Abstract

Early-diverging land plants such as mosses are known for their outstanding abilities to grow in various terrestrial habitats, incorporating tremendous structural and physiological innovations, as well as many lineage-specific genes. How these genes and functional innovations evolved remains unclear. In this study, we show that a dual-coding gene YAN/AltYAN in the moss Physcomitrella patens evolved from a pre-existing hemerythrin gene. Experimental evidence indicates that YAN/AltYAN is involved in fatty acid and lipid metabolism, as well as oil body and wax formation. Strikingly, both the recently evolved dual-coding YAN/AltYAN and the pre-existing hemerythrin gene might have similar physiological effects on oil body biogenesis and dehydration resistance. These findings bear important implications in understanding the mechanisms of gene origination and the strategies of plants to fine-tune their adaptation to various habitats.

Highlights

  • Early-diverging land plants such as mosses are known for their outstanding abilities to grow in various terrestrial habitats, incorporating tremendous structural and physiological innovations, as well as many lineage-specific genes

  • Because dehydration leads to an increase in both the number and size of oil bodies[18], we investigated the effects of dehydration on oil body biogenesis in the wild-type and yan/ altyan plants

  • Lineage-specific genes of distinctive functions have been under some extensive studies[9,29], and it has been shown that all non-coding genomic regions may potentially evolve into functional genes[30]

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Summary

Introduction

Early-diverging land plants such as mosses are known for their outstanding abilities to grow in various terrestrial habitats, incorporating tremendous structural and physiological innovations, as well as many lineage-specific genes. Both the recently evolved dual-coding YAN/AltYAN and the pre-existing hemerythrin gene might have similar physiological effects on oil body biogenesis and dehydration resistance These findings bear important implications in understanding the mechanisms of gene origination and the strategies of plants to fine-tune their adaptation to various habitats. We provide evidence that a gene encoding hemerythrin (Hr), a versatile oxygen-binding protein[12,13], was likely transferred from fungi to early land plants We show that this Hr gene subsequently evolved into a dual-coding gene with two overlapping reading frames in the Physcomitrium–Physcomitrella species complex. Both the later evolved dual-coding gene and the pre-existing Hr gene might have similar physiological effects on oil body biogenesis and dehydration tolerance These findings provide major insights into the origin of new genes and demonstrate how complex mechanisms of gene evolution facilitated the adaptation of plants to terrestrial environments

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