High throughput sequencing unravels tomato-pathogen interactions towards a sustainable plant breeding

Abstract

Tomato (Solanum lycopersicum) is one of the most economically important vegetables throughout the world. It is one of the best studied cultivated dicotyledonous plants, often used as a model system for plant research into classical genetics, cytogenetics, molecular genetics, and molecular biology. Tomato plants are affected by different pathogens such as viruses, viroids, fungi, oomycetes, bacteria, and nematodes, that reduce yield and affect product quality. The study of tomato as a plant-pathogen system helps to accelerate the discovery and understanding of the molecular mechanisms underlying disease resistance and offers the opportunity of improving the yield and quality of their edible products. The use of functional genomics has contributed to this purpose through both traditional and recently developed techniques, that allow the identification of plant key functional genes in susceptible and resistant responses, and the understanding of the molecular basis of compatible interactions during pathogen attack. Next-generation sequencing technologies (NGS), which produce massive quantities of sequencing data, have greatly accelerated research in biological sciences and offer great opportunities to better understand the molecular networks of plant–pathogen interactions. In this review, we summarize important research that used high-throughput RNA-seq technology to obtain transcriptome changes in tomato plants in response to a wide range of pathogens such as viruses, fungi, bacteria, oomycetes, and nematodes. These findings will facilitate genetic engineering efforts to incorporate new sources of resistance in tomato for protection against pathogens and are of major importance for sustainable plant-disease management, namely the ones relying on the plant’s innate immune mechanisms in view of plant breeding.

References

[1] Zhang, Y. et al. ShORR-1, a novel tomato gene, confers enhanced host resistance to oidium neolycopersici. Front. Plant Sci. 10, 1-15 (2019).

[2] Jones, J. D. G. & Dangl, J. L. The plant immune system. Nature 444, 323-329 (2006).

[3] Dodds, P. N. & Rathjen, J. P. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11, 539-548 (2010).

[4] Peng, Y., van Wersch, R. & Zhang, Y. Convergent and divergent signaling in PAMP-triggered immunity and effector-triggered immunity. Mol. Plant Microbe. Interact. 31, 403-409 (2017).

[5] Zipfel, C. Plant pattern-recognition receptors. Trends Immunol. 35, 345-351 (2014).

[6] Decreux, A. & Messiaen, J. Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol. 46, 268-278 (2005).

[7] Meng, X. & Zhang, S. MAPK cascades in plant disease resistance signaling. Annu. Rev. Phytopathol. 51, 245-266 (2013).

[8] Zhang, H., Gao, Z., Zheng, X. & Zhang, Z. The role of G-proteins in plant immunity. Plant Signal Behav. 7, 1284-1288 (2012).

[9] Lecourieux, D., Ranjeva, R. & Pugin, A. Calcium in plant defence-signalling pathways. N. Phytol. 171, 249-269 (2006).

[10] Marino, D., Peeters, N. & Rivas, S. Ubiquitination during plant immune signaling. Plant Physiol. 160, 15-27 (2012).

[11] Robert-Seilaniantz, A., Grant, M. & Jones, J. D. G. Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu. Rev. Phytopathol. 49, 317-343 (2011).

[12] Juge, N. Plant protein inhibitors of cell wall degrading enzymes. Trends Plant Sci. 11, 359-367 (2006).

[13] van Loon, L. C., Rep, M. & Pieterse, C. M. J. Significance of inducible defense-related proteins in infected plants. Annu Rev. Phytopathol. 44, 135-162 (2006).

[14] Andersen, E. J., Ali, S., Byamukama, E., Yen, Y. & Nepal, M. P. Disease resistance mechanisms in plants. Genes 9, 339 (2018).

[15] Gassmann, W. & Bhattacharjee, S. Effector-triggered immunity signaling: From gene-for-gene pathways to protein-protein interaction networks. Mol. Plant Microbe. Interact. 25, 862-868 (2012).

[16] Rosli, H. G. & Martin, G. B. Functional genomics of tomato for the study of plant immunity. Brief. Funct. Genomics 14, 291-301 (2015).

[17] Dangl, J. L., Horvath, D. M. & Staskawicz, B. J. Pivoting the plant immune system from dissection to deployment. Science 341, 746-751 (2013).

[18] Eulgem, T. Regulation of the Arabidopsis defense transcriptome. Trends Plant Sci. 10, 71-78 (2005).

[19] Singh V. K., Singh A. K., Singh S. & Singh B. D. Next-Generation Sequencing (NGS) Tools and Impact in Plant Breeding BT - Advances in Plant Breeding Strategies: Breeding, Biotechnology and Molecular Tools.In: Al-Khayri J. M., Jain S. M., Johnson D. V. (eds). Springer International Publishing: Cham, 2015, 563-612.

[20] Jones J. B., Zitter T. A., Momol T. M., Miller S. A. Compendium of Tomato Diseases and Pests, Second Edition. (The American Phytopathological Society, 2016)

[21] Ji Y., Scott JW . Tomato. In: Singh R. J. (ed). Genetic Resources, Chromosome Engineering, and Crop Improvement Series IV: Vegetable Crops. 2006, 59-113.

[22] Jáquez-Gutiérrez, M. et al. Phenotypic and genetic characterization of tomato mutants provides new insights into leaf development and its relationship to agronomic traits. BMC Plant Biol. 19, 141 (2019).

[23] Sun, S. et al. Agrobacterium-mediated transformation of tomato (Lycopersicon esculentum L. cv. Hezuo 908) with improved efficiency . Biotechnol. Biotechnol. Equip. 29, 861-868 (2015).

[24] Paduchuri P., Gohokar S., Thamke B., Subhas M. Transgenic tomatoes - a review. 2014.

[25] Shwartz, I., Levy, M., Ori, N. & Bar, M. Hormones in tomato leaf development. Dev. Biol. 419, 132-142 (2016).

[26] Almeida, J. et al. Genetic dissection of vitamin e biosynthesis in tomato. J. Exp. Bot. 62, 3781-3798 (2011).

[27] Stikić, R., Jovanović, Z., Vucelić-Radović, B., Marjanović, M. & Savić, S. Tomato: a model species for fruit growth and development studies. Bot. Serbica 39, 95-102 (2015).

[28] Devran, Z., Kahveci, E., Hong, Y., Studholme, D. J. & Tör, M. Identifying molecular markers suitable for Frl selection in tomato breeding. Theor. Appl. Genet. 131, 2099-2105 (2018).

[29] Causse M. & Grandillo S. Gene Mapping in Tomato BT - The Tomato Genome. In: Causse M., Giovannoni J., Bouzayen M., Zouine M. (eds). Springer Berlin Heidelberg: Berlin, Heidelberg, 2016, 23-37.

[30] Brekke, T. D., Stroud, J. A., Shaw, D. S., Crawford, S. & Steele, K. A. QTL mapping in salad tomatoes. Euphytica 215, 115 (2019).

[31] Liu, X., Geng, X., Zhang, H., Shen, H. & Yang, W. Association and genetic identification of loci for four fruit traits in tomato using InDel markers. Front. Plant Sci. 8, 1-14 (2017).

[32] Matsukura, C. et al. Comprehensive resources for tomato functional genomics based on the miniature model tomato micro-tom. Curr. Genomics 9, 436-443 (2008).

[33] Sato, S. et al. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485, 635-641 (2012).

[34] Van der Hoeven, R., Ronning, C., Giovannoni, J., Martin, G. & Tanksley, S. Deductions about the number, organization, and evolution of genes in the tomato genome based on analysis of a large expressed sequence tag collection and selective genomic sequencing. Plant Cell 14, 1441-1456 (2002).

[35] Barone, A. et al. Structural and functional genomics of tomato. Int. J. Plant Genomics 2008, 820274 (2008).

[36] Michaelson, M. J., Price, H. J., Ellison, J. R. & Johnston, J. S. Comparison of plant DNA contents determined by Feulgen microspectrophotometry and laser flow cytometry. Am. J. Bot. 78, 183-188 (1991).

[37] Gerszberg, A., Hnatuszko-Konka, K., Kowalczyk, T. & Kononowicz, A. K. Tomato (Solanum lycopersicum L.) in the service of biotechnology . Plant Cell Tissue Organ Cult. 120, 881-902 (2015).

[38] Bai, Y. & Lindhout, P. Domestication and breeding of tomatoes: what have we gained and what can we gain in the future? Ann. Bot. 100, 1085-1094 (2007).

[39] Singh, V. K., Singh, A. K. & Kumar, A. Disease management of tomato through PGPB: current trends and future perspective. 3 Biotech 7, 1-10 (2017).

[40] Arie, T., Takahashi, H., Kodama, M. & Teraoka, T. Tomato as a model plant for plant-pathogen interactions. Plant Biotechnol. 24, 135-147 (2007).

[41] Ercolano, M. R., Sanseverino, W., Carli, P., Ferriello, F. & Frusciante, L. Genetic and genomic approaches for R-gene mediated disease resistance in tomato: Retrospects and prospects. Plant Cell Rep. 31, 973-985 (2012).

[42] Meena, M. & Zehra, A. Food science and nutrition technology tomato: a model plant to study plant-pathogen interactions. Food Sci. Nutr. Technol. 4, 1-6 (2019).

[43] Schouten, H. J. et al. Breeding has increased the diversity of cultivated tomato in the Netherlands. Front Plant Sci. 10, 1606 (2019).

[44] Zsögön A., et al. De novo domestication of wild tomato using genome editing. Nat. Biotechnol. 36, 1211-1216 (2018).

[45] Salmeron, J. et al. Genetic dissection of bacterial speck disease resistance in tomato. Euphytica 79, 195-200 (1994).

[46] Milligan, S. B. et al. The root knot nematode resistance gene Mi from tomato is a member of the Leucine zipper, nucleotide binding, Leucine-rich repeat family of plant genes. Plant Cell 10, 1307-1319 (1998).

[47] Gassmann, W. & Bhattacharjee, S. Effector-triggered immunity signaling: from gene-for-gene pathways to protein-protein interaction networks. Mol. Plant Microbe Interact. 25, 862-868 (2012).

[48] Ciuffo, M., Finetti-Sialer, M. M., Gallitelli, D. & Turina, M. First report in Italy of a resistance-breaking strain of tomato spotted wilt virus infecting tomato cultivars carrying the Sw5 resistance gene. Plant Pathol. 54, 564 (2005).

[49] Saidi, M. & Warade, S. D. Tomato breeding for resistance to tomato spotted wilt virus (tswv): an overview of conventional and molecular approaches. Czech J. Genet. Plant Breed. 44, 83-92 (2008).

[50] Stevens, M. R., Scott, S. J. & Gergerich, R. C. Inheritance of a gene for resistance to tomato spotted wilt virus (TSWV) from Lycopersicon peruvianum Mill. Euphytica 59, 9-17 (1991).

[51] R C., HS A. Resistance-gene-mediated defense responses against biotic stresses in the crop model plant tomato. J. Plant Pathol. Microbiol. 8, 404 (2017).

[52] Chen, T. et al. 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, 4-6 (2013).

[53] Behare, J., Laterrot, H. & Safatti, M. Restriction fragment length polymorphism mapping of Stemphylium resistance gene in tomato. Mol. Plant Microbe. Interact. 4, 489-492 (1991).

[54] Simons, G. et al. Dissection of the fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy. Plant Cell 10, 1055-1068 (1998).

[55] Catanzariti, A. M., Lim, G. T. T. & Jones, D. A. The tomato I-3 gene: a novel gene for resistance to Fusarium wilt disease. N. Phytol. 207, 106-118 (2015).

[56] Robbins, M. D., Darrigues, A., Sim, S.-C., Masud, M. A. T. & Francis, D. M. Characterization of hypersensitive resistance to bacterial spot race T3 (Xanthomonas perforans) from tomato accession PI 128216 . Phytopathology 99, 1037-1044 (2009).

[57] Sun H. J., et al. QTL analysis of resistance to bacterial spot race T3 in tomato. ACTA Hortic. Sin. 38, 2297-2308 (2011).

[58] Pei, C. et al. Fine mapping and analysis of a candidate gene in tomato accession PI128216 conferring hypersensitive resistance to bacterial spot race T3. Theor. Appl. Genet. 124, 533-542 (2012).

[59] Wang, J., Rajakulendran, N., Amirsadeghi, S . & Vanlerberghe, G. C. Impact of mitochondrial alternative oxidase expression on the response of Nicotiana tabacum to cold temperature. Physiol. Plant 142, 339-351 (2011).

[60] Sharlach, M. et al. Fine genetic mapping of RXopJ4, a bacterial spot disease resistance locus from Solanum pennellii LA716. Theor. Appl Genet. 126, 601-609 (2013).

[61] Rodewald, J. & Trognitz, B. Solanum resistance genes against phytophthora infestans and their corresponding avirulence genes. Mol. Plant Pathol. 14, 740-757 (2013).

[62] Zhang, C. et al. The Ph-3 gene from Solanum pimpinellifolium encodes CC-NBS-LRR protein conferring resistance to phytophthora infestans. Theor. Appl. Genet. 127, 1353-1364 (2014).

[63] McDowell, J. M. & Woffenden, B. J. Plant disease resistance genes: recent insights and potential applications. Trends Biotechnol. 21, 178-183 (2003).

[64] Tzortzakis N. Physiological and proteomic approaches to address the active role of botrytis cinerea inoculation in tomato postharvest ripening. Microorganisms 7, 681 (2019).

[65] Zeiss D. R., Mhlongo M. I., Tugizimana F., Steenkamp P. A., Dubery I. A. Metabolomic profiling of the host response of tomato (Solanum lycopersicum) following infection by Ralstonia solanacearum . Int. J. Mol. Sci. 20, 3945 (2019).

[66] Rotter, A., Usadel, B., Baebler, S., Stitt, M. & Gruden, K. Adaptation of the MapMan ontology to biotic stress responses: application in solanaceous species. Plant Methods 3, 1-9 (2007).

[67] Knief, C. Analysis of plant microbe interactions in the era of next generation sequencing technologies. Front. Plant Sci. 5, 1-23 (2014).

[68] Şahin-Çevik, M., Sivri, E. D. & Çevik, B. Identification and expression analysis of genes induced in response to tomato chlorosis virus infection in tomato. plant Pathol. J. 35, 257-273 (2019).

[69] Góra-Sochacka A., Wiesyk A., Fogtmann A., Lirski M., Zagórski-Ostoja W. Root transcriptomic analysis reveals global changes induced by systemic infection of solanum lycopersicum with mild and severe variants of potato spindle tuber viroid. Viruses 11, 992 (2019).

[70] Ansorge, W. J. & Next-generation, D. N. A. sequencing techniques. N. Biotechnol. 25, 195-203 (2009).

[71] Vega, A. et al. Transcriptome analysis reveals regulatory networks underlying differential susceptibility to botrytis cinerea in response to nitrogen availability in solanum lycopersicum. Front. Plant Sci. 6, 1-17 (2015).

[72] Su, X. et al. The dynamic transcriptome and metabolomics profiling in Verticillium dahliae inoculated Arabidopsis thaliana . Sci. Rep. 8, 1-11 (2018).

[73] Jiménez-Ruiz J., et al. Transcriptomic analysis of Olea europaea L. Roots during the verticillium dahliae early infection process. Plant Genome https://doi.org/10.3835/plantgenome2016.07.0060 (2017).

[74] Oliver, J. E. & Whitfield, A. E. The genus tospovirus: emerging bunyaviruses that threaten food security. Annu. Rev. Virol. 3, 101-124 (2016).

[75] Pappu, H. R., Jones, R. A. C. & Jain, R. K. Global status of tospovirus epidemics in diverse cropping systems: successes achieved and challenges ahead. Virus Res. 141, 219-236 (2009).

[76] Padmanabhan, C. et al. Comprehensive transcriptome analysis and functional characterization of PR-5 for its involvement in tomato Sw-7 resistance to tomato spotted wilt tospovirus. Sci. Rep. 9, 1-17 (2019).

[77] Papayiannis, L. C., Katis, N. I., Idris, A. M. & Brown, J. K. Identification of weed hosts of tomato yellow leaf curl virus in cyprus. Plant Dis. 95, 120-125 (2010).

[78] Ghanim, M., Morin, S., Zeidan, M. & Czosnek, H . Evidence for transovarial transmission of tomato yellow leaf curl virus by its vector, the whitefly Bemisia tabaci . Virology 240, 295-303 (1998).

[79] Yan, Z. et al. Resistance to tomato yellow leaf curl virus in tomato germplasm. Front Plant Sci. 9, 1-14 (2018).

[80] Kovalskaya, N. & Hammond, R. W. Molecular biology of viroid-host interactions and disease control strategies. Plant Sci. 228, 48-60 (2014).

[81] Agrios G. Plant Pathology. 5th ed. 2005.

[82] Fradin, E. F. & Thomma, B. P. H. J. Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum . Mol. Plant Pathol. 7, 71-86 (2006).

[83] Klosterman, S. J., Atallah, Z. K. & Vallad, G. E. Subbarao K V . Diversity, pathogenicity, and management of verticillium species. Annu. Rev. Phytopathol. 47, 39-62 (2009).

[84] Tan G., et al. Transcriptome analysis of the compatible interaction of tomato with verticillium dahliae using RNA-sequencing. Front. Plant Sci. 6, 428 (2015).

[85] Thaines Bodah E . Root rot diseases in plants: a review of common causal agents and management strategies. Agric. Res. Technol. Open Access J. 5, 555661 (2017).

[86] Borisade, O. A., Uwaidem, Y. I. & Salami, A. E. Preliminary report on Fusarium oxysporum f. Sp. lycopersici (sensu lato) from some tomato producing agroecological areas in southwestern Nigeria and susceptibility of F1-resistant tomato hybrid (F1-lindo) to infection. Annu. Res. Rev. Biol. 18, 1-9 (2017).

[87] Zhao, M. et al. An integrated analysis of mRNA and sRNA transcriptional profiles in tomato root: Insights on tomato wilt disease. PLoS One 13, e0206765 (2018).

[88] Sarkar, D. et al. Integrated miRNA and mRNA expression profiling reveals the response regulators of a susceptible tomato cultivar to early blight disease. DNA Res. 24, 235-250 (2017).

[89] Simmons, E. G. Perfect states of stemphylium-IV. Harv. Pap. Bot. 6, 199-208 (2001).

[90] Yang, H. et al. Mapping and screening of the tomato Stemphylium lycopersici resistance gene, Sm, based on bulked segregant analysis in combination with genome resequencing. BMC Plant Biol. 17, 1-10 (2017).

[91] Yang, H. et al. Transcriptome analysis of the Sm-mediated hypersensitive response to Stemphylium lycopersici in tomato. Front Plant Sci. 8, 1-14 (2017).

[92] Thomma, B. P. H. J., Van Esse, H. P., Crous, P. W. & De Wit, P. J. G. M. Cladosporium fulvum (syn. Passalora fulva), a highly specialized plant pathogen as a model for functional studies on plant pathogenic Mycosphaerellaceae . Mol. Plant Pathol. 6, 379-393 (2005).

[93] Zhang, D. et al. Comparative transcriptome analysis reveals the response mechanism of Cf-16-mediated resistance to Cladosporium fulvum infection in tomato. BMC Plant Biol. 20, 1-16 (2020).

[94] Naveed, Z. A. & Ali, G. S. Comparative transcriptome analysis between a resistant and a susceptible wild tomato accession in response to Phytophthora parasitica . Int. J. Mol. Sci. 19, 1-26 (2018).

[95] Du, H., Wang, Y., Yang, J. & Yang, W. Comparative transcriptome analysis of resistant and susceptible tomato lines in response to infection by xanthomonas perforans race T3. Front. Plant Sci. 6, 1-14 (2015).

[96] Major, I. T., Nicole, M.-C., Duplessis, S. & Séguin, A. Photosynthetic and respiratory changes in leaves of poplar elicited by rust infection. Photosynth Res. 104, 41-48 (2010).

[97] Shi, R. & Panthee, D. R. Transcriptome-based analysis of tomato genotypes resistant to bacterial spot (Xanthomonas perforans) race t4 . Int. J. Mol. Sci. 21, 1-31 (2020).

[98] Shukla, N. et al. Transcriptome analysis of root-knot nematode (Meloidogyne incognita)-infected tomato (Solanum lycopersicum) roots reveals complex gene expression profiles and metabolic networks of both host and nematode during susceptible and resistance responses . Mol. Plant Pathol. 19, 615-633 (2018).

[99] Kulshrestha, K., Parihar, A. & Parihar, P. Next generation sequencing based transcriptome analysis for nematode resistance in different species of tomato. Plant Gene 24, 100255 (2020).

[100] Köhler, H.-R. & Triebskorn, R. Wildlife ecotoxicology of pesticides: can we track effects to the population level and beyond? Science 341, 759-765 (2013).

[101] Corsini, E., Sokooti, M., Galli, C. L., Moretto, A. & Colosio, C. Pesticide induced immunotoxicity in humans: a comprehensive review of the existing evidence. Toxicology 307, 123-135 (2013).

[102] McDonald B. A., Stukenbrock E. H. Rapid emergence of pathogens in agroecosystems: Global threats to agricultural sustainability and food security. Philos. Trans. R. Soc. B. Biol. Sci. 371, 20160026 (2016).

[103] Pombo, M. A. et al. Transcriptomic analysis reveals tomato genes whose expression is induced specifically during effector-triggered immunity and identifies the Epk1 protein kinase which is required for the host response to three bacterial effector proteins. Genome Biol. 15, 492 (2014).