Domestication and the storage starch biosynthesis pathway: signatures of selection from a whole sorghum genome sequencing strategy.

Bradley C Campbell,Emma S Mace,Peter J Prentis,Shuaishuai Tai,Edward K Gilding,Yongfu Tao,Pauline Thomelin,David R Jordan,Ian D Godwin

doi:10.1111/pbi.12578

Abstract

SummaryNext‐generation sequencing of complete genomes has given researchers unprecedented levels of information to study the multifaceted evolutionary changes that have shaped elite plant germplasm. In conjunction with population genetic analytical techniques and detailed online databases, we can more accurately capture the effects of domestication on entire biological pathways of agronomic importance. In this study, we explore the genetic diversity and signatures of selection in all predicted gene models of the storage starch synthesis pathway of Sorghum bicolor, utilizing a diversity panel containing lines categorized as either ‘Landraces’ or ‘Wild and Weedy’ genotypes. Amongst a total of 114 genes involved in starch synthesis, 71 had at least a single signal of purifying selection and 62 a signal of balancing selection and others a mix of both. This included key genes such as STARCH PHOSPHORYLASE 2 (SbPHO2, under balancing selection), PULLULANASE (SbPUL, under balancing selection) and ADP‐glucose pyrophosphorylases (SHRUNKEN2, SbSH2 under purifying selection). Effectively, many genes within the primary starch synthesis pathway had a clear reduction in nucleotide diversity between the Landraces and wild and weedy lines indicating that the ancestral effects of domestication are still clearly identifiable. There was evidence of the positional rate variation within the well‐characterized primary starch synthesis pathway of sorghum, particularly in the Landraces, whereby low evolutionary rates upstream and high rates downstream in the metabolic pathway were expected. This observation did not extend to the wild and weedy lines or the minor starch synthesis pathways.

Highlights

The study of the evolution of metabolic pathways is fundamental to understanding evolutionary change as well as key events in the domestication process (Fraser et al, 2002; Ramsay et al, 2009)
By examining the evolution of genes in an integrated metabolic pathway, we can gain some understanding of the complex forces that are shaping domesticated germplasm and question whether the differential selection acting upon certain loci conforms to previous studies that sought to explain how the structure of such pathways affects evolutionary rate (Clotault et al, 2012; Livingstone and Anderson, 2009; Ramsay et al, 2009; Rausher et al, 2008)
Does this model hold for the critical process of storage starch synthesis? Unlike other pathways, the starch synthesis pathway (SSP) is not a simple unidirectional pathway and contains several alternative branches resulting in starch as the terminal product and has to support respiration and other key processes

Summary

Introduction

The study of the evolution of metabolic pathways is fundamental to understanding evolutionary change as well as key events in the domestication process (Fraser et al, 2002; Ramsay et al, 2009). This increase in selective constraint is believed to occur because the consequence of a nonsynonymous mutation within a gene at a key branch point higher up in the synthesis process could lead to major pleiotropic effects that result in no useful end products (Rausher et al, 1999) This was the case within the plant biosynthetic pathways of isoprene (Sharkey et al, 2005), anthocyanin (Lu and Rausher, 2003; Rausher et al, 1999, 2008), carotenoid (Clotault et al, 2012; Livingstone and Anderson, 2009) and terpenoid synthesis (Ramsay et al, 2009).

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