Selection During Maize Domestication Targeted a Gene Network Controlling Plant and Inflorescence Architecture

Abstract

Selection during evolution, whether natural or artificial, acts through the phenotype. For multifaceted phenotypes such as plant and inflorescence architecture, the underlying genetic architecture is comprised of a complex network of interacting genes rather than single genes that act independently to determine the trait. As such, selection acts on entire gene networks. Here, we begin to define the genetic regulatory network to which the maize domestication gene, (), belongs. Using a combination of molecular methods to uncover either direct or indirect regulatory interactions, we identified a set of genes that lie downstream of in a gene network regulating both plant and inflorescence architecture. Additional genes, known from the literature, also act in this network. We observed that regulates both core cell cycle genes and another maize domestication gene, (). We show that several members of the MADS-box gene family are either directly or indirectly regulated by and/or, and that sits atop a cascade of transcriptional regulators controlling both plant and inflorescence architecture. Multiple members of the network appear to have been the targets of selection during maize domestication. Knowledge of the regulatory hierarchies controlling traits is central to understanding how new morphologies evolve.

The Impact of Genetic Changes during Crop Domestication

“…This agrees with the idea that regulatory changes are major players in phenotypic evolution [90]. Recently, the concept of gene networks changing under domestication, leading to multiple phenotypes with different plant and inflorescence architecture, was demonstrated in maize [91]. This might not be unexpected given that transcription factors orchestrate the activity of numerous other genes, and consequently, their alteration can potentially modify an entire suite of characters, leading to drastic phenotypic changes in relatively short time scales [45,92].…”

Maize domestication and gene interaction

“…In contrast to the largely background-specific effects of many maize alleles, tb1 remains robust to genetic background -so much so that tillering was not phenotyped in F2 crosses beyond initial work by Doebley and Stec (1991). That tb1 was so routinely implicated in differences between maize and teosinte may be true because it has an effect in every population tested thus far and because it is near the top of the shade avoidance pathway (Studer et al, 2017). Consequently, phenotypic effects can be amplified and fine-tuned through downstream targets.…”

“…Although the statistical power to detect epistasis may be poor, such examples of biological epistasis may be common. For example, much of the shade avoidance pathway downstream of tb1 contains genes shown to be targets of selection (Studer et al, 2017), but these genes are not detected in screens for statistical epistasis. Together, despite the fact that few loci have shown evidence of statistical epistasis in mapping studies, there is evidence for epistasis -both statistical and biological -contributing to domestication.…”

“…As a transcription factor, tb1 binds to many regions of the genome. It directly regulates tga1 by binding its promoter but is also intimately linked to the cell cycle as it represses two cell cycle genes (proliferating cell nuclear antigen2(pcna2) and minichromosome maintenance2/prolifera (mcm2/prl)) (Studer et al, 2017). Beyond tb1, other loci within the QTL region on 1L found by multiple studies (Doebley and Stec, 1991, 1993;Briggs et al, 2007) contribute to ear morphology Yang et al, 2016), suggesting pleiotropy is common.…”

“…Consequently, phenotypic effects can be amplified and fine-tuned through downstream targets. Additionally, several downstream targets of tb1 show signatures of selection (Studer et al, 2017), suggesting further constraint on the entire pathway. Nonallelic mutations in gene networks can result in phenotypes that look superficially similar to those selected during domestication.…”