Legume genome structures and histories inferred from Cercis canadensis and Chamaecrista fasciculata genomes

Authors: LEE, HYUN-OH - Orise Fellow; STAI, JACOB - Orise Fellow; XU, QIAOJI - University Of Ottawa; HEWAVITHANA, THULANI - University Of Saskatchewan; BATRA, RABNOOR - University Of Saskatchewan; LIU, ALEX - University Of Waterloo; Jordan, Brandon; WALSTEAD, RACHEL - Hudsonalpha Institute For Biotechnology; JENKINS, JERRY - Hudsonalpha Institute For Biotechnology; WILLIAMS, MELISSA - Hudsonalpha Institute For Biotechnology; WEBBER, JENELL - Hudsonalpha Institute For Biotechnology; GRIMWOOD, JANE - Hudsonalpha Institute For Biotechnology; LOVELL, JOHN - Hudsonalpha Institute For Biotechnology; BRUNA, TOMÁŠ - Department Of Energy Joint Genome; SHU, SHENGQIANG - Department Of Energy Joint Genome; KEYMANESH, KEYKHOSROW - Department Of Energy Joint Genome; EICHENBERGER, JOANNE - Department Of Energy Joint Genome; SCHMUTZ, JEREMY - Hudsonalpha Institute For Biotechnology; GOODSTEIN, DAVID - Department Of Energy Joint Genome; BARRY, KERRIE - Department Of Energy Joint Genome; SANKOFF, DAVID - University Of Ottawa; JIN, LINGLING - University Of Saskatchewan; LEEBENS-MACK, JAMES - University Of Georgia; Cannon, Steven

Submitted to: bioRxiv
Publication Type: Pre-print Publication
Publication Acceptance Date: 9/8/2024
Publication Date: 9/8/2024
Citation: Lee, H., Stai, J.S., Xu, Q., Hewavithana, T., Batra, R., Liu, A., Jordan, B.D., Walstead, R., Jenkins, J., Williams, M., Webber, J., Grimwood, J., Lovell, J.T., Bruna, T., Shu, S., Keymanesh, K., Eichenberger, J., Schmutz, J., Goodstein, D.M., Barry, K., Sankoff, D., Jin, L., Leebens-Mack, J.H., Cannon, S.B. 2024. Legume genome structures and histories inferred from Cercis canadensis and Chamaecrista fasciculata genomes. bioRxiv. https://doi.org/10.1101/2024.09.03.611065.
DOI: https://doi.org/10.1101/2024.09.03.611065

Interpretive Summary: The legume plant family is one of the largest and most diverse plant families, with more than 20,000 species and more than two dozen crops, such as chickpea, alfalfa, faba bean, soybean, and peanut. The family also contains many other species that are important in all terrestrial ecosystems, from tropical forests to arctic tundra. Determining the relationships among those species is important for understanding the biology of traits of legume crops. For example, symbiotic nitrogen fixation (SNF) is found in all annual legume crop species, but is found in only two of six early-diverging legume subfamilies. This research reports the genome sequences (the DNA sequence from all chromosomes) of two species from those other, predominantly non-crop subfamilies: partridge pea (Chamaecrista fasciculata), which has SNF, and the redbud tree (Cercis canadensis), which lacks SNF. This research also reports that the genome sequence of Cercis is inferred to be close to the ancestral chromosome structure of the earliest legume. These species are also important in their own right -- redbud as a common ornamental tree used throughout North America; and partridge pea as a nitrogen-fixing species that is common in North American grasslands. The genome sequences of these species will aid researchers in understanding the orign and relationships among legume species, and in understanding the biology of characteristics such as symbiotic nitrogen fixation.

Technical Abstract: The legume family originated ca. 70 million years ago and soon diversified into at least six lineages (now extant subfamilies). The signal of whole genome duplications (WGD) is apparent in species sampled from all six subfamilies. The early diversification has posed difficulties for resolving the legume backbone structure and the timing of WGDs. This study reports the genome sequences and annotations for Cercis canadensis(Cercidoideae) and Chamaecrista fasciculata (Caesalpinoideae) to help resolve the relative taxonomic placements along the legume backbone, the timings of WGDs relative to subfamily origins, and the ancestral legume karyotype. Analyses of genome assemblies from four subfamilies within Fabaceae show that the last common ancestor of all legumes likely had seven chromosomes, with a genome structure similar to the extant Cercis genome. Our analysis supports an allopolyploid origin of the subfamily Caesalpinoideae, with progenitors involving lineages along the backbone of the legume phylogeny. A probable allopolyploid origin of Caesalpinoideae subfamily provides a partial explanation for the difficulty in resolving the structure of the legume backbone. The retained karyotype structure and lack of a WGD in the last 100+ Mya, underscore the utility of the Cercis genome as an ancestral reference for the legume family.