Genetic drift, historic migration, and limited gene flow contributing to the subpopulation divergence in wild sea beet (Beta vulgaris ssp. maritima (L.) Arcang)

Authors: TEHSSEN, MUHAMMAD MASSUB - North Dakota State University; Wyatt, Nathan; Bolton, Melvin; Fugate, Karen; Preister, Lisa; Ramachandran, Vanitharani; Yang, Shengming; Chu, Chenggen; LI, XUEHUI - North Dakota State University

Submitted to: PLOS ONE
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 7/26/2024
Publication Date: 9/9/2024
Citation: Tehssen, M., Wyatt, N.A., Bolton, M.D., Fugate, K.K., Preister, L.S., Ramachandran, V., Yang, S., Chu, C.N., Li, X. 2024. Genetic drift, historic migration, and limited gene flow contributing to the subpopulation divergence in wild sea beet (Beta vulgaris ssp. maritima (L.) Arcang). PLOS ONE. 19(9):e0308626. https://doi.org/10.1371/journal.pone.0308626.
DOI: https://doi.org/10.1371/journal.pone.0308626

Interpretive Summary: All cultivated beet (sugar, table, leaf, and fodder) originated from sea beet, a wild beet species widely distributed along the coasts of the Mediterranean Sea and Atlantic Ocean in northern, western and southern Europe, as well as northern Africa. Sugarbeet is an important source of sucrose used for natural sweetening, but genetic improvements are needed to maintain the durability and sustainability of this crop. To understand the evolution of sea beet and identify regions where sea beet grows naturally that may be particularly useful for sugarbeet breeding, we analyzed genetic differences between sea beet samples collected from many countries. We found that samples harvested from the same region tend to be genetically similar whereas samples are more genetically diverse if harvested from more distant regions. Sea beet samples from seashore of the north Atlantic Ocean are the most genetically distinct from cultivated beet and sea beet collected from the rest of the regions. Sea beet samples harvested from northern Egypt and northwest Morrocco are genetically more isolated. This research indicated that sea beet likely spread from the coast of Mediterranean Sea by marine currents, which resulted in the divergence of sea beet in different regions. This study provides important information for the conservation, collection, and utilization of wild sea beet to sustain sugarbeet improvement.

Technical Abstract: All cultivated beet (sugar, table, leaf, fodder; Beta vulgaris L. ssp. vulgaris) originated from sea beet (B. vulgaris ssp. maritima), a wild beet species widely distributed along the coasts of the Mediterranean Sea and Atlantic Ocean in northern, western and southern Europe, as well as northern Africa. Understanding the evolution of sea beet will facilitate its efficient use in sugarbeet improvement. In this research, we used SNPs (single nucleotide polymorphisms) covering the whole genome to analyze a panel of 599 sea beet accessions collected from the north Atlantic Ocean and Mediterranean Sea coasts. Population structure analysis indicated that all B. maritima accessions can be grouped into eight clusters with each corresponding to a specific geographic region. Clusters 2, 3 and 4 with accessions mainly collected from Mediterranean coasts of southern Europe are genetically close to each other as well as to Cluster 6 that contained mainly cultivated beet lines. Other clusters were relatively distinct from cultivated beets with Clusters 1 and 5 containing accessions from north Atlantic Ocean coasts, Cluster 7 with accessions mainly collected from the seashore of northern Egypt and southern Europe, and Cluster 8 containing accessions from northwest Morocco. The distribution of B. maritima subpopulations aligns well with the direction of marine currents, as seawater movement was considered a main dynamic force in spreading B. maritima during evolution. Estimation of genetic diversity indices all supported the formation of B. maritima subpopulations due to local genetic drift, seed dispersal, historic migration, and limited gene flow. This study indicated that B. maritima originated from southern Europe and then spread to other regions through marine currents and then colonized as subpopulations. This research provides vital information for conserving, collecting, and utilizing wild sea beet to sustain sugarbeet improvement.