Divergence of a genomic island leads to the evolution of melanization in a halophyte root fungus

Zhilin Yuan,Jieyu Wang,Guohui Shi,Russell J Rodriguez,Qi Wu,Feng Cai,Huanshen Wei,Irina S Druzhinina,Yves Van De Peer,John G Gibbons,Long Peng,Zhenhui Zhong,Francis M Martin,Xinyu Wang,Zhongjian Liu

doi:10.1038/s41396-021-01023-8

Abstract

Understanding how organisms adapt to extreme living conditions is central to evolutionary biology. Dark septate endophytes (DSEs) constitute an important component of the root mycobiome and they are often able to alleviate host abiotic stresses. Here, we investigated the molecular mechanisms underlying the beneficial association between the DSE Laburnicola rhizohalophila and its host, the native halophyte Suaeda salsa, using population genomics. Based on genome-wide Fst (pairwise fixation index) and Vst analyses, which compared the variance in allele frequencies of single-nucleotide polymorphisms (SNPs) and copy number variants (CNVs), respectively, we found a high level of genetic differentiation between two populations. CNV patterns revealed population-specific expansions and contractions. Interestingly, we identified a ~20 kbp genomic island of high divergence with a strong sign of positive selection. This region contains a melanin-biosynthetic polyketide synthase gene cluster linked to six additional genes likely involved in biosynthesis, membrane trafficking, regulation, and localization of melanin. Differences in growth yield and melanin biosynthesis between the two populations grown under 2% NaCl stress suggested that this genomic island contributes to the observed differences in melanin accumulation. Our findings provide a better understanding of the genetic and evolutionary mechanisms underlying the adaptation to saline conditions of the L. rhizohalophila–S. salsa symbiosis.

Highlights

The process by which organisms become better adapted to extreme environments and how natural selection shaped organismal phenotypes and genotypes in response to these intense selective pressures are central to evolutionary biology
We propose that the genomic island contains a melanin biosynthetic gene cluster involved in melanin biosynthesis (PKS2 and melanocyte-stimulating hormone receptor (MSHR)), membrane trafficking (MFS), regulation, and remodeling (Fig. 6)
Both functional and genetic evidence support the role of a genomic island encoding a gene cluster, involved in biosynthesis, membrane trafficking, regulation, and localization of melanin, in shaping a melanizationassociated phenotype (Fig. 6)

Summary

Introduction

The process by which organisms become better adapted to extreme environments and how natural selection shaped organismal phenotypes and genotypes in response to these intense selective pressures are central to evolutionary biology. Melanin-based pigmentation has long been used as a trait to understand adaptive evolution in extreme habitats across all forms of life [1,2,3,4]. Fungi are known to adapt to many stressful environments [5]. Genome-based approaches have been used to investigate the evolution and adaptation of melanized fungi, mostly model species of plant and human pathogens, and soil fungi [9,10,11,12,13]. Our understanding of the molecular mechanisms underlying the role of melanin in the adaptation of plant-associated mutualistic fungi to extreme environments is scarce [14,15,16]

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