Comparative gene retention analysis in barley, wild emmer, and bread wheat pangenome lines reveals factors affecting gene retention following gene duplication

Abstract

Background Gene duplication is a prevalent phenomenon and a major driving force underlying genome evolution. The process leading to the fixation of gene duplicates following duplication is critical to understand how genome evolves but remains fragmentally understood. Most previous studies on gene retention are based on gene duplicate analyses in single reference genome. No population-based comparative gene retention analysis has been performed to date. Results Taking advantage of recently published genomic data in Triticeae, we dissected a divergent homogentisate phytyltransferase (HPT2) lineage caught in the middle stage of gene fixation following duplication. The presence/absence of HPT2 in barley (diploid), wild emmer (tetraploid), and bread wheat (hexaploid) pangenome lines appears to be associated with gene dosage constraint and environmental adaption. Based on these observations, we adopted a phylogeny-based orthology inference approach and performed comparative gene retention analyses across barley, wild emmer, and bread wheat. This led to the identification of 326 HPT2-pattern-like genes at whole genome scale, representing a pool of gene duplicates in the middle stage of gene fixation. Majority of these HPT2-pattern-like genes were identified as small-scale duplicates, such as dispersed, tandem, and proximal duplications. Natural selection analyses showed that HPT2-pattern-like genes have experienced relaxed selection pressure, which is generally accompanied with partial positive selection and transcriptional divergence. Functional enrichment analyses showed that HPT2-pattern-like genes are over-represented with molecular-binding and defense response functions, supporting the potential role of environmental adaption during gene retention. We also observed that gene duplicates from larger gene family are more likely to be lost, implying a gene dosage constraint effect. Further comparative gene retention analysis in barley and bread wheat pangenome lines revealed combined effects of species-specific selection and gene dosage constraint. Conclusions Comparative gene retention analyses at the population level support gene dosage constraint, environmental adaption, and species-specific selection as three factors that may affect gene retention following gene duplication. Our findings shed light on the evolutionary process leading to the retention of newly formed gene duplicates and will greatly improve our understanding on genome evolution via duplication.

Coordinated Transcriptome and Metabolome Analyses of a Barley hvhggt Mutant Reveal a Critical Role of Tocotrienols in Endosperm Starch Accumulation

“…HvHGGT is an endosperm-specific gene with a plastid membrane localization . Coinciding with spatially restricted expression in the grain endosperm, the plant morphology of the hvhggt mutant resembled that of the WT at the whole-plant level during vegetative growth (Figure ).…”

“…HvHGGT is an endosperm-specific gene with a plastid membrane localization. 4 Coinciding with spatially restricted expression in the grain endosperm, the plant morphology of the hvhggt mutant resembled that of the WT at the whole-plant level during vegetative growth (Figure 1). In addition, mutations in HvHGGT did not result in obvious changes in embryo viability or grain germination rates in barley (Figure 1), and similar results were observed with the knockdown of OsHGGT by hairpin RNA (RNAi) expression in rice.…”

“…Barley HGGT is predominantly expressed in the grain endosperm and HGGT-mediated tocotrienol synthesis is localized in plastids. 4 Overexpression of barley HGGT in dicots, such as Arabidopsis, soybeans, and tobacco results in high-level accumulation of tocotrienols, 5,6 whereas only a slight accumulation is observed in soybeans upon expression of rice HGGT. 7 Our previous study found that the overexpression of barley HGGT significantly enhances tocotrienol levels and antioxidant activities, which is accompanied by larger grain size and higher total starch content.…”

“…Homogentisate geranylgeranyl transferase (HGGT) is a key enzyme involved in tocotrienol biosynthesis. Barley HGGT is predominantly expressed in the grain endosperm and HGGT -mediated tocotrienol synthesis is localized in plastids . Overexpression of barley HGGT in dicots, such as Arabidopsis , soybeans, and tobacco results in high-level accumulation of tocotrienols, , whereas only a slight accumulation is observed in soybeans upon expression of rice HGGT .…”

Tackling redundancy: genetic mechanisms underlying paralog compensation in plants

“…Indeed, paralogs tend to functionally diverge (neofunctionalization) or revert to a singleton state (nonfunctionalization) over evolutionary time. However, comparative analyses of duplicate gene retention in Angiosperms revealed that gene families that are involved in gene regulation, signal transduction, and metabolic processes are enriched for duplicates from ancient whole‐genome duplication events that occurred at least 75 million yr ago (Ma) (Li et al ., 2015; Jia et al ., 2023). These genes tend to be dosage‐sensitive, meaning their function depends on stoichiometric relationships between products (Birchler et al ., 2005).…”