An NMRA-Like Protein Regulates Gene Expression in Phytophthora capsici to Drive the Infection Cycle on Tomato

Abstract

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 pathogens 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 characterize PcNMRAL1 (Phyca11_505845), 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 coexpressed with the biotrophic marker gene PcHmp1 (haustorial membrane protein 1) and, when overexpressed, extends the biotrophic infection stage. Microarray analyses revealed that PcNmrAL1 overexpression in P. capsici leads to large-scale transcriptional changes during infection and in vitro. Importantly, detailed analysis reveals that PcNmrAL1 overexpression induces biotrophy-associated genes while 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 mechanisms that regulate infection-related processes in Phytophthora spp. and provides a platform for further studies aimed at disabling pathogenesis and preventing crop losses.

Exchanges at the Plant-Oomycete Interface That Influence Disease

“…infestans (Ah-Fong et al, 2017a). NMRA also was proposed to control the transcription of late-induced effectors in Phytophthora capsici (Pham et al, 2018). Spiking at the same time are mRNAs for genes used to assimilate nitrate, which is a nonpreferred nitrogen source compared with amino acids (Abrahamian et al, 2016).…”

Structure and functions of cellular redox sensor HSCARG/NMRAL1, a linkage among redox status, innate immunity, DNA damage response, and cancer

“…Since the structure of NmrA was resolved, researchers have discovered several NmrA-like proteins which are able to bind coenzymes NAD(H) or NADP(H) but lack the function of dehydrogenation, including PadA from Dictyostelium discoideum , QOR2 from Escherichia coli , PcNMRAL1 from Phytophthora capsica [ [5] , [6] , [7] ]. While NmrA and the majority of NmrA-like proteins are identified in bacteria or fungi, HSCARG, which is also known as NMRAL1, is widely present in higher animals.…”

Niche-specific metabolic adaptation in biotrophic and necrotrophic oomycetes is manifested in differential use of nutrients, variation in gene content, and enzyme evolution

“…The same expression profiles were observed in early and late rye media cultures (Fig 10B). As this paper was being written, a microarray study of Phytophthora capsici infecting tomato was published [48]. Our analysis of data from that paper deposited in ArrayExpress showed that the patterns of NR and NMRA expression in Ph .…”

“…capsici were obtained from ArrayExpress accession E-MTAB-5620. Reported in Results are the median-normalized expression values from 8 and 24 hr dpi, based on three biological replicates [48]. Expression of the Hmp1 , Npp1 , and Cdc14 marker genes indicated that these timepoints represent biotrophic and necrotrophic stages similar to the early and late tuber timepoints described for Ph .…”