Caught in the Act: Variation in plastid genome inverted repeat expansion within and between populations of <i>Medicago minima</i>

Choi, In‐Su; Jansen, Robert K.; Ruhlman, Tracey A.

doi:10.1002/ece3.6839

Cited by 15 publications

(16 citation statements)

References 47 publications

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“…1 b) showed even distribution of reads over the assembled plastome sequence when both copies of the IR are included and ~ two-fold higher depth of coverage over the IR region compared with SC regions when only one IR copy is considered. This adds another evidence to the IR reemergence in the IRLC in addition to previous findings in M. minima [ 11 , 31 ]. The IR reemergence in Melilotus dentata was further confirmed by multiple individuals, but with some INDELs (insertions and deletions) between the two IR copies in Melilotus dentata 02 and Melilotus dentata 03 (Fig.…”

Section: Resultssupporting

confidence: 82%

“…A direct link between recombination and mutation hotspots was reported from the IR-lacking plastome of Lathyrus , in which c. 1.5 kb localized hypermutation region around ycf4 was caused by repeated DNA breakage and repair [ 20 ]. In addition, repeat-mediated recombination-dependent replication has caused a ~ 9 kb IR reemergence in Medicago minima [ 11 , 31 ]. Notably, plastomes of the IRLC species have abundant repetitive DNA and this seems to be rare in angiosperms’ chloroplast DNA (cpDNA) [ 22 ].…”

Section: Introductionmentioning

confidence: 99%

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

Chen

Liu

et al. 2021

BMC Plant Biol

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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.

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Section: Resultssupporting

confidence: 82%

Section: Introductionmentioning

confidence: 99%

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

Chen

Liu

et al. 2021

BMC Plant Biol

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“…Apart from concerns as to whether it is reasonable to recognize the plastome as a single locus ( Gonçalves et al, 2020 ; Doyle, 2021 ), one of the main and practical criticisms about whole plastome alignment without further filtration is that most gaps are located in AT-rich and low complexity regions, which are prone to high-level length polymorphisms in simple sequence repeats and falsely aligned non-orthologous sequences ( Duvall et al, 2020 ). The much longer whole plastome alignment of 244 legumes (313,335 bp) compared to the alignment lacking indels (64,099 bp) is not surprising when considering the dynamic gene, intron, intergenic, and repeat content across papilionoids (e.g., Milligan et al, 1989 ; Doyle et al, 1995 ; Bailey et al, 1997 ; Cai et al, 2008 ; Jansen et al, 2008 ; Sabir et al, 2014 ; Sveinsson and Cronk, 2014 ; Schwarz et al, 2015 ; Choi et al, 2019 , 2020a ; Jin et al, 2019 ; Oyebanji et al, 2020 ; Lee et al, 2021 ). The WP alignment extended well beyond the length of a typical plastome to accommodate for poorly aligned sequences.…”

Section: Discussionmentioning

confidence: 99%

Highly Resolved Papilionoid Legume Phylogeny Based on Plastid Phylogenomics

et al. 2022

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Comprising 501 genera and around 14,000 species, Papilionoideae is not only the largest subfamily of Fabaceae (Leguminosae; legumes), but also one of the most extraordinarily diverse clades among angiosperms. Papilionoids are a major source of food and forage, are ecologically successful in all major biomes, and display dramatic variation in both floral architecture and plastid genome (plastome) structure. Plastid DNA-based phylogenetic analyses have greatly improved our understanding of relationships among the major groups of Papilionoideae, yet the backbone of the subfamily phylogeny remains unresolved. In this study, we sequenced and assembled 39 new plastomes that are covering key genera representing the morphological diversity in the subfamily. From 244 total taxa, we produced eight datasets for maximum likelihood (ML) analyses based on entire plastomes and/or concatenated sequences of 77 protein-coding sequences (CDS) and two datasets for multispecies coalescent (MSC) analyses based on individual gene trees. We additionally produced a combined nucleotide dataset comprising CDS plus matK gene sequences only, in which most papilionoid genera were sampled. A ML tree based on the entire plastome maximally supported all of the deep and most recent divergences of papilionoids (223 out of 236 nodes). The Swartzieae, ADA (Angylocalyceae, Dipterygeae, and Amburaneae), Cladrastis, Andira, and Exostyleae clades formed a grade to the remainder of the Papilionoideae, concordant with nine ML and two MSC trees. Phylogenetic relationships among the remaining five papilionoid lineages (Vataireoid, Dermatophyllum, Genistoid s.l., Dalbergioid s.l., and Baphieae + Non-Protein Amino Acid Accumulating or NPAAA clade) remained uncertain, because of insufficient support and/or conflicting relationships among trees. Our study fully resolved most of the deep nodes of Papilionoideae, however, some relationships require further exploration. More genome-scale data and rigorous analyses are needed to disentangle phylogenetic relationships among the five remaining lineages.

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“…Repeated sequences and rearrangements pose challenges to plastome assembly, and the choice of reference in reference-guided assembly or de novo assembly using sets of reads that map to references may bias against the detection of novel rearrangements. Plastome rearrangements are also not necessarily fixed within single taxa ( Gurdon and Maliga 2014 ; Choi et al 2020 ) and may not be fixed within single individuals sampled ( Guo et al 2014 ). Other forms of heteroplasmy, though not considered in this study, have been observed in an Astragalus plastome ( Lei et al 2016 ) as well.…”

Section: Discussionmentioning

confidence: 99%

Plastome Structural Evolution and Homoplastic Inversions in Neo-Astragalus (Fabaceae)

Charboneau

Cronn

Liston

et al. 2021

Genome Biology and Evolution

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The plastid genomes of photosynthetic green plants have largely maintained conserved gene content and order as well as structure over hundreds of millions of years of evolution. Several plant lineages, however, have departed from this conservation and contain many plastome structural rearrangements, which have been associated with an abundance of repeated sequences both overall and near rearrangement endpoints. We sequenced the plastomes of 25 taxa of Astragalus L. (Fabaceae), a large genus in the inverted repeat–lacking clade of legumes, to gain a greater understanding of the connection between repeats and plastome inversions. We found plastome repeat structure has a strong phylogenetic signal among these closely related taxa mostly in the New World clade of Astragalus called Neo-Astragalus. Taxa without inversions also do not differ substantially in their overall repeat structure from four taxa each with one large-scale inversion. For two taxa with inversion endpoints between the same pairs of genes, differences in their exact endpoints indicate the inversions occurred independently. Our proposed mechanism for inversion formation suggests the short inverted repeats now found near the endpoints of the four inversions may be there as a result of these inversions rather than their cause. The longer inverted repeats now near endpoints may have allowed the inversions first mediated by shorter microhomologous sequences to propagate, something that should be considered in explaining how any plastome rearrangement becomes fixed regardless of the mechanism of initial formation.

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Caught in the Act: Variation in plastid genome inverted repeat expansion within and between populations of Medicago minima

Cited by 15 publications

References 47 publications

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

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

Highly Resolved Papilionoid Legume Phylogeny Based on Plastid Phylogenomics

Plastome Structural Evolution and Homoplastic Inversions in Neo-Astragalus (Fabaceae)

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