Pangenome analyses reveal impact of transposable elements and ploidy on the evolution of potato species

Authors: Anglin, Noelle; BOZAN, ILLAYDA - McGill University - Canada; ACHAKKAGARI, SAI - McGill University - Canada; ELLIS, DAVID - International Potato Center; TAI, HELEN - Agriculture And Agri-Food Canada; STROMVIK, MARTINA - McGill University - Canada

Submitted to: Proceedings of the National Academy of Sciences (PNAS)
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/9/2023
Publication Date: 7/24/2023
Citation: Anglin, N.L., Bozan, I., Achakkagari, S., Ellis, D., Tai, H., Stromvik, M. 2023. The potato super pan-genome: impact of transposable elements and ploidy in the evolution of potato species. Proceedings of the National Academy of Sciences (PNAS). 31 e2211117120. https://doi.org/10.1073/pnas.2211117120.
DOI: https://doi.org/10.1073/pnas.2211117120

Interpretive Summary: Potato genetics are complex due to the high variability and multiple copies that can exist within their DNA. A comparative analysis of available potato genomes was made which included landraces, wild species, and cultivated material sourced from South America, North America, and Europe. The potatoes utilized in this study contained either two, three, four, or five copies of DNA in their cells and represented all the cultivated potato species and numerous wild species. Presence or absence variation of the genes was investigated and clear divisions were observed. Species with an endosperm balance number of one, grouped together and had less genes than other material used in this study. Species with an endosperm balance number of one typically from Central America are known to not be able to hybridize readily with other potato species which have higher endosperm balance numbers. Cultivated material with high ploidy levels (4 or 5 copies of DNA) had significantly higher gene content relative to wild species. Transposable elements or jumping genes were also investigated and found to highly dictate similarity among different samples in this study. Many of the modern propagated material included in this study had significantly more transposable elements than wilds species. Overall, there were clear divisions in samples based on geographic origin, hybridization barriers, gene content, and transposable elements.

Technical Abstract: Potato (Solanum sp., family Solanaceae) is the economically most important non-cereal crop globally. It has over 100 wild relatives in Solanum section Petota, which features species with both sexual and asexual reproduction, varying ploidy levels and complexity in species concept. We have constructed a pan-genome of Solanum section Petota from 296 accessions including diploids and polyploids and compared presence/absence variation (PAV). The Petota core and shell genomes are enriched in basic molecular and cellular functions with the cloud genome showing enrichment in transposable elements (TEs). The phylogenetic tree constructed based on PAVs grouped accessions into different clades, similar to phylogenies produced by others using DNA markers. A cladewise pan-genome approach was used to identify core genes unique to each clade. The unique clade genes show enrichment for functions involved in abiotic stress response (Clade 1+2 and Clade 3) and flowering/tuberization (Clade 4). A novel discovery was made of differences in TE content where Clade 1+2, which is composed of species from North and Central America with reproductive isolation from other clades, had low TE content compared to other clades. Furthermore, a subgrouping within Clade 4 of accessions with in vitro propagation history was identified and found to have high levels of TEs. Together the results suggest an important role for TE in adaptation to new environments, both natural and artificial, for Solanum section Petota.