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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., (© 2022 The Authors. New Phytologist © 2022 New Phytologist Foundation.)

Background: Storage roots are an ecologically and agriculturally important plant trait that have evolved numerous times in angiosperms. Storage roots primarily function to store carbohydrates underground as reserves for perennial species. In morning glories, storage roots are well characterized in the crop species sweetpotato, where starch accumulates in storage roots. This starch-storage tissue proliferates, and roots thicken to accommodate the additional tissue. In morning glories, storage roots have evolved numerous times. The primary goal of this study is to understand whether this was through parallel evolution, where species use a common genetic mechanism to achieve storage root formation, or through convergent evolution, where storage roots in distantly related species are formed using a different set of genes. Pairs of species where one forms storage roots and the other does not were sampled from two tribes in the morning glory family, the Ipomoeeae and Merremieae. Root anatomy in storage roots and fine roots was examined. Furthermore, we sequenced total mRNA from storage roots and fine roots in these species and analyzed differential gene expression., Results: Anatomical results reveal that storage roots of species in the Ipomoeeae tribe, such as sweetpotato, accumulate starch similar to species in the Merremieae tribe but differ in vascular tissue organization. In both storage root forming species, more genes were found to be upregulated in storage roots compared to fine roots. Further, we find that fifty-seven orthologous genes were differentially expressed between storage roots and fine roots in both storage root forming species. These genes are primarily involved in starch biosynthesis, regulation of starch biosynthesis, and transcription factor activity., Conclusions: Taken together, these results demonstrate that storage roots of species from both morning glory tribes are anatomically different but utilize a common core set of genes in storage root formation. This is consistent with a pattern of parallel evolution, thus highlighting the importance of examining anatomy together with gene expression to understand the evolutionary origins of ecologically and economically important plant traits.

* Premise of the study: Morning glories are an emerging model system, and resolving phylogenetic relationships is critical for understanding their evolution. Phylogenetic studies demonstrated that the largest morning glory genus, lpomoea, is not monophyletic, and nine other genera are derived from within lpomoea. Therefore, systematic research is focused on the monophyletic tribe Ipomoeeae (ca. 650-900 species). We used whole plastomes to infer relationships across Ipomoeeae. * Methods: Whole plastomes were sequenced for 29 morning glory species, representing major lineages. Phylogenies were estimated using alignments of 82 plastid genes and whole plastomes. Divergence times were estimated using three fossil calibration points. Finally, evolution of root architecture, flower color, and ergot alkaloid presence was examined. * Key results: Phylogenies estimated from both data sets had nearly identical topologies. Phylogenetic results are generally consistent with prior phylogenetic hypotheses. Higher-level relationships with weak support in previous studies were recovered here with strong support. Molecular dating analysis suggests a late Eocene divergence time for the Ipomoeeae. The two clades within the tribe, Argyreiinae and Astripomoeinae, diversified at similar times. Reconstructed most recent common ancestor of the Ipomoeeae had blue flowers, an association with ergot-producing fungi, and either tuberous or fibrous roots. * Conclusions: Phylogenetic results provide confidence in relationships among Ipomoeeae lineages. Divergence time estimation results provide a temporal context for diversification of morning glories. Ancestral character reconstructions support previous findings that morning glory morphology is evolutionarily labile. Taken together, our study provides strong resolution of the morning glory phylogeny, which is broadly applicable to the evolution and ecology of these fascinating species. [ABSTRACT FROM AUTHOR]