Recent structural variations in the Medicago chloroplast genomes and their horizontal transfer into nuclear chromosomes

Authors: JIAO, YINGXUE - Beijing Forestry University; HE, XIAOFAN - Beijing Forestry University; SONG, RUI - China Agricultural University; WANG, XUEMENG - China Agricultural University; ZHANG, HAN - China Agricultural University; AILI, R - Beijing Forestry University; CHAO, YUEHUI - Beijing Forestry University; SHEN, YUHUA - Chifeng University; Yu, Long-Xi; ZHANG, TIEJUN - Beijing Forestry University; JIA, SHANGGANG - China Agricultural University

Submitted to: Journal of Systematics and Evolution
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/8/2022
Publication Date: 6/15/2022
Citation: Jiao, Y., He, X., Song, R., Wang, X., Zhang, H., Aili, R., Chao, Y., Shen, Y., Yu, L., Zhang, T., Jia, S. 2022. Recent structural variations in the Medicago chloroplast genomes and their horizontal transfer into nuclear chromosomes. Journal of Systematics and Evolution. 61(4):627-642. https://doi.org/10.1111/jse.12900.
DOI: https://doi.org/10.1111/jse.12900

Interpretive Summary: Medicago is a genus of legumes (family Fabaceae) that resemble common clovers with pinnately trifoliate leaves and spirally coiled seed pods, and Medicago sativa is one of the most commercially important forage crops in the world. In this study, we systematically assembled the complete DNA sequence of the chloroplast genomes of 35 Medicago accessions. We built the genetic family tree based on common proteins of 55 Medicago accessions in 38 species, which were placed into six related groups that diverged 10.08 million years ago (Mya). Side by side comparison of the DNA sequences of different Medicago species revealed independent evolutionary events of different genomes, including eight inversions (when pieces of DNA are reversed) in nine species and four intron losses (ILs, when pieces of DNA that are not used to make proteins are lost) in ten species, among which four inversions and two ILs were not reported previously. Structural variations were found extensively in some accessions of Medicago. The current findings expand our understanding of the chloroplast genomes for Medicago species. The family tree results further confirmed the Medicago taxonomies, and divergence time of species and inversions provided insight into the evolutionary history of chloroplast genomes of Medicago. The information would be useful for better understanding the genetic background and diversity of germplasm.

Technical Abstract: Medicago is a genus of legumes (family Fabaceae) that resemble common clovers with pinnately trifoliate leaves and spirally coiled seed pods, and Medicago sativa is one of the most commercially important forage crops in the world. In this study, we systematically assembled the complete plastid genomes of 35 Medicago accessions, which ranged from ~119 to 125 kb. We identified one novel inverted repeat (IR) in two accessions of M. soleirolii (PI537242 and PI537243), but most accessions contained no IRs. In addition, we built a phylogenetic tree based on common proteins of 55 Medicago accessions in 38 species, which were placed into six clades that diverged 10.08 million years ago (Mya). Global alignment revealed independent evolutionary events of different genomes, including eight inversions in nine species and four intron losses (ILs) in ten species, among which four inversions and two ILs were not reported previously. Interestingly, we identified multiple genome assemblies in single accessions, including Medicago coronata (PI498790), Medicago constricta (PI534177), Medicago littoralis (PI537201), and Medicago soleirolii (PI537242 and PI537243), suggesting frequent recent evolutionary events of the Medicago chloroplast genome. Within the 109~111 unique genes identified, ndhA, rpl2, and ycf3 were under positive selection in 54 accessions. Finally, by aligning chloroplast genes against the nuclear genome assembly of “Zhongmu No.1”, we found that a large number of chloroplast gene fragments were horizontally transferred to nuclear chromosomes in alfalfa, especially on chromosome 3. Our comprehensive exploration of Medicago chloroplast genomes provide insights for the understanding of Medicago speciation and genomic evolutionary events.