DOWNY MILDEW RESISTANT 6 and DMR6-LIKE OXYGENASE 1 are partially redundant but distinct suppressors of immunity in Arabidopsis

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Abstract

Arabidopsisdowny mildew resistant 6 (dmr6)mutants have lost their susceptibility to the downy mildewHyaloperonospora arabidopsidis. Here we show thatdmr6is also resistant to the bacteriumPseudomonas syringaeand the oomycetePhytophthora capsici. Resistance is accompanied by enhanced defense gene expression and elevated salicylic acid levels. The suppressive effect of the DMR6 oxygenase was confirmed in transgenic Arabidopsis lines overexpressingDMR6that show enhanced susceptibility toH.arabidopsidis,P.capsici, andP.syringae. Phylogenetic analysis of the superfamily of 2-oxoglutarate Fe(II)-dependent oxygenases revealed a subgroup of DMR6-LIKE OXYGENASEs (DLOs). Within Arabidopsis, DMR6 is most closely related to DLO1 and DLO2. Overexpression ofDLO1andDLO2in thedmr6mutant restored the susceptibility to downy mildew indicating that DLOs negatively affect defense, similar to DMR6.DLO1, but notDLO2, is co-expressed withDMR6, showing strong activation during pathogen attack and following salicylic acid treatment.DMR6andDLO1differ in their spatial expression pattern in downy mildew-infected Arabidopsis leaves;DMR6is mostly expressed in cells that are in contact with hyphae and haustoria ofH.arabidopsidis, whileDLO1is expressed mainly in the vascular tissues near infection sites. Strikingly, thedmr6-3_dlo1double mutant, that is completely resistant toH.arabidopsidis, showed a strong growth reduction that was associated with high levels of salicylic acid. We conclude that DMR6 and DLO1 redundantly suppress plant immunity, but also have distinct activities based on their differential localization of expression.

Significance Statement

Two related oxygenases each suppress immune responses inArabidopsisbut act at different locations in the leaf during downy mildew infection. The partially redundant DMR6/DLO proteins are conserved in all flowering plants and play an important role as suppressors of plant immunity.

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