Advertisement

Plant Cell Reports

, Volume 38, Issue 1, pp 1–13 | Cite as

Comparative transcriptome analysis shows the defense response networks regulated by miR482b

  • Ning Jiang
  • Jun Cui
  • Guanglei Yang
  • Xiaoli He
  • Jun Meng
  • Yushi LuanEmail author
Original Article

Abstract

Key message

The transcriptomic profile in the leaves of miR482b-overexpressing tomato plants revealed that miR482b may suppress alpha-linolenic acid metabolism, cysteine and methionine metabolism, plant–pathogen interaction, and the MAPK pathway to reduce resistance to Phytophthora infestans.

Abstract

Our previous study showed that tomato miR482b acted as a negative regulator during tomato resistance to Phytophthora infestans by silencing NBS-LRR genes. To investigate pathways related to miR482b, the transcriptomic profile of tomato plants that overexpressed miR482b was constructed. A total of 47,124,670 raw sequence reads from the leaves of miR482b-overexpressing tomato plants were generated by Illumina sequencing. A total of 746 genes in miR482b-overexpressing tomato plants were found to show significantly differential expression relative to those in wild-type tomato plants, including 132 up-regulated genes and 614 down-regulated genes. GO and KEGG enrichment analyses showed that plant–pathogen interaction, the MAPK pathway, and the pathways related to JA and ET biosynthesis were affected by miR482b in tomato. qRT-PCR results showed that all the enriched genes in these pathways were down-regulated in tomato plants that overexpressed miR482b and up-regulated in tomato plants that overexpressed an NBS-LRR gene (Soly02g036270.2, the target gene of miR482b). After P. infestans infection, the expression of the enriched genes showed a time-dependent response, and the genes played different roles between resistant tomato (Solanum pimpinellifolium L3708) and tomato susceptible to P. infestans (S. lycopersicum Zaofen No. 2). Our results have, therefore, demonstrated that miR482b is an important component of defense response network. This will also help to identify candidate genes involved in plant–pathogen interaction.

Keywords

MiR482b Overexpressing Phytophthora infestans RNA-Seq Tomato Regulatory network 

Abbreviations

ACC

1-Aminocyclopropane-1-carboxylic acid

ACS

1-Aminocyclopropane-1-carboxylic acid synthase

AOS

Allene oxide synthase

CaM

Calmodulin

DEGs

Differentially expressed genes

ET

Ethylene

ETI

Effector-triggered immunity

FPKM

Fragments per kilobase of exon model per Million mapped reads

GO

Gene ontology

HR

Hypersensitive response

JA

Jasmonic acid

KEGG

Kyoto encyclopedia of genes and genomes

LOX

Linoleate 13S-lipoxygenase

OPCL1

OPC-8:0 CoA ligase 1

P/MAMPs

Pathogen/microbe-associated molecular patterns

PRRs

Pattern-recognition receptors

PTI

PAMP-triggered immunity

Rbo

Respiratory burst oxidase

ROS

Reactive oxygen species

SA

Salicylic acid

SAM

S-Adenosyl-methionine

SAMS

S-Adenosylmethionine synthetase

Notes

Acknowledgements

The authors thank Prof. Weixing Shan (Northwest A&F University of China) for providing Phytophthora infestans. This work was supported by grants from the National Natural Science Foundation of China (Nos. 31471880 and 61472061).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

299_2018_2344_MOESM1_ESM.tif (390 kb)
Fig. S1 Experiment design in this study (TIF 390 KB)
299_2018_2344_MOESM2_ESM.tif (59 kb)
Fig. S2 Expression level of miR482b in the S. lycopersicum Zaofen No. 2 at 3 dpi. Actin expression was used as a control. Data are the means ± SEs of three independent experiments. Letters indicate significant differences among samples, and letters shared in common between or among the groups indicate no significant difference at the P < 0.05 level (TIF 59 KB)
299_2018_2344_MOESM3_ESM.tif (552 kb)
Fig. S3 Differentially expressed genes identified by RNA-Seq and validated by qRT-PCR. SlPOD, peroxidase (Solyc11g018800.1); SlCCoAOMT, caffeoyl-CoA O-methyltransferase (Solyc02g093230.2); Sl4CL, 4-coumarate--CoA ligase (Solyc03g097030.2); SlPAL, phenylalanine ammonia-lyase (Solyc05g056170.2). The Y-axis represents normalized relative expression values. The samples are labeled along the X-axis. Actin expression was used as a control. Data are the means ± SEs of three independent experiments. Letters indicate significant differences among samples, and letters shared in common between or among the groups indicate no significant difference at the P < 0.05 level (TIF 552 KB)
299_2018_2344_MOESM4_ESM.docx (16 kb)
Supplementary material 4 (DOCX 15 KB)
299_2018_2344_MOESM5_ESM.xlsx (46 kb)
Supplementary material 5 (XLSX 45 KB)
299_2018_2344_MOESM6_ESM.docx (27 kb)
Supplementary material 6 (DOCX 27 KB)
299_2018_2344_MOESM7_ESM.docx (16 kb)
Supplementary material 7 (DOCX 15 KB)

References

  1. Adams DO, Yang SF (1979) Ethylene biosynthesis: Identification of 1-aminocyclopropane-1-carboxylic acid as an intermediate in the conversion of methionine to ethylene. Proc Natl Acad Sci USA 76:170–174PubMedGoogle Scholar
  2. Ahmad P, Rasool S, Gul A, Sheikh SA, Akram NA, Ashraf M, Kazi AM, Gucel S (2016) Jasmonates: multifunctional roles in stress tolerance. Front Plant Sci 7:813PubMedPubMedCentralGoogle Scholar
  3. Ajengui A, Bertolini E, Ligorio A, Chebil S, Ippolito A, Sanzani SM (2018) Comparative transcriptome analysis of two citrus germplasms with contrasting susceptibility to Phytophthora nicotianae provides new insights into tolerance mechanisms. Plant Cell Rep 37:483–499PubMedGoogle Scholar
  4. Anders S, Huber W (2010) Differential expression analysis for sequence count data. Genome Biol 11:R106PubMedPubMedCentralGoogle Scholar
  5. Apostol I, Heinstein PF, Low PS (1989) Rapid stimulation of an oxidative burst during elicitation of cultured plant cells: role in defense and signal transduction. Plant Physiol 90:109–116PubMedPubMedCentralGoogle Scholar
  6. Åsman AK, Vetukuri RR, Jahan SN, Fogelqvist J, Corcoran P, Avrova AO, Whisson SC, Dixelius C (2014) Fragmentation of tRNA in Phytophthora infestans asexual life cycle stages and during host plant infection. BMC Microbiol 14:308PubMedPubMedCentralGoogle Scholar
  7. Baldrich P, San Segundo B (2016) MicroRNAs in rice innate immunity. Rice (NY) 9:6Google Scholar
  8. Baysal-Gurel E, Li R, Ling KS, Miller SA (2015) First report of Tomato chlorotic spot virus infecting tomatoes in Ohio. Plant Dis 99:163–164Google Scholar
  9. Beckers GJ, Spoel SH (2006) Fine-tuning plant defence signalling: salicylate versus jasmonate. Plant Biol (Stuttg) 8:1–10Google Scholar
  10. Bell E, Creelman RA, Mullet JE (1995) A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proc Natl Acad Sci USA 92:8675–8679PubMedGoogle Scholar
  11. Bhattarai K, Louws FJ, Williamson JD, Panthee DR (2016) Differential response of tomato genotypes to Xanthomonas-specific pathogen-associated molecular patterns and correlation with bacterial spot (Xanthomonas perforans) resistance. Hortic Res 3:16035PubMedPubMedCentralGoogle Scholar
  12. Cacas JL, Pré M, Pizot M, Cissoko M, Diedhiou I, Jalloul A, Doumas P, Nicole M, Champion A (2017) GhERF-IIb3 regulates the accumulation of jasmonate and leads to enhanced cotton resistance to blight disease. Mol Plant Pathol 18:825–836PubMedGoogle Scholar
  13. Caldelari D, Wang G, Farmer EE, Dong X (2011) Arabidopsis lox3 lox4 double mutants are male sterile and defective in global proliferative arrest. Plant Mol Biol 75:25–33PubMedGoogle Scholar
  14. Cui J, Luan Y, Jiang N, Bao H, Meng J (2017) Comparative transcriptome analysis between resistant and susceptible tomato allows the identification of lncRNA16397 conferring resistance to Phytophthora infestans by co-expressing glutaredoxin. Plant J 89:577–589PubMedGoogle Scholar
  15. Cui J, Xu P, Meng J, Li J, Jiang N, Luan Y (2018) Transcriptome signatures of tomato leaf induced by Phytophthora infestans and functional identification of transcription factor SpWRKY3. Theor Appl Genet 131:787–800PubMedGoogle Scholar
  16. de Miranda BEC, Suassuna ND, Reis A (2010) Mating type, mefenoxam sensitivity, and pathotype diversity in Phytophthora infestans isolates from tomato in Brazil. Pesq Agropecu Bras 45:671–679Google Scholar
  17. De Vleesschauwer D, Gheysen G, Höfte M (2013) Hormone defense networking in rice: tales from a different world. Trends Plant Sci 18:555–565PubMedGoogle Scholar
  18. de Vries S, Kloesges T, Rose LE (2015) Evolutionarily dynamic, but robust, targeting of resistance genes by the miR482/2118 gene family in the Solanaceae. Genome Biol Evol 7:3307–3321PubMedPubMedCentralGoogle Scholar
  19. de Vries S, Kukuk A, von Dahlen JK, Schnake A, Kloesges T, Rose LE (2018) Expression profiling across wild and cultivated tomatoes supports the relevance of early miR482/2118 suppression for Phytophthora resistance. Proc Biol Sci 285:20172560PubMedPubMedCentralGoogle Scholar
  20. De Vos M, Van Oosten VR, Van Poecke RM, Van Pelt JA, Pozo MJ, Mueller MJ, Buchala AJ, Métraux JP, Van Loon LC, Dicke M, Pieterse CM (2005) Signal signature and transcriptome changes of Arabidopsis during pathogen and insect attack. Mol Plant Microbe Interact 18:923–937PubMedGoogle Scholar
  21. Desikan R, Reynolds A, Hancock JT, Neill SJ (1998) Harpin and hydrogen peroxide both initiate programmed cell death but have differential effects on defence gene expression in Arabidopsis suspension cultures. Biochem J 330:115–120PubMedPubMedCentralGoogle Scholar
  22. Doherty HM, Selvendran RR, Bowles DJ (1988) The wound response of tomato plants can be inhibited by aspirin and related hydroxy-benzoic acids. Physiol Mol Plant Pathol 33:377–384Google Scholar
  23. Duan X, Bi HG, Li T, Wu GX, Li QM, Ai XZ (2017) Root characteristics of grafted peppers and their resistance to Fusarium solani. Biol Plant 61:579–586Google Scholar
  24. Feng J, Liu S, Wang M, Lang Q, Jin C (2014) Identification of microRNAs and their targets in tomato infected with Cucumber mosaic virus based on deep sequencing. Planta 240:1335–1352PubMedGoogle Scholar
  25. Glazebrook J (2005) Contrasting mechanisms of defense against biotrophic and necrotrophic pathogens. Annu Rev Phytopathol 43:205–227Google Scholar
  26. Gnanaprakash PH, Jogaiah S, Sreedhara AP, Prashanth GN, Kini RK, Shetty SH (2013) Association between accumulation of allene oxide synthase activity and development of resistance against downy mildew disease of pearl millet. Mol Biol Rep 40:6821–6829Google Scholar
  27. Gómez-Gómez L, Carrasco P (1998) Differential expression of the S-adenosyl-l-methionine synthase genes during pea development. Plant Physiol 117:397–405PubMedPubMedCentralGoogle Scholar
  28. Gravino M, Savatin DV, Macone A, De Lorenzo G (2015) Ethylene production in Botrytis cinerea- and oligogalacturonide-induced immunity requires calcium-dependent protein kinases. Plant J 84:1073–1086PubMedGoogle Scholar
  29. Halitschke R, Baldwin IT (2003) Antisense LOX expression increases herbivore performance by decreasing defense responses and inhibiting growth-related transcriptional reorganization in Nicotiana attenuata. Plant J 36:794–807PubMedGoogle Scholar
  30. Harms K, Atzorn R, Brash A, Kuhn H, Wasternack C, Willmitzer L, Pena-Cortes H (1995) Expression of a flax allene oxide synthase cDNA leads to increased endogenous jasmonic acid (JA) levels in transgenic potato plants but not to a corresponding activation of JA-responding genes. Plant Cell 7:1645–1654PubMedPubMedCentralGoogle Scholar
  31. He L, Hannon GJ (2004) MicroRNAs: small RNAs with a big role in gene regulation. Nat Rev Genet 5:522–531PubMedGoogle Scholar
  32. He X, Jiang J, Wang CQ, Dehesh K (2017) ORA59 and EIN3 interaction couples jasmonate-ethylene synergistic action to antagonistic salicylic acid regulation of PDF expression. J Integr Plant Biol 59:275–287PubMedPubMedCentralGoogle Scholar
  33. Huang X, Wang A, Xu X, Li J, Li N (2010) Construction of genetic linkage map and QTL analysis of Phytophthora infestans resistant gene Ph-2 in tomato. Acta Hortic Sin 37:1085–1092Google Scholar
  34. Hwang IS, Hwang BK (2010) The pepper 9-lipoxygenase gene CaLOX1 functions in defense and cell death responses to microbial pathogens. Plant Physiol 152:948–967PubMedPubMedCentralGoogle Scholar
  35. Jiang Z, Dong X, Zhang Z (2016) Network-based comparative analysis of Arabidopsis immune responses to Golovinomyces orontii and Botrytis cinerea infections. Sci Rep 6:19149PubMedPubMedCentralGoogle Scholar
  36. Jiang N, Cui J, Meng J, Luan Y (2018a) A tomato nucleotide binding sites-leucine rich repeat gene is positively involved in plant resistance to Phytophthora infestans. Phytopathology 108:980–987PubMedGoogle Scholar
  37. Jiang N, Meng J, Cui J, Sun G, Luan Y (2018b) Function identification of miR482b, a negative regulator during tomato resistance to Phytophthora infestans. Hortic Res 5:9PubMedPubMedCentralGoogle Scholar
  38. Jing M, Ma H, Li H, Guo B, Zhang X, Ye W, Wang H, Wang Q, Wang Y (2015) Differential regulation of defense-related proteins in soybean during compatible and incompatible interactions between Phytophthora sojae and soybean by comparative proteomic analysis. Plant Cell Rep 34:1263–1280PubMedGoogle Scholar
  39. Jones JD, Dangl JL (2006) The plant immune system. Nature 444:323–329Google Scholar
  40. Kawalleck P, Plesch G, Hahlbrock K, Somssich IE (1992) Induction by fungal elicitor of S-adenosyl-l-methionine synthetase and S-adenosyl-l-homocysteine hydrolase mRNAs in cultured cells and leaves of Petroselinum crispum. Proc Natl Acad Sci USA 89:4713–4717PubMedGoogle Scholar
  41. Kim VN (2005) MicroRNA biogenesis: coordinated cropping and dicing. Nat Rev Mol Cell Biol 6:376–385PubMedGoogle Scholar
  42. Kim MJ, Mutschler MA (2005) Transfer to processing tomato and characterization of late blight resistance derived from Solanum pimpinellifolium L. L3708. J Am Soc Hortic Sci 130:877–884Google Scholar
  43. 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 121:749–759PubMedGoogle Scholar
  44. Kim SH, Kim SH, Palaniyandi SA, Yang SH, Suh JW (2015) Expression of potato S-adenosyl-l-methionine synthase (SbSAMS) gene altered developmental characteristics and stress responses in transgenic Arabidopsis plants. Plant Physiol Biochem 87:84–91PubMedGoogle Scholar
  45. Larsen PB (2015) Mechanisms of ethylene biosynthesis and response in plants. Essays Biochem 58:61–70PubMedGoogle Scholar
  46. Laudert D, Weiler EW (1998) Allene oxide synthase: a major control point in Arabidopsis thaliana octadecanoid signalling. Plant J 15:675–684PubMedGoogle Scholar
  47. Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593PubMedGoogle Scholar
  48. Li JH, Liu YQ, Lü P, Lin HF, Bai Y, Wang XC, Chen YL (2009) A signaling pathway linking nitric oxide production to heterotrimeric G protein and hydrogen peroxide regulates extracellular calmodulin induction of stomatal closure in Arabidopsis. Plant Physiol 150:114–124PubMedPubMedCentralGoogle Scholar
  49. Li X, Wang X, Zhang S, Liu D, Duan Y, Dong W (2012) Identification of soybean microRNAs involved in soybean cyst nematode infection by deep sequencing. PLoS One 7:e39650PubMedPubMedCentralGoogle Scholar
  50. Li J, Luan Y, Liu Z (2015) SpWRKY1 mediates resistance to Phytophthora infestans and tolerance to salt and drought stress by modulating reactive oxygen species homeostasis and expression of defense-related genes in tomato. Plant Cell Tissue Organ Cult 123:67–81Google Scholar
  51. Li K, Yang F, Zhang G, Song S, Li Y, Miao Y, Song CP (2017) AIK1, a mitogen-activated protein kinase, modulates abscisic acid responses through the MKK5-MPK6 kinase Cascade. Plant Physiol 173:1391–1408PubMedGoogle Scholar
  52. Lin Z, Zhong S, Grierson D (2009) Recent advances in ethylene research. J Exp Bot 60:3311–3336PubMedGoogle Scholar
  53. Loake G, Grant M (2007) Salicylic acid in plant defence-the players and protagonists. Curr Opin Plant Biol 10:466–472PubMedGoogle Scholar
  54. Luan Y, Cui J, Zhai J, Li J, Han L, Meng J (2015) High-throughput sequencing reveals differential expression of miRNAs in tomato inoculated with Phytophthora infestans. Planta 241:1405–1416PubMedGoogle Scholar
  55. Luan Y, Cui J, Wang W, Meng J (2016) MiR1918 enhances tomato sensitivity to Phytophthora infestans infection. Sci Rep 6:35858PubMedPubMedCentralGoogle Scholar
  56. Luan Y, Cui J, Li J, Jiang N, Liu P, Meng J (2018) Effective enhancement of resistance to Phytophthora infestans by overexpression of miR172a and b in Solanum lycopersicum. Planta 247:127–138PubMedGoogle Scholar
  57. Mansfeld BN, Colle M, Kang Y, Jones AD, Grumet R (2017) Transcriptomic and metabolomic analyses of cucumber fruit peels reveal a developmental increase in terpenoid glycosides associated with age-related resistance to Phytophthora capsici. Hortic Res 4:17022PubMedPubMedCentralGoogle Scholar
  58. McCormack E, Tsai YC, Braam J (2005) Handling calcium signaling: Arabidopsis CaMs and CMLs. Trends Plant Sci 10:383–389PubMedGoogle Scholar
  59. Mei C, Qi M, Sheng G, Yang Y (2006) Inducible overexpression of a rice allene oxide synthase gene increases the endogenous jasmonic acid level, PR gene expression, and host resistance to fungal infection. Mol Plant Microbe Interact 19:1127–1137PubMedGoogle Scholar
  60. Menke FL, van Pelt JA, Pieterse CM, Klessig DF (2004) Silencing of the mitogen-activated protein kinase MPK6 compromises disease resistance in Arabidopsis. Plant Cell 16:897–907PubMedPubMedCentralGoogle Scholar
  61. Miranda VJ, Porto WF, Fernandes GDR, Pogue R, Nolasco DO, Araujo ACG, Cota LV, Freitas CG, Dias SC, Franco OL (2017) Comparative transcriptomic analysis indicates genes associated with local and systemic resistance to Colletotrichum graminicola in maize. Sci Rep 7:2483PubMedPubMedCentralGoogle Scholar
  62. Nalam VJ, Alam S, Keereetaweep J, Venables B, Burdan D, Lee H, Trick HN, Sarowar S, Makandar R, Shah J (2015) Facilitation of Fusarium graminearum infection by 9-lipoxygenases in Arabidopsis and Wheat. Mol Plant Microbe Interact 28:1142–1152PubMedGoogle Scholar
  63. O’Donnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO, Bowles DJ (1996) Ethylene as a signal mediating the wound response of tomato plants. Science 274:1914–1917PubMedGoogle Scholar
  64. Ouyang S, Park G, Atamian HS, Han CS, Stajich JE, Kaloshian I, Borkovich KA (2014) MicroRNAs suppress NB domain genes in tomato that confer resistance to Fusarium oxysporum. PLoS Pathog 10:e1004464PubMedPubMedCentralGoogle Scholar
  65. Park Y, Hwang J, Kim K, Kang J, Kim B (2013) Development of the gene-based SCARs for the Ph-3 locus, which confers late blight resistance in tomato. Sci Hortic 164:9–16Google Scholar
  66. Penninckx IAMA, Thomma BPHJ, Buchala A, Métraux J-P, Broekaert WF (1998) Concomitant activation of jasmonate and ethylene response pathways is required for induction of a plant defensin gene in Arabidopsis. Plant Cell 10:2103–2113PubMedPubMedCentralGoogle Scholar
  67. Pieterse CM, Leon-Reyes A, Van der Ent S, Van Wees SC (2009) Networking by small-molecule hormones in plant immunity. Nat Chem Biol 5:308–316PubMedGoogle Scholar
  68. Pilcher RL, Moxon S, Pakseresht N, Moulton V, Manning K, Seymour G, Dalmay T (2007) Identification of novel small RNAs in tomato (Solanum lycopersicum). Planta 226:709–717PubMedGoogle Scholar
  69. Pozo MJ, Van Loon LC, Pieterse CMJ (2004) Jasmonates-signals in plant-microbe interactions. J Plant Growth Regul 23:211–222Google Scholar
  70. Robert-Seilaniantz A, Grant M, Jones JD (2011) Hormone crosstalk in plant disease and defense: more than just jasmonate-salicylate antagonism. Annu Rev Phytopathol 49:317–343PubMedGoogle Scholar
  71. Royo J, León J, Vancanneyt G, Albar JP, Rosahl S, Ortego F, Castañera P, Sánchez-Serrano JJ (1999) Antisense-mediated depletion of a potato lipoxygenase reduces wound induction of proteinase inhibitors and increases weight gain of insect pests. Proc Natl Acad Sci USA 96:1146–1151PubMedGoogle Scholar
  72. Salvucci A, Aegerter BJ, Miyao EM, Stergiopoulos I (2016) First report of powdery mildew caused by Oidium lycopersici in field-grown tomatoes in California. Plant Dis 100:1497Google Scholar
  73. Sánchez-Vallet A, McDonald MC, Solomon PS, McDonald BA (2015) Is Zymoseptoria tritici a hemibiotroph? Fungal Genet Biol 79:29–32PubMedGoogle Scholar
  74. Shi Q, Febres VJ, Jones JB, Moore GA (2016) A survey of FLS2 genes from multiple citrus species identifies candidates for enhancing disease resistance to Xanthomonas citri ssp. citri. Hortic Res 3:16022PubMedPubMedCentralGoogle Scholar
  75. Shivaprasad PV, Chen HM, Patel K, Bond DM, Santos BA, Baulcombe DC (2012) A microRNA superfamily regulates nucleotide binding site–leucine-rich repeats and other mRNAs. Plant Cell 24:859–874PubMedPubMedCentralGoogle Scholar
  76. Sivasankar S, Sheldrick B, Rothstein SJ (2000) Expression of allene oxide synthase determines defense gene activation in tomato. Plant Physiol 122:1335–1342PubMedPubMedCentralGoogle Scholar
  77. Takahashi F, Yoshida R, Ichimura K, Mizoguchi T, Seo S, Yonezawa M, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K (2007) The mitogen-activated protein kinase cascade MKK3-MPK6 is an important part of the jasmonate signal transduction pathway in Arabidopsis. Plant Cell 19:805–818PubMedPubMedCentralGoogle Scholar
  78. Tao JJ, Chen HW, Ma B, Zhang WK, Chen SY, Zhang JS (2015) The role of ethylene in plants under salinity stress. Front Plant Sci 6:1059PubMedPubMedCentralGoogle Scholar
  79. Tomato Genome Consortium (2012) The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635–641Google Scholar
  80. Torres MA, Dangl JL (2005) Functions of the respiratory burst oxidase in biotic interactions, abiotic stress and development. Curr Opin Plant Biol 8:397–403PubMedGoogle Scholar
  81. Trapnell C, Pachter L, Salzberg SL (2009) TopHat: discovering splice junctions with RNA-SEq. Bioinformatics 25:1105–1111PubMedPubMedCentralGoogle Scholar
  82. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, Pimentel H, Salzberg SL, Rinn JL, Pachter L (2012) Differential gene and transcript expression analysis of RNA-seq experiments with tophat and cufflinks. Nat Protoc 7:562–578PubMedPubMedCentralGoogle Scholar
  83. Tsushima D, Adkar-Purushothama CR, Taneda A, Sano T (2015) Changes in relative expression levels of viroid-specific small RNAs and microRNAs in tomato plants infected with severe and mild symptom-inducing isolates of Potato spindle tuber viroid. J Gen Plant Pathol 81:49–62Google Scholar
  84. Van Loon LC, Geraats BPJ, Linthorst HJM (2006) Ethylene as a modulator of disease resistance in plants. Trends Plant Sci 11:184–191PubMedGoogle Scholar
  85. Wang W, Luan Y (2015) The advance of tomato disease-related microRNAs. Plant Cell Rep 34:1089–1097PubMedGoogle Scholar
  86. Wasternack C, Kombrink E (2010) Jasmonates: structural requirements for lipid-derived signals active in plant stress responses and development. ACS Chem Biol 5:63–77PubMedGoogle Scholar
  87. Woeste KE, Ye C, Kieber JJ (1999) Two Arabidopsis mutants that overproduce ethylene are affected in the posttranscriptional regulation of 1-aminocyclopropane-1-carboxylic acid synthase. Plant Physiol 119:521–530PubMedPubMedCentralGoogle Scholar
  88. Yang L, Mu X, Liu C, Cai J, Shi K, Zhu W, Yang Q (2015) Overexpression of potato miR482e enhanced plant sensitivity to Verticillium dahliae infection. J Integr Plant Biol 57:1078–1088PubMedGoogle Scholar
  89. Yin ZJ, Shen FF (2010) Identification and characterization of conserved microRNAs and their target genes in wheat (Triticum aestivum). Genet Mol Res 9:1186–1196PubMedGoogle Scholar
  90. Yin X, Wang J, Cheng H, Wang X, Yu D (2013) Detection and evolutionary analysis of soybean miRNAs responsive to soybean mosaic virus. Planta 237:1213–1225PubMedGoogle Scholar
  91. Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol 11:R14PubMedPubMedCentralGoogle Scholar
  92. Zhai J, Jeong DH, De Paoli E, Park S, Rosen BD, Li Y, González AJ, Yan Z, Kitto SL, Grusak MA, Jackson SA, Stacey G, Cook DR, Green PJ, Sherrier DJ, Meyers BC (2011) MicroRNAs as master regulators of the plant NB-LRR defense gene family via the production of phased, trans-acting siRNAs. Genes Dev 25:2540–2553PubMedPubMedCentralGoogle Scholar
  93. Zhang L, Xi D, Luo L, Meng F, Li Y, Wu CA, Guo X (2011) Cotton GhMPK2 is involved in multiple signaling pathways and mediates defense responses to pathogen infection and oxidative stress. FEBS J 278:1367–1378PubMedGoogle Scholar
  94. Zhang C, Liu L, Zheng Z, Sun Y, Zhou L, Yang Y, Cheng F, Zhang Z, Wang X, Huang S, Xie B, Du Y, Bai Y, Li J (2013) Fine mapping of the Ph-3 gene conferring resistance to late blight (Phytophthora infestans) in tomato. Theor Appl Genet 126:2643–2653PubMedGoogle Scholar
  95. Zhang CZ, Liu L, Wang XX, Vossen J, Li GC, Li T, Zheng Z, Gao J, Guo Y, Visser RG, Li J, Bai Y, Du Y (2014) The Ph-3 gene from Solanum pimpinellifolium encodes CC-NBS-LRR protein conferring resistance to Phytophthora infestans. Theor Appl Genet 127:1353–1364PubMedPubMedCentralGoogle Scholar
  96. Zhang Y, Wang W, Chen J, Liu J, Xia M, Shen F (2015a) Identification of miRNAs and their targets in cotton inoculated with Verticillium dahliae by high-throughput sequencing and degradome analysis. Int J Mol Sci 16:14749–14768PubMedPubMedCentralGoogle Scholar
  97. Zhang B, Yang Y, Wang J, Ling X, Hu Z, Liu T, Chen T, Zhang W (2015b) A CC-NBS-LRR type gene GHNTR1 confers resistance to southern root-knot nematode in Nicotiana benthamiana and Nicotiana tabacum. Eur J Plant Pathol 142:715–729Google Scholar
  98. Zhang QY, Zhang LQ, Song LL, Duan K, Li N, Wang YX, Gao QH (2016) The different interactions of Colletotrichum gloeosporioides with two strawberry varieties and the involvement of salicylic acid. Hortic Res 3:16007PubMedPubMedCentralGoogle Scholar
  99. Zhu QH, Fan L, Liu Y, Xu H, Llewellyn D, Wilson I (2013) MiR482 regulation of NBS-LRR defense genes during fungal pathogen infection in cotton. PLoS One 8:e84390PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Ning Jiang
    • 1
  • Jun Cui
    • 1
  • Guanglei Yang
    • 1
  • Xiaoli He
    • 1
  • Jun Meng
    • 2
  • Yushi Luan
    • 1
    Email author
  1. 1.School of Life Science and BiotechnologyDalian University of TechnologyDalianChina
  2. 2.School of Computer Science and TechnologyDalian University of TechnologyDalianChina

Personalised recommendations