Transcriptome Profiling Reveals Differential Gene Expression of Secreted Proteases and Highly Specific Gene Repertoires Involved in Lactarius-Pinus Symbioses.

Nianwu Tang,Francis M Martin,Wenjun Xu,Annie Lebreton,Fuqiang Yu,Yucheng Dai

doi:10.3389/fpls.2021.714393

Abstract

Ectomycorrhizal fungi establish a mutualistic symbiosis in roots of most woody plants. The molecular underpinning of ectomycorrhizal development was only explored in a few lineages. Here, we characterized the symbiotic transcriptomes of several milkcap species (Lactarius, Russulales) in association with different pine hosts. A time-course study of changes in gene expression during the development of L. deliciosus–Pinus taeda symbiosis identified 6 to 594 differentially expressed fungal genes at various developmental stages. Up- or down-regulated genes are involved in signaling pathways, nutrient transport, cell wall modifications, and plant defenses. A high number of genes coding for secreted proteases, especially sedolisins, were induced during root colonization. In contrast, only a few genes encoding mycorrhiza-induced small secreted proteins were identified. This feature was confirmed in several other Lactarius species in association with various pines. Further comparison among all these species revealed that each Lactarius species encodes a highly specific symbiotic gene repertoire, a feature possibly related to their host-specificity. This study provides insights on the genetic basis of symbiosis in an ectomycorrhizal order, the Russulales, which was not investigated so far.

Highlights

Ectomycorrhiza (EcM) is a mutualistic association formed between soil-borne ectomycorrhizal fungi and roots of most woody plants
Up- or down-regulation of genes related to signaling pathways, nutrient transport, cell wall modifications, and plant defenses have been characterized in most EcM interactions investigated so far, indicating their importance for the symbiosis development
This study identified several features in the Lactarius symbiosis-related gene repertoires which have not been reported in other EcM lineages so far, providing new insights on the molecular mechanisms underlying the development of ectomycorrhizal symbioses

Summary

Introduction

Ectomycorrhiza (EcM) is a mutualistic association formed between soil-borne ectomycorrhizal fungi and roots of most woody plants. The establishment of EcM symbiosis entails a series of developmental stages, initiating with a molecular dialogue between rhizospheric hyphae and root cells, proceeding with hyphal proliferation on the root epidermis and culminating with the formation of characteristic extraradical mantle and intraradical Hartig net (Garcia et al, 2015; Genre et al, 2020). These steps require coordinated gene regulations in both partners. Recent large-scale analyses confirmed the lineage-specificity of MiSSPs (Kohler et al, 2015; Miyauchi et al, 2020) and it has been suggested that these specific genes may play a role in EcM host-specificity (Liao et al, 2016; Martin et al, 2016)

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