System drift in the evolution of plant meristem development

Abstract

Developmental system drift (DSD) is a process where a phenotypic trait is conserved over evolutionary time, while the genetic basis for the trait changes. DSD has been identified in models with simpler genotype-phenotype maps (GPMs), such as RNA folding, however the extent of DSD in more complex GPMs, such as developmental pattern formation, is debated. To investigate the occurrence of DSD in complex developmental GPMs, we constructed a multi-scale computational model of the evolution of gene regulatory networks (GRNs) governing plant meristem (stem cell niche) development. We found that, during adaptation, some regulatory interactions became essential for the correct expression of stem cell niche genes. These regulatory interactions were subsequently conserved for thousands of generations. Nevertheless, we observed that these deeply conserved regulatory interactions could be lost over the extended period of stabilising evolution. These losses were compensated by changes elsewhere in the GRN, which then became conserved as well. This gain and loss of regulatory interactions resulted in a continual cis-regulatory rewiring in which accumulated changes caused changes in the expression of several genes. Using two publicly available datasets we found frequent changes in conserved non-coding sequences across six evolutionarily divergent plant species, and showed that these changes do not correlate with changes in gene expression patterns, demonstrating the occurrence of DSD. These findings align with the results from our computational model, showing that DSD is pervasive in the evolution of complex developmental systems. Author SummaryA key open question in evolution of development (evo-devo) is the evolvability of complex phenotypes. Developmental system drift (DSD) contributes to evolvability by exploring different genotypes with similar phenotypic outcome, but with mutational neighbourhoods that have different, potentially adaptive, phenotypes. We investigated the potential for DSD in plant development using a computational model of developmental evolution. We found that the regulatory interactions between genes changed extensively, resulting in the continual neutral rewiring of the gene regulatory network underpinning development. Even regulatory interactions that were essential for correct development were replaced over long evolutionary time scales. Using plant genome and gene expression data from two publicly available datasets, we found high turnover of conserved non-coding sequences, which often contain regulatory sequences, occurring at both short and long time scales. This did not correlate consistently with gene expression changes in plant tissue, supporting the prevalence of DSD as predicted by our model.