Genomic constraints on domestication: the role of plasticity and transposable elements

Abstract

Crop domestication is an important evolutionary process that transforms wild plants into cultivated crops, facilitating our shift from foraging to agriculture. Despite our reliance on domesticated crops, only a small proportion of edible plant species are domesticated. Is there a genomic constraint on domestication that allows the domestication of certain species over others? Our understanding of crop domestication has focused on the selection that transformed the progenitor into the domesticated crop, whereas little is known about the selection between wild species in early domestication. Here, we investigate the role of plasticity and transposable elements (TEs) on the selective advantage of the tomato progenitor over never-domesticated wild species (referred here as ‘wilds’). Plasticity is the ability of an organism to respond to new environments. Phenotypic and gene expression plasticity were assessed in domesticated, progenitor and wild species. A greater number of traits and genes were plastic in the progenitor than in the wild species, linked to important fruit traits and plant processes. Underlying genetic diversity may have contributed to this enhanced plasticity. The ability of TEs to move from one location of the genome to another makes them a great contributor to diversity generation. Annotation of single nucleotide polymorphism (SNP) and transposon insertion polymorphism (TIP) to characterise genetic diversity revealed greater nucleotide and TIP diversity in the progenitor than in wild species with evidence of TIPs associated with genes that were putatively selected during domestication. Since mutation rates underpin the maintenance of high genetic diversity, we employed mutation accumulation (MA) lines to estimate the haploid mutation rate for single nucleotide variants (SNVs), indels and TE insertions. SNV and indel mutation rates were higher in the progenitor than in wild species, although there was no detectable difference in TE insertion rates. We provide the first mutation accumulation experiment to estimate mutation rates in tomatoes. Overall, we found evidence for the role of plasticity, genetic diversity and mutation rates in the domestication of the tomato progenitor. Uncovering genomic mechanisms that facilitate domestication could identify adaptive variation in crop wild relatives and could be important in crop breeding to tackle food security challenges.

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Identifiers

ORCID for Mark Chapman: orcid.org/0000-0002-7151-723X

ORCID for Tom Ezard: orcid.org/0000-0001-8305-6605

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