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Lineage-specific plastid degradation in subtribe Gentianinae (Gentianaceae).

ABSTRACT: The structure and sequence of plastid genomes is highly conserved across most land plants, except for a minority of lineages that show gene loss and genome degradation. Understanding the early stages of plastome degradation may provide crucial insights into the repeatability and predictability of genomic evolutionary trends. We investigated these trends in subtribe Gentianinae of the Gentianaceae, which encompasses ca. 450 species distributed around the world, particularly in alpine and subalpine environments. We sequenced, assembled, and annotated the plastomes of 41 species, representing all six genera in subtribe Gentianinae and all main sections of the species-rich genus Gentiana L. We reconstructed the phylogeny, estimated divergence times, investigated the phylogenetic distribution of putative gene losses, and related these to substitution rate shifts and species' habitats. We obtained a strongly supported topology consistent with earlier studies, with all six genera in Gentianinae recovered as monophyletic and all main sections of Gentiana having full support. While closely related species have very similar plastomes in terms of size and structure, independent gene losses, particularly of the ndh complex, have occurred in multiple clades across the phylogeny. Gene loss was usually associated with a shift in the boundaries of the small single-copy and inverted repeat regions. Substitution rates were variable between clades, with evidence for both elevated and decelerated rate shifts. Independent lineage-specific loss of ndh genes occurred at a wide range of times, from Eocene to Pliocene. Our study illustrates that diverse degradation patterns shape the evolution of the plastid in this species-rich plant group.

SUBMITTER: Fu PC

PROVIDER: S-EPMC8019047 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundSubtribe Swertiinae, a medicinally significant and highly speciose Subtribe of family Gentianaceae. Despite previous extensive studies based on both morphology and molecular data, intergeneric and infrageneric relationships within subtribe Swertiinae remain controversial.MethodsHere, we employed four newly generated Swertia chloroplast genomes with thirty other published genomes to elucidate their genomic characteristics.ResultsThe 34 chloroplast genomes were small and ranged in size from 149,036 to 154,365 bp, each comprising two inverted repeat regions (size range 25,069-26,126 bp) that separated large single-copy (80,432-84,153 bp) and small single-copy (17,887-18,47 bp) regions, and all the chloroplast genomes showed similar gene orders, contents, and structures. These chloroplast genomes contained 129-134 genes each, including 84-89 protein-coding genes, 37 tRNAs, and 8 rRNAs. The chloroplast genomes of subtribe Swertiinae appeared to have lost some genes, such as rpl33, rpl2 and ycf15 genes. Comparative analyses revealed that two mutation hotspot regions (accD-psaI and ycf1) could serve as effective molecular markers for further phylogenetic analyses and species identification in subtribe Swertiinae. Positive selection analyses showed that two genes (ccsA and psbB) had high Ka/Ks ratios, indicating that chloroplast genes may have undergone positive selection in their evolutionary history. Phylogenetic analysis showed that the 34 subtribe Swertiinae species formed a monophyletic clade, with Veratrilla, Gentianopsis and Pterygocalyx located at the base of the phylogenetic tree. Some genera of this subtribe, however, were not monophyletic, including Swertia, Gentianopsis, Lomatogonium, Halenia, Veratrilla and Gentianopsis. In addition, our molecular phylogeny was consistent with taxonomic classification of subtribe Swertiinae in the Roate group and Tubular group. The results of molecular dating showed that the divergence between subtrib Gentianinae and subtrib Swertiinae was estimated to occur in 33.68 Ma. Roate group and Tubular group in subtribe Swertiinae approximately diverged in 25.17 Ma.ConclusionOverall, our study highlighted the taxonomic utility of chloroplast genomes in subtribe Swertiinae, and the genetic markers identified here will facilitate future studies on the evolution, conservation, population genetics, and phylogeography of subtribe Swertiinae species.

Project description:Australia harbours a rich and highly endemic orchid flora with over 90% of native species found nowhere else. However, little is known about the assembly and evolution of Australia's orchid flora. Here, we used a phylogenomic approach to infer evolutionary relationships, divergence times and range evolution in Pterostylidinae (Orchidoideae), the second largest subtribe in the Australian orchid flora, comprising the genera Pterostylis and Achlydosa. Phylogenetic analysis of 75 plastid genes provided well-resolved and supported phylogenies. Intrageneric relationships in Pterostylis were clarified and monophyly of eight of 10 sections supported. Achlydosa was found to not form part of Pterostylidinae and instead merits recognition at subtribal level, as Achlydosinae. Pterostylidinae were inferred to have originated in eastern Australia in the early Oligocene, coinciding with the complete separation of Australia from Antarctica and the onset of the Antarctic Circumpolar Current, which led to profound changes in the world's climate. Divergence of all major lineages occurred during the Miocene, accompanied by increased aridification and seasonality of the Australian continent, resulting in strong vegetational changes from rainforest to more open sclerophyllous vegetation. The majority of extant species were inferred to have originated in the Quaternary, from the Pleistocene onwards. The rapid climatic oscillations during the Pleistocene may have acted as important driver of speciation in Pterostylidinae. The subtribe underwent lineage diversification mainly within its ancestral range, in eastern Australia. Long-distance dispersals to southwest Australia commenced from the late Miocene onwards, after the establishment of the Nullarbor Plain, which constitutes a strong edaphic barrier to mesic plants. Range expansions from the mesic into the arid zone of eastern Australia (Eremaean region) commenced from the early Pleistocene onwards. Extant distributions of Pterostylidinae in other Australasian regions, such as New Zealand and New Caledonia, are of more recent origin, resulting from long-distance dispersals from the Pliocene onwards. Temperate eastern Australia was identified as key source area for dispersals to other Australasian regions.

Project description:BackgroundThe genus Swertia is of great medicinal importance and one of the most taxonomically challenging taxa within Gentianaceae, largely due to the morphological similarities of species within this genus and with its closely related genera. Previous molecular studies confirmed its polyphyly but suffered from low phylogenetic resolutions because only limited sequence loci were used. Thus, we conducted the structural, gene evolutionary, and phylogenetic analyses of 11 newly obtained plastomes of Swertia. Our result greatly improved the phylogenetic resolutions in Swertia, shed new light on the plastome evolution and phylogenetic relationships of this genus.ResultsThe 11 Swertia plastomes together with the published seven species proved highly similar in overall size, structure, gene order, and content, but revealed some structural variations caused by the expansion and contraction of the IRb region into the LSC region, due to the heterogeneous length of the ψycf1. The gene rps16 was found to be in a state flux with pseudogenes or completely lost. Similar situation was also documented in other genera of Gentianaceae. This might imply loss of the gene in the common ancestor of Gentianaceae. The distribution plot of ENC vs. GC3 showed all these plastomes arranging very close in the Wright line with an expected ENC value (49-52%), suggesting the codon usage of Swertia was mainly constrained by a GC mutation bias. Most of the genes remained under the purifying selection, however, the cemA was identified under positive selection, possibly reflecting an adaptive response to low CO2 atmospheric conditions during the Late Miocene. Our phylogenomic analyses, based on 74 protein-coding genes (CDS), supported the polyphyly of Swertia with its close allies in the subtribe Swertiinae, presumably due to recent rapid radiation. The topology inferred from our phylogenetic analyses partly supported the current taxonomic treatment. Finally, several highly variable loci were identified, which can be used in future phylogenetic studies and accurate identification of medicinal genuineness of Swertia.ConclusionsOur study confirmed the polyphyly of Swertia and demonstrated the power of plastome phylogenomics in improvement of phylogenetic resolution, thus contributing to a better understanding of the evolutionary history of Swertia.

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Lineage-specific plastid degradation in subtribe Gentianinae (Gentianaceae).

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