An NMRA-like protein regulates gene expression in Phytophthora capsici to drive the infection cycle on tomato

Phytophthora spp. cause devastating disease epidemics on important crop plants and pose a grave threat to global crop production. Critically, Phytophthora pathogens represent a distinct evolutionary lineage in which pathogenicity has been acquired independently. Therefore, there is an urgent need to understand and disrupt the processes that drive infection, if we aspire to defeat oomycete parasites in the field. One area that has received little attention thus far in this respect is the regulation of Phytophthora gene expression during infection. Here, we characterise PcNMRAL1, a homolog of the Aspergillus nidulans Nitrogen Metabolite Repression regulator NMRA and demonstrate a role for this protein in progression of the Phytophthora capsici infection cycle. PcNmrAL1 is co-expressed with the biotrophic marker gene Haustorial Membrane Protein 1 (PcHmp1) and when over-expressed, extends the biotrophic infection stage. Microarray analyses revealed that PcNmrAL1 over-expression in P. capsici leads to global transcriptional changes during infection and in vitro. Importantly, detailed analyses reveals that PcNmrAL1 over-expression induces biotrophy-associated genes whilst repressing those associated with necrotrophy. In addition to factors controlling transcription, translation and nitrogen metabolism, PcNMRAL1 helps regulate the expression of a considerable effector repertoire in P. capsici. Our data suggests that PcNMRAL1 is a transcriptional regulator that mediates the biotrophy to necrotrophy transition. PcNMRAL1 represents a novel factor that may drive the Phytophthora disease cycle on crops. This study provides the first insight into the mechanisms that regulate infection-related processes in Phytophthora and provides a platform for further studies aimed at disabling pathogenesis and preventing crop losses.