期刊论文详细信息
BMC Genomics
Transcriptome dynamics of Arabidopsis thaliana root penetration by the oomycete pathogen Phytophthora parasitica
Mathieu Gourgues2  Michel Ponchet2  Cindy Maggio2  Emeline Deleury2  Franck Panabières2  Naïma Kebdani-Minet2  Edouard Evangelisti1  Agnès Attard2 
[1] Sainsbury Laboratory (SLCU), University of Cambridge, Bateman Street, Cambridge CB2 1LR, UK;Université de Nice Sophia-Antipolis, UMR Institut Sophia Agrobiotech, INRA1355-CNRS7254-UNSA, 400 route des chappes, F-06903 Sophia Antipolis, France
关键词: Root infection;    Transcriptome;    Appressorium;    Arabidopsis thaliana;    Phytophthora;   
Others  :  856801
DOI  :  10.1186/1471-2164-15-538
 received in 2013-10-04, accepted in 2014-06-03,  发布年份 2014
PDF
【 摘 要 】

Background

Oomycetes are a group of filamentous microorganisms that includes both animal and plant pathogens and causes major agricultural losses. Phytophthora species can infect most crops and plants from natural ecosystems. Despite their tremendous economic and ecologic importance, few effective methods exist for limiting the damage caused by these species. New solutions are required, and their development will require improvements in our understanding of the molecular events governing infection by these pathogens. In this study, we characterized the genetic program activated during penetration of the plant by the soil-borne pathogen Phytophthora parasitica.

Results

Using all the P. parasitica sequences available in public databases, we generated a custom oligo-array and performed a transcriptomic analysis of the early events of Arabidopsis thaliana infection. We characterized biological stages, ranging from the appressorium-mediated penetration of the pathogen into the roots to the occurrence of first dead cells in the plant. We identified a series of sequences that were transiently modulated during host penetration. Surprisingly, we observed an overall down regulation of genes encoding proteins involved in lipid and sugar metabolism, and an upregulation of functions controlling the transport of amino acids. We also showed that different groups of genes were expressed by P. parasitica during host penetration and the subsequent necrotrophic phase. Differential expression patterns were particularly marked for cell wall-degrading enzymes and other proteins involved in pathogenicity, including RXLR effectors. By transforming P. parasitica with a transcriptional fusion with GFP, we showed that an RXLR-ecoding gene was expressed in the appressorium and infectious hyphae during infection of the first plant cell.

Conclusion

We have characterized the genetic program activated during the initial invasion of plant cells by P. parasitica. We showed that a specific set of proteins, including effectors, was mobilized for penetration and to facilitate infection. Our detection of the expression of an RXLR encoding gene by the appressorium and infection hyphae highlights a role of this structure in the manipulation of the host cells.

【 授权许可】

   
2014 Attard et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20140723040637658.pdf 2692KB PDF download
120KB Image download
254KB Image download
111KB Image download
134KB Image download
【 图 表 】

【 参考文献 】
  • [1]Erwin DC, Ribeiro OK: Phytophthora Diseases Worldwide. St. Paul, MN: American Phytopathological Society; 1996.
  • [2]Beakes GW, Glockling SL, Sekimoto S: The evolutionary phylogeny of the oomycete “fungi”. Protoplasma 2011, 249:3-19.
  • [3]Cavalier-Smith T, Chao EE-Y: Phylogeny and Megasystematics of Phagotrophic Heterokonts (Kingdom Chromista). J Mol Evol 2006, 62:388-420.
  • [4]Swiecki TJ, Donald M: Histology of chrysanthemum roots exposed to salinity stress and Phytophthora cryptogea. Can J Bot 1988, 66:280-288.
  • [5]Dale ML, Irwin JAG: Stomata as an infection court for Phytophtora megasperma f. sp. medicaginis in chickpea and a histological study of infection. Phytopathology 1991, 91:375-379.
  • [6]Enkerli K, Hahn MG, Mims CW: Ultrastructure of compatible and incompatible interactions of soybean roots infected with the plant pathogenic oomycete Phytophthora sojae. Can J Bot 1997, 75:1493-1508.
  • [7]Widmer TL, Graham JH, Mitchell DJ: Histological Comparison of Fibrous Root Infection of Disease-Tolerant and Susceptible Citrus Hosts by Phytophthora nicotianae and P. palmivora. Phytopathology 1998, 88:389-395.
  • [8]Kebdani N, Pieuchot L, Deleury E, Panabieres F, Le Berre JY, Gourgues M: Cellular and molecular characterization of Phytophthora parasitica appressorium-mediated penetration. New Phytol 2010, 185:248-257.
  • [9]Bircher U, Hohl HR: Environmental signalling during induction of appressorium formation in Phytophthora. Mycol Res 1997, 101:395-402.
  • [10]Bircher U, Hohl HR: A role for calcium in appressorium induction in Phytophthora palmivora. Bot Helv 1999, 109:55-65.
  • [11]Grenville-Briggs LJ, Anderson VL, Fugelstad J, Avrova AO, Bouzenzana J, Williams A, Wawra S, Whisson SC, Birch PR, Bulone V, van West P: Cellulose Synthesis in Phytophthora infestans Is Required for Normal Appressorium Formation and Successful Infection of Potato. Plant Cell 2008, 20(6):1725.
  • [12]Avrova AO, Boevink PC, Young V, Grenville-Briggs LJ, van West P, Birch PR, Whisson SC: A novel Phytophthora infestans haustorium-specific membrane protein is required for infection of potato. Cell Microbiol 2008, 10:2271-2284.
  • [13]Blanco FA, Judelson HS: A bZIP transcription factor from Phytophthora interacts with a protein kinase and is required for zoospore motility and plant infection. Mol Microbiol 2005, 56:638-648.
  • [14]Li A, Wang Y, Tao K, Dong S, Huang Q, Dai T, Zheng X, Wang Y: PsSAK1, a stress-activated MAP kinase of Phytophthora sojae, is required for zoospore viability and infection of soybean. Mol Plant Microbe Interact 2010, 23:1022-1031.
  • [15]Krämer R, Freytag S, Schmelzer E: In vitro formation of infection structures of Phytophthora infestans is associated with synthesis of stage specific polypeptides. Eur J Plant Pathol 1997, 103:43-53.
  • [16]Grenville-Briggs LJ, Avrova AO, Bruce CR, Williams A, Whisson SC, Birch PR, van West P: Elevated amino acid biosynthesis in Phytophthora infestans during appressorium formation and potato infection. Fungal Genet Biol 2005, 42:244-256.
  • [17]Ebstrup T, Saalbach G, Egsgaard H: A proteomics study of in vitro cyst germination and appressoria formation in Phytophthora infestans. Proteomics 2005, 5:2839-2848.
  • [18]Grenville-Briggs LJ, Avrova AO, Hay RJ, Bruce CR, Whisson SC, van West P: Identification of appressorial and mycelial cell wall proteins and a survey of the membrane proteome of Phytophthora infestans. Fungal Biol 2010, 114:702-723.
  • [19]Judelson HS, Ah-Fong AM, Aux G, Avrova AO, Bruce C, Cakir C, da Cunha L, Grenville-Briggs L, Latijnhouwers M, Ligterink W, Meijer HJ, Roberts S, Thurber CS, Whisson SC, Birch PR, Govers F, Kamoun S, van West P, Windass J: Gene expression profiling during asexual development of the late blight pathogen Phytophthora infestans reveals a highly dynamic transcriptome. Mol Plant Microbe Interact 2008, 21:433-447.
  • [20]Ye W, Wang X, Tao K, Lu Y, Dai T, Dong S, Dou D, Gijzen M, Wang Y: Digital gene expression profiling of the Phytophthora sojae transcriptome. Mol Plant Microbe Interact 2011, 24:1530-1539.
  • [21]Jupe J, Stam R, Howden AJ, Morris JA, Zhang R, Hedley PE, Huitema E: Phytophthora capsici-tomato interaction features dramatic shifts in gene expression associated with a hemi-biotrophic lifestyle. Genome Biol 2013, 14:R63.
  • [22]Attard A, Gourgues M, Galiana E, Panabieres F, Ponchet M, Keller H: Strategies of attack and defense in plant-oomycete interactions, accentuated for Phytophthora parasitica Dastur (syn. P. Nicotianae Breda de Haan). J Plant Physiol 2008, 165:83-94.
  • [23]Attard A, Gourgues M, Callemeyn-Torre N, Keller H: The immediate activation of defense responses in Arabidopsis roots is not sufficient to prevent Phytophthora parasitica infection. New Phytol 2010, 187:449-460.
  • [24]Galiana E, Riviere MP, Pagnotta S, Baudouin E, Panabieres F, Gounon P, Boudier L: Plant-induced cell death in the oomycete pathogen Phytophthora parasitica. Cell Microbiol 2005, 7:1365-1378.
  • [25]Pillitteri LJ, Peterson KM, Horst RJ, Torii KU: Molecular Profiling of Stomatal Meristemoids Reveals New Component of Asymmetric Cell Division and Commonalities among Stem Cell Populations in Arabidopsis. Plant Cell 2011, 23:3260-3275.
  • [26]Laroche-Raynal M, Aspart L, Delseny M, Penon P: Characterization of radish mRNA at three developmental stages. Plant Sci 1984, 35:139-146.
  • [27]Panabières F, Anselem J, Galiana E, Le Berre J-Y: Gene identification in the oomycete pathogen Phytophthora parasitica during in vitro vegetative growth through Expressed sequence tags (ESTs). Fungal Genet Biol 2005, 42:611-623.
  • [28]Shan W, Marshall JS, Hardham AR: Gene expression in germinated cysts of Phytophthora nicotianae. Mol Plant Pathol 2004, 5:317-330.
  • [29]Skalamera D, Wasson AP, Hardham AR: Genes expressed in zoospores of Phytophthora nicotianae. Mol Genet Genomics 2004, 270:549-557.
  • [30]Le Berre JY, Engler G, Panabières F: Exploration of the late stages of the tomato-Phytophthora parasitica interactions through histological analysis and generation of expressed sequence tags. New Phytol 2008, 177:480-492.
  • [31]Apweiler R, Attwood TK, Bairoch A, Bateman A, Birney E, Biswas M, Bucher P, Cerutti L, Corpet F, Croning MD, Durbin R, Falquet L, Fleischmann W, Gouzy J, Hermjakob H, Hulo N, Jonassen I, Kahn D, Kanapin A, Karavidopoulou Y, Lopez R, Marx B, Mulder NJ, Oinn TM, Pagni M, Servant F, Sigrist CJ, Zdobnov EM: The InterPro database, an integrated documentation resource for protein families, domains and functional sites. Nucleic Acids Res 2001, 29:37-40.
  • [32]Gotz S, Garcia-Gomez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, Robles M, Talon M, Dopazo J, Conesa A: High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res 2008, 36:3420-3435.
  • [33]Simon A, Biot E: ANAIS: analysis of NimbleGen arrays interface. Bioinformatics 2010, 26:2468-2469.
  • [34]Sturn A, Quackenbush J, Trajanoski Z: Genesis: Cluster analysis of microarray data. Bioinformatics 2002, 18:207-208.
  • [35]Yan HZ, Liou RF: Selection of internal control genes for real-time quantitative RT-PCR assays in the oomycete plant pathogen Phytophthora parasitica. Fungal Genet Biol 2006, 43:430-438.
  • [36]Livak KJ, Schmittgen TD: Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C(T)) Method. Methods 2001, 25:402-408.
  • [37]Earley KW, Haag JR, Pontes O, Opper K, Juehne T, Song K, Pikaard CS: Gateway-compatible vectors for plant functional genomics and proteomics. Plant J 2006, 45:616-629.
  • [38]Evangelisti E, Govetto B, Minet-Kebdani N, Kuhn M-L, Attard A, Ponchet M, Panabières F, Gourgues M: The Phytophthora parasitica RXLR effector Penetration-Specific Effector 1 favours Arabidopsis thaliana infection by interfering with auxin physiology. New Phytol 2013, 199(2):476-489.
  • [39]Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong MR, Grouffaud S, van West P, Chapman S, Hein I, Toth IK, Pritchard L, Birch PR: A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 2007, 450:115-118.
  • [40]Oh YY, Donofrio N, Pan H, Coughlan S, Brown DE, Meng S, Mitchell T, Dean RA: Transcriptome analysis reveals new insight into appressorium formation and function in the rice blast fungus Magnporthe orizae. Genome Biol 2008, 9:R85. doi:10.1186/gb-2008-9-5-r85
  • [41]O’Connell RJ, Thon MR, Hacquard S, Amyotte SG, Kleemann J, Torres MF, Damm U, Buiate EA, Epstein L, Alkan N, Altmüller J, Alvarado-Balderrama L, Bauser CA, Becker C, Birren BW, Chen Z, Choi J, Crouch JA, Duvick JP, Farman MA, Gan P, Heiman D, Henrissat B, Howard RJ, Kabbage M, Koch C, Kracher B, Kubo Y, Law AD, Lebrun M-H, et al.: Lifestyle transitions in plant pathogenic Colletotrichum fungi deciphered by genome and transcriptome analyses. Nat Genet 2012, 44:1060-1065.
  • [42]Wang Q, Han C, Ferreira AO, Yu X, Ye W, Tripathy S, Kale SD, Gu B, Sheng Y, Sui Y, Wang X, Zhang Z, Cheng B, Dong S, Shan W, Zheng X, Dou D, Tyler BM, Wang Y: Transcriptional programming and functional interactions within the Phytophthora sojae RXLR effector repertoire. Plant Cell 2011, 23:2064-2086.
  文献评价指标  
  下载次数:79次 浏览次数:12次