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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.

Multiple Candidate Effectors from the Oomycete Pathogen Hyaloperonospora arabidopsidis Suppress Host Plant Immunity