Grain dispersal mechanism in cereals arose from a genome duplication followed by changes in spatial expression of genes involved in pollen development

Abstract

Key message Grain disarticulation in wild progenitor of wheat and barley evolved through a local duplication event followed by neo-functionalization resulting from changes in location of gene expression. Abstract One of the most critical events in the process of cereal domestication was the loss of the natural mode of grain dispersal. Grain dispersal in barley is controlled by two major genes, Btr1 and Btr2, which affect the thickness of cell walls around the disarticulation zone. The barley genome also encodes Btr1-like and Btr2-like genes, which have been shown to be the ancestral copies. While Btr and Btr-like genes are non-redundant, the biological function of Btr-like genes is unknown. We explored the potential biological role of the Btr-like genes by surveying their expression profile across 212 publicly available transcriptome datasets representing diverse organs, developmental stages and stress conditions. We found that Btr1-like and Btr2-like are expressed exclusively in immature anther samples throughout Prophase I of meiosis within the meiocyte. The similar and restricted expression profile of these two genes suggests they are involved in a common biological function. Further analysis revealed 141 genes co-expressed with Btr1-like and 122 genes co-expressed with Btr2-like, with 105 genes in common, supporting Btr-like genes involvement in a shared molecular pathway. We hypothesize that the Btr-like genes play a crucial role in pollen development by facilitating the formation of the callose wall around the meiocyte or in the secretion of callase by the tapetum. Our data suggest that Btr genes retained an ancestral function in cell wall modification and gained a new role in grain dispersal due to changes in their spatial expression becoming spike specific after gene duplication.

Grain Disarticulation in Wild Wheat and Barley

“…Btr-like genes are expressed at anther primordia shown with purple highlight. This is supported by RNA-seq expression data, which showed that Btr1-like and Btr2-like genes are exclusively expressed at the immature anther ( Cross et al. 2022 ).…”

“…How the Btr genes evolved and gained the brittle rachis function has been debated ( Zeng et al. 2020 , Cross et al. 2022 ).…”

“…2015 ). Btr1-like / Btr2-like pairs are exclusively expressed at the immature anther stage ( Cross et al 2022 ). Interestingly, the expression time coincides with the Btr1 / Btr2 expression, meaning that at the same immature spike stage, Btr1-like / Btr2-like is expressed at anther primordia, whereas Btr1 / Btr2 is expressed at separation zone primordia.…”

“…2020 ). The biological and molecular functions of Btr-like genes were investigated to infer Btr function and divergence ( Cross et al. 2022 ).…”