Extensive genomic rearrangements mediated by repetitive sequences in plastomes of Medicago and its relatives

Abstract

Background Although plastomes are highly conserved with respect to gene content and order in most photosynthetic angiosperms, extensive genomic rearrangements have been reported in Fabaceae, particularly within the inverted repeat lacking clade (IRLC) of Papilionoideae. Two hypotheses, i.e., the absence of the IR and the increased repeat content, have been proposed to affect the stability of plastomes. However, this is still unclear for the IRLC species. Here, we aimed to investigate the relationships between repeat content and the degree of genomic rearrangements in plastomes of Medicago and its relatives Trigonella and Melilotus, which are nested firmly within the IRLC. Results We detected abundant repetitive elements and extensive genomic rearrangements in the 75 newly assembled plastomes of 20 species, including gene loss, intron loss and gain, pseudogenization, tRNA duplication, inversion, and a second independent IR gain (IR ~ 15 kb in Melilotus dentata) in addition to the previous first reported cases in Medicago minima. We also conducted comparative genomic analysis to evaluate plastome evolution. Our results indicated that the overall repeat content is positively correlated with the degree of genomic rearrangements. Some of the genomic rearrangements were found to be directly linked with repetitive sequences. Tandem repeated sequences have been detected in the three genes with accelerated substitution rates (i.e., accD, clpP, and ycf1) and their length variation could be explained by the insertions of tandem repeats. The repeat contents of the three localized hypermutation regions around these three genes with accelerated substitution rates are also significantly higher than that of the remaining plastome sequences. Conclusions Our results suggest that IR reemergence in the IRLC species does not ensure their plastome stability. Instead, repeat-mediated illegitimate recombination is the major mechanism leading to genome instability, a pattern in agreement with recent findings in other angiosperm lineages. The plastome data generated herein provide valuable genomic resources for further investigating the plastome evolution in legumes.

New insights into the phylogeny of the complex thalloid liverworts (Marchantiopsida) based on chloroplast genomes

“…Thus, RNA editing of organellar genomes might have been absent in Marchantiopsida except for Cyathodium , which should be taken into consideration in future studies involving dense taxon sampling and transcriptome data of this genus. Additionally, repetitive DNA can induce rearrangements and promote genomic instability (Blazier et al., 2016; Sinn et al., 2018; Wu et al., 2021), whereas the abundance of repetitive sequences of plastomes in Cyathodium is slightly lower than in other genera of Marchantiopsida. Specifically, although intron II of the chloroplast gene ycf3 , which has two introns, is missing from all plastomes of Marchantiidae, intron I also is absent in C. cavernarum Kunze and C. smaragdinum .…”

Fragariamitogenomes evolve rapidly in structure but slowly in sequence and incur frequent multinucleotide mutations mediated by microinversions

“…Similarly, repeats of hundreds to thousands of base pairs are abundant in plant mitogenomes (Wynn & Christensen, 2019), whereas in the plastome, repeats > 100 bp are generally absent except for the single large inverted repeat (Mower & Vickrey, 2018). In many seed plants, rearrangement endpoints in organellar genomes are often associated with repeats ranging in size from tens to hundreds of nucleotides (Marechal & Brisson, 2010;Cole et al, 2018;Mower & Vickrey, 2018;Wu et al, 2021) New Phytologist the plastome (Cui et al, 2006;Wicke et al, 2011) than in the mitogenome (Liu et al, 2020;Wang et al, 2020). Finally, we speculate that, in plant mitogenomes, the rearrangements themselves may be an adaptive phenomenon, potentially serving as a mechanism to prevent runaway size expansion.…”

Plastomes of limestone karst gesneriad genera Petrocodon and Primulina, and the comparative plastid phylogenomics of Gesneriaceae

“…Comparative plastome analyses across diverse plant lineages such as cupressophytes 41 , Fabaceae 42 , Geraniaceae 43 , Asarum L. (Aristolochiaceae) 44 , and Trachelium L. (Camapnulaceae) 45 revealed a positive correlation between the number of repeats and the extent of plastome rearrangement, suggesting a general trend of the repeat-mediated recombination that could have resulted in plastome structural variation 42 . Although plastomes of some species such as the hot pepper Capsicum annuum L. possess a considerable number of repetitive sequences www.nature.com/scientificreports/ and yet are structurally highly conserved 46 , the relatively low number of repeats (Fig.…”