Abstract
Tomato leaf curl Bangalore virus (ToLCBaV) is one of the most important plant viruses. The infection causes substantial yield losses in tomato crop. The current viral disease management is based mainly on introgression of Ty locus into new tomato cultivars. Unfortunately, strains of the leaf curl virus have been evolving and are breaking Ty based tolerance in tomato. In this study, the defence response to ToLCBaV infection has been compared between contrasting tomato genotypes, resistant line (IIHR 2611; without any known Ty markers) and the susceptible line (IIHR 2843). We carried out comparative transcriptome profiling, and gene expression analysis in an effort to identify gene networks that are associated with a novel ToLCBaV resistance. A total of 22,320 genes were examined to identify differentially expressed genes (DEGs). We found that 329 genes of them were expressed significantly and differentially between ToLBaV-infected samples of both IIHR 2611 and IIHR 2843. A good number of DEGs were related to defence response, photosynthesis, response to wounding, toxin catabolic process, glutathione metabolic process, regulation of transcription DNA-template, transcription factor activity, and sequence-specific DNA binding. A few selected genes such as, nudix hydrolase 8, MIK 2-like, RING-H2 finger protein ATL2-like, MAPKKK 18-like, EDR-2, SAG 21 wound-induced basic protein, GRXC6 and P4 were validated using qPCR. The pattern of gene expression was significantly different in resistant and susceptible plants during disease progression. Both positive and negative regulators of virus resistance were found in the present study. These findings will facilitate breeding and genetic engineering efforts to incorporate novel sources of ToLCBaV resistance in tomatoes.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Al-Shihi AA, Hanson P, Al-Sadi AM, Al-Yahyai RA, Briddon RW, Deadman M, Shahid MS (2018) Evaluation of tomato inbred lines for resistance to the tomato yellow leaf curl disease complex in Oman. Crop Prot 110:91–98. https://doi.org/10.1016/j.cropro.2018.04.001
Barbieri M, Acciarri N, Sabatini E, Sardo L, Accotto GP, Pecchioni N (2010) Introgression of resistance to two Mediterranean virus species causing tomato yellow leaf curl into a valuable traditional tomato variety. J Plant Pathol 92:485–493
Camara M, Mbaye AA, Noba K, Samb PI, Diao S, Cilas C (2013) Field screening of tomato genotypes for resistance to tomato yellow leaf curl virus (TYLCV) disease in Senegal. Crop Prot 44:59–65. https://doi.org/10.1016/j.cropro.2012.10.007
Chen T, Lv Y, Zhao T, Li N, Yang Y, Yu W, He X, Liu T, Zhang B (2013) Comparative transcriptome profiling of a resistant vs. susceptible tomato (Solanum lycopersicum) cultivar in response to infection by tomato yellow leaf curl virus. PLoS ONE 8(11):e80816. https://doi.org/10.1371/journal.pone.0080816
Chowda-Reddy RV, Kirankumar M, Seal SE, Muniyappa V, Valand GB, Govindappa MR, Colvin J (2012) Bemisia tabaci phylogenetic groups in India and the relative transmission efficacy of tomato leaf curl Bangalore virus by an indigenous and an exotic population. J Integr Agric 11(2):235–248. https://doi.org/10.1016/S2095-3119(12)60008-2
Coleman AD, Maroschek J, Raasch L, Takken FL, Ranf S, Huckelhoven R (2021) The Arabidopsis leucine rich repeat receptor like kinase MIK2 is a crucial component of early immune responses to a fungal derived elicitor. New Phytol 229(6):3453–3466. https://doi.org/10.1111/nph.17122
Dennis G, Sherman BT, Hosack DA, Yang J, Gao W, Lane HC, Lempicki RA (2003) DAVID: database for annotation, visualization, and integrated discovery. Genome Biol 4:1–3
Fonseca JP, Dong X (2014) Functional characterization of a nudix hydrolase AtNUDX8 upon pathogen attack indicates a positive role in plant immune responses. PLoS ONE 9(12):114–119. https://doi.org/10.1371/journal.pone.0114119
Garcia-Cano E, Resende RO, Boiteux LS, Giordano LB, Fernandez-Munoz R, Moriones E (2008) Phenotypic expression, stability, and inheritance of a recessive resistance to monopartite begomoviruses associated with tomato yellow leaf curl disease in tomato. Phytopathology 98(5):618–627. https://doi.org/10.1094/PHYTO-98-5-0618
Gelbart D, Chen L, Alon T, Dobrinin S, Levin I, Lapidot M (2020) The recent association of a DNA betasatellite with tomato yellow leaf curl virus in Israel—a new threat to tomato production. Crop Protect 128:104995. https://doi.org/10.1016/j.cropro.2019.104995
Hanssen IM, Lapidot M, Thomma BP (2010) Emerging viral diseases of tomato crops. Mol Plant Microbe Interact 23(5):539–548. https://doi.org/10.1094/MPMI-23-5-0539
Heim MA, Jakoby M, Werber M, Martin C, Weisshaar B, Bailey PC (2003) The basic helix–loop–helix transcription factor family in plants: a genome-wide study of protein structure and functional diversity. Mol Bio Evol 20(5):735–747. https://doi.org/10.1093/molbev/msg088
Ji Y, Scott JW, Schuster DJ, Maxwell DP (2009) Molecular mapping of Ty-4, a new tomato yellow leaf curl virus resistance locus on chromosome 3 of tomato. J Am Soc Hortic Sci 134(2):281–288. https://doi.org/10.21273/JASHS.134.2.281
Kang WH, Yeom SI (2018) Genome-wide identification, classification, and expression analysis of the receptor-like protein family in tomato. Plant Pathol J 34(5):435–444. https://doi.org/10.5423/PPJ.OA.02.2018.0032
Kaushal A, Sadashiva AT, Krishna Reddy M, Srinivasa Rao E, Singh TH, Sriram S, Dhananjay MV, Venugopalan R, Ravishankar KV (2020) Assessment of the effectiveness of Ty genes in tomato against Tomato leaf curl Bangalore virus. Plant Pathol 69(9):1777–1786. https://doi.org/10.1111/ppa.13260
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12(4):357–360
Kwon J, Kasai A, Maoka T, Masuta C, Sano T, Nakahara KS (2020) RNA silencing-related genes contribute to tolerance of infection with potato virus X and Y in a susceptible tomato plant. Virol J 17(1):1–13. https://doi.org/10.1186/s12985-020-01414-x
Lacerda ALM, Fonseca LN, Blawid R, Boiteux LS, Ribeiro SG, Brasileiro ACM (2015) Reference gene selection for qPCR analysis in tomato-bipartite begomovirus interaction and validation in additional tomato-virus pathosystems. PLoS ONE 10(8):e0136820. https://doi.org/10.1371/journal.pone.0136820
Lex A, Gehlenborg N, Strobelt H, Vuillemot R, Pfister H (2014) UpSet: visualization of intersecting sets. IEEE Trans vis Comput Graph 20:1983–1992. https://doi.org/10.1109/TVCG.2014.2346248
Li JF, Li L, Sheen J (2010) Protocol: a rapid and economical procedure for purification of plasmid or plant DNA with diverse applications in plant biology. Plant Methods 6(1):1–8. https://doi.org/10.1186/1746-4811-6-1
Li T, Huang Y, Xu ZS, Wang F, Xiong AS (2019) Salicylic acid-induced differential resistance to the tomato yellow leaf curl virus among resistant and susceptible tomato cultivars. BMC Plant Biol 19(1):1–14. https://doi.org/10.1186/s12870-019-1784-0
Liebrand TW, Van den Burg HA, Joosten MH (2014) Two for all: receptor-associated kinases SOBIR1 and BAK1. Trends Plant Sci 19(2):123–132. https://doi.org/10.1016/j.tplants.2013.10.003
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408. https://doi.org/10.1006/meth.2001.1262
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15(e550):8. https://doi.org/10.1186/s13059-014-0550-8
Matsuoka D, Yasufuku T, Furuya T, Nanmori T (2015) An abscisic acid inducible Arabidopsis MAPKKK, MAPKKK18 regulates leaf senescence via its kinase activity. Plant Mol Biol 87(6):565–575. https://doi.org/10.1007/s11103-015-0295-0
Miao Y, Zentgraf U (2010) A HECT E3 ubiquitin ligase negatively regulates Arabidopsis leaf senescence through degradation of the transcription factor WRKY53. Plant J 63(2):179–188. https://doi.org/10.1111/j.1365-313X.2010.04233.x
Miao Y, Laun T, Zimmermann P, Zentgraf U (2004) Targets of the WRKY53 transcription factor and its role during leaf senescence in Arabidopsis. Plant Mol Biol 55(6):853–867
Mowla SB, Cuypers A, Driscoll SP, Kiddle G, Thomson J, Foyer CH, Theodoulou FL (2006) Yeast complementation reveals a role for an Arabidopsis thaliana late embryogenesis abundant (LEA) like protein in oxidative stress tolerance. Plant J 48(5):743–756. https://doi.org/10.1111/j.1365-313X.2006.02911.x
Ohnishi J, Yamaguchi H, Saito A (2016) Analysis of the Mild strain of tomato yellow leaf curl virus, which overcomes Ty-2 gene-mediated resistance in tomato line H24. Arch Virol 161(8):2207–2217. https://doi.org/10.1007/s00705-016-2898-4
Reddy MS, Boucher O, Balkanski Y, Schulz M (2005a) Aerosol optical depths and direct radiative perturbations by species and source type. Geophys Res Lett. https://doi.org/10.1029/2004GL021743
Reddy RC, Colvin J, Muniyappa V, Seal S (2005b) Diversity and distribution of begomoviruses infecting tomato in India. Arch Virol 150:845–867. https://doi.org/10.1007/s00705-004-0486-5
Riechmann JL, Heard J, Martin G, Reuber L, Jiang CZ, Keddie J, Adam L, Pineda O, Ratcliffe OJ, Samaha RR, Creelman R (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290(5499):2105–2110. https://doi.org/10.1126/science.290.5499.2105
Ronde D, Butterbach P, Kormelink R (2014) Dominant resistance against plant viruses. Front Plant Sci 5:307. https://doi.org/10.3389/fpls.2014.00307
Sadashiva AT, Hanson P, Reddy MK, Ravishankar KV, Prasad M, Prasanna HC, Reddy KM, Singh TH, Saritha RK, Hussain Z, Mythili JB (2017) Breeding tomato (Solanum lycopersicum L.) for resistance to biotic and abiotic stresses. Soc Promot Hortic 12(2):91–105. http://krishi.icar.gov.in/jspui/handle/123456789/23810
Sade D, Sade N, Brotman Y, Czosnek H (2020) Tomato yellow leaf curl virus (TYLCV)-resistant tomatoes share molecular mechanisms sustaining resistance with their wild progenitor Solanum habrochaites but not with TYLCV-susceptible tomatoes. Plant Sci 295:e110439. https://doi.org/10.1016/j.plantsci.2020.110439
Salinas-Mondragon RE, Garciduenas-Pina C, Guzman P (1999) Early elicitor induction in members of a novel multigene family coding for highly related RING-H2 proteins in Arabidopsis thaliana. Plant Mol Biol 40(4):579–590
Salleh FM, Evans K, Goodall B, Machin H, Mowla SB, Mur LA, Runions J, Theodoulou FL, Foyer CH, Rogers HJ (2012) A novel function for a redox related LEA protein (SAG21/AtLEA5) in root development and biotic stress responses. Plant Cell Environ 35(2):418–429. https://doi.org/10.1111/j.1365-3040.2011.02394.x
Santos AA, Lopes KV, Apfata JA, Fontes EP (2010) NSP-interacting kinase, NIK: a transducer of plant defence signalling. J Exp Bot 61:3839–3845. https://doi.org/10.1093/jxb/erq219
Seo JK, Kim MK, Kwak HR, Choi HS, Nam M, Choe J, Choi B, Han SJ, Kang JH, Jung C (2018) Molecular dissection of distinct symptoms induced by tomato chlorosis virus and tomato yellow leaf curl virus based on comparative transcriptome analysis. Virology 516:1–20. https://doi.org/10.1016/j.virol.2018.01.001
Singh R, Rai N, Singh M, Singh S, Srivastava K (2015) Selection of tomato genotypes resistant to tomato leaf curl virus disease using biochemical and physiological markers. J Agric Sci 153(4):646–655. https://doi.org/10.1017/S0021859614000616
Song S, Qi T, Fan M, Zhang X, Gao H, Huang H, Wu D, Guo H, Xie D (2013) The bHLH subgroup IIId factors negatively regulate jasmonate-mediated plant defense and development. PLoS Genet 9(7):e1003653. https://doi.org/10.1371/journal.pgen.1003653
Steinbrenner AD, Munoz-Amatriain M, Chaparro AF, Aguilar-Venegas JM, Lo S, Okuda S, Glauser G, Dongiovanni J, Shi D, Hall M, Crubaugh D (2020) A receptor-like protein mediates plant immune responses to herbivore-associated molecular patterns. Proc Natl Acad Sci 117(49):31510–31518. https://doi.org/10.1073/pnas.2018415117
Verlaan MG, Hutton SF, Ibrahem RM, Kormelink R, Visser RG, Scott JW, Edwards JD, Bai Y (2013) The tomato yellow leaf curl virus resistance genes Ty-1 and Ty-3 are allelic and code for DFDGD-class RNA-dependent RNA polymerases. PLoS Genet 9(3):e1003399. https://doi.org/10.1371/journal.pgen.1003399
Vorwerk S, Schiff C, Santamaria M, Koh S, Nishimura M, Vogel J, Somerville C, Somerville S (2007) EDR2 negatively regulates salicylic acid-based defenses and cell death during powdery mildew infections of Arabidopsis thaliana. BMC Plant Biol 7(1):1–14. http://www.biomedcentral.com/1471-2229/7/35
Walter W, Sanchez-Cabo F, Ricote M (2015) GOplot: an R package for visually combining expression data with functional analysis. Bioinformatics 31(17):2912–2914. https://doi.org/10.1093/bioinformatics/btv300
Wang Y, Jiang J, Zhao L, Zhou R, Yu W, Zhao T (2018) Application of whole genome resequencing in mapping of a tomato yellow leaf curl virus resistance gene. Sci Rep 8(1):1–11. https://doi.org/10.1186/s12870-018-1616-7
Yamaguchi H, Ohnishi J, Saito A, Ohyama A, Nunome T, Miyatake K, Fukuoka H (2018) An NB-LRR gene, TYNBS1, is responsible for resistance mediated by the Ty-2 Begomovirus resistance locus of tomato. Theor Appl Genet 131(6):1345–1362. https://doi.org/10.1007/s00122-018-3082-x
Yang X, Caro M, Hutton SF, Scott JW, Guo Y, Wang X, Rashid MH, Szinay D, de Jong H, Visser RG, Bai Y (2014) Fine mapping of the tomato yellow leaf curl virus resistance gene Ty-2 on chromosome 11 of tomato. Mol Breed 34(2):749–760. https://doi.org/10.1007/s11032-014-0072-9
Yu G, Wang LG, Han Y, He QY, Huang DW, Sherman BT, Lempicki RA (2009) Systematic and integrative analysis of large gene lists using DAVID Bioinformatics Resources. Nat Protoc 4(1):44–57
Zhao W, Zhou Y, Zhou X, Wang X, Ji Y (2021) Host GRXC6 restricts tomato yellow leaf curl virus infection by inhibiting the nuclear export of the V2 protein. PLoS Pathog. 17(8):e1009844. https://doi.org/10.1371/journal.ppat.1009844
Acknowledgements
BC is grateful for the PhD fellowship from the DBT–JRF Programme. KVR, ATS and KRM are thankful for the financial support received from DBT New Delhi, India, through the project titled “Introgression of Bogomovirus resistance genes in Tomato (Solanum lycopersicus L.) using MAS and genomic approach”.
Funding
Received financial support from Department of Biotechnology (DBT)-JRF fellowship programme (Award no. DBT/JRF/BET-17/I/2017/AL/297), and DBT-Government of India, New Delhi, India, through the project titled “Introgression of Bogomovirus resistance genes in Tomato (Solanum lycopersicus L.) using MAS and genomic approach”.
Author information
Authors and Affiliations
Contributions
BC: investigation; methodology; data curation; formal analysis; original draft; writing—review and editing. GM: data curation; formal analysis. ATS: conceptualization; funding acquisition; project administration; resources; review and editing. MKR: conceptualization; funding acquisition; project administration. KVR: conceptualization; funding acquisition; project administration; resources; investigation; methodology; validation; visualization; original draft; writing—review and editing; supervision.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Chidambara, B., Muthaiah, G., Sadashiva, A.T. et al. Transcriptome analysis during ToLCBaV disease development in contrasting tomato genotypes. 3 Biotech 13, 226 (2023). https://doi.org/10.1007/s13205-023-03629-5
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s13205-023-03629-5