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Comprehensive biochemical approach for understanding the interaction between host “common bean” and pathogen “Colletotrichum lindemuthianum” causing bean anthracnose

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Abstract

Anthracnose (ANT) caused by Colletotrichum lindemuthianum is the most devastating seed-borne fungal disease of common bean. In response to fungal infections, it is hypothesized that pathogen–plant interactions typically cause hypersensitive reactions by producing reactive oxygen species, hydrogen peroxide and lipid peroxidation of cell membranes. esent study was conducted by inoculating susceptible bean genotype “SB174” and resistant bean genotype “E10” with pathogen “C. lindemuthianum”. Defense-related enzymes (ascorbate peroxidase, peroxidase, lipid peroxidase, and catalase) and C-based compounds (total phenols and flavonoids) were studied using the detached bean leaf method. Comparative defense response was studied in different plant tissues (pod, stem, and seed) in susceptible and resistant bean genotypes under uninoculated and pathogen-inoculated conditions. The host‒pathogen interaction was studied at mock inoculation, 2, 4 and 6 days after inoculation (dai). Comparing the pathogen-inoculated bean leaves to water-treated bean leaves, defense enzymes as well as total phenols and flavonoids exhibited differential expression. In a comparative study, the enzyme activity also displayed differential biochemical responses in pods, stems and seeds in both contrasting genotypes. For example, 5.1-fold (pod), 1.5-fold (stem) and 1.06-fold (seed) increases in ascorbate peroxidase activity were observed in the susceptible genotype at 6 dai compared to mock inoculation. Similarly, catalase activity in pods was upregulated (1.47-fold) in the resistant genotype and downregulated (1.30-fold) in the susceptible genotype at 6 dai. The study revealed that defense-related antioxidative enzymes, phenols and flavonoids are fine-tuned to detoxify important reactive oxygen species (ROS) molecules, induce systemic resistance and are successfully controlled in common bean plants against pathogen invasion.

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References

  • Agrawal GK, Jwa NS, Rakwal R (2002) A pathogen-induced novel rice (Oryza sativa L.) gene encodes a putative protein homologous to type II glutathione-S-transferases. Plant Sci 163:1153–1160. https://doi.org/10.1016/S0168-9452(02)00331-X

    Article  CAS  Google Scholar 

  • Ait-El-Mokhtar M, Laouane RB, Anli M, Boutasknit A, Wahbi S, Meddich A (2019) Use of mycorrhizal fungi in improving tolerance of the date palm (Phoenix dactylifera L.) seedlings to salt stress. Sci Hortic 253:429–438. https://doi.org/10.1016/j.scienta.2019.04.066

    Article  Google Scholar 

  • Aly AA, Mansour M, Mohamed HI, Abd-Elsalam KA (2012) Examination of correlations between several biochemical components and powdery mildew resistance of flax cultivars. Plant Pathol J 28(2):149–155

    Article  CAS  Google Scholar 

  • Arauz L (2000) Mango anthracnose: economic impact and current options for integrate management. Plant Dis 84:600–611

    Article  PubMed  Google Scholar 

  • Baysal O, Soylu EM and Soylu S (2003) Induction of defense-related enzyme and resistance by the plant activator acibenzolar-S-methyl in tomato seedlings against bacterial canker caused by Clavibacter michiganensis ssp. michiganensis. Plant Pathol 52:747e53.

  • Beebe S, Gonzalez AV, Rengifo J (2000) Research on trace minerals in the common bean. Food Nutr Bull 21:387–391

    Article  Google Scholar 

  • Bindschedler LV, Dewdney J, Blee KA, Stone JM, Asai T, Plotnikov J et al (2006) Peroxidase-dependent apoplastic oxidative burst in Arabidopsis required for pathogen resistance. Plant J 4:851e63.

  • Borges LL, Santana FA, Castro ISL, Arruda KMA, Ramos HJO, Barros EG (2015) Two-dimensional electrophoresis-based proteomic analysis of Phaseolus vulgaris in response to Colletotrichum lindemuthianum. J Plant Pathol 97:249–257

    Google Scholar 

  • Buragohain R (2015) Screening and quantification of phytochemicals and evaluation of antioxidant activity of Albizia chinensis (vang): one of the tree foliages commonly utilized for feeding to cattle and buffaloes in Mizoram. Int J Cur Microbiol App Sci 4(9):305–313

    CAS  Google Scholar 

  • Cakmak I, Strbac D, Marschner H et al (1993) Activities of hydrogen peroxide scavenging enzymes in germinating wheat seeds. J Exp Bot 44(1):127–132. https://doi.org/10.1093/jxb/44.1.127

    Article  CAS  Google Scholar 

  • Campa A, Rodriguez-Suarez C, Giraldez R. and Ferreira JJ (2014) Genetic analysis of the response to eleven Colletotrichum lindemuthianum races in a RIL population of common bean (Phaseolus vulgaris L.). BMC Plant Biol 14:115.

  • Cao S, Du XH, Li LH, Liu YD, Zhang L, Pan X, Li Y, Li H, Lu H (2017) Overexpression of Populus tomentosa cytosolic ascorbate peroxidase enhances abiotic stress tolerance in tobacco plants. Russ J Plant Physiol 64:224–234

    Article  CAS  Google Scholar 

  • Chakraborty N, Mukherjee K, Sarkar A, Acharya K (2019) Interaction between bean and Colletotrichum gloeosporioides: understanding through a biochemical approach. Plants 8(9):345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chance B, Maehly AC (1955) “Methods in Enzymology”, Assay of Catalases and Peroxidases. Academic Press, New York, pp 764–775. https://doi.org/10.1016/S0076-6879(55)02300-8.

  • Choudhary N, Hamid A, Singh B, Khandy I, Sofi PA, Bhat MA, Mir RR (2018b) Insight into the origin of common bean (Phaseolus vulgaris L.) grown in the state of Jammu and Kashmir of north-western Himalayas. Genet Resour Crop Evol 65:963–977

    Article  Google Scholar 

  • Choudhary N, Bawa V, Paliwal R, Singh B, Bhat MA, Mir JI. et al. (2018a) Gene/QTL discovery for Anthracnose in common bean (Phaseolus vulgaris L.) from the northwestern Himalayas. PLoS ONE 13(2):e0191700. https://doi.org/10.1371/journal.pone.0191700

  • Choudhary N, Gupta M, Shafi S, Jan S, Mir AH, Singh B, Varshney R (2022) Molecular diversity and nutriment studies of common bean (Phaseolus vulgaris L.) from the two hot-spots of Western Himalayas of Jammu and Kashmir. Crop Pasture Sci 73(3):249–262.

  • Costa BHG, de Resende MLV, Monteiro ACA, Ribeiro Júnior PM, Botelho DMDS, Silva BMD (2018) Potassium phosphites in the protection of common bean plants against anthracnose and biochemical defense responses. J Phytopathol 166(2):95–102

    Article  CAS  Google Scholar 

  • Dallagnol LJ, Rodrigues FA, DaMatta FM, Mielli MV, Pereira SC (2011) Deficiency in silicon uptake affects cytological, physiological, and biochemical events in the rice–Bipolaris oryzae interaction. Phytopathology 101(1):92–104

    Article  PubMed  Google Scholar 

  • Djeridane A, Yousfi M, Nadjemi B, Vidal N, Lesgard JF, Stocker P (2006) Antioxidant activity of some Algerian medicinal plant extracts containing phenolic compounds. Food Chem 97(4):654–660. https://doi.org/10.1016/j.foodchem

    Article  CAS  Google Scholar 

  • Garcı́a-Limones C, Hervás A, Navas-Cortés JA, Jiménez-Dı́az RM, Tena M (2002) Induction of an antioxidant enzyme system and other oxidative stress markers associated with compatible and incompatible interactions between chickpea (Cicer arietinum L.) and Fusarium oxysporum f. sp. ciceris. Physiol. Mol. Plant Pathol 61(6):325–337.

  • Jan S, Rather IA, Sofi PA, Wani MA, Sheikh FA, Bhat MA, Mir RR (2021) Characterization of common bean (Phaseolus vulgaris L.) germplasm for morphological and seed nutrient traits from Western Himalayas. Legume Sci 3(2):e86.

  • Karoney EM, Ochieno DM, Baraza DL, Muge EK, Nyaboga EN, Naluyange V (2020) Rhizobium improves nutritive suitability and tolerance of Phaseolus vulgaris to Colletotrichum lindemuthianum by boosting organic nitrogen content. Appl Soil Eco 149:103534

    Article  Google Scholar 

  • Kuźniak E, Urbanek H (2000) The involvement of hydrogen peroxide in plant responses to stresses. Acta Physiol Plant 22:195–203

    Article  Google Scholar 

  • Latef AAHA, Chaoxing H (2011) Effect of arbuscular mycorrhizal fungi on growth, mineral nutrition, antioxidant enzymes activity and fruit yield of tomato grown under salinity stress. Sci Hortic 127(3):228–233. https://doi.org/10.1016/j.scienta.2010.09.020

    Article  CAS  Google Scholar 

  • Lubaina AS, Murugan K (2013) Ultrastructural changes and oxidative stress markers in wild and cultivar Sesamum orientale L. following Alternaria sesame (Kawamura) Mohanty and Behera. inoculation. Indian J Exp Biol 51:670–680

    CAS  PubMed  Google Scholar 

  • Maruta T, Tanouchi A, Tamoi M, Yabuta Y, Yoshimura K, Ishikawa T, Shigeoka S (2010) Arabidopsis chloroplastic ascorbate peroxidase isoenzymes play a dual role in photoprotection and gene regulation under photooxidative stress. Plant Cell Physiol 51:190–200

    Article  CAS  PubMed  Google Scholar 

  • Meena M, Zehra A, Dubey MK, Aamir M, Gupta VK, Upadhyay RS (2016) Co mparative Evaluation of Biochemical Changes in Tomato (Lycopersicon esculentum Mill.) Infected by Alternaria alternata and Its Toxic Metabolites (TeA, AOH, and AME). Front Plant Sci 7:1408. https://doi.org/10.3389/fpls.2016.01408

  • Mir RR, Choudhary N, Bawa V, Jan S, Singh B, Bhat MA, Paliwal R, Kumar A, Chitikineni A, Thudi M, Varshney RK (2021) Allelic diversity, structural analysis, and Genome-Wide Association Study (GWAS) for yield and related traits using unexplored common bean (Phaseolus vulgaris L.) germplasm from Western Himalayas. Front Genet 11:609603.

  • Misra RS, Sharma K, Misra AK, Sriram S (2008) Biochemical alterations induced in taro in response to Phytophthora colocasiae infection. Adv Nat Appl Sci 2(3):112e21.

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410. https://doi.org/10.1016/S1360-1385(02)02312-9

    Article  CAS  PubMed  Google Scholar 

  • Mohamed MA, Hasabo SA (2005) Biochemical alterations induced by Meloidogyne incognita infection in cotton. Inter J Nematol 15:145e54.

  • Montillet JL, Chamnongpol S, Rusterucci C, Dat J, Van de Cotte B, Agnel JP, Battesti C, Inze D, Van Breusegem F, Triantaphylides C (2005) Fatty acid hydroperoxides and H2O2 in the execution of hypersensitive cell death in tobacco leaves. Plant Physiol 138:1516–1526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Moraes SRG, Pozza EA, Alves E, Pozza AAA, Carvalho JG, Lima PH, Botelho AO (2006) Efeito de fontes de silício na incidência e na severidade da antracnose do feijoeiro. Fitopatol Bras 31:069–075

    Article  Google Scholar 

  • Nabavi SM, Ebrahimzadeh MA, Nabavi SF, Jafari M (2008) Free radical scavenging activity and antioxidant capacity of eryngium Caucasicum trautv and Frozripia subpinnata. Pharmacologyonline 3:19–25

    Google Scholar 

  • Palma JM, Sandalio LM, Corpas FJ, Romero-Puertas MC, McCarthy I, del Río LA (2002) Plant proteases, protein degradation, and oxidative stress: role of peroxisomes. Plant Physiol Biochem 40:521–530. https://doi.org/10.1016/S0981-9428(02)01404-3

    Article  CAS  Google Scholar 

  • Patel RV, Joshi KR, Solanky KU, Sabalpara AN (2005) Colletotrichum gloeosporioides: a new leaf spot pathogen of turmeric in Gujarat. Ind Phytopathol 58:125

    Google Scholar 

  • Pinto JMA, Pereira R, Mota SF, Ishikawa FH, Souza EA (2012) Investigating phenotypic variability in Colletotrichum lindemuthianum populations. Phytopathology 102:490–497

    Article  CAS  PubMed  Google Scholar 

  • Polanco LR, Rodrigues FA, Nascimento KJT, Shulman P, Silva LC, Neves FW, Vale FXR (2012) Biochemical aspects of bean resistance to anthracnose mediated by silicon. Ann Appl Biol 161:140–150

    Article  CAS  Google Scholar 

  • Reuveni R, Shimoni M, Karchi Z, Kuc I (1992) Peroxidase activity as a biochemical marker for resistance of muskmelon (Cucumis melo) to Pseudoperonospora cubensis. Phytopathology 82:749e53.

  • Ribeiro CF, de Borba MC, Geller AC, Pontes ES, Kulcheski FR, de Freitas MB, Stadnik MJ (2023) Enhanced oxidative enzymes activity and lipid peroxidation are associated with hypersensitive response and atypical lesions in resistant bean plants infected with Colletotrichum lindemuthianum. Physiol Mol Plant Pathol 127:102099

    Article  CAS  Google Scholar 

  • Saenen E, Horemans N, Vanhoudt N, Vandenhove H, Biermans G, Van Hees M, Cuypers A (2015) Oxidative stress responses induced by uranium exposure at low pH in leaves of Arabidopsis thaliana plants. J Environ Radioact 150:36–43. https://doi.org/10.1016/j.jenvrad.2015.07.021

    Article  CAS  PubMed  Google Scholar 

  • Sarowar S, Kim EN, Kim YJ, Ok SH, Kim KD, Hwang BK, Shin JS (2005) Overexpression of a pepper ascorbate peroxidase-like 1 gene in tobacco plants enhances tolerance to oxidative stress and pathogens. Plant Sci 169(1):55–63

    Article  CAS  Google Scholar 

  • Scandalios JG (2005) Oxidative stress: molecular perception and transduction of signals triggering antioxidant gene defenses. Braz J Med Biol Res 38:995–1014

    Article  CAS  PubMed  Google Scholar 

  • Schneider J, Bundschuh J, de Melo RW, Guilherme LRG (2017) Potential of different AM fungi (native from As-contaminated and uncontaminated soils) for supporting Leucaena leucocephala growth in As-contaminated soil. Environ Pollut 224:125–135. https://doi.org/10.1016/j.envpol.2017.01.071

    Article  CAS  PubMed  Google Scholar 

  • Shafi S, Saini DK, Khan MA, Bawa V, Choudhary N, Dar WA, Pandey AK, Varshney RK, Mir RR (2022) Delineating meta-quantitative trait loci for anthracnose resistance in common bean (Phaseolus vulgaris L.). Front. Plant Sci 13:966339.

  • Sharma N, Kumari N, Sharma SK, Padder BA, Sharma PN (2019) Investigating the virulence and genetic diversity of Colletotrichum lindemuthianum populations distributed in the North Western Himalayan hill states. J Plant Pathol 101(3):677–688

    Article  Google Scholar 

  • Shigeoka S, Ishikawa T, Tamoi M, Miyagawa Y, Takeda T, Yabuta Y, Yoshimura K (2002) Regulation and function of ascorbate peroxidase isoenzymes. J Exp Bot 53:1305–1319

    Article  CAS  PubMed  Google Scholar 

  • Shigeto J, Tsutsumi Y (2016) Diverse functions and reactions of class III peroxidases. New Phytol 209(4):1395–1402

    Article  CAS  PubMed  Google Scholar 

  • Shimizu N, Hosogi N, Hyon GS, Jiang S, Inoue K, Park P (2006) Reactive oxygen species (ROS) generation and ROS induced lipid peroxidation are associated with plant membrane modifications in host cells in response to AK-toxin from Alternaria alternata Japanese pear pathotype. J Gen Plant Pathol 72:6–15. https://doi.org/10.1007/s10327-005-0245-9

    Article  CAS  Google Scholar 

  • Siegrist L, Glenewinkel D, Kolle C, Schidtke M (1997) Chemically induced resistance in green bean against bacterial and fungal pathogens. Zeit Pfl Pflanzen 104:599e610

  • Vandana VV, Azeez S (2014) Biochemical defense responses of black pepper (Piper nigrum L.) lines to Phytophthora capsici. Physiol Mol Plant Pathol 88:18–27

    Article  Google Scholar 

  • Wink M (2008) Plant secondary metabolism: diversity, function and its evolution. Nat Prod Commun 3:1205–1216

    CAS  Google Scholar 

  • Zaynab M, Fatima M, Abbas S, Sharif Y, Umair M, Zafar MH, Bahadar K (2018) Role of secondary metabolites in plant defense against pathogens. Microb Pathog 124:198–202. https://doi.org/10.1016/j.micpath.2018.08.034

    Article  CAS  PubMed  Google Scholar 

  • Zhang J, Jia X, Wang GF, Ma S, Wang S, Yang Q, Wu L (2022) Ascorbate peroxidase 1 confers resistance to southern corn leaf blight in maize. J Integr Plant Biol 64(6):1196–1211

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The facilities provided by the Head, Division of Genetics and Plant Breeding and Head, Division of Microbiology, Faculty of Agriculture, SKUAST-K are acknowledged. We are thankful to Dean, Faculty of Agriculture, SKUAST-K for supporting the research. Dr. R. R. Mir is highly thankful for DBT, GOI for providing funds (BT/Ag/Network/Wheat/2019-20).

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The authors did not receive support from any organization for the submitted work.

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Authors and Affiliations

  1. Division of Genetics and Plant Breeding, Faculty of Agriculture, SKUAST-Kashmir, Wadura, 193201, India

    Safoora Shafi, Mohd Anwar Khan, Farooq Ahmad Sheikh, Asif Bashir Shikari & Reyazul Rouf Mir

  2. Division of Agricultural Economics & Statistics, SKUAST-Kashmir, Wadura, 193201, India

    Fehim Jeelani Wani

  3. Division of Basic Sciences & Humanities, Faculty of Agriculture, SKUAST-Kashmir, Wadura, 193201, India

    Shabir Ahmad Ganai

  4. Division of Plant Pathology, SKUAST-Kashmir, Shalimar, Srinagar, 190025, India

    Najeeb M Mughal

  5. Centre for Crop & Food Innovation, State Agricultural Biotechnology Centre, Food Futures Institute, Murdoch University, Murdoch, WA, Australia

    Rajeev Kumar Varshney

  6. Institute of Field and Vegetable Crops, National Institute of the Republic of Serbia, Maxim Gorki 30, Novi Sad, Serbia

    Ivica Djalovic

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  1. Safoora Shafi
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Contributions

SS, MAK, FJ, FAS, SAG and RRM conceived the idea and designed the methodology; SS collected the data; FJW, FAS, SAG analyzed the data; and NM, ABS, RKV, ID helped in writing and reviewed the manuscript. The manuscript was written by all the author team, who also provided valuable feedback on early revisions and ultimately approved its publishing.

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Correspondence to Mohd Anwar Khan or Reyazul Rouf Mir.

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Shafi, S., Khan, M.A., Wani, F.J. et al. Comprehensive biochemical approach for understanding the interaction between host “common bean” and pathogen “Colletotrichum lindemuthianum” causing bean anthracnose. Physiol Mol Biol Plants 29, 2005–2020 (2023). https://doi.org/10.1007/s12298-023-01394-6

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