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

Abstract

Sweetpotato (Ipomoea batatas (L.) Lam.) is one of the most important root crops cultivated worldwide. Because of its adaptability, high yield potential, and nutritional value, sweetpotato has become an important food crop, particularly in developing countries. To ensure adequate crop yields to meet increasing demand, it is essential to enhance the tolerance of sweetpotato to environmental stresses and other yield-limiting factors. The highly heterozygous hexaploid genome of I. batatas complicates genetic studies and limits improvement of sweetpotato through traditional breeding. However, application of next-generation sequencing and high-throughput genotyping and phenotyping technologies to sweetpotato genetics and genomics research has provided new tools and resources for crop improvement. In this review, we discuss the genomics resources that are available for sweetpotato, including the current reference genome, databases, and available bioinformatics tools. We systematically review the current state of knowledge on the polyploid genetics of sweetpotato, including studies of its origin and germplasm diversity and the associated mapping of important agricultural traits. We then outline the conventional and molecular breeding approaches that have been applied to sweetpotato. Finally, we discuss future goals for genetic studies of sweetpotato and crop improvement via breeding in combination with state-of-the-art multi-omics approaches such as genomic selection and gene editing. These approaches will advance and accelerate genetic improvement of this important root crop and facilitate its sustainable global production.

Keywords: breeding; genomics; polyploid genetics; sweetpotato.

Figure 1

Milestones in sweetpotato genetics and breeding Chronological achievements in the development of genetics tools/techniques and breeding are summarized. The references (Eserman et al., 2014; Schafleitner et al., 2010; Wang et al., 2010) are given in Supplemental Table 1. QTL, quantitative trait locus; GWAS, genome-wide association study; CRISPR-Cas9, clustered regularly interspaced short palindromic repeats-CRISPR-associated protein 9.

Figure 2

The phylogeny of sweetpotato and its wild relatives The phylogenetic relationships were inferred from a concatenated alignment matrix of 9776 single-copy ortholog sequences across six Ipomoea species with published genomes. Values at the nodes indicate bootstrap support (1 = 100%). The phylogenetic clades are based on those of Wood et al. (2020). Shown are photographs of Ipomoea flowers by Yuqin Wang (I. triloba and I. aquatica), M.Y. (I. purpurea), and Ming Li (I. batatas, I. trifida, and I. nil).

Figure 3

Hypotheses to describe the origin of cultivated sweetpotato (A) The autopolyploid hypothesis suggests that I. trifida is the only progenitor of sweetpotato. Adapted from Shiotani (1988). (B) Sweetpotato originated from I. trifida, and after the speciation of sweetpotato, a hybridization event occurred between sweetpotato and I. trifida. Adapted from Muñoz-Rodríguez et al. (2018). (C) The species tree embodying the two hybridization networks demonstrates the segmental allopolyploid hypothesis. From Gao et al. (2020). (D) The allopolyploid hypothesis of Nishiyama (1971): sweetpotato is derived from a triploid I. trifida that arose from hybridization of Ipomoea ×leucantha and I. littoralis. (E) The allopolyploid hypothesis of Austin (1988): sweetpotato arose via hybridization between I. trifida and I. triloba. (F) The allopolyploid hypothesis of Gao et al. (2011a, : sweetpotato arose via hybridization between I. tenuissima and I. littoralis. (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. (H) The allopolyploid hypothesis of Muñoz-Rodríguez et al. (2022): I. aequatoriensis arose from a whole-genome duplication in I. trifida. Sweetpotato (I. batatas) is likely to be derived from a cross between I. trifida and I. aequatoriensis. Subsequent introgression between I. trifida and sweetpotato resulted in chloroplast capture from I. trifida.

Figure 4

Strategies for sweetpotato genetics and breeding in the future (1) Genome resources. Haplotype-phased genomes and pan-genome sequencing provide basic information for genetics and breeding. CWR, crop wild relative. (2) Genetic mapping and marker-assisted selection (MAS). Genetic mapping enables association of specific genes, SNPs, or markers with agricultural traits and facilitates MAS. QTL, quantitative trait locus; GWAS, genome-wide association study; SNP, single-nucleotide polymorphism. (3) Genomic selection (GS). GS targets multiple complex traits simultaneously and accelerates breeding in sweetpotato. (4) High-throughput phenotyping. Automatic and high-throughput phenotyping technologies make it possible to handle a large number of progeny in breeding programs. UAV, unmanned aerial vehicle; AI, artificial intelligence. (5) Conventional hybridization. Hybridization of selected clones, visual evaluation of progeny, and subsequent selection. (6) Mutagenesis. Creating random mutations in the genome using chemical or radiation treatment with subsequent selection of plants with desirable traits. (7) Genome editing. Precise editing of the target site using CRISPR-Cas9-based tools. The transgene cassette is removed by chromosomal segregation after self-pollination or outcrossing in subsequent generations. (8) Multi-omics. An efficient means to identify the genes and gene networks involved in controlling a target trait. mGWAS, metabolite genome-wide association study.