Abstract
BackgroundAlthough 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.ResultsWe 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.ConclusionsOur 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.
Highlights
Plastomes are highly conserved with respect to gene content and order in most photosynthetic angiosperms, extensive genomic rearrangements have been reported in Fabaceae, within the inverted repeat lacking clade (IRLC) of Papilionoideae
We focus on Medicago (M.) L. and its relatives Trigonella (T.) L. and Melilotus Miller, all belonging to the tribe Trifolieae, which is nested firmly within the IRLC
Inverted repeat (IR) reemergence in Melilotus dentata Assembly and annotation of plastomes of Melilotus dentata using a series of parameters suggested the presence of a large inverted repeat (~ 15 kb, ranging in size from 15,336 bp to 15,553 bp), which contained 10 coding genes, including ycf1, the conserved four ribosomal RNA (rRNA) genes (4.5S, 5S, 16S, and 23S rRNA) and five transfer RNA (tRNA) genes in the seed plants (Fig. 1a; Fig. S2)
Summary
Plastomes are highly conserved with respect to gene content and order in most photosynthetic angiosperms, extensive genomic rearrangements have been reported in Fabaceae, within the inverted repeat lacking clade (IRLC) of Papilionoideae. Because of the advent of high-throughput sequencing technologies, over 4500 land plant plastomes have been sequenced since the first tobacco plastome published in 1986 [4] and are publicly available in NCBI (accessed November 19, 2020). The size of these plastomes ranges from 16 to 242 kb. The IR loss, which causes reduction in plastome size, have been documented in many independent lineages, including two lineages of Erodium (Geraniaceae) [8, 9], Carnegiea gigantean (Cactaceae) [10], Tahina spectabilis (Arecaceae) [11], the Putranjivoid clade of Malpighiales [12] and the IR-lacking clade (IRLC) of Papilionoideae (Fabaceae) [13]
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