Abstract
Purpureocillium lilacinum of Ophiocordycipitaceae is one of the most promising and commercialized agents for controlling plant parasitic nematodes, as well as other insects and plant pathogens. However, how the fungus functions at the molecular level remains unknown. Here, we sequenced two isolates (PLBJ-1 and PLFJ-1) of P. lilacinum from different places Beijing and Fujian. Genomic analysis showed high synteny of the two isolates, and the phylogenetic analysis indicated they were most related to the insect pathogen Tolypocladium inflatum. A comparison with other species revealed that this fungus was enriched in carbohydrate-active enzymes (CAZymes), proteases and pathogenesis related genes. Whole genome search revealed a rich repertoire of secondary metabolites (SMs) encoding genes. The non-ribosomal peptide synthetase LcsA, which is comprised of ten C-A-PCP modules, was identified as the core biosynthetic gene of lipopeptide leucinostatins, which was specific to P. lilacinum and T. ophioglossoides, as confirmed by phylogenetic analysis. Furthermore, gene expression level was analyzed when PLBJ-1 was grown in leucinostatin-inducing and non-inducing medium, and 20 genes involved in the biosynthesis of leucionostatins were identified. Disruption mutants allowed us to propose a putative biosynthetic pathway of leucinostatin A. Moreover, overexpression of the transcription factor lcsF increased the production (1.5-fold) of leucinostatins A and B compared to wild type. Bioassays explored a new bioactivity of leucinostatins and P. lilacinum: inhibiting the growth of Phytophthora infestans and P. capsici. These results contribute to our understanding of the biosynthetic mechanism of leucinostatins and may allow us to utilize P. lilacinum better as bio-control agent.
Highlights
Plant parasitic nematodes with wide host ranges cause enormous crop and economic losses amounting to $157 billion annually worldwide [1, 2]
Phylogenomic analysis showed that P. lilacinum was most closely related to T. inflatum and T. ophioglossoides, and the cluster of nematode parasitic fungi and insect pathogens indicated their common origin
polyketide synthase (PKS) and non-ribosomal peptide synthetase (NRPS)-encoding genes were thoroughly characterized and analyzed by phylogenetic analysis, from which we found that lcsA was specific to P. lilacinum and T. ophioglossoides
Summary
Plant parasitic nematodes with wide host ranges cause enormous crop and economic losses amounting to $157 billion annually worldwide [1, 2]. One of the most promising and commercialized agents, Purpureocillium lilacinum, has been evaluated to assess its bio-control activity against plant nematodes in a number of studies [2, 4]. P. lilacinum has been reported to effectively control such species as the cotton aphid Aphis gossypii [5], the greenhouse whitefly Trialeurodes vaporariorum, the glasshouse red spider mite Tetranychus urticae [6], and the leaf-cutting ant Acromyrmex lundii [7]. P. lilacinum is commonly isolated from soil, plant roots, nematodes and insects, and it occasionally infects people. This fungus employs flexible lifestyles, including soil-saprobes, plant-endophytes and nematode pathogens. Opportunistic infection occurs when nematode eggs encounter P. lilacinum; parasitism can be a mechanism for nematode bio-control (Fig 1A). It has been confirmed that a serine protease [9], a cuticle-degrading protease [10] and chitinase [11] play important roles in infection by degrading nematode eggshells
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