Expanding the Biological Role of Lipo-Chitooligosaccharides and Chitooligosaccharides in Laccaria bicolor Growth and Development.

Manuel I Villalobos Solis,Sylvain Cottaz,Robert L Hettich,Tomás A Rush,Paul E Abraham,Junko Maeda,Nancy L Engle,Jean-Michel Ané,Jesse L Labbé,Margaret K Spangler,Timothy J Tschaplinski,Sébastien Fort

doi:10.3389/ffunb.2022.808578

Abstract

The role of lipo-chitooligosaccharides (LCOs) as signaling molecules that mediate the establishment of symbiotic relationships between fungi and plants is being redefined. New evidence suggests that the production of these molecular signals may be more of a common trait in fungi than what was previously thought. LCOs affect different aspects of growth and development in fungi. For the ectomycorrhizal forming fungi, Laccaria bicolor, the production and effects of LCOs have always been studied with a symbiotic plant partner; however, there is still no scientific evidence describing the effects that these molecules have on this organism. Here, we explored the physiological, molecular, and metabolomic changes in L. bicolor when grown in the presence of exogenous sulfated and non-sulfated LCOs, as well as the chitooligomers, chitotetraose (CO4), and chitooctaose (CO8). Physiological data from 21 days post-induction showed reduced fungal growth in response to CO and LCO treatments compared to solvent controls. The underlying molecular changes were interrogated by proteomics, which revealed substantial alterations to biological processes related to growth and development. Moreover, metabolite data showed that LCOs and COs caused a downregulation of organic acids, sugars, and fatty acids. At the same time, exposure to LCOs resulted in the overproduction of lactic acid in L. bicolor. Altogether, these results suggest that these signals might be fungistatic compounds and contribute to current research efforts investigating the emerging impacts of these molecules on fungal growth and development.

Highlights

Mycorrhizal associations are important mutualisms between plant roots and fungi that allow plants to acquire water and nutrients from the environment in exchange for photosynthates (Jeffries et al, 2003; Bonfante and Anca, 2009; Plett and Martin, 2018; Tedersoo et al, 2020)
There was an exception for growth on day 3, where treatments, C18:1 sulfated (C18):1 sulfated LCOs (sLCOs) and non-sulfated LCOs (nsLCOs), caused decreased radial growth compared to the solvent control
We noticed the presence of a protein annotated as a CMGC/CDK/CDC2 protein kinase

Summary

Introduction

Mycorrhizal associations are important mutualisms between plant roots and fungi that allow plants to acquire water and nutrients from the environment in exchange for photosynthates (Jeffries et al, 2003; Bonfante and Anca, 2009; Plett and Martin, 2018; Tedersoo et al, 2020). The immediate response of plants to the perception of LCOs or COs, produced by symbiotic or beneficial endophytic fungi, are oscillations in nuclear calcium (Ca+2) concentration levels in the epidermal cells of host roots, which subsequently cause Ca+2/calmodulin-dependent protein kinases to regulate the activity of several transcription factors necessary for the establishment of symbiosis or mutualistic associations (Chabaud et al, 2011; Genre et al, 2013; Buendia et al, 2016; Luginbuehl and Oldroyd, 2017; Choi et al, 2018; Cope et al, 2019, 2021; Feng et al, 2019; Skiada et al, 2020). It remains unknown if LCOs and COs from saprotrophic and pathogenic fungi trigger the CSP and if they could use this signaling pathway for colonization of a host plant

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