Evolution of crop species: genetics of domestication and diversification

Key Points

  • Quantitative trait locus mapping techniques, genome-wide association studies and next-generation sequencing technologies have led to the discovery of genes that drive domestication and that lead to evolutionary diversification of cultivated plant species.

  • Molecular data have provided insights into the nature of selection on these evolutionary genes in crops, as well as the nature of the genes and mutations that are associated with the process.

  • Early steps in domestication seem to be associated with transcription factor loci, whereas in later crop diversification, enzyme-coding genes are targeted by selection.

  • Loss-of-function point mutations are the most common mutational lesion that is found in domestication genes.

  • Although only a handful of species have been studied in-depth, shifts in both domestication- and diversification-related traits can be examined in population demographic analyses using molecular, historic and archaeological data.

Abstract

Domestication is a good model for the study of evolutionary processes because of the recent evolution of crop species (<12,000 years ago), the key role of selection in their origins, and good archaeological and historical data on their spread and diversification. Recent studies, such as quantitative trait locus mapping, genome-wide association studies and whole-genome resequencing studies, have identified genes that are associated with the initial domestication and subsequent diversification of crops. Together, these studies reveal the functions of genes that are involved in the evolution of crops that are under domestication, the types of mutations that occur during this process and the parallelism of mutations that occur in the same pathways and proteins, as well as the selective forces that are acting on these mutations and that are associated with geographical adaptation of crop species.

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Figure 1: The evolutionary stages of domestication and diversification.
Figure 2: Demographic models of crop domestication.
Figure 3: From discovery to characterization of domestication genes.
Figure 4: Types of mutations in crop domestication and diversification genes.

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Acknowledgements

The authors thank the members of the Purugganan laboratory for their feedback, particularly J. Flowers, A. Plessis and U. Rosas. R.S.M. is supported by a postdoctoral fellowship from the US National Science Foundation Plant Genome Research Program (NSF PGRP). Work on domestication in the Purugganan laboratory is also funded by grants from NSF PGRP and the New York University Abu Dhabi Research Institute, United Arab Emirates.

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Correspondence to Michael D. Purugganan.

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FURTHER INFORMATION

Plants for a future

PowerPoint slides

Supplementary information

Supplementary information S1 (table)

List of 353 global domesticated food crops (PDF 351 kb)

Supplementary information S2 (table)

Expanded table of domestication and diversification genes (XLSX 33 kb)

Supplementary information S3 (table)

(PDF 329 kb)

Glossary

Quantitative trait locus

(QTL). A genomic region with a gene (or multiple linked genes) that contains mutations which result in phenotypic variation in populations.

Genome-wide association studies

(GWASs). Studies that use linkage disequilibrium between dense, usually single-nucleotide polymorphism, markers across the genome to identify significant associations between genes (or genomic regions) and trait phenotypes.

Conscious selection

The intentional choice, made by humans, of preferred phenotypes in cultivated plants for use and propagation.

Unconscious selection

Natural selection in crop species as a result of human cultivation practices and of growth in agro-ecological environments.

Green Revolution

A series of research, breeding and technology transfer programmes in the mid-twentieth century that resulted in marked increases in agricultural productivity in developing countries.

Complementation

Introduction of a wild-type allele into a mutant individual, through either genetic crosses or transgenic methods, to confirm that a particular gene causes a specific phenotype.

Causative mutations

Mutations that lead to altered gene functions, which result in specific phenotypes.

Fixation

Increase in the frequency of an allelic variant until it is found in all individuals in a population.

Selective sweeps

Rapid increases in population frequencies of positively selected mutations and linked neutral mutations, which result in significant reductions in nucleotide diversity in localized regions of the genome that flank the selected mutations.

Introgression

Recurrent crossing that leads to the sharing of alleles between gene pools (which can be unidirectional), such as between domesticated and wild populations.

Genetic bottlenecks

Marked decreases in genetic diversity that are caused by reductions in effective population sizes.

Domestication syndrome

The selection of traits that distinguish domesticated species from their wild progenitors; similar traits were often observed to occur in different crops, which led people to view them as a 'syndrome'.

Nonsense mutations

Point mutations that transform amino acid-encoding codons into premature stop codons, which result in the generation of truncated proteins.

cis-regulatory mutations

Mutations in linked, usually non-coding portions, of genes that alter levels and/or patterns of transcription of the linked gene.

Missense mutations

Point mutations that change the identities of encoded amino acids, which result in changes in protein sequences.

Nucleotide diversity

The number of single-nucleotide polymorphism in a genomic region, usually estimated as the mean level of pairwise nucleotide divergence in a sample or a population.

Parallel evolution

Independent evolution of the same trait in different species.

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Meyer, R., Purugganan, M. Evolution of crop species: genetics of domestication and diversification. Nat Rev Genet 14, 840–852 (2013). https://doi.org/10.1038/nrg3605

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