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Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome.

ABSTRACT: Many oomycete and fungal plant pathogens are obligate biotrophs, which extract nutrients only from living plant tissue and cannot grow apart from their hosts. Although these pathogens cause substantial crop losses, little is known about the molecular basis or evolution of obligate biotrophy. Here, we report the genome sequence of the oomycete Hyaloperonospora arabidopsidis (Hpa), an obligate biotroph and natural pathogen of Arabidopsis thaliana. In comparison with genomes of related, hemibiotrophic Phytophthora species, the Hpa genome exhibits dramatic reductions in genes encoding (i) RXLR effectors and other secreted pathogenicity proteins, (ii) enzymes for assimilation of inorganic nitrogen and sulfur, and (iii) proteins associated with zoospore formation and motility. These attributes comprise a genomic signature of evolution toward obligate biotrophy.

SUBMITTER: Baxter L

PROVIDER: S-EPMC3971456 | biostudies-literature | 2010 Dec

REPOSITORIES: biostudies-literature

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Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome.

Baxter Laura L Tripathy Sucheta S Ishaque Naveed N Boot Nico N Cabral Adriana A Kemen Eric E Thines Marco M Ah-Fong Audrey A Anderson Ryan R Badejoko Wole W Bittner-Eddy Peter P Boore Jeffrey L JL Chibucos Marcus C MC Coates Mary M Dehal Paramvir P Delehaunty Kim K Dong Suomeng S Downton Polly P Dumas Bernard B Fabro Georgina G Fronick Catrina C Fuerstenberg Susan I SI Fulton Lucinda L Gaulin Elodie E Govers Francine F Hughes Linda L Humphray Sean S Jiang Rays H Y RHY Judelson Howard H Kamoun Sophien S Kyung Kim K Meijer Harold H Minx Patrick P Morris Paul P Nelson Joanne J Phuntumart Vipa V Qutob Dinah D Rehmany Anne A Rougon-Cardoso Alejandra A Ryden Peter P Torto-Alalibo Trudy T Studholme David D Wang Yuanchao Y Win Joe J Wood Jo J Clifton Sandra W SW Rogers Jane J Van den Ackerveken Guido G Jones Jonathan D G JDG McDowell John M JM Beynon Jim J Tyler Brett M BM

Science (New York, N.Y.) 20101201 6010

Many oomycete and fungal plant pathogens are obligate biotrophs, which extract nutrients only from living plant tissue and cannot grow apart from their hosts. Although these pathogens cause substantial crop losses, little is known about the molecular basis or evolution of obligate biotrophy. Here, we report the genome sequence of the oomycete Hyaloperonospora arabidopsidis (Hpa), an obligate biotroph and natural pathogen of Arabidopsis thaliana. In comparison with genomes of related, hemibiotrop ...[more]

PMID: 21148394

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Project description:Oomycete pathogens cause diverse plant diseases. To successfully colonize their hosts, they deliver a suite of effector proteins that can attenuate plant defenses. In the oomycete downy mildews, effectors carry a signal peptide and an RxLR motif. Hyaloperonospora arabidopsidis (Hpa) causes downy mildew on the model plant Arabidopsis thaliana (Arabidopsis). We investigated if candidate effectors predicted in the genome sequence of Hpa isolate Emoy2 (HaRxLs) were able to manipulate host defenses in different Arabidopsis accessions. We developed a rapid and sensitive screening method to test HaRxLs by delivering them via the bacterial type-three secretion system (TTSS) of Pseudomonas syringae pv tomato DC3000-LUX (Pst-LUX) and assessing changes in Pst-LUX growth in planta on 12 Arabidopsis accessions. The majority (~70%) of the 64 candidates tested positively contributed to Pst-LUX growth on more than one accession indicating that Hpa virulence likely involves multiple effectors with weak accession-specific effects. Further screening with a Pst mutant (ΔCEL) showed that HaRxLs that allow enhanced Pst-LUX growth usually suppress callose deposition, a hallmark of pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI). We found that HaRxLs are rarely strong avirulence determinants. Although some decreased Pst-LUX growth in particular accessions, none activated macroscopic cell death. Fewer HaRxLs conferred enhanced Pst growth on turnip, a non-host for Hpa, while several reduced it, consistent with the idea that turnip's non-host resistance against Hpa could involve a combination of recognized HaRxLs and ineffective HaRxLs. We verified our results by constitutively expressing in Arabidopsis a sub-set of HaRxLs. Several transgenic lines showed increased susceptibility to Hpa and attenuation of Arabidopsis PTI responses, confirming the HaRxLs' role in Hpa virulence. This study shows TTSS screening system provides a useful tool to test whether candidate effectors from eukaryotic pathogens can suppress/trigger plant defense mechanisms and to rank their effectiveness prior to subsequent mechanistic investigation.

Dataset Information

Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome.

Publications

Signatures of adaptation to obligate biotrophy in the Hyaloperonospora arabidopsidis genome.

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