Proteomic analysis of the tripartite interaction between black pepper, Trichoderma harzianum and Phytophthora capsici provides insights into induced systemic resistance mediated by Trichoderma spp.
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Trichoderma harzianum (MTCC5179) is the biocontrol agent in the black pepper (Piper nigrum.L) production system against the destructive pathogen Phytophthora capsici which causes foot and root rot. We employed label-free quantitative proteomics to study the T. harzianum mediated induced systemic response in this system. We studied the defence response in leaves in T. harziznum primed plant roots which are also infected with P. capsici. The pattern of interactions was studied as black pepper × T. harzianum (two-way), black pepper × P. capsici (two-way) and black pepper × T. harzianum × P. capsici (three-way). The proteins induced only in the three-way interaction were identified as Trichoderma induced resistance proteins. Eighteen reactive oxygen species-related proteins and 22 defence-related proteins were identified as marker proteins. Apart from these groups, the ethylene synthesis, isoflavanoid pathway and lignin synthesis proteins were found to be enhanced. We report the early induced systemic resistance in leaves after Trichoderma priming at roots (72, and 96 h after interaction) against Phytophthora capsici after 12 and 24 h of infection at roots. The peptides/proteins from this study will serve as important marker peptides/proteins for the induced systemic resistance in plants by Trichoderma.
KeywordsProteomics Peptides ROS related proteins Defense-related proteins Phytophthora capsici T-ISR
The authors acknowledge with thanks the financial support from ICAR-Outreach programme on Phytophthora, Fusarium and Ralstonia diseases of horticultural and field crops (PhytoFuRa). The mass spectrometry performed by C-CAMP, Bangalore, is gratefully acknowledged.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
Involvement of human participants and /or animals
The present research did not involve any experimentation on humans or animals.
Authors are ready to provide any additional information of the present study to the readers.
- Ahmed, A. S., Sanchez, C. P., & Candela, M. E. (2000). Evaluation of induction of systemic resistance in pepper plants (Capsicum annum) to Phytophthora capsici using Trichoderma harzianum and its relation with capsidiol accumulation. European Journal of Plant Pathology, 106, 817–824.CrossRefGoogle Scholar
- Anandaraj, M. (2000). Diseases of black pepper. In P. N. Ravindran (Ed.), Black pepper (Piper nigrum L.) (pp. 239–268). Harwood Academic Publisher.Google Scholar
- Anandaraj, M., & Sarma, Y.R. (2003). The potential of PGPRs in disease management of spice crop. In 6th International PGPR workshop, Calicut, India,5–10 October 2003.Google Scholar
- Bolton, M. D. (2009). Primary metabolism and plant-defense-fuel for the fire. Molecular Plant Microbe Interaction, 11, 1196–1206.Google Scholar
- Chabannes, M., Barakate, A., Lapierre, C., Marita, J. M., Ralph, J., Pean, M., Danoun, S., Halpin, C., Grima-Pettenati, J., & Boudet, A. M. (2001). Strong decrease in lignin content without significant alteration of plant development is induced by simultaneous down regulation of cinnamoyl CoA reductase (CCR) and cinnamyl alcohol dehydrogenase (CAD) in tobacco plants. The Plant Journal, 28, 257–270.CrossRefGoogle Scholar
- Cheng, Q., Li, N., Dong, L., Zhang, D., Fan, S., Jiang, L., Wang, X., Xu, P., & Zhang, P. (2015). Overexpression of soybean Isoflavone reductase (GmIFR) enhances resistance to Phytophthora sojae in soybean. Frontiers in Plant Science, 6, 1024.Google Scholar
- Contreras-Cornejo, H. A., Macias-rodriguez, L., Beltran–Pena, E., Herrera– Estrella, A., & Lopez-Bucio, J. (2011). Trichoderma –induced plant immunity likely involves both hormonal and camalexin dependent mechanisms in Arabidopsis thaliana and confers resistance against necrotrophic fungus Botrytis cinerea. Plant Signaling Behaviuor, 6, 1554–1563.CrossRefGoogle Scholar
- Dorey, S., Baillieul, F., Saindrenan, P., Fritig, B., & Kauffmann, S. (1998). Spatial and temporal induction of cell death, defense genes, and accumulation of salicylic acid in tobacco leaves reacting hypersensitivity to a fungal glycoprotein elicitor. Molecualr Plant Microbe Interaction, 11, 1102–1109.CrossRefGoogle Scholar
- Duijff, B. J., Pouhair, D., Olivain, C., Alabouvette, C., & Lemanceau, P. (1998). Implication of systemic induced resistance in the suppression of fusarium wilt of tomato by Pseudomonas fluorescens WCS417r and by nonpathogenic Fusarium oxysporum Fo47. European Journal of Plant Pathology, 104, 903–910.CrossRefGoogle Scholar
- Gray, W. M., Carlos del Pozo, J., Walker, L., Hobbie, L., Risseeuw, E., Banks, T., Crosby, W. L., Ming Yang, M., Hong Ma, H., & Estelle, M. (1999). Identification of an SCF ubiquitin–ligase complex required for auxin response in Arabidopsis thaliana. Genes and Development, 13, 1678–1691.CrossRefGoogle Scholar
- Gullner, G., & Komives, T. (2001). The role of glutathione and glutathione-related enzymes in plant-pathogen interactions. In D. Grill, M. Tausz, & L. Kok (Eds.), Significance of glutathione in plant adaptation to the environment (pp. 207–239). Dordrecht: Kluwer Academic Publishers.CrossRefGoogle Scholar
- Karolev, N., Rav David, D., & Elad, Y. (2008). The role of phytohormones in basal resisance and Trichoderma- induced resistance to Botrytis cinerea in Arabidopsis thaliana. Biological Control, 53, 667–682.Google Scholar
- Kawasaki, T., Koita, H., Nakatsubo, T., Hasegawa, K., Wakabayashi, K., Takahashi, H., Umemura, K., Umezawa, T., & Shimamoto, K. (2006). Cinnamoyl-CoA reductase, a key enzyme in lignin biosynthesis, is an effector of small GTPase Rac in defense signaling in rice. Proceedings of the National Academy of Sciences U.S.A, 103, 230–235.CrossRefGoogle Scholar
- Keswani, C., Bisen, K., Singh, S. P., Sarma, B. K., & Singh, H. B. (2016). A proteomic approach to understand the Tripartite interataions between Plant-Trichoderma- Pathogen: Investigating the potential for efficient biological control. In K. R. Hakeem & M. S. Akhtar (Eds.), Plant, Soil and Microbes (pp. 79–93). Switzerland: Springer Publications.CrossRefGoogle Scholar
- Lowry, O.H., Rosebrough, N. J., Farr, A. L. & Randal, R. J. (1951). Protein measurement with the folin phenol reagent. The Journal of Biological Chemistry, 193(1), 265–75.Google Scholar
- Marra, R., Ambrosino, P., Carbone, V., Vinale, F., Woo, S. L., Ruocco, M., Ciliento, R., Lanzuise, S., Ferraioli, S., Soriente, I., Gigante, S., Turra, D., Fogliano, V., Scala, F., & Lorito, M. (2006). Study of the three-way interaction between Trichoderma atroviride, plant and fungal pathogens by using a proteomic approach. Current Genetics, 50, 307–321.CrossRefGoogle Scholar
- Martinez-Medina, A., Fernandez, I., Sanchez-Guzman, M. J., Jung, S. C., Pascual, J. A., & Pozo, M. J. (2013). Deciphering the hormonal signaling network behind the systemic resistance induced by Trichoderma in tomato. Frontiers in Plant Sciences, 24, 206.Google Scholar
- Mathys, J., DeCremer, K., Timmermans, P., VanKerckhove, S., Lievens, B., & Vanhaecke, M. (2012). Genome-wide characterization of ISR induced in Arabidopsis thaliana by Trichoderma hamatum T382 against Botrytis cinerea infection. Frontiers in Plant Sciences, 3, 108.Google Scholar
- Mhamdi, A., Mauve, A. C., Gouia, H., Saindrenan, P., Hodges, M., & Noctor, G. (2010). Cytosolic NADP-dependent isocitrate dehydrogenase contributes to redox homeostasis and the regulation of pathogen responses in Arabidopsis leaves. Plant Cell &Environment, 33, 1112–1123.Google Scholar
- Niehaus, T. D., Nguyen, T. N. D., Gidda, S. K., ElBadawi-Sidhu, M., Lambrecht, J. A., McCarty, D. R., Downs, D. M., Cooper, A. J. L., Fiehn, O., Mullen, R. T., & Hanson, A. D. (2014). Arabidopsis and maize RidA proteins preempt reactive enamine/imine damage to branched-chain amino acid biosynthesis in plastids. Plant Cell, 26, 3010–3022.CrossRefGoogle Scholar
- Paul, D., Saju, K. A., Jisha, P., Sarma, Y. R., Kumar, A., & Anandaraj, M. (2005). Mycolitic enzymes produced by Pseudomonas fluorescens and Trichoderma spp. against Phytophthora capsici, the foot rot pathogen of black pepper (Piper nigrum L.). Annals of Microbiology, 55, 129–133.Google Scholar
- Rajan, P. P., Sarma, Y. R., & Anandaraj, M. (2002). Management of foot rot disease of black pepper with Trichoderma spp. Indian Phytopathology, 55, 34–38.Google Scholar
- Scandiolios, J. G., Tsaftaris, J. M., Chandlee, T. M., & Skadsen, R. W. (1984). Expression of the developmentally regulated catalase (Cat) genes in maize. Developmental Genetics, 4, 2–293.Google Scholar
- Sibi, M. C. (2013). Development of biocontrol consortia for tissue cultured black pepper (Piper nigrum L.,) plants. Mangalore University: Dissertation.Google Scholar
- Stammers, D. K., Ren, J., Leslie, K., Nichols, C. E., Lamb, H. K., Cocklin, S., Dodds, A., & Hawkins, A. R. (2001). The structure of the negative transcriptional regulator NmrA reveals a structural superfamily which includes the short chain dehydrogenase/reductases. TheEMBO Journal, 20, 6619–6626.Google Scholar
- Umadevi, P., & Anandaraj, M. (2015). An efficient protein extraction method for proteomic analysis of black pepper (Piper nigrum L.) and generation of protein map using nano LC-LTQ Orbitrap mass spectrometry. Plant Omics, 8, 500–507.Google Scholar
- Umadevi, P., Anandaraj, M., & Benjamin, S. (2017a). Endophytic interactions of Trichoderma harzianum in a tropical perennial rhizo – Ecosystem. Research Journal of Biotechnology, 12, 22–30.Google Scholar
- Umadevi, P., Anandaraj, M., Srivastav, V., & Benjamin, S. (2017b). Trichoderma harzianum MTCC 5179 impacts the population and functional dynamics of microbial community in the rhizosphere of black pepper (Piper nigrum L.). Brazilian Journal of Micorbiology. https://doi.org/10.1016/j.bjm.2017.05.011.
- Velazquez-Robledo, R., Contreras-Cornejo, H. A., Macias- Rodriguez, L., Hernandez-Morals, A., Aguirre, J., Casas-Flores, S., Lopez-Bucio, J., & Herrera- Estrella, A. (2011). Role of the 4- phosphopantetheinyl transferase of Trichoderma virens in secondary metabolism and induction of plant defense responses. American Phytopathological Society, 24, 1459–1471.Google Scholar
- Waller, F., Achatz, B., Baltruschat, H., Fodor, J., Becker, K., & Fischer, M. (2005). The endophytic fungus Piriformospora indica reprograms barley to salt-stress tolerance, disease resistance, and higher yield. Proceedings of the National Academy of Sciences U.S.A., 102, 13386–13391.CrossRefGoogle Scholar
- Yedidia, I., Shoresh, M., Kerem, Z., Ben-hamou, N., Kapulnik, Y., & Chet, I. (2003). Concomitant induction of systemic resistance to Pseudomonas syringae pv. lachrymans in cucumber by Trichoderma asperellum (T-203) and accumulation of phytoalexins. Applied and Environmental Microbiology, 69, 7343–7373.CrossRefGoogle Scholar