Abstract
Crop protection strategies that are effective but that reduce our reliance on chemical pesticides are urgently needed to meet the UN sustainable development goals for global food security. Mycoparasitic oomycetes such as Pythium oligandrum and Pythium periplocum, have potential for the biological control of plant diseases that threaten crops and have attracted much attention due to their abilities to antagonize plant pathogens and modulate plant immunity. Studies of the molecular and genetic determinants of mycoparasitism in these species have been less well developed than those of their fungal counterparts. Carbohydrate-active enzymes (CAZymes) from P. oligandrum and P. periplocum are predicted to be important components of mycoparasitism, being involved in the degradation of the cell wall of their oomycete and fungal prey species. To explore the evolution of CAZymes of these species we performed an in silico identification and comparison of the full CAZyme complement (CAZyome) of the two mycoparasitic Pythium species (P. oligandrum and P. periplocum), with seven other Pythium species, and four Phytophthora species. Twenty CAZy gene families involved in the degradation of cellulose, hemicellulose, glucan, and chitin were expanded in, or unique to, mycoparasitic Pythium species and several of these genes were expressed during mycoparasitic interactions with either oomycete or fungal prey, as revealed by RNA sequencing and quantitative qRT-PCR. Genes from three of the cellulose and chitin degrading CAZy families (namely AA9, GH5_14, and GH19) were expanded via tandem duplication and predominantly located in gene sparse regions of the genome, suggesting these enzymes are putative pathogenicity factors able to undergo rapid evolution. In addition, five of the CAZy gene families were likely to have been obtained from other microbes by horizontal gene transfer events. The mycoparasitic species are able to utilize complex carbohydrates present in fungal cell walls, namely chitin and N-acetylglucosamine for growth, in contrast to their phytopathogenic counterparts. Nonetheless, a preference for the utilization of simple sugars for growth appears to be a common trait within the oomycete lineage.
Highlights
The oomycetes are notorious as plant pathogens that cause devastating diseases in crop plants and our natural landscapes
Whilst it is well known that mycoparasitic fungi such as species within the Trichoderma Genus secrete an array of cell wall degrading enzymes during mycoparasitism of their prey, there is more limited information on the molecular mechanisms of mycoparasitism in the oomycete lineage
Through a detailed in silico and transcriptomic analysis, we have investigated the CAZyome of both P. oligandrum and P. periplocum in relation to plant pathogenic oomycetes
Summary
The oomycetes are notorious as plant pathogens that cause devastating diseases in crop plants and our natural landscapes. They typically grow faster than their plant pathogenic counterparts, meaning that they can outcompete other species for rhizosphere space and nutrition and they are able to promote both plant growth (Le Floch et al, 2003), and induced resistance in host plants (Takenaka et al, 2011; Ouyang et al, 2015) Whilst these experiments demonstrate their potential as biological control agents and detailed microscopic analysis has revealed the nature of their mycoparasitic interactions with various prey species (Benhamou et al, 1999; Picard et al, 2000b), there have been fewer mechanistic studies investigating the molecular or genetic determinants of their mycoparasitic lifestyle. These studies were limited either in their methodology (a small sequencing study of 3,000 cDNA clones) or scope (focus on changes in plant roots), respectively, and we still lack a detailed mechanistic understanding of mycoparasitism in the oomycete lineage
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