Holub, E. B.. (2008) Natural history of Arabidopsis thaliana and oomycete symbioses. European Journal of Plant Pathology, Vol.122 (No.1). pp. 91-109. ISSN 0929-1873

Preview

PDF WRAP_Holub_Natural_history_of_Arabidopsis_thaliana_and_oomycete_symbioses.pdf - Requires a PDF viewer such as GSview, Xpdf or Adobe Acrobat Reader Download (789Kb)

Abstract

Molecular ecology of plant–microbe interactions has immediate significance for filling a gap in knowledge between the laboratory discipline of molecular biology and the largely theoretical discipline of evolutionary ecology. Somewhere in between lies conservation biology, aimed at protection of habitats and the diversity of species housed within them. A seemingly insignificant wildflower called Arabidopsis thaliana has an important contribution to make in this endeavour. It has already transformed botanical research with deepening understanding of molecular processes within the species and across the Plant Kingdom; and has begun to revolutionize plant breeding by providing an invaluable catalogue of gene sequences that can be used to design the most precise molecular markers attainable for marker-assisted selection of valued traits. This review describes how A. thaliana and two of its natural biotrophic parasites could be seminal as a model for exploring the biogeography and molecular ecology of plant–microbe interactions, and specifically, for testing hypotheses proposed from the geographic mosaic theory of co-evolution.

Item Type:	Journal Article
Subjects:	Q Science > QK Botany S Agriculture > SB Plant culture
Divisions:	Faculty of Science > Life Sciences (2010- ) > Warwick HRI (2004-2010)
Library of Congress Subject Headings (LCSH):	Biogeography, Molecular ecology
Journal or Publication Title:	European Journal of Plant Pathology
Publisher:	Springer Verlag
ISSN:	0929-1873
Date:	31 July 2008
Volume:	Vol.122
Number:	No.1
Page Range:	pp. 91-109
Identification Number:	10.1007/s10658-008-9286-1
Status:	Peer Reviewed
Access rights to Published version:	Open Access
Description:	Final version (as published)
References:	Aarts, M. G. M., Hekkert, B. L., Holub, E. B., Beynon, J. L., Stiekema, W. J., & Pereira, A. (1998a). Identification of R-gene homologous DNA fragments genetically linked to disease resistance loci in Arabidopsis thaliana. Molecular Plant–Microbe Interactions, 11, 251–258. PubMed CrossRef ChemPort Aarts, N., Metz, M., Holub, E. B., Staskawicz, B. J., Daniels, M. J., & Parker, J. E. (1998b). Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R gene-mediated signalling pathways in Arabidopsis. Proceedings of the National Academy of Science, USA, 95, 10306–10311. CrossRef ChemPort Allen, R. L., Bittner-Eddy, P. D., Grenville-Briggs, L. J., Meitz, J. C., Rehmany, A. P., Rose, L. E., et al. (2004). Host–parasite coevolutionary conflict between Arabidopsis and downy mildew. Science, 306, 1957–1960. PubMed CrossRef ChemPort Arabidopsis Genome Initiative (2000). Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature, 408, 796–815. CrossRef Austin, M. J., Muskett, P., Kahn, K., Feys, B. J., Jones, J. D., & Parker, J. E. (2002). Regulatory role of SGT1 in early R gene-mediated plant defences. Science, 15, 2077–2080. CrossRef Ayers, P. (2005). The fungal thread of death p. 168. St Paul, MN, USA: American Phytopathological Society Press. Azevedo, C., Betsuyaku, S., Peart, J., Takahashi, A., Noël, L., Sadanandom, A., et al. (2006). Role of SGT1 in resistance protein accumulation in plant immunity. The EMBO Journal, 25, 2007–2016. PubMed CrossRef ChemPort Bakker, E. G., Stahl, E. A., Toomajian, C., Nordborg, M., Krietman, M., & Bergelson, J. (2006). Distribution of genetic variation within and among local populations of Arabidopsis thaliana over its species range. Molecular Ecology, 15, 1405–1418. PubMed CrossRef ChemPort Bittner-Eddy, P. D., Crute, I. R., Holub, E. B., & Beynon, J. L. (2000). RPP13 is a simple locus in Arabidopsis for alleles that specify downy mildew resistance to different avirulence determinants in Peronospora parasitica. The Plant Journal, 21, 177–188. PubMed CrossRef ChemPort Borevitz, J. O., Hazen, S. P., Michael, T. P., Morris, G. P., Baxter, I. R., et al. (2007). Genome-wide patterns of single-feature polymorphism in Arabidopsis thaliana. Proceedings of the National Academy of Science, USA, 104, 12057–12062. CrossRef ChemPort Borhan, M. H., Brose, E., Beynon, J. L., & Holub, E. B. (2001). White rust (Albugo candida) resistance loci on three Arabidopsis chromosomes are closely linked to downy mildew (Peronospora parasitica) resistance loci. Molecular Plant Pathology, 2, 87–95. CrossRef ChemPort Borhan, M. H., Gunn, N., Cooper, A., Gulden, S., Tör, M., Rimmer, S. R., et al. (2008). WRR4 encodes a TIR-NB-LRR protein that confers broad spectrum white rust resistance in Arabidopsis thaliana to four physiological races of Albugo candida. Molecular Plant–Microbe Interactions, (in press). Borhan, M. H., Holub, E. B., Beynon, J. L., Rozwadowski, K., & Rimmer, S. R. (2004). The Arabidopsis TIR-NB-LRR gene RAC1 confers resistance to Albugo candida (white rust) and is dependent on EDS1 but not PAD4. Molecular Plant–Microbe Interactions, 17, 711–719. PubMed CrossRef ChemPort Botella, M. A., Coleman, M. J., Hughes, D. E., Nishimura, M. T., Jones, J. D., & Somerville, S. C. (1997). Map positions of 47 Arabidopsis sequences with sequence similarity to disease resistance genes. The Plant Journal, 12, 1197–1211. PubMed CrossRef ChemPort Botella, M. A., Parker, J. E., Frost, L. N., Bittner-Eddy, P. D., Beynon, J. L., Holub, E. B., et al. (1998). Three genes of the Arabidopsis RPP1 complex locus recognize distinct Peronospora parasitica (downy mildew) avirulence determinants. The Plant Cell, 10, 1847–1860. PubMed CrossRef ChemPort Century, K. S., Holub, E. B., & Staskawicz, B. J. (1995). NDR1, a locus of Arabidopsis thaliana that is required for disease resistance to both a bacterial and a fungal pathogen. Proceedings of the National Academy of Science, USA, 92, 6597–6601. CrossRef ChemPort Century, K., Shapiro, A. D., Repetti, P. P., Dahlbeck, D., Holub, E. B., & Staskawicz, B. J. (1997). NDR1, a pathogen induced component required for Arabidopsis disease resistance. Science, 278, 1963–1965. PubMed CrossRef ChemPort Chou, H.-M., Bundock, N., Rolfe, S. A., & Scholes, J. D. (2000). Infection of Arabidopsis thaliana leaves with Albugo candida (white blister rust) causes a reprogramming of host metabolism. Molecular Plant Pathology, 1, 99–113. CrossRef ChemPort Clark, R. M., Schweikert, G., Toomajian, C., Ossowski, S., Zeller, G., et al. (2007). Common sequence diversity in Arabidopsis thaliana. Science, 317, 338–342. PubMed CrossRef ChemPort Cooley, M. B., Pathirana, S., Wu, H. J., Kachroo, P., & Klessig, D. F. (2000). Members of the Arabidopsis HRT/RPP8 family of resistance genes confer resistance to both viral and oomycete pathogens. The Plant Cell, 12, 663–676. PubMed CrossRef ChemPort Cooper, A. J., Latunde-Dada, A. O, Woods-Tör, A., Lynn, J., Lucas, J. A., Crute, I. R., et al. (2008). Basic compatibility of Albugo candida in Arabidopsis thaliana and Brassica juncea causes broad-spectrum suppression of innate immunity. Molecular Plant–Microbe Interactions, (in press). Constantinescu, O., & Fatehi, J. (2002). Peronospora-like fungi (Chromista, Peronosporales) parasitic on Brassicaceae and related hosts. Nova Hedwigia, 74, 291–338. CrossRef Damgaard, C., & Jensen, B. D. (2002). Disease resistance in Arabidopsis thaliana increases the competitive ability and the predicted probability of long-term ecological success under disease pressure. Oikos, 98, 459–466. CrossRef Ellingboe, A. H. (1976). Genetics of host–parasite interactions. In R. Heitefuss, & P. H. Williams (Eds.) Physiological plant pathology (Encyclopedia of plant physiology, new series, vol 4 (pp. 761–778). Berlin: Springer. Ellingboe, A. H. (2001). Plant–pathogen interactions: Genetic and comparative analyses. European Journal of Plant Pathology, 107, 79–84. SpringerLink Eulgem, T., Wang, X. J., Tsuchiya, T., Beasley, B., Tör, M., Zhu, T., et al. (2007). EDM2 is a novel component of RPP7-dependent disease resistance in Arabidopsis that controls RPP7 transcript levels. The Plant Journal, 49, 829–839. PubMed CrossRef ChemPort Eulgem, T., Weigman, V. J., Chang, H. S., McDowell, J. M., Holub, E. B., Glazebrook, J., et al. (2004). Three genetically separable R gene signaling pathways converge to regulate a largely overlapping transcriptome. Plant Physiology, 135, 1129–1144. PubMed CrossRef ChemPort Falk, A., Feys, B. J., Frost, L. N., Jones, J. D., Daniels, M. J., & Parker, J. E. (1999). EDS1, an essential component of R gene-mediated disease resistance in Arabidopsis has homology to eukaryotic lipases. Proceedings of the National Academy of Science, USA, 96, 3292–3297. CrossRef ChemPort Gassmann, W., Hinsch, M. E., & Staskawicz, B. J. (1999). The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. The Plant Journal, 20, 265–277. PubMed CrossRef ChemPort Gäumann, E. (1918). Ueber die Formen der Peronospora parasitica (Pers.) Fries. Beih. Bot. Zentralblatt, 35(1. Abt.), 395–533. Glazebrook, J. (2007). Use of microarry analysis to dissect the plant defence response. Methods of Molecular Biology, 354, 121–130. ChemPort Glazebrook, J., Zook, M., Mert, F., Kagan, I., Rogers, E. E., Crute, I. R., et al. (1997). Phytoalexin-deficient mutants of Arabidopsis reveal that PAD4 encodes a regulatory factor and that four PAD genes contribute to downy mildew resistance. Genetics, 146, 381–392. PubMed ChemPort Göker, M., Riethmüller, A., Voglmayr, H., Weiss, M., & Oberwinkler, F. (2004). Phylogeny of Hyaloperonospora based on nuclear ribosomal internal transcribed spacer sequences. Mycological Progress, 3, 83–94. SpringerLink Gomulkiewicz, R., Drown, D. M., Dybdahl, M. F., Godsoe, W., Nuismer, S. L., Pepin, K. M., et al. (2007). Dos and don’ts of testing the geographic mosaic theory of coevolution. Heredity, 98, 249–258. PubMed CrossRef ChemPort Grant, S. R., Fisher, E. J., Chang, J. H., Mole, B. M., & Dangl, J. L. (2006). Subterfuge and manipulation: Type III effector proteins of phytopathogenic bacteria. Annual Review of Microbiology, 60, 425–449. PubMed CrossRef ChemPort Gunn, N., Byrne, J., & Holub, E. B. (2002). Outcrossing of two homothallic isolates of Peronospora parasitica and segregation of avirulence matching six resistance loci in Arabidopsis thaliana. In P. T. N. Spencer-Phillips, U. Gisi, & A. Lebeda (Eds.) Advances in downy mildew research (pp. 185–188). Dordrecht: Kluwer Academic Publishers. SpringerLink Holt, B. F., Belkhadir, Y., & Dangl, J. L. (2005). Antagonistic control of disease resistance protein stability in the plant immune system. Science, 309, 929–932. PubMed CrossRef ChemPort Holub, E. B. (1997). Organization of resistance genes in Arabidopsis. In I. R. Crute, E. B Holub, & J. J. Burdon (Eds.) The gene-for-gene relationship in plant parasite interactions (pp. 5–26). Wallingford, UK: CAB International. Holub, E. B. (2001). The Arms race is ancient history in Arabidopsis, the wildflower. Nature Reviews Genetics, 2, 516–527. PubMed CrossRef ChemPort Holub, E. B. (2006). Evolution of symbioses between plants and filamentous parasites. Current Opinion of Plant Biology, 9, 397–405. CrossRef ChemPort Holub, E. B. (2007). Natural variation in innate immunity of a pioneer species. Current Opinion of Plant Biology, 10, 415–424. CrossRef ChemPort Holub, E. B., & Beynon, J. L. (1997). Symbiology of mouse-ear cress (Arabidopsis thaliana) and oomycetes. Advances in Botanical Research, 24, 227–273. CrossRef Holub, E. B., Beynon, J. L., & Crute, I. R. (1994). Phenotypic and genotypic characterisation of interactions between isolates of Peronospora parasitica and accessions of Arabidopsis thaliana. Molecular Plant–Microbe Interactions, 7, 223–239. ChemPort Holub, E. B., Brose, E., Tör, M., Clay, C., Crute, I. R., & Beynon, J. L. (1995). Phenotypic_and genotypic variation in the interaction between Arabidopsis thaliana and Albugo candida. Molecular Plant–Microbe Interactions, 8, 916–928. PubMed ChemPort Holub, E. B., & Cooper, A. (2004). Matrix, reinvention in plants: How genetics is unveiling secrets from non-host disease resistance. Trends Plant Science, 9, 211–214. CrossRef ChemPort Jirage, D., Tootle, T. L., Reuber, T. L., Frost, L. N., Feys, B. J., Parker, J. E., et al. (1999). Arabidopsis thaliana PAD4 encodes a lipase-like gene that is important for salicylic acid signaling. Proceedings of the National Academy of Science, USA, 96, 13583–13588. CrossRef ChemPort Jönsson, H., Heisler, M. G., Shapiro, B. E., Meyerowitz, E. M., & Mjolsness, E. (2006). An auxin-driven polarized transport model for phyllotaxis. Proceedings National Academy of Science, USA, 103, 1633–1638. CrossRef Kamoun, S. (2007). Groovy times: Filamentous pathogen effectors revealed. Current Opinion of Plant Biology, 10, 358–365 (Aug issue). CrossRef ChemPort Kazan, K., & Schenk, P. M. (2007). Genomics in induced resistance. In D. Walters, A. Newton, & G. Lyon (Eds.) Induced resistance for plant defence (pp. 31–64). Oxford: Blackwell. CrossRef Koch, E., & Slusarenko, A. (1990). Arabidopsis is susceptible to infection by a downy mildew fungus. The Plant Cell, 2, 437–445. PubMed CrossRef ChemPort Lawton, K., Weymann, K., Friedrich, L., Vernooij, B., Uknes, S., & Ryals, J. (1995). Systemic acquired resistance in Arabidopsis requires salicylic acid but not ethylene. Molecular Plant–Microbe Interactions, 8, 863–870. PubMed ChemPort Lindau, G. (1901). Hilfsbuch für das Sammein Parasitischer Pilze. Berlin: Bornträger Verlag. McCouch, S. (2004). Diversifying selection in plant breeding. PLoS Biology, 2, 1507–1512. CrossRef ChemPort McDowell, J. M., Cuzick, A., Can, C., Beynon, J. L., Dangl, J. D., & Holub, E. B. (2000). Downy mildew (Peronospora parasitica) resistance genes in Arabidopsis vary in functional requirements for NDR1, EDS1, NPR1, and salicylic acid accumulation. The Plant Journal, 22, 523–529. PubMed CrossRef ChemPort McDowell, J. M., Dhandaydham, M., Long, T. A., Aarts, M. G. M., Goff, S., Holub, E. B., et al. (1998). Intragenic recombination and diversifying selection contribute to the evolution of downy mildew resistance at the RPP8 locus of Arabidopsis. The Plant Cell, 10, 1861–1874. PubMed CrossRef ChemPort Michelmore, R. W. & Wong, J. W. (2008). Classical and molecular genetics of Bremia lactucae, lettuce downy mildew. European Journal of Plant Pathology, (this issue). Mitchell-Olds, T., & Schmitt, J. (2006). Genetic mechanisms and evolutionary significance of natural variation in Arabidopsis. Nature, 441, 264–271. CrossRef Muskett, P. R., Kahn, K., Austin, M. J., Moisan, L. J., Sadanandom, A., Shirasu, K., et al. (2002). Arabidopsis RAR1 exerts rate-limiting control of R gene-mediated defences against multiple pathogens. The Plant Cell, 14, 979–992. PubMed CrossRef ChemPort Parker, J. E., Coleman, M. J., Szado, V., Frost, L. N., Schmidt, R., van der Biezen, E. A., et al. (1997). The Arabidopsis downy mildew resistance gene RPP5 shares similarity to the Toll and interleukin-1 receptors with N and L6. The Plant Cell, 9, 879–894. PubMed CrossRef ChemPort Parker, J. E., Holub, E. B., Frost, L. N., Falk, A., Gunn, N. D., & Daniels, M. J. (1996). Characterisation of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes. The Plant Cell, 8, 2033–2046. PubMed CrossRef ChemPort Preston, C. D., Pearman, D. A., & Hall, A. R. (2004). Archaeophytes in Britain. Botanical Journal of the Linnean Society, 145, 257–294. CrossRef Prusinkiewicz, P., Erasmus, Y., Lane, B., Harder, L. D., & Coen, E. (2007). Evolution and development of inflorescence architectures. Science, 316, 1452–1456. PubMed CrossRef ChemPort Rehmany, A. P., Gordon, A., Rose, L. E., Allen, R. L., Armstrong, M. R., Whisson, S. C., et al. (2005). Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. The Plant Cell, 17, 1839–1850. PubMed CrossRef ChemPort Rehmany, A. P., Lynn, J. R., Tör, M., Holub, E. B., & Beynon, J. L. (2000). A comparison of Peronospora parasitica (downy mildew) isolates from Arabidopsis thaliana and Brassica oleracea using amplified fragment length polymorphism and internal transcribed spacer 1 sequence analyses. Fungal Genetics & Biology, 30, 95–103. CrossRef ChemPort Rentel, M. C., Leonelli, L., Dahlbeck, D., Zhao, B., & Staskawicz, B. J. (2008). Recognition of the Hyaloperonospora parasitica effector ATR13 triggers resistance against oomycete, bacterial, and viral pathogens. Proceedings of the National Academy of Science, USA, 105, 1091–1096. Riethmüller, A., Voglmayer, H., Göker, M., Weiß, M., & Oberwinkler, F. (2002). Phylogenetic relationships of the downy mildew (Peronosporales) and related groups based on nuclear large subunit ribosomal DNA sequences. Mycologia, 94, 834–849. CrossRef Rose, L. E., Bittner-Eddy, P. D., Holub, E. B., Langley, C. H., Michelmore, R. W., & Beynon, J. L. (2004). The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis. Genetics, 166, 1517–1527. PubMed CrossRef ChemPort Roetschi, A., Si-Ammour, A., Belbahri, L., Mauch, F., & Mauch-Mani, B. (2001). Characterisation of an Arabidopsis–Phytophthora pathosystem: Resistance requires a functional PAD2 gene and is independent of salicylic acid, ethylene and jasmonic acid signalling. The Plant Journal, 28, 293–305. PubMed CrossRef ChemPort Segal, S. (1969). Ecological notes on wall vegetation p. 326. The Hague, Netherlands: Dr W. Junk. Shen, K. A., Chin, D. B., Arroyo-Garcia, R., Ochoa, O. E., Lavelle, D. O., Wroblewski, T., et al. (2002). Dm3 is one member of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. Molecular Plant–Microbe Interactions, 15, 251–261. PubMed CrossRef
URI:	http://wrap.warwick.ac.uk/id/eprint/102

Data sourced from Thomson Reuters' Web of Knowledge

Request changes to a record

Actions (login required)

View Item