Abstract

Pochonia chlamydosporia infects eggs and females of economically important plant-parasitic nematodes. The fungal isolates parasitizing different nematodes are genetically distinct. To understand their intraspecific genetic differentiation, parasitic mechanisms, and adaptive evolution, we assembled seven putative chromosomes of P. chlamydosporia strain 170 isolated from root-knot nematode eggs (~44 Mb, including 7.19% of transposable elements) and compared them with the genome of the strain 123 (~41 Mb) isolated from cereal cyst nematode. We focus on secretomes of the fungus, which play important roles in pathogenicity and fungus-host/environment interactions, and identified 1,750 secreted proteins, with a high proportion of carboxypeptidases, subtilisins, and chitinases. We analyzed the phylogenies of these genes and predicted new pathogenic molecules. By comparative transcriptome analysis, we found that secreted proteins involved in responses to nutrient stress are mainly comprised of proteases and glycoside hydrolases. Moreover, 32 secreted proteins undergoing positive selection and 71 duplicated gene pairs encoding secreted proteins are identified. Two duplicated pairs encoding secreted glycosyl hydrolases (GH30), which may be related to fungal endophytic process and lost in many insect-pathogenic fungi but exist in nematophagous fungi, are putatively acquired from bacteria by horizontal gene transfer. The results help understanding genetic origins and evolution of parasitism-related genes.

Highlights

  • The fungus Pochonia chlamydosporia is a promising biological control agent for sedentary endoparasitic nematodes, including root-knot nematodes Meloidogyne spp., cyst nematodes Heterodera spp. and Globodera spp., and other plant parasitic nematodes (Nacobbus spp. and Rotylenchulus spp.)[1,2]

  • P. chlamydosporia treated with different nutritional stresses shows marked transcriptional reprogramming between treatments, suggesting that special gene families and signal transduction events may be involved in multitrophic lifestyle transitions[1,11]

  • Transcriptome analysis shows that a large fraction of secreted proteins in the P. chlamydosporia strain 123 (PC123) genome are expressed during the endophytic process[12], suggesting essential roles for secreted proteins in the multiple lifestyles of P. chlamydosporia

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Summary

Introduction

The fungus Pochonia chlamydosporia is a promising biological control agent for sedentary endoparasitic nematodes, including root-knot nematodes Meloidogyne spp., cyst nematodes Heterodera spp. and Globodera spp., and other plant parasitic nematodes (Nacobbus spp. and Rotylenchulus spp.)[1,2]. The fungus P. chlamydosporia has a multitrophic lifestyle, which includes soil saprophytism, nematode egg parasitism, and plant root endophytism[1,6,7], suggesting that P. chlamydosporia is able to evolve and adapt to various conditions and environments. We use a low-cost and efficient method, based on Illumina short reads and SMRT sequencing long reads, without optical mapping data, to acquire chromosome assemblies and a high-quality, complete genome of P. chlamydosporia strain 170 (PC170) isolated from the root-knot nematode Meloidogyne incognita, a distinct biotype from PC123. Our results will facilitate a deeper understanding of the genetic mechanisms of parasitism and adaptive evolution of the fungus P. chlamydosporia, and enable the effective development and utilization of this biocontrol agent

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