RNA-Seq analysis of resistant and susceptible potato varieties during the early stages of potato virus Y infection

BMC Genomics

Jeff H. Chang¹  Alex Buchanan²  James M. Crosslin³  Launa Hamlin³  Aymeric Goyer¹ 

[1] Center for Genome Research and Biocomputing, Oregon State University, Corvallis, OR, USA;Department of Botany and Plant Pathology, Oregon State University, Corvallis, OR, USA;USDA-ARS, Prosser, WA, USA

关键词: Resistance;    Leaf;    RNA-Seq;    Potato;    Potato virus Y;   

Others  :  1221250
DOI  :  10.1186/s12864-015-1666-2

 received in 2015-01-07, accepted in 2015-05-29,  发布年份 2015

【 摘 要 】

Background

Potato virus Y (PVY) is one of the most important plant viruses affecting potato production. The interactions between potato and PVY are complex and the outcome of the interactions depends on the potato genotype, the PVY strain, and the environmental conditions. A potato cultivar can induce resistance to a specific PVY strain, yet be susceptible to another. How a single potato cultivar responds to PVY in both compatible and incompatible interactions is not clear.

Results

In this study, we used RNA-sequencing (RNA-Seq) to investigate and compare the transcriptional changes in leaves of potato upon inoculation with PVY. We used two potato varieties: Premier Russet, which is resistant to the PVY strain O (PVY ^O ) but susceptible to the strain NTN (PVY ^NTN ), and Russet Burbank, which is susceptible to all PVY strains that have been tested. Leaves were inoculated with PVY ^Oor PVY ^NTN , and samples were collected 4 and 10 h post inoculation (hpi). A larger number of differentially expressed (DE) genes were found in the compatible reactions compared to the incompatible reaction. For all treatments, the majority of DE genes were down-regulated at 4 hpi and up-regulated at 10 hpi. Gene Ontology enrichment analysis showed enrichment of the biological process GO term “Photosynthesis, light harvesting” specifically in PVY ^O -inoculated Premier Russet leaves, while the GO term “nucleosome assembly” was largely overrepresented in PVY ^NTN -inoculated Premier Russet leaves and PVY ^O -inoculated Russet Burbank leaves but not in PVY ^O -inoculated Premier Russet leaves. Fewer genes were DE over 4-fold in the incompatible reaction compared to the compatible reactions. Amongst these, five genes were DE only in PVY ^O -inoculated Premier Russet leaves, and all five were down-regulated. These genes are predicted to encode for a putative ABC transporter, a MYC2 transcription factor, a VQ-motif containing protein, a non-specific lipid-transfer protein, and a xyloglucan endotransglucosylase-hydroxylase.

Conclusions

Our results show that the incompatible and compatible reactions in Premier Russet shared more similarities, in particular during the initial response, than the compatible reactions in the two different hosts. Our results identify potential key processes and genes that determine the fate of the reaction, compatible or incompatible, between PVY and its host.

【 授权许可】

   
2015 Goyer et al.

【 图 表 】

Fig. 1.

Fig. 2.

Fig. 3.

Fig. 4.

【 参考文献 】

• [1]Karasev AV, Gray SM. Continuous and emerging challenges of potato virus Y in Potato. Annu Rev Phytopathol. 2013; 51:571-86.
• [2]Karasev AV, Gray SM. Genetic diversity of potato virus Y Complex. Am J Potato Res. 2013; 90(1):7-13.
• [3]Rowley JS, Gray SM, Karasev AV. Screening potato cultivars for new sources of resistance to Potato virus Y. Am J Potato Res. 2014; 92(1):38-48.
• [4]Baebler S, Stare K, Kovac M, Blejec A, Prezelj N, Stare T, et al. Dynamics of responses in compatible potato - Potato virus Y interaction are modulated by salicylic acid. PLos One. 2011;6, e29009.
• [5]Kogovsek P, Ravnikar M. Physiology of the potato-Potato Virus Y interaction. In: Progress in botany. 4th ed. Luttge U, Beyschlag W, Francis D, Cushman J, editors. Springer, Berlin, Heidelberg; 2013: p.101-33.
• [6]Novy RG, Whitworth JL, Stark JC, Love SL, Corsini DL, Pavek JJ, et al. Premier Russet: A dual-purpose, potato cultivar with significant resistance to low temperature sweetening during long-term storage. Am J Potato Res. 2008;85(3):198–209.
• [7]Baebler S, Krecic-Stres H, Rotter A, Kogovsek P, Cankar K, Kok EJ, et al. PVYNTN elicits a diverse gene expression response in different potato genotypes in the first 12 h after inoculation. Mol Plant Pathol. 2009;10(2):263–75.
• [8]Baebler S, Witek K, Petek M, Stare K, Tusek-Znidaric M, Pompe-Novak M, et al. Salicylic acid is an indispensable component of the Ny-1 resistance-gene-mediated response against Potato virus Y infection in potato. J Exp Bot. 2014;65(4):1095–109.
• [9]Celebi-Toprak F, Slack SA, Jahn MM. A new gene, Ny(tbr), for hypersensitivity to Potato virus Y from Solanum tuberosum Maps to chromosome IV. Theor Appl Genet. 2002; 104(4):669-74.
• [10]Xu X, Pan SK, Cheng SF, Zhang B, Mu DS, Ni PX, et al. Genome sequence and analysis of the tuber crop potato. Nature. 2011;475(7355):189–95.
• [11]Lozano R, Ponce O, Ramirez M, Mostajo N, Orjeda G. Genome-wide identification and mapping of NBS-encoding resistance genes in Solanum tuberosum Group Phureja. PLos One. 2012; 7(4): Article ID e34775
• [12]Jupe F, Pritchard L, Etherington GJ, MacKenzie K, Cock PJA, Wright F, et al. Identification and localisation of the NB-LRR gene family within the potato genome. BMC Genomics. 2012;13:75.
• [13]Jupe F, Witek K, Verweij W, Sliwka J, Pritchard L, Etherington GJ, et al. Resistance gene enrichment sequencing (RenSeq) enables reannotation of the NB-LRR gene family from sequenced plant genomes and rapid mapping of resistance loci in segregating populations. Plant J. 2013;76(3):530–44.
• [14]Gao LL, Tu ZJ, Millett BP, Bradeen JM. Insights into organ-specific pathogen defense responses in plants: RNA-seq analysis of potato tuber-Phytophthora infestans interactions. BMC Genomics. 2013; 14:340. BioMed Central Full Text
• [15]Aulakh SS, Veilleux RE, Dickerman AW, Tang GZ, Flinn BS. Characterization and RNA-seq analysis of underperformer, an activation-tagged potato mutant. Plant Mol Biol. 2014; 84(6):635-58.
• [16]Zhang N, Liu BL, Ma CY, Zhang GD, Chang J, Si HJ, et al. Transcriptome characterization and sequencing-based identification of drought-responsive genes in potato. Mol Biol Rep. 2014;41(1):505–17.
• [17]Gao L, Tu Z, Katagiri F, Bradeen JM. RNA-seq analysis of potato tuber transcriptome dynamics in response to the late blight pathogen Phytophthora infestans. Phytopathology. 2011; 101(6):S58.
• [18]Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012;7(3):562–78.
• [19]Cumbie JS, Kimbrel JA, Di YM, Schafer DW, Wilhelm LJ, Fox SE, et al. GENE-counter: a computational pipeline for the analysis of RNA-Seq data for gene expression differences. PLos One. 2011;6(10):e25279.
• [20]Di YM, Schafer DW, Cumbie JS, Chang JH. The NBP negative binomial model for assessing differential gene expression from RNA-Seq. Stat Appl Genet Mol Biol. 2011; 10(1):Article 24.
• [21]Rapaport F, Khanin R, Liang YP, Pirun M, Krek A, Zumbo P, et al. Comprehensive evaluation of differential gene expression analysis methods for RNA-seq data. Genome Biol. 2013;14(9):R95.
• [22]Soneson C, Delorenzi M. A comparison of methods for differential expression analysis of RNA-seq data. BMC Bioinformatics. 2013; 14:91. BioMed Central Full Text
• [23]Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005; 21(18):3674-6.
• [24]Dean JD, Goodwin PH, Hsiang T. Induction of glutathione S-transferase genes of Nicotiana benthamiana following infection by Colletotrichum destructivum and C. orbiculare and involvement of one in resistance. J Exp Bot. 2005; 56(416):1525-33.
• [25]Vlot AC, Dempsey DA, Klessig DF. Salicylic acid, a multifaceted hormone to combat disease. In: Annual review of phytopathology. Annual Reviews, Palo Alto; 2009: p.177-206.
• [26]Gutierrez-Campos R, Torres-Acosta JA, Saucedo-Arias LJ, Gomez-Lim MA. The use of cysteine proteinase inhibitors to engineer resistance against potyviruses in transgenic tobacco plants. Nat Biotechnol. 1999; 17(12):1223-6.
• [27]Tian YP, Valkonen JPT. Genetic determinants of potato virus Y required to overcome or trigger hypersensitive resistance to PVY Strain Group O Controlled by the Gene Ny in Potato. Mol Plant Microbe Interact. 2013; 26(3):297-305.
• [28]Krattinger SG, Lagudah ES, Spielmeyer W, Singh RP, Huerta-Espino J, McFadden H, et al. A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science. 2009;323(5919):1360–3.
• [29]Wang XD, Liu Y, Chen L, Zhao D, Wang XF, Zhang ZY. Wheat resistome in response to barley yellow dwarf virus infection. Funct Integr Genomics. 2013; 13(2):155-65.
• [30]Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, et al. MYC2 differentially modulates diverse jasmonate-dependent functions in Arabidopsis. Plant Cell. 2007;19(7):2225–45.
• [31]Anderson JP, Badruzsaufari E, Schenk PM, Manners JM, Desmond OJ, Ehlert C, et al. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell. 2004;16(12):3460–79.
• [32]Lorenzo O, Chico JM, Sanchez-Serrano JJ, Solano R. Jasmonate-insensitive1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell. 2004; 16(7):1938-50.
• [33]Nickstadt A, Thomma B, Feussner I, Kangasjarvi J, Zeier J, Loeffler C, et al. The jasmonate-insensitive mutant jin1 shows increased resistance to biotrophic as well as necrotrophic pathogens. Mol Plant Pathol. 2004;5(5):425–34.
• [34]Laurie-Berry N, Joardar V, Street IH, Kunkel BN. The Arabidopsis thaliana JASMONATE INSENSITIVE 1 gene is required for suppression of salicylic acid-dependent defenses during infection by Pseudomonas syringae. Mol Plant Microbe Interact. 2006; 19(7):789-800.
• [35]Li N, Li XH, Xiao JH, Wang SP. Comprehensive analysis of VQ motif-containing gene expression in rice defense responses to three pathogens. Plant Cell Rep. 2014; 33(9):1493-505.
• [36]Lai ZB, Li Y, Wang F, Cheng Y, Fan BF, Yu JQ, et al. Arabidopsis sigma factor binding proteins are activators of the WRKY33 transcription factor in Plant Defense. Plant Cell. 2011;23(10):3824–41.
• [37]Pecher P, Eschen-Lippold L, Herklotz S, Kuhle K, Naumann K, Bethke G, et al. The Arabidopsis thaliana mitogen-activated protein kinases MPK3 and MPK6 target a subclass of “VQ-motif”-containing proteins to regulate immune responses. New Phytol. 2014;203(2):592–606.
• [38]Cheng Y, Zhou Y, Yang Y, Chi YJ, Zhou J, Chen JY, et al. Structural and functional analysis of VQ motif-containing proteins in arabidopsis as interacting proteins of WRKY transcription factors. Plant Physiol. 2012;159(2):810–25.
• [39]García-Olmedo F, Molina A, Segura A, Moreno M. The defensive role of nonspecific lipid-transfer proteins in plants. Trends Microbiol. 1995; 3:72-4.
• [40]Hyodo H, Yamakawa S, Takeda Y, Tsuduki M, Yokota A, Nishitani K, et al. Active gene expression of a xyloglucan endotransglucosylase/hydrolase gene, XTH9, in inflorescence apices is related to cell elongation in Arabidopsis thaliana. Plant Mol Biol. 2003;52(2):473–82.
• [41]Dobnik D, Baebler S, Kogovsek P, Pompe-Novak M, Stebih D, Panter G, et al. beta-1,3-glucanase class III promotes spread of PVYNTN and improves in planta protein production. Plant Biotechnol Rep. 2013;7(4):547–55.
• [42]Shin YK, Yum H, Kim ES, Cho H, Gothandam KM, Hyun J, et al. BcXTH1, a Brassica campestris homologue of Arabidopsis XTH9, is associated with cell expansion. Planta. 2006;224(1):32–41.
• [43]Auer PL, Doerge RW. Statistical design and analysis of RNA sequencing data. Genetics. 2010; 185(2):405-16.
• [44]Nicot N, Hausman JF, Hoffmann L, Evers D. Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress. J Exp Bot. 2005; 56(421):2907-14.
• [45]Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C-T method. Nat Protoc. 2008; 3(6):1101-8.
• [46]Oliveros JC. An interactive tool for comparing lists with Venn Diagrams. 2007. http://bioinfogp. cnb.csic.es/tools/venny/index.html webcite