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      A new species of Albugo parasitic to Arabidopsis thaliana reveals new evolutionary patterns in white blister rusts ( Albuginaceae)

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          Abstract

          The obligate biotrophic lineages of the white blister rusts ( Albuginales, Oomycota) are of ancient origin compared to the rather recently evolved downy mildews, and sophisticated mechanisms of biotrophy and a high degree of adaptation diversity are to be expected in these organisms. Speciation in the biotrophic Oomycetes is usually thought to be the consequence of host adaptation or geographic isolation. Here we report the presence of two distinct species of Albugo on the model plant Arabidopsis thaliana, Albugo candida and Albugo laibachii, the latter being formally described in this manuscript. Both species may occupy the same host within the same environment, but are nevertheless phylogenetically distinct, as inferred from analyses of both mitochondrial and nuclear DNA sequences. Different ways of adapting to their host physiology might constitute an important factor of their different niches. Evidence for this can be gained from the completely different host range of the two pathogens. While Albugo candida is a generalist species, consisting of several physiological varieties, which is able to parasitize a great variety of Brassicaceae, Albugo laibachii has not been found on any host other than Arabidopsis thaliana. Therefore, Albugo laibachii belongs to a group of highly specialised species, like the other known specialist species in Albugo s.s., Albugo koreana, Albugo lepidii and Albugo voglmayrii. The comparative investigation of the effector genes and host targets in the generalist and the specialist species may constitute a model system for elucidating the fundamental processes involved in plant pathogen co-adaptation and speciation.

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          A molecular phylogeny of Phytophthora and related oomycetes.

          Phylogenetic relationships among 50 Phytophthora species and between Phytophthora and other oomycetes were examined on the basis of the ITS sequences of genomic rDNA. Phytophthora grouped with Pythium, Peronospora, and Halophytophthora, distant from genera in the Saprolegniales. Albugo was intermediate between these two groups. Unlike Pythium, Phytophthora was essentially monophyletic, all but three species forming a cluster of eight clades. Two clades contained only species with nonpapillate sporangia. The other six clades included either papillate and semipapillate, or semipapillate and nonpapillate types, transcending traditional morphological groupings, which are evidently not natural assemblages. Peronospora was related to P. megakarya and P. palmivora and appears to be derived from a Phytophthora that has both lost the ability to produce zoospores and become an obligate biotroph. Three other Phytophthoras located some distance from the main Phytophthora-Peronospora cluster probably represent one or more additional genera.
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            Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes.

            Oomycete plant pathogens deliver effector proteins inside host cells to modulate plant defense circuitry and to enable parasitic colonization. These effectors are defined by a conserved motif, termed RXLR (for Arg, any amino acid, Leu, Arg), that is located downstream of the signal peptide and that has been implicated in host translocation. Because the phenotypes of RXLR effectors extend to plant cells, their genes are expected to be the direct target of the evolutionary forces that drive the antagonistic interplay between pathogen and host. We used the draft genome sequences of three oomycete plant pathogens, Phytophthora sojae, Phytophthora ramorum, and Hyaloperonospora parasitica, to generate genome-wide catalogs of RXLR effector genes and determine the extent to which these genes are under positive selection. These analyses revealed that the RXLR sequence is overrepresented and positionally constrained in the secretome of Phytophthora relative to other eukaryotes. The three examined plant pathogenic oomycetes carry complex and diverse sets of RXLR effector genes that have undergone relatively rapid birth and death evolution. We obtained robust evidence of positive selection in more than two-thirds of the examined paralog families of RXLR effectors. Positive selection has acted for the most part on the C-terminal region, consistent with the view that RXLR effectors are modular, with the N terminus involved in secretion and host translocation and the C-terminal domain dedicated to modulating host defenses inside plant cells.
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              Characterization of eds1, a mutation in Arabidopsis suppressing resistance to Peronospora parasitica specified by several different RPP genes.

              The interaction between Arabidopsis and the biotrophic oomycete Peronospora parasitica (downy mildew) provides an attractive model pathosystem to identify molecular components of the host that are required for genotype-specific recognition of the parasite. These components are the so-called RPP genes (for resistance to P. parasitica). Mutational analysis of the ecotype Wassilewskija (Ws-0) revealed an RPP-nonspecific locus called EDS1 (for enhanced disease susceptibility) that is required for the function of RPP genes on chromosomes 3 (RPP1/RPP14 and RPP10) and 4 (RPP12). Genetic analyses demonstrated that the eds1 mutation is recessive and is not a defective allele of any known RPP gene, mapping to the bottom arm of chromosome 3 (approximately 13 centimorgans below RPP1/RPP14). Phenotypically, the Ws-eds1 mutant seedlings supported heavy sporulation by P. parasitica isolates that are each diagnostic for one of the RPP genes in wild-type Ws-0; none of the isolates is capable of sporulating on wild-type Ws-0. Ws-eds1 seedlings exhibited enhanced susceptibility to some P. parasitica isolates when compared with a compatible wild-type ecotype, Columbia, and the eds1 parental ecotype, Ws-0. This was observed as earlier initiation of sporulation and elevated production of conidiosporangia. Surprisingly, cotyledons of Ws-eds1 also supported low sporulation by five isolates of P. parasitica from Brassica oleracea. These isolates were unable to sporulate on > 100 ecotypes of Arabidopsis, including wild-type Ws-0. An isolate of Albugo candida (white blister) from B. oleracea also sporulated on Ws-eds1, but the mutant exhibited no alteration in phenotype when inoculated with several oomycete isolates from other host species. The bacterial resistance gene RPM1, conferring specific recognition of the avirulence gene avrB from Pseudomonas syringae pv glycinea, was not compromised in Ws-eds1 plants. The mutant also retained full responsiveness to the chemical inducer of systemic acquired resistance, 2,6-dichloroisonicotinic acid; Ws-eds1 seedlings treated with 2,6-dichloroisonicotinic acid became resistant to the Ws-0-compatible and Ws-0-incompatible P. parasitica isolates Emwa1 and Noco2, respectively. In summary, the EDS1 gene appears to be a necessary component of the resistance response specified by several RPP genes and is likely to function upstream from the convergence of disease resistance pathways in Arabidopsis.
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                Author and article information

                Journal
                Persoonia
                Persoonia
                Persoonia
                Nationaal Herbarium Nederland & Centraallbureau voor Schimmelcultures
                0031-5850
                1878-9080
                26 May 2009
                June 2009
                : 22
                : 123-128
                Affiliations
                [1 ]University of Hohenheim, Institute of Botany 210, 70593 Stuttgart, Germany;
                [2 ]Sainsbury Laboratory, Colney Lane, Norwich NR4 7UH, United Kingdom.
                [3 ]Korea University, Division of Environmental Science and Ecological Engineering, Seoul 136-701, Korea.
                [4 ]University of Warwick, Warwick Life Sciences, Wellesbourne campus, CV35 9EF, United Kingdom.
                Author notes
                corresponding author e-mail: thines@ 123456uni-hohenheim.de.
                Article
                10.3767/003158509X457931
                2789544
                20198144
                5fec79a8-9d6e-4b17-8651-026e69481085
                © 2009 Nationaal Herbarium Nederland & Centraalbureau voor Schimmelcultures

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                History
                : 3 February 2009
                : 20 April 2009
                Categories
                Research Article

                Plant science & Botany
                phylogeny,effector gene,albuginales,oospore morphology,speciation,plant pathogen

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