Abstract
Most angiosperms bear hermaphroditic flowers, but a few species have evolved outcrossing strategies, such as dioecy, the presence of separate male and female individuals. We previously investigated the mechanisms underlying dioecy in diploid persimmon (D. lotus) and found that male flowers are specified by repression of the autosomal gene MeGI by its paralog, the Y-encoded pseudo-gene OGI. This mechanism is thought to be lineage-specific, but its evolutionary path remains unknown. Here, we developed a full draft of the diploid persimmon genome (D. lotus), which revealed a lineage-specific whole-genome duplication event and provided information on the architecture of the Y chromosome. We also identified three paralogs, MeGI, OGI and newly identified Sister of MeGI (SiMeGI). Evolutionary analysis suggested that MeGI underwent adaptive evolution after the whole-genome duplication event. Transformation of tobacco plants with MeGI and SiMeGI revealed that MeGI specifically acquired a new function as a repressor of male organ development, while SiMeGI presumably maintained the original function. Later, a segmental duplication event spawned MeGI’s regulator OGI on the Y-chromosome, completing the path leading to dioecy, and probably initiating the formation of the Y-chromosome. These findings exemplify how duplication events can provide flexible genetic material available to help respond to varying environments and provide interesting parallels for our understanding of the mechanisms underlying the transition into dieocy in plants.
Highlights
Most species of flowering plants are hermaphrodite, but a small proportion have genetically determined separate sexes [1]
We previously investigated the mechanisms underlying dioecy in diploid persimmon (D. lotus) and found that male flowers are specified by repression of the autosomal gene MeGI by its paralog, the Y-encoded pseudo-gene OGI
Functional differentiation between paralogs, which had been derived from whole-genome duplication (WGD), resulted in the establishment of ripening characteristics in tomato fruits [12], and potentially enabled the adaptation to life underwater in seagrass (Zostera marina) [13]
Summary
Most species of flowering plants are hermaphrodite, but a small proportion have genetically determined separate sexes [1]. Consistent with theoretical models [8, 9], the results indicate that at least one gain-offunction mutation occurred in the evolution of dioecy, creating a dominant gynoecium or androecium suppressor. Data from these species is consistent with gene duplication events as the first event leading to these gain-of-function mutations, because the redundancy provided by the presence of duplicate copies allows one copy to be neofunctionalized without loss of the original function [10]. Functional differentiation between paralogs, which had been derived from whole-genome duplication (WGD), resulted in the establishment of ripening characteristics in tomato fruits [12], and potentially enabled the adaptation to life underwater in seagrass (Zostera marina) [13]
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