In vitro resynthesis of lichenization reveals the genetic background of symbiosis-specific fungal-algal interaction in U

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RESEARCH ARTICLE

Open Access

In vitro resynthesis of lichenization reveals the genetic background of symbiosisspecific fungal-algal interaction in Usnea hakonensis Mieko Kono1,2* , Yoshiaki Kon3, Yoshihito Ohmura4, Yoko Satta1 and Yohey Terai1

Abstract Background: Symbiosis is central to ecosystems and has been an important driving force of the diversity of life. Close and long-term interactions are known to develop cooperative molecular mechanisms between the symbiotic partners and have often given them new functions as symbiotic entities. In lichen symbiosis, mutualistic relationships between lichen-forming fungi and algae and/or cyanobacteria produce unique features that make lichens adaptive to a wide range of environments. Although the morphological, physiological, and ecological uniqueness of lichens has been described for more than a century, the genetic mechanisms underlying this symbiosis are still poorly known. Results: This study investigated the fungal-algal interaction specific to the lichen symbiosis using Usnea hakonensis as a model system. The whole genome of U. hakonensis, the fungal partner, was sequenced by using a culture isolated from a natural lichen thallus. Isolated cultures of the fungal and the algal partners were co-cultured in vitro for 3 months, and thalli were successfully resynthesized as visible protrusions. Transcriptomes of resynthesized and natural thalli (symbiotic states) were compared to that of isolated cultures (non-symbiotic state). Sets of fungal and algal genes up-regulated in both symbiotic states were identified as symbiosis-related genes. Conclusion: From predicted functions of these genes, we identified genetic association with two key features fundamental to the symbiotic lifestyle in lichens. The first is establishment of a fungal symbiotic interface: (a) modification of cell walls at fungal-algal contact sites; and (b) production of a hydrophobic layer that ensheaths fungal and algal cells;. The second is symbiosis-specific nutrient flow: (a) the algal supply of photosynthetic product to the fungus; and (b) the fungal supply of phosphorous and nitrogen compounds to the alga. Since both features are widespread among lichens, our result may indicate important facets of the genetic basis of the lichen symbiosis. Keywords: Lichen symbiosis, Resynthesis, Mycobiont-photobiont interaction, Genetic background

* Correspondence: [email protected] 1 SOKENDAI (The Graduate University for Advanced Studies), Department of Evolutionary Studies of Biosystems, Shonan Village, Hayama, Kanagawa 240-0193, Japan 2 Department of Botany, Swedish Museum of Natural History, P.O. Box 50007, SE-104 05 Stockholm, Sweden 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