Intraspecific diploidization of a halophyte root fungus drives heterosis

Zhongfeng Li, Zhiyong Zhu, Kun Qian, Boping Tang, Baocai Han, Zhenhui Zhong, Tao Fu, Peng Zhou (), Eva H. Stukenbrock, Francis M. Martin () and Zhilin Yuan ()
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Zhongfeng Li: Chinese Academy of Forestry
Zhiyong Zhu: Chinese Academy of Forestry
Kun Qian: Zhejiang University
Boping Tang: Yancheng Teachers University
Baocai Han: Chinese Academy of Sciences
Zhenhui Zhong: Sichuan University
Tao Fu: Shenzhen Zhuoyun Haizhi Medical Research Center Co., Ltd
Peng Zhou: Chinese Academy of Agricultural Sciences
Eva H. Stukenbrock: Christian-Albrechts University
Francis M. Martin: Chinese Academy of Forestry
Zhilin Yuan: Chinese Academy of Forestry

Nature Communications, 2024, vol. 15, issue 1, 1-18

Abstract: Abstract How organisms respond to environmental stress is a key topic in evolutionary biology. This study focused on the genomic evolution of Laburnicola rhizohalophila, a dark-septate endophytic fungus from roots of a halophyte. Chromosome-level assemblies were generated from five representative isolates from structured subpopulations. The data revealed significant genomic plasticity resulting from chromosomal polymorphisms created by fusion and fission events, known as dysploidy. Analyses of genomic features, phylogenomics, and macrosynteny have provided clear evidence for the origin of intraspecific diploid-like hybrids. Notably, one diploid phenotype stood out as an outlier and exhibited a conditional fitness advantage when exposed to a range of abiotic stresses compared with its parents. By comparing the gene expression patterns in each hybrid parent triad under the four growth conditions, the mechanisms underlying growth vigor were corroborated through an analysis of transgressively upregulated genes enriched in membrane glycerolipid biosynthesis and transmembrane transporter activity. In vitro assays suggested increased membrane integrity and lipid accumulation, as well as decreased malondialdehyde production under optimal salt conditions (0.3 M NaCl) in the hybrid. These attributes have been implicated in salinity tolerance. This study supports the notion that hybridization-induced genome doubling leads to the emergence of phenotypic innovations in an extremophilic endophyte.

Date: 2024
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DOI: 10.1038/s41467-024-49468-7

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