Genomic and phenotypic evidence for an incomplete domestication of South American grain amaranth (Amaranthus caudatus)

Abstract

The domestication syndrome comprises phenotypic changes that differentiate crops from their wild ancestors. We compared the genomic variation and phenotypic differentiation of the two putative domestication traits seed size and seed colour of the grain amaranth Amaranthus caudatus, which is an ancient crop of South America, and its two close wild relatives and putative ancestors A. hybridus and A. quitensis. Genotyping 119 accessions of the three species from the Andean region using genotyping by sequencing (GBS) resulted in 9485 SNPs that revealed a strong genetic differentiation of cultivated A. caudatus from its two relatives. A. quitensis and A. hybridus accessions did not cluster by their species assignment but formed mixed groups according to their geographic origin in Ecuador and Peru, respectively. A. caudatus had a higher genetic diversity than its close relatives and shared a high proportion of polymorphisms with their wild relatives consistent with the absence of a strong bottleneck or a high level of recent gene flow. Genome sizes and seed sizes were not significantly different between A. caudatus and its relatives, although a genetically distinct group of A. caudatus from Bolivia had significantly larger seeds. We conclude that despite a long history of human cultivation and selection for white grain colour, A. caudatus shows a weak genomic and phenotypic domestication syndrome and proposes that it is an incompletely domesticated crop species either because of weak selection or high levels of gene flow from its sympatric close undomesticated relatives that counteracted the fixation of key domestication traits.

Diversity in Grain Amaranths and Relatives Distinguished by Genotyping by Sequencing (GBS)

“…We believe that since the Amaranthus genome is now of a very high quality and full length macromolecules are available that the reference genome approach is best even across related species. The number of SNP loci we discovered compared favorably with previous GBS studies that used two-enzyme digestion library preparation or both reference based and non-reference based ( de novo ) assembly methods ( Stetter and Schmid, 2017 ; Stetter et al, 2017 ).…”

Genetics and breeding for climate change in Orphan crops

“…The grains are highly nutritious (Ssepuuya et al 2018 ) with medicinal properties (Aditya and Bhattacharjee 2018 ), and the plants have incredible agronomic versatility (Rodriguez et al 2020 ). The plants are considered autogamous but there are varying amounts of interspecific and inter-varietal hybridization (Suresh et al 2014 ) that have further resulted in significant morphological and genetic diversity (Stetter et al 2017 ) and a wider adaptability to different eco-geographical environments (Lee et al 2008 ). Domestication syndrome remains indistinct in amaranth with strong photoperiod sensitivity and very small shattering seeds (Sauer 1967 ; Brenner et al 2010 ).…”

Genomic approaches for studying crop evolution

“…In addition to the analysis of experimental populations, GBS has been widely adopted for population genetic studies. For example, it has been used to compare diversity between crops and their wild progenitors in chickpea [ 136 ], amaranth [ 137 ], and cassava [ 138 ]; to study geneflow between wild and domesticated sunflower taxa [ 139 , 140 ]; and to elucidate the demographic history of wild Phaseolus vulgaris , the progenitor of common bean [ 141 ].…”