The Road to Sorghum Domestication: Evidence From Nucleotide Diversity and Gene Expression Patterns.

Concetta Burgarella,David Pot,Nancy Terrier,Monique Deu,Jacques David,Angélique Berger,Sylvain Glémin

doi:10.3389/fpls.2021.666075

Abstract

Native African cereals (sorghum, millets) ensure food security to millions of low-income people from low fertility and drought-prone regions of Africa and Asia. In spite of their agronomic importance, the genetic bases of their phenotype and adaptations are still not well-understood. Here we focus on Sorghum bicolor, which is the fifth cereal worldwide for grain production and constitutes the staple food for around 500 million people. We leverage transcriptomic resources to address the adaptive consequences of the domestication process. Gene expression and nucleotide variability were analyzed in 11 domesticated and nine wild accessions. We documented a downregulation of expression and a reduction of diversity both in nucleotide polymorphism (30%) and gene expression levels (18%) in domesticated sorghum. These findings at the genome-wide level support the occurrence of a global reduction of diversity during the domestication process, although several genes also showed patterns consistent with the action of selection. Nine hundred and forty-nine genes were significantly differentially expressed between wild and domesticated gene pools. Their functional annotation points to metabolic pathways most likely contributing to the sorghum domestication syndrome, such as photosynthesis and auxin metabolism. Coexpression network analyzes revealed 21 clusters of genes sharing similar expression patterns. Four clusters (totaling 2,449 genes) were significantly enriched in differentially expressed genes between the wild and domesticated pools and two were also enriched in domestication and improvement genes previously identified in sorghum. These findings reinforce the evidence that the combined and intricated effects of the domestication and improvement processes do not only affect the behaviors of a few genes but led to a large rewiring of the transcriptome. Overall, these analyzes pave the way toward the identification of key domestication genes valuable for genetic resources characterization and breeding purposes.

Highlights

Domestication is an evolutionary process in which species evolve dramatic functional and phenotypic changes under selection for characters that fit the agricultural environment and human necessities
We examined the functional characterization of differentially expressed (DE) genes and assessed if particular gene categories or functions were overrepresented in DE vs. non-DE genes, which could be the result of selection
Our genome-wide screen of expressed genes showed a loss of diversity in the domesticated pool up to 30%, both in nucleotide and in expression diversity, supporting the general model of sorghum domestication from a reduced representation of the wild pool (e.g., Hamblin et al, 2006) and serial founder effects combined with different adaptation and deterioration steps during crop evolution (Wang et al, 2017; Allaby et al, 2019; Smith et al, 2019)

Summary

Introduction

Domestication is an evolutionary process in which species evolve dramatic functional and phenotypic changes under selection for characters that fit the agricultural environment and human necessities (such as taste, yield, cultivation, harvesting and storage practices). The suite of traits that have been modified in the domesticated forms are collectively referred to as “domestication syndrome” (Hammer, 1984, as cited in Allaby, 2014) In plants they typically include characters related to seed dispersal (e.g., reduction of dehiscence and dormancy), plant architecture (e.g., branching) and properties of the harvested part (such as size, shape, nutritional content of seed, fruit and tubers). The domestication’s term that is used of this article refers to the dynamic effects that led to the divergence of the current cultivated forms compared to the wild ones This general reduction of genetic diversity is expected to be stronger for annual than perennial species and in autogamous than allogamous crops (Gaut et al, 2015). Experimental evidence supports this hypothesis, as a reduction of genetic diversity has been found in major domesticated species when compared with their wild progenitors, e.g., maize (Hufford et al, 2013), rice (Caicedo et al, 2007; Huang et al, 2012; Nabholz et al, 2014), soybean (Lam et al, 2010) and tomato (Koenig et al, 2013; Sauvage et al, 2017)

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Conclusion