Potato (Solanum tuberosum L.) is the world’s most important non-cereal food crop, and the vast majority of commercially grown cultivars are highly heterozygous tetraploids. Advances in diploid hybrid breeding based on true seeds have the potential to revolutionize future potato breeding and production1–4. So far, relatively few studies have examined the genome evolution and diversity of wild and cultivated landrace potatoes, which limits the application of their diversity in potato breeding. Here we assemble 44 high-quality diploid potato genomes from 24 wild and 20 cultivated accessions that are representative of Solanum section Petota, the tuber-bearing clade, as well as 2 genomes from the neighbouring section, Etuberosum. Extensive discordance of phylogenomic relationships suggests the complexity of potato evolution. We find that the potato genome substantially expanded its repertoire of disease-resistance genes when compared with closely related seed-propagated solanaceous crops, indicative of the effect of tuber-based propagation strategies on the evolution of the potato genome. We discover a transcription factor that determines tuber identity and interacts with the mobile tuberization inductive signal SP6A. We also identify 561,433 high-confidence structural variants and construct a map of large inversions, which provides insights for improving inbred lines and precluding potential linkage drag, as exemplified by a 5.8-Mb inversion that is associated with carotenoid content in tubers. This study will accelerate hybrid potato breeding and enrich our understanding of the evolution and biology of potato as a global staple food crop.

Missing heritability in genome-wide association studies defines a major problem in genetic analyses of complex biological traits1,2. The solution to this problem is to identify all causal genetic variants and to measure their individual contributions3,4. Here we report a graph pangenome of tomato constructed by precisely cataloguing more than 19 million variants from 838 genomes, including 32 new reference-level genome assemblies. This graph pangenome was used for genome-wide association study analyses and heritability estimation of 20,323 gene-expression and metabolite traits. The average estimated trait heritability is 0.41 compared with 0.33 when using the single linear reference genome. This 24% increase in estimated heritability is largely due to resolving incomplete linkage disequilibrium through the inclusion of additional causal structural variants identified using the graph pangenome. Moreover, by resolving allelic and locus heterogeneity, structural variants improve the power to identify genetic factors underlying agronomically important traits leading to, for example, the identification of two new genes potentially contributing to soluble solid content. The newly identified structural variants will facilitate genetic improvement of tomato through both marker-assisted selection and genomic selection. Our study advances the understanding of the heritability of complex traits and demonstrates the power of the graph pangenome in crop breeding.

By analyses of potato pan-genome and transcriptome, we discovered a TCP transcription factor, Soltu.DM.06G025210, determining tuber identity, on the basis of which we named this gene Identity of Tuber 1 (IT1).After our manuscript was accepted in principle, a study by Nicolas et al. 1 showed that BRANCHED1b acts as a tuberization repressor in aerial axillary buds in tetraploid potato. We note that IT1 and BRANCHED1b are the same gene. The name BRANCHED1b represents the A. thaliana nomenclature system 2 . We chose the name IT1 because the function of Soltu.DM.06G025210 in potato had not been reported before and our study suggests that it acts as a key regulator in potato tuberization, a new function that is different from its orthologue in tomato and Arabidopsis where it represses branching. Considering the difference in the function, we proposed the new name IT1 for Soltu.DM.06G025210.Both studies confirmed that IT1/BRANCHED1b interacts with the mobile tuberization inductive signal SP6A and plays an essential role in tuberization. Further investigation is awaited into how the same gene promotes tuberization in underground shoots (stolons) and represses tuberization in aerial axillary buds.