Abstract
Elicitor-induced defense response against potential plant pathogens has been widely reported in several crop plants; however, transcriptome dynamics underlying such defense response remains elusive. Our previous study identified and characterized a novel elicitor, κ-carrageenan, from Kappaphycus alvarezii, a marine red seaweed. Our preliminary studies have shown that the elicitor-treatment enhances the tolerance of a susceptible tomato cultivar to Septoria lycopersici (causative agent of leaf spot disease). To gain further insights into the genes regulated during elicitor treatment followed by pathogen infection, we have performed RNA-Seq experiments under different treatments, namely, control (untreated and uninfected), elicitor treatment, pathogen infection alone, and elicitor treatment followed by pathogen infection. To validate the results, forty-three genes belonging to five different classes, namely, ROS activating and detoxifying enzyme encoding genes, DEAD-box RNA helicase genes, autophagy-related genes, cysteine proteases, and pathogenesis-related genes, were chosen. Expression profiling of each gene was performed using qRT-PCR, and the data was correlated with the RNA-seq data. Altogether, the study has pinpointed a repertoire of genes that could be potential candidates for further functional characterization to provide insights into novel elicitor-induced fungal defense and develop transgenic lines resistant to foliar diseases.
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The sequencing data associated with this work have been submitted to the NCBI SRA (Bioproject number is PRJNA622013).
References
Arneson PA, Durbin DR (1967) Hydrolysis of tomatine by Septoria lycopersici: a detoxification mechanism. Phytopathology 57:1358–1360
Basse CW, Bock K, Boller T (1992) Elicitors and suppressors of the defense response in tomato cells. Purification and characterization of glycopeptide elicitors and glycan suppressors generated by enzymatic cleavage of yeast invertase. J Biol Chem 267:10258–10265
Blancard D (2012) Tomato Diseases, 2nd edn. CRC Press, United States
Boller T (1995) Chemoperception of microbial signals in plant cells. Annu Rev Plant Physiol Plant Mol Biol 46:189–214
Boughton AJ, Hoover K, Felton GW (2006) Impact of chemical elicitor applications on greenhouse tomato plants and population growth of the green peach aphid, Myzus persicae. Entomol Exp Appl 120:175–188
Cao SN, Yuan Y, Qin YH, Zhang MZ, Figueiredo P, Li GH, Qin QM (2018) The pre-rRNA processing factor Nop53 regulates fungal development and pathogenesis via mediating production of reactive oxygen species. Environ Microbiol 20:1531–1549
Cárdenas PD, Sonawane PD, Heinig U, Jozwiak A, Panda S, Abebie B, Kazachkova Y, Pliner M, Unger T, Wolf D, Ofner I, Vilaprinyo E, Meir S, Davydov O, Gal-on A, Burdman S, Giri A, Zamir D, Scherf T, Szymanski J, Rogachev I, Aharoni A (2019) Pathways to defense metabolites and evading fruit bitterness in genus Solanum evolved through 2-oxoglutarate-dependent dioxygenases. Nat Commun 10:1–13
Chakraborty N, Ghosh S, Chandra S, Sengupta S, Acharya K (2016) Abiotic elicitors mediated elicitation of innate immunity in tomato: an ex vivo comparison. Physiol Mol Biol Plants 22:307–320
Chakraborty S, Kumar M (2020) Tomato leaf curl New Delhi virus (Geminiviridae). Ref Module Life Sci. https://doi.org/10.1016/B978-0-12-809633-8.21561-6
Chandra S, Chakraborty N, Dasgupta A, Sarkar J, Panda K, Acharya K (2015) Chitosan nanoparticles: a positive modulator of innate immune responses in plants. Sci Rep 5:1–14
Choudhary P, Aggarwal PR, Rana S, Nagarathnam R, Muthamilarasan M (2021) Molecular and metabolomic interventions for identifying potential bioactive molecules to mitigate diseases and their impacts on crop plants. Physiol Mol Plant Pathol 114:101624
Cui B, Pan Q, Clarke D, Villarreal MO, Umbreen S, Yuan B, Shan W, Jiang J, Loake GJ (2018) S-nitrosylation of the zinc finger protein SRG1 regulates plant immunity. Nat Commun 9:1–12
Eckardt NA (2017) The plant cell reviews plant immunity: receptor-like kinases, ROS-RLK crosstalk, quantitative resistance, and the growth/defense trade-off. Plant Cell 29:601–602
Fang LJ, Qin RL, Liu Z, Liu CR, Gai YP, Ji XL (2019) Expression and functional analysis of a PR-1 Gene, MuPR1, involved in disease resistance response in mulberry (Morus multicaulis). J Plant Interact 14:376–385
Fones H, Gurr S (2015) The impact of Septoria tritici blotch disease on wheat: an EU perspective. Fungal Genet Biol 79:3–7
Gilroy EM, Hein I, Van Der Hoorn R, Boevink PC, Venter E, McLellan H, Kaffarnik F, Hrubikova K, Shaw J, Holeva M, López EC, Borras-Hidalgo O, Pritchard L, Loake GJ, Lacomme C, Birch PRJ (2007) Involvement of cathepsin B in the plant disease resistance hypersensitive response. Plant J 52:1–13
Goupil P, Benouaret R, Charrier O, ter Halle A, Richard C, Eyheraguibel B, Thiery D, Ledoigt G (2012) Grape marc extract acts as elicitor of plant defence responses. Ecotoxicology 21:1541–1549
Hamed SM, Abd El-Rhman AA, Abdel-Raouf N, Ibraheem IBM (2018) Role of marine macroalgae in plant protection and improvement for sustainable agriculture technology. Beni-Suef Univ J Basic Appl Sci 7:104–110
Hammond RW (2017) Economic Significance of Viroids in Vegetable and Field Crops. In: Hadidi A, Flores R, Palukaitis P, Randles J (eds) Viroids and Satellites. Academic Press, San Diego, pp 5–13
Hastoy C, Le Bihan Z, Gaudin J, Cosson P, Rolin DS-LV (2019) First report of Septoria sp. infecting Stevia rebaudiana in France and screening of Stevia rebaudiana genotypes for host resistance. Plant Dis 103:1544–1550
Hirt H (2016) Aquaporins link ROS signaling to plant immunity. Plant Physiol 171:1540
Hu Z, Cools T, De Veylder L (2016) Mechanisms used by plants to cope with DNA damage. Annu Rev Plant Biol 67:439–462
Huang J, Gu L, Zhang Y, Yan T, Kong G, Kong L, Guo B, Qiu M, Wang Y, Jing M, Xing W, Ye W, Wu Z, Zhang Z, Zheng X, Gijzen M, Wang Y, Dong S (2017) An oomycete plant pathogen reprograms host pre-mRNA splicing to subvert immunity. Nat Commun 8:2051
Hussein NK, Sabr LJ, Lobo E, Booth J, Ariens E, Detchanamurthy S, Schenk PM (2020) Suppression of Arabidopsis mediator subunit-encoding MED18 confers broad resistance against DNA and RNA viruses while MED25 is required for virus defense. Front Plant Sci 11:1–12
Hwang IS, Hwang BK (2010) The pepper 9-lipoxygenase gene CaLOX1 functions in defense and cell death responses to microbial pathogens. Plant Physiol 152:948–967
Kapooria RG, Ndunguru J (1998) Rare symptoms and conidial variation in Septoria lycopersici in Zambia. Mycopathologia 142:101–105
Kariola T, Brader G, Li J, Palva ET (2005) Chlorophyllase 1, a damage control enzyme, affects the balance between defense pathways in plants. Plant Cell 17:282–294
Kavroulakis N, Ntougias S, Zervakis GI, Ehaliotis C, Haralampidis K, Papadopoulou KK (2007) Role of ethylene in the protection of tomato plants against soil-borne fungal pathogens conferred by an endophytic Fusarium solani strain. J Exp Bot 58:3853–3864
Kazan K, Manners JM (2009) Linking development to defense: auxin in plant-pathogen interactions. Trends Plant Sci 14:373–382
Kim MG, Da Cunha L, McFall AJ, Belkhadir Y, DebRoy S, Dangl JL, Mackey D (2005) Two pseudomonas syringae type III effectors inhibit RIN4-regulated basal defense in arabidopsis. Cell 121:749–759
Lee S, Fu F, Xu S, Lee SY, Yun DJ, Mengiste T (2016) Global regulation of plant immunity by histone lysine methyl transferases. Plant Cell 28:1640–1661
Li TG, Wang BL, Yin CM, Zhang DD, Wang D, Song J, Zhou L, Kong ZQ, Klosterman SJ, Li JJ, Adamu S, Liu TL, Subbarao KV, Chen JY, Dai XF (2019) The Gossypium hirsutum TIR-NBS-LRR gene GhDSC1 mediates resistance against verticillium wilt. Mol Plant Pathol 20:857–876
Li X, Fan S, Hu W, Liu G, Wei Y, He C, Shi H (2017) Two Cassava basic leucine zipper (bZIP) transcription factors (MebZIP3 and MebZIP5) confer disease resistance against cassava bacterial Blight. Front Plant Sci 8:2110
Lin NC, Martin GB (2007) Pto- and Prf-mediated recognition of AvrPto and AvrPtoB restricts the ability of diverse Pseudomonas syringae pathovars to infect tomato. Mol Plant-Microbe Interact 20:806–815
Liu F, Xu Y, Zhou L, Ali A, Jiang H, Zhu S, Li X (2019) DNA repair gene ZmRAd51A improves rice and arabidopsis resistance to disease. Int J Mol Sci 20:807
Liu H, Dong S, Gu F, Liu W, Yang G, Huang M, Xiao W, Liu Y, Guo T, Wang H, Chen Z, Wang J (2017) NBS-LRR protein Pik-H4 interacts with OsBIHD1 to balance rice blast resistance and growth by coordinating ethylene-brassinosteroid pathway. Front Plant Sci 8:1–13
Liu S, Bartnikas LM, Volko SM, Ausubel FM, Tang D (2016) Mutation of the glucosinolate biosynthesis enzyme cytochrome P450 83A1 monooxygenase increases camalexin accumulation and powdery mildew resistance. Front Plant Sci 7:1–13
Lv T, Li X, Fan T, Luo H, Xie C, Zhou Y, Tian CE (2019) The calmodulin-binding protein IQM1 interacts with CATALASE2 to affect pathogen defense. Plant Physiol 181:1314–1327
Mandal S, Kar I, Mukherjee AK, Acharya P (2013) Elicitor-induced defense responses in Solanum lycopersicum against Ralstonia solanacearum. Sci World J 2013:561056
Mani SD, Nagarathnam R (2018) Sulfated polysaccharide from Kappaphycus alvarezii (Doty) Doty ex P.C. Silva primes defense responses against anthracnose disease of Capsicum annuum Linn. Algal Res 32:121–130
Martin-Hernandez AM, Dufresne M, Hugouvieux V, Melton R, Osbourn A (2000) Effects of targeted replacement of the tomatinase gene on the interaction of Septoria lycopersici with tomato plants. Mol Plant-Microbe Interact 13:1301–1311
Melton RE, Flegg LM, Brown JK, Oliver RP, Daniels MJ, Osbourn AE (1998) Heterologous expression of Septoria lycopersici tomatinase in Cladosporium fulvum: Effects on compatible and incompatible interactions with tomato seedlings. Mol Plant-Microbe Interact 11:228–236
Misra RC, Sandeep KM, Kumar S, Ghosh S (2016) A thaumatin-like protein of Ocimum basilicum confers tolerance to fungal pathogen and abiotic stress in transgenic Arabidopsis. Sci Rep 6:1–14
Müller M, Munné-Bosch S (2015) Ethylene response factors: a key regulatory hub in hormone and stress signaling. Plant Physiol 169:32–41
Muthamilarasan M, Prasad M (2013) Plant innate immunity: An updated insight into defense mechanism. J Biosci 38:433–449
Nandety RS, Caplan JL, Cavanaugh K, Perroud B, Wroblewski T, Michelmore RW, Meyers BC (2013) The role of TIR-NBS and TIR-X Proteins in plant basal defense responses. Plant Physiol 162:1459–1472
Osbourn A, Bowyer P, Lunness P, Clarke B, Daniels M (1995) Fungal pathogens of oat roots and tomato leaves employ closely related enzymes to detoxify different host plant saponins. Mol Plant-Microbe Interact 8:971–978
Pandey S, Muthamilarasan M, Sharma N, Chaudhry V, Dulani P, Shweta S, Jha S, Mathur S, Prasad M (2019) Characterization of DEAD-box family of RNA helicases in tomato provides insights into their roles in biotic and abiotic stresses. Environ Exp Bot 158:107–116
Pandey S, Sahu PP, Kulshreshtha R, Prasad M (2018) Role of host transcription factors in modulating defense response during plant-virus interaction. In: Patil BL (ed) Genes, Genetics and Transgenics for Virus Resistance in Plants. Caister Academic Press, U.K., pp 25–54
Panthee D, Chen F (2010) Genomics of fungal disease resistance in tomato. Curr Genomics 11:30–39
Park S, Gupta R, Krishna R, Kim ST, Lee DY, Hwang DJ, Bae SC, Ahn IP (2016) Proteome analysis of disease resistance against Ralstonia solanacearum in potato cultivar CT206-10. Plant Pathol J 32:25–32
Parker SK, Nutter FW, Gleason ML (1997) Directional spread of Septoria leaf spot in tomato rows. Plant Dis 81:272–276
Paudel S, Rajotte EG, Felton GW (2014) Benefits and costs of tomato seed treatment with plant defense elicitors for insect resistance. Arthropod Plant Interact 8:539–545
Qi J, Wang J, Gong Z, Zhou JM (2017) Apoplastic ROS signaling in plant immunity. Curr Opin Plant Biol 38:92–100
Qiu Y, Xi J, Du L, Poovaiah BW (2012) The function of calreticulin in plant immunity: new discoveries for an old protein. Plant Signal Behav 7:907–910
Sangha JS, Ravichandran S, Prithiviraj K, Critchley AT, Prithiviraj B (2010) Sulfated macroalgal polysaccharides λ-carrageenan and ι-carrageenan differentially alter Arabidopsis thaliana resistance to Sclerotinia sclerotiorum. Physiol Mol Plant Pathol 75:38–45
Schreinemachers P, Simmons EB, Wopereis MCS (2018) Tapping the economic and nutritional power of vegetables. Global Food Security 16:36–45
Singh VK, Singh AK, Kumar A (2017) Disease management of tomato through PGPB: current trends and future perspective. 3 Biotech 7:255
Song G, Walley JW (2016) Dynamic protein acetylation in plant-pathogen interactions. Front Plant Sci 7:1–6
Stadnik MJ, de Freitas MB (2014) Algal polysaccharides as source of plant resistance inducers. Trop Plant Pathol 39:111–118
Thaler JS, Owen B, Higgins VJ (2004) The role of the jasmonate response in plant susceptibility to diverse pathogens with a range of lifestyles. Plant Physiol 135:530–538
van den Burg HA, Tsitsigiannis DI, Rowland O, Lo J, Rallapalli G, Maclean D, Takken FL, Jones JD (2008) The F-box protein ACRE189/ACIF1 regulates cell death and defense responses activated during pathogen recognition in tobacco and tomato. Plant Cell 20:697–719
Wei Y, Liu W, Hu W, Liu G, Wu C, Liu W, Zeng H, He C, Shi H (2017) Genome-wide analysis of autophagy-related genes in banana highlights MaATG8s in cell death and autophagy in immune response to Fusarium wilt. Plant Cell Rep 36:1237–1250
Xu HY, Zhang C, Li ZC, Wang ZR, Jiang XX, Shi YF, Tian SN, Braun E, Mei Y, Qiu WL, Li S, Wang B, Xu J, Navarre D, Ren D, Cheng N, Nakata PA, Graham MA, Whitham SA, Liu JZ (2018a) The MAPK kinase kinase GMMEKK1 regulates cell death and defense responses. Plant Physiol 178:907–922
Xu Y, Liu F, Zhu S, Li X (2018b) The Maize NBS-LRR Gene ZmNBS25 enhances disease resistance in rice and Arabidopsis. Front Plant Sci 9:1033
Xun H, Yang X, He H, Wang M, Guo P, Wang Y, Pang J, Dong Y, Feng X, Wang S, Liu B (2019) Over-expression of GmKR3, a TIR–NBS–LRR type R gene, confers resistance to multiple viruses in soybean. Plant Mol Biol 99:95–111
Yu J, Chai C, Ai G, Jia Y, Liu W, Zhang X, Bai T, Dou D (2020) A Nicotiana benthamiana AP2/ERF transcription factor confers resistance to Phytophthora parasitica. Phytopathol Res 2:4
Zhang G, Yan X, Zhang S, Zhu Y, Zhang X, Qiao H, van Nocker S, Li Z, Wang X (2019) The jasmonate-ZIM domain gene VqJAZ4 from the Chinese wild grape Vitis quinquangularis improves resistance to powdery mildew in Arabidopsis thaliana. Plant Physiol Biochem 143:329–339
Zhou B, Zeng L (2018) The tomato U-box type E3 ligase PUB13 acts with group III ubiquitin E2 enzymes to modulate FLS2-mediated immune signaling. Front Plant Sci 9:1–14
Acknowledgements
The authors thank The Director, CAS in Botany, University of Madras, for providing the laboratory facility. The corresponding author thank Department of Science and Technology, Science and Engineering Research Board (DST-SERB) for financial support.
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The funding was provided by Department of Science and Technology, Science and Engineering Research Board, Govt. of India (File No.: ECR/2016/000165).
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RN conceived and designed the experiments. SDM, SP, MG performed the experiments. MM, RN analyzed the data. MM, RN wrote the manuscript. All authors have read and approved the final version of this manuscript.
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Mani, S.D., Pandey, S., Govindan, M. et al. Transcriptome dynamics underlying elicitor-induced defense responses against Septoria leaf spot disease of tomato (Solanum lycopersicum L.). Physiol Mol Biol Plants 27, 873–888 (2021). https://doi.org/10.1007/s12298-021-00970-y
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DOI: https://doi.org/10.1007/s12298-021-00970-y