Expansion of inverted repeat does not decrease substitution rates in <i>Pelargonium</i> plastid genomes

Weng, Mao‐Lun; Ruhlman, Tracey A.; Jansen, Robert K.

doi:10.1111/nph.14375

Cited by 104 publications

(123 citation statements)

References 53 publications

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“…Duplication of rpoA has also been documented in Pelargonium but in this case duplicate copies reside in the IR (Blazier et al 2016a; Weng et al 2017). Up to six copies of rpoA are present in each IR in some species and although rates of nucleotide substitutions are very high and levels of amino acid sequence identity is as low as 19% compared with the outgroup Eucalyptus , this gene is experiencing purifying selection and functional domains remain intact, suggesting that the rpoA is functional in Pelargonium .…”

Section: Discussionmentioning

confidence: 91%

“…Organelle sequencing across the angiosperm family Geraniaceae revealed accelerated substitution rates and rapid structural evolution in plastomes (Guisinger et al 2008, 2011; Weng et al 2014, 2017; Blazier et al 2016b; Ruhlman et al 2017) as well as highly accelerated substitution rates in mitogenomes (Parkinson et al 2005, Bakker et al 2006, Weng et al 2012). However, because only one to three species of the largest genus Geranium with >400 species (Aedo et al 1998) were included in previous studies, little is known about the evolution of their organelle genomes.…”

Section: Discussionmentioning

confidence: 99%

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Contrasting Patterns of Nucleotide Substitution Rates Provide Insight into Dynamic Evolution of Plastid and Mitochondrial Genomes of Geranium

Park

Ruhlman

Weng

et al. 2017

Genome Biology and Evolution

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Geraniaceae have emerged as a model system for investigating the causes and consequences of variation in plastid and mitochondrial genomes. Incredible structural variation in plastid genomes (plastomes) and highly accelerated evolutionary rates have been reported in selected lineages and functional groups of genes in both plastomes and mitochondrial genomes (mitogenomes), and these phenomena have been implicated in cytonuclear incompatibility. Previous organelle genome studies have included limited sampling of Geranium, the largest genus in the family with over 400 species. This study reports on rates and patterns of nucleotide substitutions in plastomes and mitogenomes of 17 species of Geranium and representatives of other Geraniaceae. As detected across other angiosperms, substitution rates in the plastome are 3.5 times higher than the mitogenome in most Geranium. However, in the branch leading to Geranium brycei/Geranium incanum mitochondrial genes experienced significantly higher dN and dS than plastid genes, a pattern that has only been detected in one other angiosperm. Furthermore, rate accelerations differ in the two organelle genomes with plastomes having increased dN and mitogenomes with increased dS. In the Geranium phaeum/Geranium reflexum clade, duplicate copies of clpP and rpoA genes that experienced asymmetric rate divergence were detected in the single copy region of the plastome. In the case of rpoA, the branch leading to G. phaeum/G. reflexum experienced positive selection or relaxation of purifying selection. Finally, the evolution of acetyl-CoA carboxylase is unusual in Geraniaceae because it is only the second angiosperm family where both prokaryotic and eukaryotic ACCases functionally coexist in the plastid.

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Section: Discussionmentioning

confidence: 91%

Section: Discussionmentioning

confidence: 99%

Contrasting Patterns of Nucleotide Substitution Rates Provide Insight into Dynamic Evolution of Plastid and Mitochondrial Genomes of Geranium

Park

Ruhlman

Weng

et al. 2017

Genome Biology and Evolution

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“…Large scale IR expansion as seen in P. auriculata (subg. Decaloba) with an IR of ∼47 kb has been documented in only a few other seed plants, including Pelargonium transvaalense, which has the largest IR reported in seed plants so far at ∼88 kb (Weng et al, ).…”

Section: Discussionmentioning

confidence: 99%

“…The quadripartite structure comprises two single copy regions, the large and small single copy (LSC and SSC, respectively), separated by a large inverted repeat (IR). Most plastomes retain 30 tRNAs, four rRNAs and about 80 protein‐coding genes packed into a unit‐genome of average size ∼153 kilobases (kb) (Weng et al, ). The majority of protein coding sequences are involved in photosynthesis and maintenance of the plastome genetic system (Bock, ; Ruhlman & Jansen, ).…”

Section: Introductionmentioning

confidence: 99%

“…Larger variation in plastome size due to IR expansion and contraction has been documented in several unrelated lineages, including Geraniaceae (Chumley et al, ; Blazier et al, ; Weng et al, , 2017), Plantago (Zhu et al, ), Ericaceae (Fajardo et al, ; Martínez‐Alberola et al, ), Berberis (Ma et al, ), Annona (Blazier et al, ) and Trochodendraceae (Sun et al, ). Among these lineages, Geraniaceae has the broadest range of IR sizes including species with enormous IR expansion to ∼88 kb in Pelargonium transvaalense (Weng et al, ), significant reduction to ∼7 kb in Monsonia speciosa (Guisinger et al, ) and species lacking an IR entirely in Erodium and Monsonia (Blazier et al, ; Ruhlman et al, ). Inverted repeat loss has been documented in other angiosperm lineages such as Fabaceae (Palmer & Thompson, ; Downie & Palmer, ) and Cactaceae (Sanderson et al, ).…”

Section: Introductionmentioning

confidence: 99%

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Passifloraplastome sequencing reveals widespread genomic rearrangements

Rabah

Shrestha

Hajrah

et al. 2018

J of Sytematics Evolution

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Although past studies have included Passiflora among angiosperm lineages with highly rearranged plastid genomes (plastomes), knowledge about plastome organization in the genus is limited. So far only one draft and one complete plastome have been published. Expanded sampling of Passiflora plastomes is needed to understand the extent of the genomic rearrangement in the genus, which is also unusual in having biparental plastid inheritance and plastome‐genome incompatibility. We sequenced 15 Passiflora plastomes using either Illumina paired‐end or shotgun cloning and Sanger sequencing approaches. Assembled plastomes were annotated using Dual Organellar GenoMe Annotator (DOGMA) and tRNAscan‐SE. The Populus trichocarpa plastome was used as a reference to estimate genomic rearrangements in Passiflora by performing whole genome alignment in progressiveMauve. The phylogenetic distribution of rearrangements was plotted on the maximum likelihood tree generated from 64 plastid encoded protein genes. Inverted repeat (IR) expansion/contraction and loss of the two largest hypothetical open reading frames, ycf1 and ycf2, account for most plastome size variation, which ranges from 139 262 base pairs (bp) in P. biflora to 161 494 bp in P. pittieri. Passiflora plastomes have experienced numerous inversions, gene and intron losses along with multiple independent IR expansions and contractions resulting in a distinct organization in each of the three subgenera examined. Each Passiflora subgenus has a unique plastome structure in terms of gene content, order and size. The phylogenetic distribution of rearrangements shows that Passiflora has experienced widespread genomic changes, suggesting that such events may not be reliable phylogenetic markers.

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Plastid phylogenomics and molecular evolution of Thismiaceae (Dioscoreales)

Garrett

Viruel

Klimpert

et al. 2023

American J of Botany

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Premise Species in Thismiaceae can no longer photosynthesize and instead obtain carbon from soil fungi. Here we infer Thismiaceae phylogeny using plastid genome data and characterize the molecular evolution of this genome. Methods We assembled five Thismiaceae plastid genomes from genome skimming data, adding to previously published data for phylogenomic inference. We investigated plastid‐genome structural changes, considering locally colinear blocks (LCBs). We also characterized possible shifts in selection pressure in retained genes by considering changes in the ratio of nonsynonymous to synonymous changes (ω). Results Thismiaceae experienced two major pulses of gene loss around the early diversification of the family, with subsequent scattered gene losses across descendent lineages. In addition to massive size reduction, Thismiaceae plastid genomes experienced occasional inversions, and there were likely two independent losses of the plastid inverted repeat (IR) region. Retained plastid genes remain under generally strong purifying selection (ω << 1), with significant and sporadic weakening or strengthening in several instances. The bifunctional trnE‐UUC gene of Thismia huangii may retain a secondary role in heme biosynthesis, despite a probable loss of functionality in protein translation. Several cis‐spliced group IIA introns have been retained, despite the loss of the plastid intron maturase, matK. Conclusions We infer that most gene losses in Thismiaceae occurred early and rapidly, following the initial loss of photosynthesis in its stem lineage. As a species‐rich, fully mycoheterotrophic lineage, Thismiaceae provide a model system for uncovering the unique and divergent ways in which plastid genomes evolve in heterotrophic plants.

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Expansion of inverted repeat does not decrease substitution rates in Pelargonium plastid genomes

Cited by 104 publications

References 53 publications

Contrasting Patterns of Nucleotide Substitution Rates Provide Insight into Dynamic Evolution of Plastid and Mitochondrial Genomes of Geranium

Contrasting Patterns of Nucleotide Substitution Rates Provide Insight into Dynamic Evolution of Plastid and Mitochondrial Genomes of Geranium

Passifloraplastome sequencing reveals widespread genomic rearrangements

Plastid phylogenomics and molecular evolution of Thismiaceae (Dioscoreales)

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