Plant Cell Reports

, Volume 25, Issue 10, pp 1094–1103 | Cite as

Screening and expression analysis of Phytophthora infestans induced genes in potato leaves with horizontal resistance

Genetics and Genomics

Abstract

Horizontal resistance to late blight with quantitative and durable characteristics is a major objective for potato breeding programs. With the aim of investigating the molecular aspects of horizontal resistance, a cDNA microarray was used to identify Phytophthora infestans-induced genes from 100 expressed sequence tags (ESTs) selected from a subtractive cDNA library. Of the 100 cDNA clones represented on the array, 76 were differentially expressed in infected plants as compared with mock-inoculated control plants. Four groups of genes could be identified according to their expression patterns at three time points, 24, 48 and 72 h postinoculation (hpi). Group A appeared to be strongly induced (>10-fold) at 72 hpi. Group B demonstrated up-regulated expression patterns at all the three time points. The transcripts of group C peaked at 48 hpi, while genes of group D were up-regulated at 24 hpi and decreased slightly thereafter. Blast algorithm searches revealed that the largest set of up-regulated genes (about 35%) was assigned to the primary/secondary metabolism. Other genes with known or putative functions included disease defense or cell rescue (about 18%), transcription, signal transduction, cellular transporter/transport facilitation, development, protein synthesis/destination, as well as those playing roles in cellular organization. Furthermore, 15 genes encoding unknown function proteins were also identified. The results indicated that multiple defense mechanisms are involved in horizontal potato resistance to late blight and alteration in metabolic pathways is one of the most important defense responses.

Keywords

Horizontal resistance Late blight Pathogen-induced gene Phytophthora infestans Solanum tuberosum L. 

References

  1. Avrova AO, Stewart HE, De Jong W, Heilbronn J, Lyon GD, Birch PRJ (1999) A cysteine protease gene is expressed early in resistant potato interactions with Phytophthora infestans. Mol Plant Microbe Interact 12:1114–1119PubMedCrossRefGoogle Scholar
  2. Avrova AO, Taleb N, Rokka VM, Heilbronn J, Campbell E, Hein I, Gilroy EM, Cardle L, Bradshaw JE, Stewart HE, Fakim YJ, Loake G, Birch PRJ (2004) Potato oxysterol binding protein and cathepsin B are rapidly up-regulated in independent defense pathways that distinguish R gene-mediated and fieldresistances to Phytophthora infestans. Mol Plant Pathol 5:45–56CrossRefPubMedGoogle Scholar
  3. Ballvora A, Ercolano MR, Weiss J, Meksem K, Bormann CA, Oberhagemann P, Salamini F, Gebhardt C (2002) The R1 gene for potato resistance to late blight belongs to the leucine zipper/NBS/LRR class of plant resistance genes. Plant J 30:361–371PubMedCrossRefGoogle Scholar
  4. Beyer K, Binder A, Boller T, Collinge M (2001) Identification of potato genes induced during colonization by Phytophthora infestans. Mol Plant Pathol 2:125–134CrossRefPubMedGoogle Scholar
  5. Birch PRJ, Avrova AO, Duncan JM, Lyon GD, Toth RL (1999) Isolation of potato genes that are induced during an early stage of the hypersensitive response to Phytophthora infestans. Mol Plant Microbe Interact 12:356–361CrossRefGoogle Scholar
  6. Birch PRJ, Kamoun S (2000) Studying interaction transcriptomes: coordinated analyses of gene expression during plant–microorganism interactions. In: Wood R (ed) New technologies for life science: a trends guide. Elsevier Science, New York, pp 77–82Google Scholar
  7. Birch PRJ, Whisson SC (2001) Phytophthora infestans enters the genomics era. Mol Plant Pathol 2:257–263CrossRefPubMedGoogle Scholar
  8. Collinge M, Boller T (2001) Differential induction of two potato genes, Stprx2 and StNAC, in response to infection by Phytophthora infestans and to wounding. Plant Mol Biol 46:521–529PubMedCrossRefGoogle Scholar
  9. Conrath U, Linke C, Jeblick W, Geigenberger P, Quick PW, Neuhaus HE (2003) Enhanced resistance to Phytophthora infestans and Alternaria solani in leaves or tubers, respectively, of potato plants with decreased activity of the plastic ATP/ADP transporter. Planta 217:75–83PubMedGoogle Scholar
  10. Cooke DEL, Lees AK (2004) Markers, old and new, for examining Phytophthora infestans diversity. Plant Pathol 53:692–704CrossRefGoogle Scholar
  11. Cruickshank G, Stewart HE, Wastie RL (1982) An illustrated assessment key for foliage blight of potatoes. Potato Res 25:213–214CrossRefGoogle Scholar
  12. Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833PubMedCrossRefGoogle Scholar
  13. De Luca V, St-Pierre B (2000) The cell and developmental biology of alkaloid biosynthesis. Trends Plant Sci 5:349–364CrossRefGoogle Scholar
  14. Dellagi A, Heilbronn J, Avrova AO, Montesano M, Palva TE, Stewart HE, Toth IK, Cooke DEL, Lyon GD, Birch PRJ (2000) A potato gene encoding a WRKY-like transcription factor is induced in interactions with Erwinia carotovora subsp. atroseptica and Phytophthora infestans and is coregulated with a class I endochitinase expression. Mol Plant Microbe Interact 13:1092–1101PubMedCrossRefGoogle Scholar
  15. Deyholos M, Galbraith DW (2001) High-density microarrays for gene expression analysis. Cytometry 43:229–238PubMedCrossRefGoogle Scholar
  16. Eulgem T, Rushton PJ, Robatzek S, Somssich IE (2000) The WRKY superfamily of plant transcription factors. Trends Plant Sci 5:199–206PubMedCrossRefGoogle Scholar
  17. Evers D, Ghislain M, Hausman JF, Dommes J (2003) Differential gene expression in two potato lines differing in their resistance to Phytophthora infestans. Plant Physiol 160:709–712CrossRefGoogle Scholar
  18. Fry WE, Goodwin SB (1997) Resurgence of the Irish potato famine fungus. Bioscience 47:363–371CrossRefGoogle Scholar
  19. Gebhardt C, Valkonen JPT (2001) Organization of genes controlling disease resistance in the potato genome. Annu Rev Phytopathol 39:79–102PubMedCrossRefGoogle Scholar
  20. Hammond-Kosack KE, Jones JDG (1996) Resistance gene-dependent plant defense responses. Plant Cell 8:1773–1791PubMedCrossRefGoogle Scholar
  21. Heath MC (2000) Hypersensitive response-related death. Plant Mol Biol 44:321–334PubMedCrossRefGoogle Scholar
  22. Hegedus D, Yu M, Baldwin D, Gruber M, Sharpe A, Parkin I, Whitwill S, Lydiate D (2003) Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Mol Biol 53:383–397PubMedCrossRefGoogle Scholar
  23. Inglis DA, Johnson DA, Legard DE, Fry WE, Hamm PB (1996) Relative resistances of potato clones in response to new and old populations of Phytophthora infestans. Plant Dis 80:575–578CrossRefGoogle Scholar
  24. Jung HW, Hwang KB (2000) Isolation, partial sequencing, and expression of pathogenesis- related cDNA genes from pepper leaves infected by Xanthomonas campestris pv. Vesicatoria. Mol Plant Microbe Interact 13:136–142PubMedCrossRefGoogle Scholar
  25. Kamoun S, Huitema E, Vleeshouwers VGAA (1999) Resistance to oomycetes: a general role for the hypersensitive response? Trends Plant Sci 4:196–200PubMedCrossRefGoogle Scholar
  26. Karrer EE, Beachy RN, Holt CA (1998) Cloning of tobacco genes that elicit the hypersensitive response. Plant Mol Biol 36:681–690PubMedCrossRefGoogle Scholar
  27. Kasinathan V, Wingler A (2004) Effect of reduced arginine decarboxylase activity on salt tolerance and on polyamine formation during salt stress in Arabidopsis thaliana. Physiol Plant 121:101–107PubMedCrossRefGoogle Scholar
  28. Kikuchi K, Ueguchi-Tanaka M, Yoshida KT, Nagato Y, Matsusoka M, Hirano HY (2000) Molecular analysis of the NAC gene family in rice. Mol Gen Genet 262:1047–1051PubMedCrossRefGoogle Scholar
  29. Kuriyama H, Fukuda H (2002) Developmental programmed cell death in plants. Curr Opin Plant Biol 5:568–573PubMedCrossRefGoogle Scholar
  30. Laity JH, Lee BM, Wright PE (2001) Zinc finger proteins: new insights into structural and functional diversity. Curr Opin Struct Bio 11:39–46CrossRefGoogle Scholar
  31. Lee S, Kim SY, Chung E, Joung YH, Pai HS, Hur CG, Choi D (2004) EST and microarray analyses of pathogen-responsive genes in hot pepper (Capsicum annuum L.) non-host resistance against soybean pustule pathogen (Xanthomonas axonopodis pv.glycines). Funct Integr Genomics 4:196–205PubMedCrossRefGoogle Scholar
  32. Linke C, Conrath U, Jeblick W, Betsche T, Mahn A, Duering K, Neuhaus E (2002) Inhibition of the plastidic ATP/ADP transporter protein primes potato tubers for augmented elicitation of defense responses and enhances their resistance against Erwinia carotovora. Plant Physiol 129:1607–1615PubMedCrossRefGoogle Scholar
  33. Mahalingam R, Gomez-Buitrago A, Eckardt N, Shah N, Guevara-Garcia A, Day P, Raina R, Fedoroff NV (2003) Characterizing the stress/defense transcriptome of Arabidopsis. Genome Biol 4(R20):1–14Google Scholar
  34. Maleck K, Levine A, Eulgem T, Morgen A, Schmid J, Lawton K, Dangl JL, Dietrich RA (2000) The transcriptome of Arabidopsis thaliana during systemic acquired resistance. Nat Genet 26:403–410PubMedCrossRefGoogle Scholar
  35. Ozturk N, Talame V, Deyholos M, Michalowski CB, Galbraith DW, Gozukirmizi N, Tuberosa R, Bohnert H (2002) Monitoring large–scale changes in transcript abundance in drought- and salt-stressed barley. Plant Mol Biol 48:551–573CrossRefGoogle Scholar
  36. Peters RD, Platt HW, Hall R, Medina M (1999) Variation in aggressiveness of Canadian isolates of Phytophthora infestans as indicated by their relative abilities to cause potato tuber rot. Plant Dis 83:652–661CrossRefGoogle Scholar
  37. Pontier D, Balague C, Roby D (1999) The hypersensitive response: a programmed cell death associated with plant resistance. Mol Boil Genet 321:721–734Google Scholar
  38. Ren T, Qu F, Morris TJ (2000) HRT gene function requires interaction between a NAC protein and viral capsid protein to confer resistance to turnip crinkle virus. Plant Cell 12:1917–1926PubMedCrossRefGoogle Scholar
  39. Ronning CM, Stegalkina SS, Ascenzi RA, Bougri O, Hart AL, Utterback TR, Vanaken SE, Riedmuller SB, White JA, Cho J, Pertea GM, Lee Y, Karamycheva S, Sultana R, Tsai J, Quackenbush J, Griffiths HM, Restrepo S, Smart CD, Fry WE, Van Der Hoeven R, Tanksley S, Zhang P, Jin H, Yamamoto ML, Bake BJ, Buell CR (2003) Comparative analyses of potato expressed sequence tag libraries. Plant Physiol 131:419–429PubMedCrossRefGoogle Scholar
  40. Ros B, Thümmler F, Wenzel G (2004) Analysis of differentially expressed genes in a susceptible and moderately resistant potato cultivar upon Phytophthora infestans infection. Mol Plant Pathol 5:191–201CrossRefPubMedGoogle Scholar
  41. Ross H (1986) Potato breeding. Problems and perspectives. Adv Plant Breed (Suppl) 13:82–86Google Scholar
  42. Scheideler M, Schlaich NL, Fellenberg K, Beissbarth T, Hauser NC, Vingron M, Slusarenko AJ, Hoheisel JD (2002) Monitoring the switch from housekeeping to pathogen defense metabolism in Arabidopsis thaliana using cDNA arrays. J Biol Chem 277:10555–10561PubMedCrossRefGoogle Scholar
  43. Schenk PM, Kazan K, Wilson I, Anderson JP, Richmond T, Somerville SC, Manners JM (2000) Coordinated plant defense responses in Arabidopsis revealed by microarray analysis. Proc Natl Acad Sci USA 97:11655–11660PubMedCrossRefGoogle Scholar
  44. Smart CD, Fry WE (2001) Invasions of the late blight pathogen: renewed sex and enhanced fitness. Biol Invasions 3:235–243CrossRefGoogle Scholar
  45. Smith TF, Gaiatzes CG, Saxena K, Neer EJ (1999) The WD repeat: a common architecture for diverse functions. Trends Biochem Sci 24:181–185PubMedCrossRefGoogle Scholar
  46. Song J, Bradeen JM, Naess SK, Raasch JA, Wielgus SM, Haberlach GT, Liu J, Kuang H, Austin-Phillips S, Buell CR, Helgeson JP, Jiang J (2003) Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc Natl Acd Sci USA 100:9128–9133CrossRefGoogle Scholar
  47. Taylor MA, Wright F, Davies HV (1994) Characterization of the cDNA clones of two beta-tubulin genes and their expression in the potato plant (Solanum tuberosum L.). Plant Mol Biol 26:1013–1018PubMedCrossRefGoogle Scholar
  48. Tian ZD, Liu J, Xie CH (2003a) Isolation of resistance related-genes to Phytophthora infestans with suppression subtractive hybridization in the R-gene free potato. Acta Genetica Sinica 30:597–605PubMedGoogle Scholar
  49. Tian ZD, Liu J, Xie CH, Song BT (2003b) Cloning of potato POTHR-1 gene and its expression in response to infection by Phytophthora infestans and other abiotic stimuli. Acta Bot Sin 45:959–965Google Scholar
  50. Turkensteen LJ, Flier WG, Wanningen R, Mulder A (2000) Production, survival and infectivity of oospores of Phytophthora infestans. Plant Pathol 49:688–696CrossRefGoogle Scholar
  51. Turner JG, Ellis C, Devoto A (2002) The jasmonate signal pathway. Plant Cell 14:S153–S164Google Scholar
  52. Ŭlker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491–498PubMedCrossRefGoogle Scholar
  53. Vleeshouwers VGAA, Dooijeweert WV, Govers F, Kamoun S, Collen LT (2000) The hypersensitive response is associated with host and nohost resistance to Phytophthora infestans. Planta 210:853–864PubMedCrossRefGoogle Scholar
  54. Walden R, Cordeiro A, Tiburcio AF (1997) Polyamines: small molecules triggering pathways in plant growth and development. Plant Physiol 113:1009–1013PubMedCrossRefGoogle Scholar
  55. Wastie RL (1991) In Phytophthora infestans: The cause of late blight of potato. In: Ingram DS, Williams PH (eds) Advances in plant pathology, vol 7. Academic Press, London, pp 193–223Google Scholar
  56. Weaver LM, Herrmann KM (1997) Dynamics of the shikimate pathway in plants. Trends Plant Sci 2:346–351CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2006

Authors and Affiliations

  1. 1.Key Laboratory of Horticultural Plant BiologyMinistry of Education/National Center for Vegetable Improvement (Central China), Huazhong Agricultural UniversityWuhanPeople’s Republic of China

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