Transcriptome responses to Ralstonia solanacearum infection in the roots of the wild potato Solanum commersonii

Springer Science and Business Media LLC - Tập 16 - Trang 1-16 - 2015
A Paola Zuluaga1, Montserrat Solé1, Haibin Lu1, Elsa Góngora-Castillo2, Brieanne Vaillancourt2, Nuria Coll1, C Robin Buell2, Marc Valls1
1Genetics Department, Universitat de Barcelona and Centre for Research in Agricultural Genomics (CSIC-IRTA-UAB-UB) Edifici CRAG, Campus UAB, Catalonia, Spain
2Department of Plant Biology, Michigan State University, East Lansing, USA

Tóm tắt

Solanum commersonii is a wild potato species that exhibits high tolerance to both biotic and abiotic stresses and has been used as a source of genes for introgression into cultivated potato. Among the interesting features of S. commersonii is resistance to the bacterial wilt caused by Ralstonia solanacearum, one of the most devastating bacterial diseases of crops. In this study, we used deep sequencing of S. commersonii RNA (RNA-seq) to analyze the below-ground plant transcriptional responses to R. solanacearum. While a majority of S. commersonii RNA-seq reads could be aligned to the Solanum tuberosum Group Phureja DM reference genome sequence, we identified 2,978 S. commersonii novel transcripts through assembly of unaligned S. commersonii RNA-seq reads. We also used RNA-seq to study gene expression in pathogen-challenged roots of S. commersonii accessions resistant (F118) and susceptible (F97) to the pathogen. Expression profiles obtained from read mapping to the S. tuberosum reference genome and the S. commersonii novel transcripts revealed a differential response to the pathogen in the two accessions, with 221 (F118) and 644 (F97) differentially expressed genes including S. commersonii novel transcripts in the resistant and susceptible genotypes. Interestingly, 22.6% of the F118 and 12.8% of the F97 differentially expressed genes had been previously identified as responsive to biotic stresses and half of those up-regulated in both accessions had been involved in plant pathogen responses. Finally, we compared two different methods to eliminate ribosomal RNA from the plant RNA samples in order to allow dual mapping of RNAseq reads to the host and pathogen genomes and provide insights on the advantages and limitations of each technique. Our work catalogues the S. commersonii transcriptome and strengthens the notion that this species encodes specific genes that are differentially expressed to respond to bacterial wilt. In addition, a high proportion of S. commersonii-specific transcripts were altered by R. solanacearum only in F118 accession, while phythormone-related genes were highly induced in F97, suggesting a markedly different response to the pathogen in the two plant accessions studied.

Tài liệu tham khảo

Peeters N, Guidot A, Vailleau F, Valls M. Ralstonia solanacearum, a widespread bacterial plant pathogen in the post-genomic era. Mol Plant Pathol. 2013;14(7):651–62.

Coll NS, Valls M. Current knowledge on the Ralstonia solanacearum type III secretion system. Microb Biotech. 2013;6(6):614–20.

Priou S. Integrated management of bacterial wilt and soil-borne diseases of potato in farmer communities of the inter-Andean valleys of Peru and Bolivia. In: Final Technical Report DFID-funded project CRF 7862(C). Lima: CIP; 2004.

Genin S, Denny TP. Pathogenomics of the Ralstonia solanacearum species complex. Ann Rev Phyto. 2012;50:67–89.

Hong J, Ji P, Momol MT, Jones JB, Olson SM, Pradhanang P, et al. Ralstonia solanacearum detection in tomato irrigation ponds and weeds. In: Proceedings of the First International Symposium on Tomato Diseases: 2005. Orlando, FL: ISHS; 2005. p. 309–11.

Qian YL, Wang XS, Wang DZ, Zhang LN, Zu CL, Gao ZL, et al. The detection of QTLs controlling bacterial wilt resistance in tobacco (N. tabacum L.). Euphytica. 2012;192(2):259–66.

Carmeille ACC, Dintinger J, Prior P, Luisetti J, Besse P. Identification of QTLs for Ralstonia solanacearum race 3-phylotype II resistance in tomato. Theor Appl Genet. 2006;113(1):110–21.

Wang JF, Ho FI, Truong HTH, Huang SM, Balatero CH, Dittapongpitch V, et al. Identification of major QTLs associated with stable resistance of tomato cultivar ‘Hawaii 7996’ to Ralstonia solanacearum. Euphytica. 2013;190(2):241–52.

Lebeau AGM, Daunay MC, Wicker E, Chiroleu F, Prior P, Frary A, et al. Genetic mapping of a major dominant gene for resistance to Ralstonia solanacearum in eggplant. Theor Appl Genet. 2013;126(1):143–58.

Ben C, Debell F, Berges H, Bellec A, Jardinaud MF, Anson P, et al. MtQRRS1, an R-locus required for Medicago truncatula quantitative resistance to Ralstonia solanacearum. New Phytol. 2013;199:758–72.

Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, et al. Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. PNAS USA. 2003;100(13):8024–9.

Deslandes L, Olivier J, Theulieres F, Hirsch J, Feng DX, Bittner-Eddy P, et al. Resistance to Ralstonia solanacearum in Arabidopsis thaliana is conferred by the recessive RRS1-R gene, a member of a novel family of resistance genes. PNAS USA. 2002;99(4):2404–9.

Deslandes L, Pileur F, Liaubet L, Camut S, Can C, Williams K, et al. Genetic characterization of RRS1, a recessive locus in Arabidopsis thaliana that confers resistance to the bacterial soilborne pathogen Ralstonia solanacearum. MPMI. 1998;11(7):659–67.

Carputo D, Aversano R, Barone A, Di Matteo A, Iorizzo M, Sigillo L, et al. Resistance to Ralstonia solanacearum of Sexual Hybrids Between Solanum commersonii and S. tuberosum. American J Pot Res. 2009;86(3):196–202.

Narancio R, Zorrilla P, Robello C, Gonzalez M, Vilaro F, Pritsch C, et al. Insights on gene expression response of a characterized resistance genotype of Solanum commersonii Dun. against Ralstonia solanacearum. European J Plant Pathol. 2013;136(4):823–35.

Sequeira L, Rowe PR. Selection and utilization of Solanum phureja clones with high resistance to different strains of Pseudomonas solanacearum. American J Potato Res. 1969;46:451–62.

French ER, De Lindo L. Resistance to Pseudomonas solanacearum in potato. Specificity and temperature sensitivity. Phytopath. 1982;72:1408–12.

Tung PX, Rasco Jr ET, Vander Zaag P, Schmiediche P. Resistance to Pseudomonas solanacearum in the potato: II. Aspects of host-pathogen-environment interaction. Euphytica. 1990;45(3):211–5.

Zuluaga P, Ferreira V, Pianzzola MJ, Siri MI, Coll NS, Valls M. A novel, sensitive method to evaluate potato germplasm for bacterial wilt resistance using a luminescent Ralstonia solanacearum reporter strain. MPMI. 2014;27(3):277–85.

Hawkes JG. Origins of cultivated potatoes and species relationships. In: Bradshaw JE, Mackay GR, editors. Potato Genetics. Wallingford: CAB International; 1994. p. 3–42.

Galván G, Fraguas F, Quirici L, Santos C, Silvera E, Siri M, et al. Solanum Commersonii: una especie con gran potencial para el mejoramiento genético de papa por resistencia a Ralstonia Solanacearum. In: Avances de investigación en recursos genéticos en el cono sur I. Uruguay: Publisher Procisur I. Agrociencia; 2006. p. 87–102.

Gonzalez M, Galvan G, Siri MI, Borges A, Vilaro F. Resistencia a la marchitez bacteriana de la papa en Solanum commersonii Dun. Agrociencia. 2013;17(1):45–54.

Kim-Lee H, Moon JS, Hong YJ, Kim MS, Cho HM. Bacterial wilt resistance in the progenies of the fusion hybrids between haploid of potato and Solanum commersonii. American J Potato Res. 2005;82(2):129–37.

Laferriere LT, Helgeson JP, Allen C. Fertile Solanum tuberosum+S. commersonii somatic hybrids as sources of resistance to bacterial wilt caused by Ralstonia solanacearum. Theor App Genet. 1999;98(8):1272–8.

Siri MI, Galván GA, Quirici L, Silvera E, Villanueva P, Ferreira F, et al. Molecular marker diversity and bacterial wilt resistance in wild Solanum commersonii accessions from Uruguay. Euphytica. 2009;165(2):371–82.

Tao Y, Xie Z, Chen W, Glazebrook J, Chang HS, Han B, et al. Quantitative nature of Arabidopsis responses during compatible and incompatible interactions with the bacterial pathogen Pseudomonas syringae. Plant Cell. 2003;15(2):317–30.

Ren H, Gu G, Long J, Yin Q, Wu T, Song T, et al. Combinative effects of a bacterial type-III effector and a biocontrol bacterium on rice growth and disease resistance. J Biosci. 2006;31(5):617–27.

Gao L, Tu Jin Z, 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):1–12.

Baebler S, Krecic-Stres H, Rotter A, Kogovsek P, Cankar K, Kok EJ, et al. PVY(NTN) 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.

Draffehn AM, Li L, Krezdorn N, Ding J, Lübeck J, Strahwald J, et al. Comparative transcript profiling by SuperSAGE identifies novel candidate genes for controlling potato quantitative resistance to late blight not compromised by late maturity. Frontiers Plant Sci. 2013;4(423):1–21.

Hu J, Barlet X, Deslandes L, Hirsch J, Feng DX, Somssich I, et al. Transcriptional responses of Arabidopsis thaliana during wilt disease caused by the soil-borne phytopathogenic bacterium. Ralstonia solanacearum. PLoS One. 2008;3(7):e2589.

Ishihara T, Mitsuhara, I, Takahashi H, Nakaho K. Transcriptome analysis of quantitative resistance-specific response upon Ralstonia solanacearum infection in tomato. PlosOne 2012; doi:10.1371/journal.pone.0046763.

Esposito N, Ovchinnikova OG, Barone A, Zoina A, Holst O, Evidente A. Host and non-host plant response to bacterial wilt in potato: role of the lipopolysaccharide isolated from Ralstonia solanacearum and molecular analysis of plant-pathogen interaction. Chem Biodivers. 2008;5(12):2662–75.

Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5(7):621–8.

Monteiro F, Genin S, van Dijk I, Valls M. A luminescent reporter evidences active expression of Ralstonia solanacearum type III secretion system genes throughout plant infection. Microbiology. 2012;158(Pt 8):2107–16.

Consortium TPGS. Genome sequence and analysis of the tuber crop potato. Nature. 2011;475(7355):189–95.

Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009;25(9):1105–11.

Schulz MH, Zerbino DR, Vingron M, Birney E. Oases: robust de novo RNA-seq assembly across the dynamic range of expression levels. Bioinformatics. 2012;28(8):1086–92.

Suzek BE, Huang H, McGarvey P, Mazumder R, Wu CH. UniRef: comprehensive and non-redundant UniProt reference clusters. Bioinformatics. 2007;23(10):1282–8.

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215(3):403–10.

Góngora-Castillo E, Fedewa G, Yeo Y, Chappell J, DellaPenna D, Buell CR. Genomic approaches for interrogating the biochemistry of medicinal plant species. Methods Enzymol. 2012;517:139–59.

Wu TD, Watanabe CK. GMAP: a genomic mapping and alignment program for mRNA and EST sequences. Bioinformatics. 2005;21(9):1859–75.

Trapnell C, Williams BA, Pertea G, Mortazavi A, Kwan G, van Baren MJ, et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotech. 2010;28(5):511–5.

Chandran D, Rickert J, Huang Y, Steinwand MA, Marr SK, Wildermuth MC. Atypical E2F transcriptional repressor DEL1 acts at the intersection of plant growth and immunity by controlling the hormone salicylic acid. Cell Host Microbe. 2014;15(4):506–13.

Massa AN, Childs KL, Buell CR. Abiotic and Biotic Stress Responses in Solanum tuberosum Group Phureja DM1-3 516 R44 as Measured through Whole Transcriptome Sequencing. Plant Gen. 2013;6(3):15.

Beffa RS, Neuhaus JM, Meins F. Physiological compensation in antisense transformants: specific induction of an “ersatz” glucan endo-1,3-beta-glucosidase in plants infected with necrotizing viruses. PNAS USA. 1993;90(19):8792–6.

Kombrink E, Schroder M, Hahlbrock K. Several “pathogenesis-related” proteins in potato are 1,3-beta-glucanases and chitinases. PNAS USA. 1988;85(3):782–6.

Melchers LS, Apotheker-de Groot M, van derKnaap JA, Ponstein AS, Sela-Buurlage MB, Bol JF, et al. A new class of tobacco chitinases homologous to bacterial exo-chitinases displays antifungal activity. Plant J: for cell and molecular biology. 1994;5(4):469–80.

Jordá L, Coego A, Conejero V, Vera P. A Genomic Cluster Containing Four Differentially Regulated Subtilisin-like Processing Protease Genes Is in Tomato Plants. J Biol Chem. 1999;274(4):2360–5.

Jorda L, Conejero V, Vera P. Characterization of P69E and P69F, two differentially regulated genes encoding new members of the subtilisin-like proteinase family from tomato plants. Plant Physiol. 2000;122(1):67–74.

Villanueva J, Canals F, Prat S, Ludevid D, Querol E, Aviles FX. Characterization of the wound-induced metallocarboxypeptidase inhibitor from potato. cDNA sequence, induction of gene expression, subcellular immunolocalization and potential roles of the C-terminal propeptide. FEBS Lett. 1998;440(1–2):175–82.

Gonzalez-Lamothe R, El Oirdi M, Brisson N, Bouarab K. The conjugated auxin indole-3-acetic acid-aspartic acid promotes plant disease development. Plant Cell. 2012;24(2):762–77.

Staswick PE, Serban B, Rowe M, Tiryaki I, Maldonado MT, Maldonado MC, et al. Characterization of an Arabidopsis Enzyme Family That Conjugates Amino Acids to Indole-3-Acetic Acid. Plant Cell Online. 2005;17(2):616–27.

Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y. Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. PNAS USA. 2007;104(46):18333–8.

Gutierrez L, Mongelard G, Floková K, Păcurar DI, Novák O, Staswick P, et al. Auxin Controls Arabidopsis Adventitious Root Initiation by Regulating Jasmonic Acid Homeostasis. Plant Cell Online. 2012;24(6):2515–27.

Igarashi D, Tsuda K, Katagiri F. The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J: for cell and, molecular biology. 2012;71(2):194–204.

Mazarei M, Lennon KA, Puthoff DP, Rodermel SR, Baum TJ. Expression of an Arabidopsis phosphoglycerate mutase homologue is localized to apical meristems, regulated by hormones, and induced by sedentary plant-parasitic nematodes. Plant Mol Biol. 2003;53(4):513–30.

Van Ooijen G, Lukasik E, Van Den Burg HA, Vossen JH, Cornelissen BJ, Takken FL. The small heat shock protein 20 RSI2 interacts with and is required for stability and function of tomato resistance protein I-2. Plant J: for cell and, molecular biology. 2010;63(4):563–72.

Maimbo M, Ohnishi K, Hikichi Y, Yoshioka H, Kiba A. Induction of a small heat shock protein and its functional roles in Nicotiana plants in the defense response against Ralstonia solanacearum. Plant Physiol. 2007;145(4):1588–99.

Jiang HW, Liu MJ, Chen IC, Huang CH, Chao LY, Hsieh HL. A glutathione S-transferase regulated by light and hormones participates in the modulation of Arabidopsis seedling development. Plant Physiol. 2010;154(4):1646–58.

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 botany. 2005;56(416):1525–33.

Mur LA, Aubry S, Mondhe M, Kingston-Smith A, Gallagher J, Timms-Taravella E, et al. Accumulation of chlorophyll catabolites photosensitizes the hypersensitive response elicited by Pseudomonas syringae in Arabidopsis. New Phytol. 2010;188(1):161–74.

Meng X, Zhang S. MAPK cascades in plant disease resistance signaling. Ann Rev Phytopatho. 2013;51:245–66.

Carter CJ, Thornburg RW. Tobacco nectarin V is a flavin-containing berberine bridge enzyme-like protein with glucose oxidase activity. Plant Physiol. 2004;134(1):460–9.

Schilmiller AL, Koo AJ, Howe GA. Functional diversification of acyl-coenzyme A oxidases in jasmonic acid biosynthesis and action. Plant Physiol. 2007;143(2):812–24.

X-y Z, Spivey NW, Zeng W, Liu P-P, Fu ZQ, Klessig DF, et al. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe. 2012;11(6):587–96.

Hirsch J, Deslandes L, Feng DX, Balague C, Marco Y. Delayed Symptom Development in ein2-1, an Arabidopsis Ethylene-Insensitive Mutant, in Response to Bacterial Wilt Caused by Ralstonia solanacearum. Phytopathology. 2002;92(10):1142–8.

D’Ovidio R, Mattei B, Roberti S, Bellincampi D. Polygalacturonases, polygalacturonase-inhibiting proteins and pectic oligomers in plant-pathogen interactions. Bioch et biophys acta. 2004;1696(2):237–44.

Zhu W, Ouyang S, Iovene M, O’Brien K, Vuong H, Jiang J, et al. Analysis of 90 Mb of the potato genome reveals conservation of gene structures and order with tomato but divergence in repetitive sequence composition. BMC Genomics. 2008;9:286.

Siri MI, Pianzzola MJ. Genetic diversity and agressiveness of Ralstonia solanacearum strains causing bacterial wilt of potato in Uruguay. Plant Dis. 2011;95(10):1292–301.

Blankenberg D, Gordon A, Von Kuster G, Coraor N, Taylor J, Nekrutenko A, et al. Manipulation of FASTQ data with Galaxy. Bioinformatics. 2010;26(14):1783–5.

Martin M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J. 2011;17(1):10–2.

Langmead B, Trapnell C, Pop M, Salzberg S. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009;10(3):R25.

Li H, Handsaker B, Wysoker A, Fennell T, Ruan J, Homer N, et al. The Sequence Alignment/Map format and SAMtools. Bioinformatics. 2009;25(16):2078–9.

Zerbino DR, Birney E. Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res. 2008;18(5):821–9.

Harris MA, Clark J, Ireland A, Lomax J, Ashburner M, Foulger R, et al. The Gene Ontology (GO) database and informatics resource. Nuc acids res. 2004;32(Database issue):D258–261.

Iseli C, Jongeneel CV, Bucher P. ESTScan: a program for detecting, evaluating, and reconstructing potential coding regions in EST sequences. Proceedings/International Conference on Intelligent Systems for Molecular Biology1999;138-148.

Quevillon E, Silventoinen V, Pillai S, Harte N, Mulder N, Apweiler R, et al. InterProScan: protein domains identifier. Nucl acids res. 2005;33(Web Server issue):W116–120.

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