Changes in transcriptomic and metabolomic profiles of morphotypes of Ophiocordyceps sinensis within the hemocoel of its

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RESEARCH ARTICLE

Open Access

Changes in transcriptomic and metabolomic profiles of morphotypes of Ophiocordyceps sinensis within the hemocoel of its host larvae, Thitarodes xiaojinensis Miaomiao Li1,2, Qian Meng1, Huan Zhang1, Ruihao Shu1,2, Yanni Zhao1,2, Peipei Wu1,2, Xuan Li1, Guiling Zhou1, Qilian Qin1* and Jihong Zhang1*

Abstract Background: Ophiocordyceps sinensis (Berk.) is a well-known entomopathogenic and medicinal fungus. It parasitizes and mummifies the underground ghost moth larvae to produce a fruiting body named Chinese cordyceps. Specific for the fungus, O. sinensis experiences a biotrophic vegetative growth period spanning over 5 months. During this vegetative growth, it appears successively in the host hemocoel in three/four morphotypes, namely, the yeast-like blastospores (subdivided into proliferative (BP) and stationary phase (BS)), prehyphae (PreHy) and the hyphae (Hy). This peculiar morphogenesis has been elucidated through morphological and ultrastructural observations, but its molecular basis remains cryptic. In this study, transcriptome and metabolome profiling of BP, BS, PreHy and Hy stages were performed to characterize the key genes, metabolites, and signaling pathways that regulated the vegetative development of O. sinensis in Thitarodes xiaojinensis larva. Results: The molecular events and metabolic pathways that regulated different intracellular processes at various stages were examined. Cluster analyses of differentially expressed genes across the four stages revealed the stage specifically enriched pathways. Analysis of metabolome profiles showed that carbon metabolism and several amino acids biosynthesis were significantly perturbed during the tested development stages of O. sinensis in the host hemocoel. Genes homologous to Saccharomyces cerevisiae MAPK cascade were significantly up-regulated during the transition from blastospore to hypha. The up-regulation of Sho1, a regulator protein, suggested nutrient starvation act a role in activation of MAPK pathway and filamentous growth. In addition, up-regulation of several fatty acid synthesis genes and their corresponding products accumulation in the samples of BS might explain more lipid droplets were observed in BS than in BP. Coupled with the upregulation of fatty acid degradation during PreHy and Hy stages, it is presumed that lipid accumulation and mobilization play important roles in filamentous development. (Continued on next page)

* Correspondence: [email protected]; [email protected] 1 State Key Laboratory of Integrated Management of Pest Insects and Rodents, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China Full list of author information is available at the end of the article © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative