszies S., Wang Y., 2018. Effects of arbuscular mycorrhizal inoculation and biochar amendment on maize growth, cadmium uptake and soil cadmium speciation in Cd-contaminated soil. Chemosphere 194: 495-503.‏
Liu L., Li D., Ma Y., Shen H., Zhao, S., Wang Y., 2020. Combined Application of Arbuscular Mycorrhizal Fungi and Exogenous Melatonin Alleviates Drought Stress and Improves Plant Growth in Tobacco Seedlings. Journal of Plant Growth Regulation: 1-14.‏
Li X., Zhang R., Zhang X., Zhu P., Yao T., 2020. Silver‐Catalyzed Decarboxylative Allylation of Difluoroarylacetic Acids with Allyl Sulfones in Water. Chemistry–An Asian Journal 15, 1175-1179.‏
Matrood A.A., Khrieba M.I., Okon O.G., 2020. Synergistic interaction of Glomus mosseae T. and Trichoderma harzianum R. in the induction of systemic resistance of Cucumis sativus L. to Alternaria alternata (Fr.) K. Plant Sci Today 7: 101-108.
McNeece B.T., Sharma K., Lawrence G.W., Lawrence K.S., Klink V.P., 2019. The mitogen activated protein kinase (MAPK) gene family functions as a cohort during the Glycine max defense response to Heterodera glycines. Plant Physiol Biochem 137: 25-41.
Moghaddam G.A., Rezayatmand Z., Esfahani M.N., Khozaei M., 2019. Genetic defense analysis of tomatoes in response to early blight disease, Alternaria alternata. Plant Physiol Biochem 142: 500-509.
Moghaddam G. A, Rezayatmand Z, Nasr Esfahani M, Khozaei M. 2020. Bio-genetic analysis of resistance in tomato to early blight disease, Alternaria alternata. Phytochemistry 179: 112486.
Naderi N., NasrEsfahani M., Bakhshi Khaniki G., 2020. Analysis of molecular characterizations of beets, Beta vulgaris in response to cyst nematodes, Heterodera schachtii. Physiol. Mol. Plant Pathol. 112: 297-307.
Nasr Esfahani M., Hashemi L., Nasehi A, Nasr Esfahani N., NasrEsfahani A., 2020. Novel Cucumis enzymes associated with host-specific disease resistance to Phytophthora melonis Katsura. Biotechnology and Biotechnological Equipment 34: 873-884.
Nasr Esfahan M., 2018. Identification of Ulocladium atrum causing potato leaf blight in Iran. Phytopathologia Mediterranea 57: 112−114.
Nasr-Esfahani M., 2019. An IPM plan for early blight disease of potato Alternaria solani sorauer and A. alternata (Fries.) Keissler. Archives Phytopathol Plant Pro 45: 1-12.
Nasr-Esfahani M., Alizadeh M.G., Karimkhah M.A., 2017. Susceptibility assessment of commercial potato cultivars to early blight disease under the greenhouse and field conditions. Iranian Journal of Plant Protection Science 48: 169-182.
Ogata T., Kida Y., Arai T., Kishi Y., Manago Y., Murai M., Matsushita Y., 2012. Overexpression of tobacco ethylene response factor NtERF3 gene and its homologues from tobacco and rice induces hypersensitive response-like cell death in tobacco. J Gene Plant Pathol 78: 8-17.
Pourarian A., Esfahani M.N., Sadravi M., 2018. Molecular and pathogenic characterization of Iranian isolates associated with leaf spot disease of potato. Acta Fytotechnica et Zootechnica 21: 1-5.
Prakash N., Vishunavat K., Khan G.T., Prasad P. 2020. SA, ABA and Pseudomonas fluorescens elicit defense responses in tomato against Alternaria blight. doi.org/10.1007/s13562-020-00564-x.
Qu K. Wei L., Zou Q., 2019. A review of DNA-binding proteins prediction methods. Current Bioinformatics 14: 246-254.
Radotić K., Dučić T., Mutavdžić D., 2000. Changes in peroxidase activity and isoenzymes in spruce needles after exposure to different concentrations of cadmium. Environmental and Experimental Botany 44, 105-113.
Raimo F., Pentangelo A., Pane C., Parisi B., Mandolino G., 2018. Relationships Between Internal Brown Spot and Skin Roughness in Potato Tubers Under Field Conditions. Potato Res 61: 327-339.
Raymond J., Rakariyatham N., Azanza J., 1993. Purification and some properties of polyphenoloxidase from sunflower seeds. Phytochem 34: 927-931.
Rehman S., Aziz E., Akhtar W., Ilyas M., Mahmood T., 2017. Structural and functional characteristics of plant proteinase inhibitor-II (PI-II) family. Biotechnol lett 39: 647-666.
Sohrabipour S., Sharifi M.R., Sharifi M., Talebi A., Soltani N., 2018. Effect of magnesium sulfate administration to improve insulin resistance in type 2 diabetes animal model: using the hyperinsulinemic‐euglycemic clamp technique. Fund Clinical Pharmacol 32: 603-616.
Tehrani M.M., Nasr-Esfahani M., Mousavi A., Mortezaiinezhad F., Azimi M.H., 2020. Regulation of related genes promoting resistant in Iris against root rot disease, Fusarium oxysporum f. sp. gladioli. Genomics. 112: 3013-3020.
Tian M., Wang J., Pan P. et al. 2020. Transcriptome analysis of potato leaves in response to infection with the necrotrophic pathogen Alternaria solani. bioRxiv 020.09.21.307314.
Toufiq N., Tabassum B., Bhatti M.U., Khan A., Tariq M., Shahid, N. Nasir, I.A., Husnain T., 2018. Improved antifungal activity of barley derived chitinase I gene that overexpress a 32 kDa recombinant chitinase in Escherichia coli host. Braz J Microbiol 49: 414-421.
Turra D., Lorito M., 2011. Potato type I and II proteinase inhibitors: modulating plant physiology and host resistance. Curr Protein Pept Sci 12: 374-385.
Wan R., Liu J., Yang Z., Zhu P., Cao Q., Xu T., 2020. Genome-wide identification, characterisation and expression profile analysis of DEAD-box family genes in sweet potato wild ancestor Ipomoea trifida under abiotic stresses. Genes & Genomics 42; 325-335.
Wang X., El Hadrami A., Adam L., Daayf F., 2008. Differential activation and suppression of potato defence responses by Phytophthora infestans isolates representing US‐1 and US‐8 genotypes. Plant Pathol 57: 1026-1037.
Xu L., Jiang S., Zou Q., 2020a. An in silico approach to identification, categorization and prediction of nucleic acid binding proteins. Bioinformatics doi: 10.1093/bib/bbaa171.
Xu X., Zhang L., Chen L., Liu C.. 2020b. The Role of Soil N2O Emissions in Agricultural Green Total Factor Productivity: An Empirical Study from China around 2006 when Agricultural Tax Was Abolished. Agriculture 10: 150.
Yang J., Sun C., Zhang Y., Fu D., Zheng X., Yu T., 2017. Induced resistance in tomato fruit by γ-aminobutyric acid for the control of alternaria rot caused by Alternaria alternata. Food Chem 221: 1014-1020.
Yang F., Yang F., Wang G., Kong T., Wang H., Zhang C., 2020. Effects of water temperature on tissue depletion of florfenicol and its metabolite florfenicol amine in crucian carp (Carassius auratus gibelio) following multiple oral doses. Aquaculture 515: 734542.
Zhai X., Kong Q., An P., Ren X., 2018. The Function and Mechanism of Pathogenesis-Related 5 Protein Resistance in Cherry Tomato in Response to Alternaria alternata. Food Biotechnol 32: 178-190.
Zhang J., Liu F., Yao L., Luo C., Yin Y., Wang G., Huang Y., 2012a. Development and bioassay of transgenic Chinese cabbage expressing potato proteinase inhibitor II gene. Breeding Sci 62: 105-112.
Zhang S., Xu X., Sun Y., Zhang J., Li C., 2018. Influence of drought hardening on the resistance physiology of potato seedlings under drought stress. J Integ Agr 17: 336-347.
Zhang X., Yu X., Yu Z., Zhang W., Ju L., Xue Y., 2012b. Changes on activity of defensive enzyme after inoculating with toxin of Rhizoctonia solani in potato. Acta Agr Boreali-Sinica 27: 153-157.
Zhang J., Liu B., 2019. A review on the recent developments of sequence-based protein feature extraction methods. Current Bioinformatics 14: 190-199.
Zou Q., Xing P., Wei L., Liu B., 2019. Gene2vec: gene subsequence embedding for prediction of mammalian N6-methyladenosine sites from mRNA. RNA 25: 205-218.