The impact of widespread regulatory neofunctionalization on homeolog gene evolution following whole-genome duplication in maize

Abstract

Whole-genome duplications are a widespread feature of plant genome evolution, having been detected in all flowering plant lineages. Despite the prevalence of these events, the extent to which duplicated genes (homeolog gene pairs) functionally diverge (neofunctionalization) is unclear. We present a genome-wide analysis of molecular evolution and regulatory neofunctionalization in maize (Zea mays L.). We demonstrate that 13% of all homeolog gene pairs in maize are regulatory neofunctionalized in leaves, and that regulatory neofunctionalized genes experience enhanced purifying selection. We show that significantly more genes have been regulatory neofunctionalized in foliar leaves than in husk leaves and that both leaf types have experienced selection for distinct functional roles. Furthermore, we demonstrate that biased subgenome expression dominance occurs only in the presence of regulatory neofunctionalization and that in nonregulatory neofunctionalized genes subgenome dominance is progressively acquired during development. Taken together, our study reveals several novel insights into the evolution of maize, genes, and gene expression, and provides a general model for gene evolution following whole-genome duplication in plants.

Evolutionary Fates and Dynamic Functionalization of Young Duplicate Genes in Arabidopsis Genomes

“…and mammals Bachtrog, 2013, 2015). This is also supported by previous studies in plant genomes in which subfunctionalization only plays a minor role, whereas neofunctionalization and specialization, which correspond to the reciprocal neofunctionalization expression in some studies, are more important in preserving duplicates (Ganko et al, 2007;Liu et al, 2011;Hughes et al, 2014). Alternatively, the rare cases of subfunctionalization of plant duplicate genes may be due to the stringent criteria of our methodology for identification, which cause some subfunctionalization cases to be classified into conservation and specialization categories.…”

Evolution of Gene Duplication in Plants

“…For example, Arabidopsis duplicates have likely accumulated novel environmental responses (Zou et al, 2009b) and novel developmental regulatory patterns (Liu et al, 2011). Novel leaf gene expression patterns also are observed for some maize duplicate genes (Hughes et al, 2014). However, a novel expression pattern is not necessarily adaptive.…”

Sequence and expression variation in SUPPRESSOR of OVEREXPRESSION of CONSTANS 1 (SOC1): homeolog evolution in Indian Brassicas

“…Relieved of functional constraints, duplicated copies tend to undergo neo-functionalization, sub-functionalization or pseudogenisation (Sankoff et al 2010;Cheng et al 2012). Occasionally, mutations in regulatory sequences result in functional evolution of homeologs (Hahn 2009;Hughes et al 2014). Brassica species are, hence, an interesting model to study polyploidy-associated genomic changes.…”