The chicken or the egg? Plastome evolution and an independent loss of the inverted repeat in papilionoid legumes

Abstract Background Paphiopedilum is the largest genus of slipper orchids. Previous studies showed that the phylogenetic relationships of this genus are not well resolved, and sparse taxon sampling documented inverted repeat (IR) expansion and small single copy (SSC) contraction of the chloroplast genomes of Paphiopedilum. Results Here, we sequenced, assembled, and annotated 77 plastomes of Paphiopedilum species (size range of 152,130 – 164,092 bp). The phylogeny based on the plastome resolved the relationships of the genus except for the phylogenetic position of two unstable species. We used phylogenetic and comparative genomic approaches to elucidate the plastome evolution of Paphiopedilum. The plastomes of Paphiopedilum have a conserved genome structure and gene content except in the SSC region. The large single copy/inverted repeat (LSC/IR) boundaries are relatively stable, while the boundaries of the inverted repeat and small single copy region (IR/SSC) varied among species. Corresponding to the IR/SSC boundary shifts, the chloroplast genomes of the genus experienced IR expansion and SSC contraction. The IR region incorporated one to six genes of the SSC region. Unexpectedly, great variation in the size, gene order, and gene content of the SSC regions was found, especially in the subg. Parvisepalum. Furthermore, Paphiopedilum provides evidence for the ongoing degradation of the ndh genes in the photoautotrophic plants. The estimated substitution rates of the protein coding genes show accelerated rates of evolution in clpP, psbH, and psbZ. Genes transferred to the IR region due to the boundary shift also have higher substitution rates. Conclusions We found IR expansion and SSC contraction in the chloroplast genomes of Paphiopedilum with dense sampling, and the genus shows variation in the size, gene order, and gene content of the SSC region. This genus provides an ideal system to investigate the dynamics of plastome evolution.

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Plastome Reduction in the Only Parasitic Gymnosperm Parasitaxus Is Due to Losses of Photosynthesis but Not Housekeeping Genes and Apparently Involves the Secondary Gain of a Large Inverted Repeat

Genome Biology and Evolution ◽

10.1093/gbe/evz187 ◽

2019 ◽

Vol 11 (10) ◽

pp. 2789-2796 ◽

Cited By ~ 6

Author(s):

Xiao-Jian Qu ◽

Shou-Jin Fan ◽

Susann Wicke ◽

Ting-Shuang Yi

Keyword(s):

Inverted Repeat ◽

Chlorophyll Biosynthesis ◽

Housekeeping Genes ◽

Parasitic Plants ◽

Structural Features ◽

Regulation System ◽

Biosynthesis Pathway ◽

Plastid Genomes ◽

Plastome Evolution ◽

Selection For

Abstract Plastid genomes (plastomes) of parasitic plants undergo dramatic reductions as the need for photosynthesis relaxes. Here, we report the plastome of the only known heterotrophic gymnosperm Parasitaxus usta (Podocarpaceae). With 68 unique genes, of which 33 encode proteins, 31 tRNAs, and four rRNAs in a plastome of 85.3-kb length, Parasitaxus has both the smallest and the functionally least capable plastid genome of gymnosperms. Although the heterotroph retains chlorophyll, all genes for photosynthesis are physically or functionally lost, making photosynthetic energy gain impossible. The pseudogenization of the three plastome-encoded light-independent chlorophyll biosynthesis genes chlB, chlL, and chlN implies that Parasitaxus relies on either only the light-dependent chlorophyll biosynthesis pathway or another regulation system. Nesting within a group of gymnosperms known for the absence of the large inverted repeat regions (IRs), another unusual feature of the Parasitaxus plastome is the existence of a 9,256-bp long IR. Its short length and a gene composition that completely differs from those of IR-containing gymnosperms together suggest a regain of this critical, plastome structure-stabilizing feature. In sum, our findings highlight the particular path of lifestyle-associated reductive plastome evolution, where structural features might provide additional cues of a continued selection for plastome maintenance.

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Phylogenomics and biogeography of Wisteria : implications on plastome evolution among inverted repeat‐lacking clade (IRLC) legumes

Journal of Systematics and Evolution ◽

10.1111/jse.12733 ◽

2021 ◽

Author(s):

Mao‐Qin Xia ◽

Ren‐Yu Liao ◽

Jin‐Ting Zhou ◽

Han‐Yang Lin ◽

Jian‐Hua Li ◽

...

Keyword(s):

Inverted Repeat ◽

Plastome Evolution

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The Chloroplast Genome Evolution of Venus Slipper (Paphiopedilum): IR Expansion, SSC Contraction, and Highly Rearranged SSC Regions

10.21203/rs.3.rs-257472/v1 ◽

2021 ◽

Author(s):

Yan-Yan Guo ◽

Jia-Xing Yang ◽

Guo-Qiang Zhang ◽

Zhong-Jian Liu

Keyword(s):

Gene Order ◽

Inverted Repeat ◽

Genome Structure ◽

Single Copy ◽

Gene Content ◽

Comparative Genomic ◽

Plastome Evolution ◽

Chloroplast Genomes ◽

Ideal System ◽

Small Single Copy

Abstract Background: Paphiopedilum is the largest genus of slipper orchids. Previous studies showed that the phylogenetic relationships of this genus are not well resolved, and sparse taxon sampling documented inverted repeat (IR) expansion and small single copy (SSC) contraction of the chloroplast genomes of Paphiopedilum. Here, we sequenced, assembled, and annotated 77 plastomes of Paphiopedilum species. The phylogeny based on the plastome resolved the relationships of the genus except for the phylogenetic position of two unstable species. We used phylogenetic and comparative genomic approaches to elucidate the plastome evolution of Paphiopedilum.Results: The plastomes of Paphiopedilum have conserved genome structure and gene content except in the SSC region. The large single copy/inverted repeat (LSC/IR) boundaries are relatively stable, while the boundaries of inverted repeat/small single copy (IR/SSC) boundaries varied among species. Corresponding to the IR/SSC boundary shifts, the chloroplast genomes of the genus experienced IR expansion and SSC contraction. The IR region incorporated one to six genes of the SSC region. Unexpectedly, great variation in the size, gene order, and gene content of the SSC regions was found, especially in the subg. Parvisepalum. Furthermore, Paphiopedilum provides evidence for the ongoing degradation of the ndh genes in the photoautotrophic plants. The estimated substitution rates of the protein coding genes show accelerated rates of evolution in clpP, psbH, and psbZ. Genes transferred to the IR region due to the boundary shift also have higher substitution rates.Conclusions: We found IR expansion and SSC contraction in the chloroplast genomes of Paphiopedilum with dense sampling, and the genus shows variation in the size, gene order, and gene content of the SSC region. This genus provides an ideal system to investigate the dynamics of plastome evolution.

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The chicken or the egg? Plastome evolution and a novel loss of the inverted repeat in papilionoid legumes

10.1101/2021.02.04.429812 ◽

2021 ◽

Author(s):

Chaehee Lee ◽

In-Su Choi ◽

Domingos Cardoso ◽

Haroldo C. de Lima ◽

Luciano P. de Queiroz ◽

...

Keyword(s):

Inverted Repeat ◽

Structural Changes ◽

Structural Evolution ◽

Comparative Genomic ◽

Independent Events ◽

Plastid Genomes ◽

Plastome Evolution ◽

The Family ◽

History Of

AbstractThe plastid genome (plastome), while surprisingly constant in gene order and content across most photosynthetic angiosperms, exhibits variability in several unrelated lineages. During the diversification history of the legume family Fabaceae, plastomes have undergone many rearrangements, including inversions, expansion, contraction and loss of the typical inverted repeat (IR), gene loss and repeat accumulation in both shared and independent events. While legume plastomes have been the subject of study for some time, most work has focused on agricultural species in the IR-lacking clade (IRLC) and the plant model Medicago truncatula. The subfamily Papilionoideae, which contains virtually all of the agricultural legume species, also comprises most of the plastome variation detected thus far in the family. In this study 33 newly sequenced plastomes of papilionoid legumes and outgroups were evaluated, along with 34 publicly available sequences, to assess plastome structural evolution in the subfamily. In an effort to examine plastome variation across the subfamily, just ∼20% of the sampling represents the IRLC with the remainder selected to represent the early-branching papilionoid clades. A number of IR-related and repeat-mediated changes were identified and examined in a phylogenetic context. Recombination between direct repeats associated with ycf2 resulted in intraindividual plastome heteroplasmy. Although loss of the inverted repeat has not been reported in legumes outside of the IRLC, one genistoid taxon was found to completely lack the typical plastome IR. The role of the IR and non-IR repeats in driving plastome change is discussed.Significance statementComparative genomic approaches employing plastid genomes (plastomes) have revealed that they are more variable across angiosperms than previously suggested. This study examined 64 species of Fabaceae and outgroups, including 33 newly sequenced taxa, to explore plastome structural evolution of the subfamily Papilionoideae in a phylogenetic context. Several unusual features of the inverted repeat highlight the importance of recombination in plastomic structural changes within and between individuals and species.

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Plastome Evolution in the Hyperdiverse Genus Euphorbia (Euphorbiaceae) Using Phylogenomic and Comparative Analyses: Large-Scale Expansion and Contraction of the Inverted Repeat Region

Frontiers in Plant Science ◽

10.3389/fpls.2021.712064 ◽

2021 ◽

Vol 12 ◽

Author(s):

Neng Wei ◽

Oscar A. Pérez-Escobar ◽

Paul M. Musili ◽

Wei-Chang Huang ◽

Jun-Bo Yang ◽

...

Keyword(s):

Inverted Repeat ◽

Large Scale ◽

Structural Variations ◽

Inverted Repeat Region ◽

Sister Relationship ◽

Comparative Analyses ◽

Coding Regions ◽

Plastome Evolution ◽

First Time ◽

Range Of Variation

With c. 2,000 species, Euphorbia is one of the largest angiosperm genera, yet a lack of chloroplast genome (plastome) resources impedes a better understanding of its evolution. In this study, we assembled and annotated 28 plastomes from Euphorbiaceae, of which 15 were newly sequenced. Phylogenomic and comparative analyses of 22 plastome sequences from all four recognized subgenera within Euphorbia revealed that plastome length in Euphorbia is labile, presenting a range of variation c. 42 kb. Large-scale expansions of the inverted repeat (IR) region were identified, and at the extreme opposite, the near-complete loss of the IR region (with only 355 bp left) was detected for the first time in Euphorbiaceae. Other structural variations, including gene inversion and duplication, and gene loss/pseudogenization, were also observed. We screened the most promising molecular markers from both intergenic and coding regions for phylogeny-based utilities, and estimated maximum likelihood and Bayesian phylogenies from four datasets including whole plastome sequences. The monophyly of Euphorbia is supported, and its four subgenera are recovered in a successive sister relationship. Our study constitutes the first comprehensive investigation on the plastome structural variation in Euphorbia and it provides resources for phylogenetic research in the genus, facilitating further studies on its taxonomy, evolution, and conservation.

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Formation of Large Palindromic DNA by Homologous Recombination of Short Inverted Repeat Sequences in Saccharomyces cerevisiae

Genetics ◽

10.1093/genetics/161.3.1065 ◽

2002 ◽

Vol 161 (3) ◽

pp. 1065-1075

Author(s):

David K Butler ◽

David Gillespie ◽

Brandi Steele

Keyword(s):

Homologous Recombination ◽

Inverted Repeat ◽

Excision Repair ◽

Strand Break ◽

Double Strand Break ◽

Repeat Sequence ◽

Inverted Repeat Sequence ◽

Repeat Sequences ◽

Dna Double Strand Break ◽

Intermolecular Reaction

Abstract Large DNA palindromes form sporadically in many eukaryotic and prokaryotic genomes and are often associated with amplified genes. The presence of a short inverted repeat sequence near a DNA double-strand break has been implicated in the formation of large palindromes in a variety of organisms. Previously we have established that in Saccharomyces cerevisae a linear DNA palindrome is efficiently formed from a single-copy circular plasmid when a DNA double-strand break is introduced next to a short inverted repeat sequence. In this study we address whether the linear palindromes form by an intermolecular reaction (that is, a reaction between two identical fragments in a head-to-head arrangement) or by an unusual intramolecular reaction, as it apparently does in other examples of palindrome formation. Our evidence supports a model in which palindromes are primarily formed by an intermolecular reaction involving homologous recombination of short inverted repeat sequences. We have also extended our investigation into the requirement for DNA double-strand break repair genes in palindrome formation. We have found that a deletion of the RAD52 gene significantly reduces palindrome formation by intermolecular recombination and that deletions of two other genes in the RAD52-epistasis group (RAD51 and MRE11) have little or no effect on palindrome formation. In addition, palindrome formation is dramatically reduced by a deletion of the nucleotide excision repair gene RAD1.

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A 160-bp Palindrome Is a Rad50·Rad32-Dependent Mitotic Recombination Hotspot inSchizosaccharomyces pombe

Genetics ◽

10.1093/genetics/161.1.461 ◽

2002 ◽

Vol 161 (1) ◽

pp. 461-468 ◽

Cited By ~ 6

Author(s):

Joseph A Farah ◽

Edgar Hartsuiker ◽

Ken-ichi Mizuno ◽

Kunihiro Ohta ◽

Gerald R Smith

Keyword(s):

Secondary Structure ◽

Schizosaccharomyces Pombe ◽

Inverted Repeat ◽

Mitotic Recombination ◽

Genome Integrity ◽

Recombination Hotspot ◽

Nuclease Domain ◽

Palindromic Sequences

AbstractPalindromic sequences can form hairpin and cruciform structures that pose a threat to genome integrity. We found that a 160-bp palindrome (an inverted repeat of 80 bp) conferred a mitotic recombination hotspot relative to a control nonpalindromic sequence when inserted into the ade6 gene of Schizosaccharomyces pombe. The hotspot activity of the palindrome, but not the basal level of recombination, was abolished by a rad50 deletion, by a rad50S “separation of function” mutation, or by a rad32-D25A mutation in the nuclease domain of the Rad32 protein, an Mre11 homolog. We propose that upon extrusion of the palindrome the Rad50·Rad32 nuclease complex recognizes and cleaves the secondary structure thus formed and generates a recombinogenic break in the DNA.

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