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

• Published in: The Plant journal : for cell and molecular biology 2015-01, Vol.81 (2), p.210-222
• Main Authors: Zeilmaker, Tieme, Ludwig, Nora R, Elberse, Joyce, Seidl, Michael F, Berke, Lidija, Van Doorn, Arjen, Schuurink, Robert C, Snel, Berend, Van den Ackerveken, Guido
• Format: Article
• Language: English
• Subjects: acid treatment; Arabidopsis; Arabidopsis - genetics; Arabidopsis - metabolism; Arabidopsis - microbiology; Arabidopsis Proteins - genetics; Arabidopsis Proteins - metabolism; Arabidopsis thaliana; bacteria; DMR6-like oxygenase; downy mildew; downy mildew resistant 6; gene overexpression; genetically modified organisms; growth retardation; hyphae; immunity; iron; leaves; Mold; mutants; negative regulator; Oomycetes; Oomycetes - pathogenicity; oxygenases; pathogens; phylogeny; Phytophthora capsici; Plant Diseases - genetics; Plant Diseases - microbiology; Plant Immunity - genetics; Plant Immunity - physiology; Plant pathology; Plant resistance; Pseudomonas syringae; Pseudomonas syringae - pathogenicity; salicylic acid; suppressor; vascular tissues
• ISSN: 0960-7412; 1365-313X
• DOI: 10.1111/tpj.12719

Arabidopsis downy mildew resistant 6 (dmr6) mutants have lost their susceptibility to the downy mildew Hyaloperonospora arabidopsidis. Here we show that dmr6 is also resistant to the bacterium Pseudomonas syringae and the oomycete Phytophthora 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 overexpressing DMR6 that show enhanced susceptibility to H. arabidopsidis, P. capsici, and P. 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 of DLO1 and DLO2 in the dmr6 mutant restored the susceptibility to downy mildew indicating that DLOs negatively affect defense, similar to DMR6. DLO1, but not DLO2, is co‐expressed with DMR6, showing strong activation during pathogen attack and following salicylic acid treatment. DMR6 and DLO1 differ in their spatial expression pattern in downy mildew‐infected Arabidopsis leaves; DMR6 is mostly expressed in cells that are in contact with hyphae and haustoria of H. arabidopsidis, while DLO1 is expressed mainly in the vascular tissues near infection sites. Strikingly, the dmr6‐3_dlo1 double mutant, that is completely resistant to H. 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.