Studies review of gene expression regulation of the plant major resistance genes against pathogens
Mariusz Świątek
Pracownia Badania Odporności na Grzyby i Bakterie, Instytut Hodowli i Aklimatyzacji Roślin — Państwowy Instytut Badawczy, Oddział w Młochowie (Poland)
Jadwiga Śliwka
j.sliwka@ihar.edu.plPracownia Badania Odporności na Grzyby i Bakterie, Instytut Hodowli i Aklimatyzacji Roślin — Państwowy Instytut Badawczy, Oddział w Młochowie (Poland)
Abstract
Plants, like animals, have developed multi-layered defense mechanisms that make them resistant to pests and pathogens. Innate basal defense response do not always provide a sufficient level of resistance to pathogens that use a wide range of adaptive mechanisms. Another type of resistance is that conferred by the major resistance genes — R genes. Proteins coded by those genes act as receptors that interact with the corresponding products of avirulence genes of the pathogens. They trigger then signal transduction pathway that leads to hypersensitive reaction, thus preventing the spreading of infection. Due to the high adaptability of pathogens, scientists are forced to search for new resistance genes in wild species of plants that would provide more durable resistance in crops. Despite the fact that the large number of R genes has been identified and cloned up to date, the expression surveys were performed only on a few of them. The R genes have structural similarities but often show different pattern of expression under the influence of biotic and abiotic factors. Most of the R genes are constitutively expressed, but there are also cases of enhancing or inducing the expression as a result of interaction with the pathogen. Molecular research including gene expression issue may have an application aspect in the near future in selection of plants for resistance breeding programs, as was demonstrated in the some experiments. The objective of this review is to pool the information obtained from previous studies on gene expression of plant resistance genes to pathogens.
Supporting Agencies
Keywords:
gene expression, plant pathogens, plant resistance, R genesReferences
Ayliffe M. A., Frost D. V., Finnegan E. J., Lawrence G. J., Anderson P. A., Ellis J. G. 1999. Analysis of alternative transcripts of the flax L6 rust resistance gene. Plant J. 17 (3): 287 — 292.
Google Scholar
Belkhadir Y., Subramaniam R., Dangl J. L. 2004. Plant disease resistance protein signaling: NBS — LRR proteins and their partners. Curr. Opin. Plant Biol. 7 (4): 391 — 399.
Google Scholar
Black W., Mastenbroek C., Mills W. R., Peterson L. C. 1953. A proposal for an international nmomenclature of races of Phytophthora infestans and of genes controlling immunity in Solanum demissum derivatives. Euphytica 2 (3): 173 — 240.
Google Scholar
Bradeen J. M., Iorizzo M., Mollov D. S., Raasch J., Kramer L. C., Millett B. P., Austin-Phillips S., Jiang J., Carputo D. 2009. Higher copy numbers of the potato RB transgene correspond to enhanced transcript and late blight resistance levels. Mol. Plant Microbe Interact. 22 (4): 437 — 446.
Google Scholar
Cao Y., Ding X., Cai M., Zhao J., Lin Y., Li X., Xu C., Wang S. 2007. The expression pattern of a rice disease resistance gene Xa3/Xa26 is differentially regulated by the genetic backgrounds and developmental stages that influence its function. Genetics 177 (1): 523 — 533.
Google Scholar
Catanzariti A., Dodds P. N., Lawrence G. J., Ayliffe M. A., Ellis J. G. 2006. Haustorially expressed secreted proteins from flax rust are highly enriched for avirulence elicitors. Plant Cell 18 (1): 243 — 256.
Google Scholar
Chin D. B., Arroyo-Garcia R., Ochoa O. E., Kesseli R. V., Lavelle D. O., Michelmore R. W. 2001. Recombination and spontaneous mutation at the major cluster of resistance genes in lettuce (Lactuca sativa). Genetics 157 (2): 831 — 849.
Google Scholar
Collier S. M., Moffett P. 2009. NB-LRRs work a ‘‘bait and switch’’ on pathogens. Trends Plant Sci. 14 (10): 521 — 529.
Google Scholar
Dangl J. L., Jones J. D. G. 2001. Plant pathogens and integrated defence responses to infection. Nature 411: 826 — 833.
Google Scholar
Dodds P. N., Rathjen J. P. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11 (8): 539 — 548.
Google Scholar
Glazebrook J., Rogers E. E., Ausubel F. M. 1997. Use of Arabidopsis for genetic dissection of plant defense responses. Annu. Rev. Genet. 31: 547 — 69.
Google Scholar
Gómez-Gómez L., Boller T. 2002. Flagellin perception: a paradigm for innate immunity. Trends Plant Sci. 7 (6): 251 — 256.
Google Scholar
Gu K., Yang B., Tian D., Wu L., Wang D., Sreekala C., Yang F., Chu Z., Wang G., White F. F., Yin Z. 2005. R gene expression induced by a type-III effector triggers disease resistance in rice. Nature 435 (7045): 1122 — 1125.
Google Scholar
Halterman D. A., Wei F., Wise R. P. 2003. Powdery mildew-induced Mla mRNAs are alternatively spliced and contain multiple upstream open reading frames. Plant Physiol. 131(2): 558 — 567.
Google Scholar
Hein I., Gilroy E. M., Armstrong M. R., Birch P. R. J. 2009 a. The zig-zag-zig in oomycete — plant interactions. Mol. Plant Path. 10 (4): 547 — 562.
Google Scholar
Hein I., Birch P. R. J., Danan S., Lefebvre V., Achieng Odeny D., Gebhardt C., Trognitz F., Bryan G. J. 2009 b. Progress in mapping and cloning qualitative and quantitative resistance against Phytophthora infestans in potato and its wild relatives. Potato Research 52: 215 — 227.
Google Scholar
Heath M. C. 2000. Hypersensitive response-related death. Plant Mol. Biol. 44 (3): 321 — 334.
Google Scholar
Huang S., van der Vossen E. A. G., Kuang H., Vleeshouwers V. G. A. A., Zhang N., Borm T. J.A., van Eck H. J., Baker B., Jacobsen E., Visser R. G.F. 2005. Comparative genomics enabled the isolation of the R3a late blight resistance gene in potato. Plant J. 42 (2): 251 — 261.
Google Scholar
Jia Y., McAdams S. A., Bryan G. T.,. Hershey H. P., Valent B. 2000. Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J. 19 (15): 4004 — 4014.
Google Scholar
Jones J. D. 2001. Putting knowledge of plant disease resistance genes to work. Curr. Opin. Plant Biol. 4 (4): 281 — 287.
Google Scholar
Jones J. D., Dangl J. L. 2006. The plant immune system. Nature 444 (7117): 323 — 329.
Google Scholar
Kaku H., Nishizawa Y., Ishii-Minami N., Akimoto-Tomiyama C., Dohmae N., Takio K., Minami E., Shibuya N. 2006. Plant cells recognize chitin fragments for defense signaling through a plasma membrane receptor. Proc. Natl. Acad. Sci. USA 103 (29): 11086 — 11091.
Google Scholar
Kramer L. C., Choudoir M. J., Wielgus S. M., Bhaskar P. B., Jiang J. 2009. Correlation between transcript abundance of the RB gene and the level of the RB-mediated late blight resistance in potato. Mol. Plant Microbe Interact. 22 (4): 447 — 455.
Google Scholar
Levy M., Edelbaum O., Sela I. 2004. Tobacco Mosaic virus regulates the expression of its own resistance gene N1. Plant Physiol. 135 (4): 2392 — 2397.
Google Scholar
Li Y., Tessaro M. J., Li X., Zhang Y. 2010. Regulation of the expression of plant resistance gene SNC1 by a protein with a conserved BAT2 domain. Plant Physiol. 153 (3): 1425 — 1434.
Google Scholar
Lokossou A. A., Park T., van Arkel G., Arens M., Ruyter-Spira C., Morales J., Whisson S. C., Birch P. R. J., Visser R. G. F., Jacobsen E., van der Vossen E. A. G. 2009. Exploiting knowledge of R/Avr genes to rapidly clone a new LZ-NBS-LRR family of late blight resistance genes from potato linkage group IV. Mol. Plant Microbe Interact. 22 (6): 630 — 641.
Google Scholar
Malcolmson J. F., Black W. 1966. New R genes in Solanum demissum Lindl. and their complementary races of Phytophthora infestans (Mont.) De Bary. Euphytica 15: 199 — 203.
Google Scholar
Mackey D., Holt III B. F., Wiig A., Dangl J. L. 2002. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108 (6): 743 — 754.
Google Scholar
Martin G. B., Bogdanove A. J., Sessa G. 2003. Understanding the functions of plant disease resistance proteins. Annu. Rev. Plant Biol. 54: 23 — 61.
Google Scholar
Millett B. P., Mollov D. S., Iorizzo M., Carputo D., Bradeen J. M. 2009. Changes in disease resistance phenotypes associated with plant physiological age are not caused by variation in R gene transcript abundance. Mol. Plant Microbe Interact. 22 (3): 362 — 368.
Google Scholar
Milligan S. B., Bodeau J., Yaghoobi J., Kaloshian I., Zabel P., Williamson V. M. 1998. The root knot nematode resistance gene Mi from tomato is a member of the leucine zipper, nucleotide binding, leucine-rich repeat family of plant genes. Plant Cell 10 (8): 1307 — 1319.
Google Scholar
Nurnberger T., Brunner F., Kemmerling B., Piater L. 2004. Innate immunity in plants and animals: striking similarities and obvious differences. Immunol. Rev. 198: 249 — 266.
Google Scholar
Radwan O., Mouzeyar S., Nicolas P., Bouzidi M. F. 2005. Induction of a sunflower CC-NBS-LRR resistance gene analogue during incompatible interaction with Plasmopara halstedii. J. Exp. Bot. 56 (412): 567 — 575.
Google Scholar
Römer P., Hahn S., Jordan T., Strauß T., Bonas U., Lahaye T. 2007. Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318 (5850): 645 — 648.
Google Scholar
Salmeron J. M., Oldroyd G. E. D., Rommens C. M. T., Scofield S. R., Kim H., Lavelle D. T., Dahlbeck D., Staskawicz B. J. 1996. Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86 (1): 123 — 133.
Google Scholar
Sanseverino W., Roma G., De Simone M., Faino L., Melito S., Stupka E., Frusciante L., Ercolano M. R. 2010. PRGdb: a bioinformatics platform for plant resistance gene analysis. Nucleic Acids Res. Database issue 38: 814 — 821.
Google Scholar
Shen K. A., Chin D. B., Arroyo-Garcia R., Ochoa O. E., Lavelle D. O., Wroblewski T., Meyers B. C., Michelmore R. W. 2002. Dm3 is one member of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. Mol. Plant Microbe Interact. 15 (3): 251 — 261.
Google Scholar
Song J., Bradeen J. M., Naess S. K., Raasch J. A., Wielgus S. M., Haberlach G. T., Liu J., Kuang H., Austin-Phillips S., Buell C. R., Helgeson J. P., Jiang J. 2003. Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc. Natl. Acad. Sci. USA 100(16): 9128 — 9133.
Google Scholar
Śliwka J. 2004. Genetic factors encoding resistance to late blight caused by Phytophthora infestans (Mont.) de Bary on the potato genetic map. Cell. Mol. Biol. Lett. 9 (4B): 855 — 867.
Google Scholar
Tan X., Meyers B. C., Kozik A., West M. A., Morgante M., St Clair D. A., Bent A. F., Michelmore R. W. 2007. Global expression analysis of nucleotide binding site-leucine rich repeat-encoding and related genes in Arabidopsis. BMC Plant Biol. 7: 56.
Google Scholar
Tian D., Traw M. B., Chen J. Q., Kreitman M., Bergelson J. 2003. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423 (6935): 74 — 77.
Google Scholar
Thurau T., Kifle S., Jung C., Cai D. 2003. The promoter of the nematode resistance gene Hs1pro-1 activates a nematode-responsive and feeding site-specific gene expression in sugar beet (Beta vulgaris L.) and Arabidopsis thaliana. Plant Mol. Biol. 52(3): 643 — 660.
Google Scholar
Tör M. 2008. Tapping into molecular conversation between oomycete plant pathogens and their hosts. Eur. J. Plant Pathol. 122: 57 — 69.
Google Scholar
van der Hoorn R. A. L., Kamoun S. 2008. From guard to decoy: A new model for perception of plant pathogen effectors. Plant Cell 20 (8): 2009 — 2017.
Google Scholar
van Ooijen G., van den Burg H. A., Cornelissen B. J. C., Takken F. L. W. 2007. Structure and function of resistance proteins in Solanaceous plants. Annu. Rev. Phytopathol. 45: 43 — 72.
Google Scholar
van der Vossen E., Sikkema A., te Lintel Hekkert B., Gros J., Stevens P., Muskens M., Wouters D., Pereira A., Stiekema W., Allefs S. 2003. An ancient R gene from the wild potato species Solanum bulbocastanum confers broad-spectrum resistance to Phytophthora infestans in cultivated potato and tomato. Plant J. 36 (6): 867 — 882.
Google Scholar
Wang Z., Yano M., Yamanouchi U., Iwamoto M., Monna L., Hayasaka H., Katayose Y., Sasaki T. 1999. The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. Plant J. 19(1): 55 — 64.
Google Scholar
Wang Z., Yamanouchi U., Y. Katayose, Sasaki T., Yano M. 2001. Expression of the Pib rice-blast-resistance gene family is up-regulated by environmental conditions favouring infection and by chemical signals that trigger secondary plant defences. Plant Mol. Biol. 47 (5): 653 — 661.
Google Scholar
Yoshimura S., Yamanouchi U., Uichikatayose Y., Toki S., Wang Z., Kono I., Kurata N., Yano M., Iwata N., Sasaki T. 1998. Expression of Xa1, a bacterial blight-resistance gene in rice, is induced by bacterial inoculation. Proc. Natl. Acad. Sci. USA 95 (4): 1663 — 1668.
Google Scholar
Authors
Mariusz ŚwiątekPracownia Badania Odporności na Grzyby i Bakterie, Instytut Hodowli i Aklimatyzacji Roślin — Państwowy Instytut Badawczy, Oddział w Młochowie Poland
Authors
Jadwiga Śliwkaj.sliwka@ihar.edu.pl
Pracownia Badania Odporności na Grzyby i Bakterie, Instytut Hodowli i Aklimatyzacji Roślin — Państwowy Instytut Badawczy, Oddział w Młochowie Poland
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