Haplotype-based phylogenetic analysis uncovers the tetraploid progenitor of sweet potato

Abstract

The hexaploid sweet potato is one of the most important root crops worldwide. However, its genetic origins, especially that of its tetraploid progenitor, are unclear. In this study, we conceived a pipeline consisting of a genome-wide variation-based phylogeny and a novel haplotype-based phylogenetic analysis (HPA) to determine that the tetraploid accession CIP695141 of Ipomoea batatas 4x from Peru is the tetraploid progenitor of sweet potato. We detected biased gene exchanges between subgenomes. The B1 to B2 subgenome conversions were almost 3-fold higher than the B2 to B1 subgenome conversions. Our analyses revealed that the genes involved in storage root formation, sugar transport, stress resistance, and maintenance of genome stability have been selected during the speciation and domestication of sweet potato. This study sheds lights on the evolution of sweet potato and paves a way for the improvement of sweet potato.

Discovery and characterization of sweetpotato’s closest tetraploid relative

“…First, the wild provenance of the samples we studied, which were not cultivated, feral or derived from breeding programmes (Notes S3). Second, I. aequatoriensis is consistently recovered as monophyletic and sister to I. batatas in nuclear phylogenies, regardless of the method of phylogenetic inference, both in our study (Figs 2a,S7,S8) and in a recent pre-print (Yan et al, 2021). Third, its genetic structure is indicative of an autopolyploid origin (Table S5; Notes S1), a requirement for the tetraploid progenitor of the sweetpotato…”

“…Second, I . aequatoriensis is consistently recovered as monophyletic and sister to I. batatas in nuclear phylogenies, regardless of the method of phylogenetic inference, both in our study (Figs 2a , S7, S8 ) and in a recent pre‐print (Yan et al ., 2021 ). Third, its genetic structure is indicative of an autopolyploid origin (Table S5 ; Notes S1 ), a requirement for the tetraploid progenitor of the sweetpotato because of the AABBBB structure of the sweetpotato genome.…”

“…Because of their parentage, such tetraploids are closely related to hexaploid I. batatas in nuclear phylogenies (Figs 2a , S7 ). Therefore, studies that rely purely on phylogenetic analysis of nuclear DNA sequence data are likely to confuse these putative hybrid tetraploids with the autotetraploid progenitor of hexaploid I. batatas (Yan et al ., 2021 ) (Notes S3 ). However, the incorporation of other lines of evidence confirms the hybrid origin of these tetraploid entities and shows they cannot be the tetraploid progenitor of sweetpotato.…”

Exploring and exploiting genetics and genomics for sweetpotato improvement: Status and perspectives

“… (G) The allopolyploid hypothesis of Yang et al. (2017a) and Yan et al. (2021) : sweetpotato is likely to be derived from a triploid that arose from a cross between I. trifida and I. batatas 4x.…”

“…Since then, the number of genetic and genomics studies has increased, and a number of bioinformatics tools/pipelines for sweetpotato have been developed. These include Ranbow, GBSapp, ngsAssocPoly, MAPpoly, QTLpoly, OutcrossSeq, and haplotype-based phylogenetic analysis (HPA) ( Wadl et al., 2018 ; Moeinzadeh et al., 2020 ; Mollinari et al., 2020 ; da Silva Pereira et al., 2020 ; Yamamoto et al., 2020 ; Chen et al., 2021 ; Yamakawa et al., 2021 ; Yan et al., 2021 ). Over the past few decades, traditional breeding and molecular breeding approaches have been widely applied to sweetpotato and have resulted in the development of many new cultivars with improved yield, nutrient content, pest resistance, and other quality factors ( Newell et al., 1995 ; Okada et al., 2001 ; Otani et al., 2003 ; Gao et al., 2011b ; Wang et al., 2019 ).…”