Abstract
Breeding for resistance is the most effective tool for controlling the corky root disease of tomato caused by Pyrenochaeta lycopersici. A comparative RNA-Seq-based transcriptomic analysis was conducted at 96 hpi (hours post infection) on two tomato cultivars: resistant Mogeor and its genetic background, and susceptible Moneymaker to investigate the differences in their transcriptomic response and identify the molecular bases of this plant-pathogen interaction. The number of differentially expressed genes (DEGs) identified was much higher in the susceptible than in the resistant genotype; however, the proportion of upregulated genes was higher in Mogeor (70.81%) than in Moneymaker (52.95%). Gene Ontology (GO) analysis enabled identification of 24 terms shared by the two cultivars that were consistent with responses to external stimulus, such as fungal infection. On the other hand, as many as 54 GO were enriched solely in Moneymaker, including terms related to defense response and cell wall metabolism. Our results could support the previous observations in other pathosystems, that susceptibility and resistance have overlapping signaling pathways and responses, suggesting that the P. lycopersici resistance gene pyl might be a recessive allele at a susceptibility locus, for which different candidate genes were identified based on the differences in induction or expression levels, observed between the resistant and susceptible genotype. MapMan analysis highlighted a complex hormone and transcription factors interplay where SA- and JA-induced pathways are modulated in a similar way in both genotypes and thus take part in a common response while the ethylene signaling pathways, induced mainly in susceptible Moneymaker, seem putatively contribute to its susceptibility.
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References
Ahuja I, Kissen R, Bones AM (2012) Phytoalexins in defense against pathogens. Trends Plant Sci 17:73–90. https://doi.org/10.1016/j.tplants.2011.11.002
Andolfo G, Sanseverino W, Rombauts S, van de Peer Y, Bradeen JM, Carputo D, Frusciante L, Ercolano MR (2013) Overview of tomato (Solanum lycopersicum) candidate pathogen recognition genes reveals important Solanum R locus dynamics. New Phytol 197:223–237
Aragona M, Infantino A (2008) Expression profiling of tomato response to Pyrenochaeta lycopersici infection. Acta Hortic 257–262. https://doi.org/10.17660/ActaHortic.2008.789.35
Aragona M, Infantino A, Papacchini M (2009) Developing a molecular method for screening the resistance to a pathogen of tomato plants to contribute to limiting the use of toxic chemicals in soil. WIT Trans Ecol Environ 120:519–524. https://doi.org/10.2495/SDP090482
Aragona M, Minio A, Ferrarini A, Valente M, Bagnaresi P, Orrù L, Tononi P, Zamperin G, Infantino A, Valè G, Cattivelli L, Delledonne M (2014) De novo genome assembly of the soil-borne fungus and tomato pathogen Pyrenochaeta lycopersici. BMC Genomics 15:313. https://doi.org/10.1186/1471-2164-15-313
Arens P, Mansilla C, Deinum D, Cavellini L, Moretti A, Rolland S, van der Schoot H, Calvache D, Ponz F, Collonnier C, Mathis R, Smilde D, Caranta C, Vosman B (2010) Development and evaluation of robust molecular markers linked to disease resistance in tomato for distinctness, uniformity and stability testing. Theor Appl Genet 120:655–664. https://doi.org/10.1007/s00122-009-1183-2
Ausubel FM (2005) Are innate immune signaling pathways in plants and animals conserved? Nat Immunol 6:973–979. https://doi.org/10.1038/ni1253
Berger S, Sinha AK, Roitsch T (2007) Plant physiology meets phytopathology: plant primary metabolism and plant-pathogen interactions. J Exp Bot 58:4019–4026. https://doi.org/10.1093/jxb/erm298
Biselli C, Bagnaresi P, Cavalluzzo D, Urso S, Desiderio F, Orasen G, Gianinetti A, Righettini F, Gennaro M, Perrini R, Ben Hassen M, Sacchi GA, Cattivelli L, Valè G (2015) Deep sequencing transcriptional fingerprinting of rice kernels for dissecting grain quality traits. BMC Genomics 16:1091. https://doi.org/10.1186/s12864-015-2321-7
Biselli C, Bagnaresi P, Faccioli P, Hu X, Balcerzak M, Mattera MG, Yan Z, Ouellet T, Cattivelli L, Valè G (2018) Comparative transcriptome profiles of near-isogenic hexaploid wheat lines differing for effective alleles at the 2DL FHB resistance QTL. Front Plant Sci 9:1–28. https://doi.org/10.3389/fpls.2018.00037
Bouchez O, Huard C, Lorrain S, Roby D, Balague C (2007) Ethylene is one of the key elements for cell death and defense response control in the Arabidopsis lesion mimic mutant vad1. Plant Physiol 145:465–477. https://doi.org/10.1104/pp.107.106302
Büschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Töpsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705. https://doi.org/10.1016/S0092-8674(00)81912-1
Causse M, Desplat N, Pascual L, le Paslier MC, Sauvage C, Bauchet G, Bérard A, Bounon R, Tchoumakov M, Brunel D, Bouchet JP (2013) Whole genome resequencing in tomato reveals variation associated with introgression and breeding events. BMC Genomics 14:791–805. https://doi.org/10.1186/1471-2164-14-791
Chu Z, Fu B, Yang H, Xu C, Li Z, Sanchez A, Park YJ, Bennetzen JL, Zhang Q, Wang S (2006) Targeting xa13, a recessive gene for bacterial blight resistance in rice. Theor Appl Genet 112:455–461. https://doi.org/10.1007/s00122-005-0145-6
Clergeot P-H, Rivetti C, Hamiduzzaman MM, Ekengren S (2011) The corky root rot pathogen Pyrenochaeta lycopersici manipulates tomato roots with molecules secreted early during their interaction. Acta Agric Scand Sect B Soil Plant Sci 62:300–310. https://doi.org/10.1080/09064710.2011.613851
Clergeot P-H, Schuler H, Mørtz E, Brus M, Vintila S, Ekengren S (2012) The corky root rot pathogen Pyrenochaeta lycopersici secretes a proteinaceous inducer of cell death affecting host plants differentially. Phytopathology 102:878–891
Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, Bittner-Eddy P, Beynon J, Marco Y (2002) Resistance to ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. Proc Natl Acad Sci 99:2404–2409. https://doi.org/10.1073/pnas.032485099
Doganlar S, Dodson J, Gabor B, Beck-Bunn T, Crossman C, Tanksley SD (1998) Molecular mapping of the py-1 gene for resistance to corky root rot (Pyrenochaeta lycopersici) in tomato. Theor Appl Genet 97:784–788. https://doi.org/10.1007/s001220050956
Dörmann P, Kim H, Ott T, Schulze-Lefert P, Trujillo M, Wewer V, Hückelhoven R (2014) Cell-autonomous defense, re-organization and trafficking of membranes in plant-microbe interactions. New Phytol 204:815–822. https://doi.org/10.1111/nph.12978
Ekengren SK (2008) Cutting the Gordian knot: taking a stab at corky root rot of tomato. Plant Biotechnol 25:265–269. https://doi.org/10.5511/plantbiotechnology.25.265
Falcon S, Gentleman R (2007) Using GOstats to test gene lists for GO term association. Bioinformatics 23:257–258. https://doi.org/10.1093/bioinformatics/btl567
Faris JD, Zhang Z, Lu H, Lu S, Reddy L, Cloutier S, Fellers JP, Meinhardt SW, Rasmussen JB, Xu SS, Oliver RP, Simons KJ, Friesen TL (2010) A unique wheat disease resistance-like gene governs effector-triggered susceptibility to necrotrophic pathogens. Proc Natl Acad Sci 107:13544–13549. https://doi.org/10.1073/pnas.1004090107
Faulkner C, Robatzek S (2012) Plants and pathogens: putting infection strategies and defence mechanisms on the map. Curr Opin Plant Biol 15:699–707
Fiume G, Fiume F (2008) Biological control of corky root in tomato. Commun Agric Appl Biol Sci 73:233–248
Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296. https://doi.org/10.1146/annurev.py.09.090171.001423
Friesen TL, Faris JD (2004) Molecular mapping of resistance to Pyrenophora tritici-repentis race 5 and sensitivity to Ptr ToxB in wheat. Theor Appl Genet 109:464–471. https://doi.org/10.1007/s00122-004-1678-9
Garcia-Brugger A, Lamotte O, Vandelle E, Bourque S, Lecourieux D, Poinssot B, Wendehenne D, Pugin A (2006) Early signaling events induced by elicitors of plant defenses. Mol Plant-Microbe Interact 19:711–724. https://doi.org/10.1094/MPMI-19-0711
Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227. https://doi.org/10.1146/annurev.phyto.43.040204.135923
Goodenough PW, Kempton RJ (1976) The activity of cell-wall degrading enzymes in tomato roots infected with Pyrenochaeta lycopersici and the effect of sugar concentrations in these roots on disease development. Physiol Plant Pathol 9:313–320. https://doi.org/10.1016/0048-4059(76)90064-3
Grove GG, Campbell RN (1987) Host range and survival in soil of Pyrenochaeta lycopersici. Plant Dis 71:806–809
Huang S, Gao Y, Liu J, Peng X, Niu X, Fei Z, Cao S, Liu Y (2012) Genome-wide analysis of WRKY transcription factors in Solanum lycopersicum. Mol Gen Genomics 287:495–513. https://doi.org/10.1007/s00438-012-0696-6
Infantino A, Pucci N (2005) A PCR-based assay for the detection and identification of Pyrenochaeta lycopersici. Eur J Plant Pathol 112:337–437. https://doi.org/10.1007/s10658-005-6605-7
Infantino A, Di Giambattista G, Porta-Puglia A (2000) First report of Pyrenochaeta lycopersici on melon in Italy [Cucumis melo L. - Latium]. Petria (Italy) 10:195–198
Iyer AS, McCouch SR (2004) The rice bacterial blight resistance gene xa5 encodes a novel form of disease resistance. Mol Plant-Microbe Interact 17:1348–1354. https://doi.org/10.1094/mpmi.2004.17.12.1348
Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329. https://doi.org/10.1038/nature05286
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biol 14:R36. https://doi.org/10.1186/gb-2013-14-4-r36
Kunkel BN, Brooks DM (2002) Cross talk between signaling pathways in pathogen defense. Curr Opin Plant Biol 5:325–331
Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:559. https://doi.org/10.1186/1471-2105-9-559
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923
Laterrot H (1987) Revised list of near isogenic tomato lines in Moneymaker type with different genes for disease resistances. Rep Tomato Genet Coop 37:91
Li J, Brader G, Kariola T, Tapio Palva E (2006) WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 46:477–491. https://doi.org/10.1111/j.1365-313X.2006.02712.x
Liu ZQ, Yan L, Wu Z, Mei C, Lu K, Yu YT, Liang S, Zhang XF, Wang XF, Zhang DP (2012) Cooperation of three WRKY-domain transcription factors WRKY18, WRKY40, and WRKY60 in repressing two ABA-responsive genes ABI4 and ABI5 in Arabidopsis. J Exp Bot 63:6371–6392. https://doi.org/10.1093/jxb/ers293
Liu M, Lima Gomes B, Mila I et al (2016) Comprehensive profiling of ethylene response factors expression identifies ripening-associated ERF genes and their link to key regulators of fruit ripening in tomato (Solanum lycopersicum). Plant Physiol 170:1732–1744. https://doi.org/10.1104/pp.15.01859
Lorang JM, T a S, Wolpert TJ (2007) Plant disease susceptibility conferred by a “resistance” gene. Proc Natl Acad Sci U S A 104:14861–14866. https://doi.org/10.1073/pnas.0702572104
Love MI, Huber W, Anders S (2014) Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol 15:550. https://doi.org/10.1186/s13059-014-0550-8
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17:10–12. https://doi.org/10.14806/ej.17.1.200
Milc J, Infantino A, Pecchioni N, Aragona M (2012) Identification of tomato genes differentially expressed during compatible interaction with Pyrenochaeta lycopersici. J Plant Patholol 94:283–296. https://doi.org/10.4454/JPP.FA.2012.035
Milc J, Infantino A, Aragona M, Pecchioni N (2015) Detection of single-feature polymorphisms (SFPs) between two tomato varieties and their application in defining the introgressions of resistance loci. Plant Breed 134:226–232. https://doi.org/10.1111/pbr.12250
Molin AD, Minio A, Griggio F et al (2018) The genome assembly of the fungal pathogen Pyrenochaeta lycopersici from single-molecule real-time sequencing sheds new light on its biological complexity. PLoS One 13:1–17. https://doi.org/10.1371/journal.pone.0200217
Montesano M, Brader G, Palva ET (2003) Pathogen derived elicitors: searching for receptors in plants. Mol Plant Pathol 4:73–79. https://doi.org/10.1046/j.1364-3703.2003.00150.x
Mur LAJ, Prats E, Pierre S, Hall MA, Hebelstrup KH (2013) Integrating nitric oxide into salicylic acid and jasmonic acid/ethylene plant defense pathways. Front Plant Sci 4:215. https://doi.org/10.3389/fpls.2013.00215
Nakayama A, Fukushima S, Goto S, Matsushita A, Shimono M, Sugano S, Jiang CJ, Akagi A, Yamazaki M, Inoue H, Takatsuji H (2013) Genome-wide identification of WRKY45-regulated genes that mediate benzothiadiazole-induced defense responses in rice. BMC Plant Biol 13:150. https://doi.org/10.1186/1471-2229-13-150
Oshlack A, Wakefield MJ (2009) Transcript length bias in RNA-seq data confounds systems biology. Biol Direct 4:14. https://doi.org/10.1186/1745-6150-4-14
Pandelova I, Figueroa M, Wilhelm LJ, Manning VA, Mankaney AN, Mockler TC, Ciuffetti LM (2012) Host-selective toxins of pyrenophora tritici-repentis induce common responses associated with host susceptibility. PLoS One 7:13–20. https://doi.org/10.1371/journal.pone.0040240
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36. https://doi.org/10.1093/nar/30.9.e36
Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST©) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30: e36. https://doi.org/10.1093/nar/30.9.e36
Robinson MD, Oshlack A (2010) A scaling normalization method for differential expression analysis of RNA-seq data. Genome Biol 11:R25. https://doi.org/10.1186/gb-2010-11-3-r25
Sakamoto T, Deguchi M, Brustolini OJB, Santos AA, Silva FF, Fontes EPB (2012) The tomato RLK superfamily: phylogeny and functional predictions about the role of the LRRII-RLK subfamily in antiviral defense. BMC Plant Biol 12:229. https://doi.org/10.1186/1471-2229-12-229
Shannon PT, Grimes M, Kutlu B, Bot JJ, Galas DJ (2013) RCytoscape: tools for exploratory network analysis. BMC Bioinformatics 14:217. https://doi.org/10.1186/1471-2105-14-217
Shen Q-H, Schulze-Lefert P (2007) Rumble in the nuclear jungle: compartmentalization, trafficking, and nuclear action of plant immune receptors. EMBO J 26:4293–4301. https://doi.org/10.1038/sj.emboj.7601854
Thimm O, Bläsing O, Gibon Y, Nagel A, Meyer S, Krüger P, Selbig J, Müller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939. https://doi.org/10.1111/j.1365-313X.2004.02016.x
Thorvaldsdóttir H, Robinson JT, Mesirov JP (2013) Integrative genomics viewer (IGV): high-performance genomics data visualization and exploration. Brief Bioinform 14:178–192. https://doi.org/10.1093/bib/bbs017
Valente MT, Infantino A, Aragona M (2011) Molecular and functional characterization of an endoglucanase in the phytopathogenic fungus Pyrenochaeta lycopersici. Curr Genet 57:241–251. https://doi.org/10.1007/s00294-011-0343-5
Van Eck L, Davidson RM, Wu S et al (2014) The transcriptional network of WRKY53 in cereals links oxidative responses to biotic and abiotic stress inputs. Funct Integr Genomics 14(2):351–362. https://doi.org/10.1007/s10142-014-0374-3
Wang KL, Li H, Ecker JR (2002) Ethylene biosynthesis and signaling networks. Plant Cell 14:131–152. https://doi.org/10.1105/tpc.001768
Wickham H (2009) ggplot2 elegant graphics for data analysis. Springer-Verlag, New York
Wolpert TJ, Dunkle LD, Ciuffetti LM (2002) Host-selective toxins and avirulence determinants: what’s in a name? Annu Rev Phytopathol 40:251–285. https://doi.org/10.1146/annurev.phyto.40.011402.114210
Yoshioka H, Yamada N, Doke N (1999) cDNA cloning of sesquiterpene cyclase and squalene synthase, and expression of the genes in potato tuber infected with Phytophthora infestans. Plant Cell Physiol 40:993–998. https://doi.org/10.1093/oxfordjournals.pcp.a029633
Zhang M, Smith JAC, Harberd NP, Jiang C (2016) The regulatory roles of ethylene and reactive oxygen species (ROS) in plant salt stress responses. Plant Mol Biol 91:651–659. https://doi.org/10.1007/s11103-016-0488-1
Zhang J, Zhao W, Fu R, Fu C, Wang L, Liu H, Li S, Deng Q, Wang S, Zhu J, Liang Y, Li P, Zheng A (2018) Comparison of gene co-networks reveals the molecular mechanisms of the rice (Oryza sativa L.) response to Rhizoctonia solani AG1 IA infection. Funct Integr Genomics 18:545–557. https://doi.org/10.1007/s10142-018-0607-y
Zhao P, Li Q, Li J, Wang L, Ren Z (2014) Genome-wide identification and characterization of R2R3MYB family in Solanum lycopersicum. Mol Gen Genomics 289:1183–1207. https://doi.org/10.1007/s00438-014-0879-4
Acknowledgments
Seeds were kindly provided by the C.M. Rick Tomato Genetics Resource Centre, Davis, CA, USA (http://tgrc.ucdavis.edu), and multiplied by Dr. N. Acciarri, Council for Agricultural Research and Economics - Research Centre for Vegetable and Ornamental Crops, Monsampolo del Tronto (AP), Italy.
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ESM_1
Sequence of primer pairs used for each locus analysed by qRT-PCRs (PDF 79 kb)
ESM_2
Tophat2-mapping statistics. MC- Mogeor control, MI-Mogeor inoculated samples; MMC- Moneymaker control, MMI- Moneymaker inoculated samples (XLSX 12 kb)
ESM_3
Sample correlation heatmaps for the 11 samples used in the study. DESeq2-normalized expression data were further subjected to Rlog transformations prior to plotting as heatmap (PNG 268 kb)
ESM_4
Global overview of Mogeor (M) and Moneymaker (MM) transcriptional changes. Mean expression versus log2 fold change plots (MA-plots) were computed for M (a) and MM (b); normalised expression mean values are plotted versus log2 fold changes and genes called DEGs (FDR < 0.05) are plotted in red. (c) Mean expression values (averages of mock and infected) were plotted on x and y axis for M and MM, respectively. Genes called as DEG in both varieties, in M only, in MM only or in neither genotype are plotted in yellow, red, green and black, respectively (PNG 707 kb)
ESM_5
Expression values reported as DESeq2-normalized read counts and fold changes for all the transcribed genes detected in the experiment (only DEGs FDR < 0.05). MC-Mogeor control samples, MI- Mogeor infected samples, MMC-Moneymaker control samples, MMI- Moneymaker infected samples (XLSX 2000 kb)
ESM_6
Genes involved in primary metabolism and modulated by P. lycopersici infection (XLSX 115 kb)
ESM_7
Genes involved in biotic stress response and modulated by P. lycopersici infection (XLSX 190 kb)
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Milc, J., Bagnaresi, P., Aragona, M. et al. Comparative transcriptome profiling of the response to Pyrenochaeta lycopersici in resistant tomato cultivar Mogeor and its background genotype—susceptible Moneymaker. Funct Integr Genomics 19, 811–826 (2019). https://doi.org/10.1007/s10142-019-00685-0
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DOI: https://doi.org/10.1007/s10142-019-00685-0