Discovery and characterization of sweetpotato's closest tetraploid relative

Abstract

The origin of sweetpotato, a hexaploid species, is poorly understood, partly because the identity of its tetraploid progenitor remains unknown. In this study, we identify, describe and characterize a new species of Ipomoea that is sweetpotato's closest tetraploid relative known to date and probably a direct descendant of its tetraploid progenitor. We integrate morphological, phylogenetic, and genomic analyses of herbarium and germplasm accessions of the hexaploid sweetpotato, its closest known diploid relative Ipomoea trifida, and various tetraploid plants closely related to them from across the American continent. We identify wild autotetraploid plants from Ecuador that are morphologically distinct from Ipomoea batatas and I. trifida, but monophyletic and sister to I. batatas in phylogenetic analysis of nuclear data. We describe this new species as Ipomoea aequatoriensis T. Wells & P. Muñoz sp. nov., distinguish it from hybrid tetraploid material collected in Mexico; and show that it likely played a direct role in the origin of sweetpotato's hexaploid genome. This discovery transforms our understanding of sweetpotato's origin.

Keywords: Ipomoea aequatoriensis; Ecuador; crop wild relatives; genomics; herbarium specimens; new species; tetraploid.

Fig. 1

Ipomoea aequatoriensis is morphologically distinct from Ipomoea batatas and Ipomoea trifida. Sepals are (a) oblong/ovate in cultivated I. batatas (Balls 5483) and (b) obovate in I. aequatoriensis (Jativa and Epling. 1191). (c) Map of the Americas showing the distribution of specimens included in the morphological analysis. Closed symbols indicate specimens also included in the genomic analyses. All hexaploid I. batatas specimens in this study are of cultivated origin and are not included in the map. (d) Principal component analysis and (e) linear discriminant analysis of 12 quantitative morphological traits widely used in sweetpotato morphological studies. Ellipses indicate 95% confidence level. In (c–e), I. batatas (green dots), I. aequatoriensis (blue triangles), I. trifida (red squares), hybrids Ipomoea tabascana (black triangle) and I. batatas var. apiculata (orange triangles). The Colombian specimens affinis to I. aequatoriensis are indicated by light blue triangles.

Fig. 2

Molecular analyses identify Ipomoea aequatoriensis as a distinct entity, phylogenetically distinct and isolated in the genetic space. (a) Approximate maximum likelihood analysis of 371 single‐copy nuclear DNA regions. Numbers on the branches indicate Shimodaira–Hasegawa‐like support values; black dots indicate branches with 100% support. (b) Principal component analysis of Ipomoea batatas (green), Ipomoea trifida (red), I. aequatoriensis (blue) and the hybrids Ipomoea tabascana and I. batatas var. apiculata (black and orange respectively). Principal component analysis inferred using 419 single nucleotide polymorphisms (SNPs) from across the 386 nuclear probes. Ellipses indicate multivariate t‐distribution. The Colombian specimen K500/CH81.3 discussed throughout the text is indicated in light blue.

Fig. 3

The analysis of chloroplast genomes shows Ipomoea aequatoriensis is associated with the sweetpotato ancestral lineage. Median Joining phylogenetic network inferred using 602 segregating sites (182 parsimony‐informative) and showing the relationships between Ipomoea batatas, Ipomoea trifida, I. aequatoriensis and the hybrid entities, Ipomoea tabascana and I. batatas var. apiculata. The one Colombian specimen sequenced (K500/CH80.3), indicated with an arrow, seems to carry a chloroplast related to sweetpotato lineage 2 chloroplast; we excluded it from our diagnosis of I. aequatoriensis pending further investigation. The size of the circles indicates the number of samples, with samples grouping in larger circles being identical for the sites studied.

Fig. 4

One of several possible scenarios of sweetpotato evolution and origin of current diversity. Tetraploid plants closely related to sweetpotato have two different origins: plants from Ecuador represent direct descendants from the autotetraploid progenitor of hexaploid Ipomoea batatas, whereas plants from Mexico and Central America are the result of a more recent hybridization between hexaploid I. batatas and diploid Ipomoea trifida. (a) One possible scenario, congruent with the data currently available, is presented here. An autotetraploid would have arisen from a whole genome duplication of a diploid common ancestor with I. trifida. This autotetraploid would have hybridized with the diploid ancestor to produce an allohexaploid. Subsequent introgression between the diploid ancestor lineage and the allohexaploid would result in chloroplast capture from I. trifida, explaining the two distinct I. batatas lineages in the chloroplast phylogenies. This separate lineage would keep a hexaploid nuclear genome but a chloroplast most similar to the diploid progenitor, and therefore to modern I. trifida, than to the ancestral sweetpotato lineage. Red and blue colours indicate the proportion of diploid (AA, red) and tetraploid (BBBB, blue) ancestral genomes in the different entities. Small, coloured circles represent the chloroplast. Dashed lines indicate hybridization and dotted line indicates introgression with chloroplast capture. (b) Summary nuclear phylogeny depicting the relationship between modern taxa, with Ipomoea aequatoriensis most closely related to I. batatas. (c) Summary chloroplast phylogeny depicting the relationship between modern taxa, with I. aequatoriensis most closely related to I. batatas lineage 1, the ancestral sweetpotato lineage.