Disentangling the Origins of Cultivated Sweet Potato (Ipomoea batatas (L.) Lam.)

Caroline Roullier,David Tay,Laure Benoit,Genoveva Rossel,Paul Wennekes,Víctor Manuel Fernández Bringas,Doyle Mckey,Anne Duputié,Vincent Lebot,Simon Joly

doi:10.1371/journal.pone.0062707

Abstract

Sweet potato (Ipomoea batatas (L.) Lam., Convolvulaceae) counts among the most widely cultivated staple crops worldwide, yet the origins of its domestication remain unclear. This hexaploid species could have had either an autopolyploid origin, from the diploid I. trifida, or an allopolyploid origin, involving genomes of I. trifida and I. triloba. We generated molecular genetic data for a broad sample of cultivated sweet potatoes and its diploid and polyploid wild relatives, for noncoding chloroplast and nuclear ITS sequences, and nuclear SSRs. Our data did not support an allopolyploid origin for I. batatas, nor any contribution of I. triloba in the genome of domesticated sweet potato. I. trifida and I. batatas are closely related although they do not share haplotypes. Our data support an autopolyploid origin of sweet potato from the ancestor it shares with I. trifida, which might be similar to currently observed tetraploid wild Ipomoea accessions. Two I. batatas chloroplast lineages were identified. They show more divergence with each other than either does with I. trifida. We thus propose that cultivated I. batatas have multiple origins, and evolved from at least two distinct autopolyploidization events in polymorphic wild populations of a single progenitor species. Secondary contact between sweet potatoes domesticated in Central America and in South America, from differentiated wild I. batatas populations, would have led to the introgression of chloroplast haplotypes of each lineage into nuclear backgrounds of the other, and to a reduced divergence between nuclear gene pools as compared with chloroplast haplotypes.

Highlights

Polyploidy is recognized as an important factor in the evolution and diversification of plants [1]
We address the issues of the botanical and geographic origin of sweet potato, using a representative sampling of I. batatas, its putative close wild diploid relatives I. trifida and I. triloba, and polyploid Ipomoea sp., using several neutral nuclear and chloroplast markers
We pose the following questions: Are I. batatas gene pools derived from a single progenitor, from differentiated conspecific populations that hybridized, or from multiple hybridizing species? Can we identify the progenitor(s) and pinpoint the geographical origin(s) of domestication? The formation of sweet potato’s hexaploid genome must have involved at least two steps, from diploidy to intermediate ploidy levels and hexaploidy

Summary

Introduction

Polyploidy is recognized as an important factor in the evolution and diversification of plants [1]. Crop domestication corresponds to an evolutionary process of species divergence, in which genetic, morphological and physiological changes result from the cultivation of plants by humans [2]. Polyploidization often triggers genomic re-patterning and gene expression changes [1], which could explain the sudden appearance of new phenotypes that diverge from those of their diploid parents in numerous traits. These genetic changes are probably more rapid and extensive in allopolyploids, they may affect autopolyploids over the longer term [7]. Human-mediated transfers of these diploids through islands of Melanesia and South-

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