Plastid phylogenomics resolves ambiguous relationships within the orchid family and provides a solid timeframe for biogeography and macroevolution

Serna-Sánchez, Maria Alejandra; Pérez‐Escobar, Oscar Alejandro; Bogarín, Diego; Torres-Jimenez, María Fernanda; Álvarez-Yela, Astrid Catalina; Arcila-Galvis, Juliana E.; Hall, Climbiê Ferreira; Barros, Fábio de; Pinheiro, Fábio; Dodsworth, Steven; Chase, Mark W.; Antonelli, Alexandre; Arias, Tatiana

doi:10.1038/s41598-021-83664-5

Cited by 40 publications

(95 citation statements)

References 81 publications

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“…An overview of our current understanding of the phylogenetic relationships of orchids was produced by Chase et al (2015). The topology provided in this review is highly congruent with studies on entire coding plastid and mitochondrial genomes (Givnish et al, 2015;Li et al, 2019b;Serna-Sánchez et al, 2021) and with that of the low-copy nuclear gene Xdh (Górniak et al, 2010). Overall, our quantitative comparisons of our much larger plastid and nuclear data sets support this view, revealing that there is a high degree of congruence between nuclear and organellar phylogenetic trees in orchids, including the monophyly of the five subfamilies and many of the tribal, subtribal, and generic relationships (Fig.…”

Section: Are Nuclear and Plastid Evolutionary Histories Broadly Congruent In Orchids?supporting

confidence: 79%

“…With few exceptions (Bateman et al, 2018; Bogarín et al, 2018; Unruh et al, 2018; Brandrud et al, 2020; Pérez‐Escobar et al, 2020), previous orchid studies (Cameron et al, 1999; Salazar et al, 2003; Neubig et al, 2012; Givnish et al, 2015; Y. Li et al, 2019; Serna‐Sánchez et al, 2021) have relied on plastid data sets, although some have employed the low‐copy nuclear gene Xdh (Górniak et al, 2010) and the nuclear ribosomal ITS (nrITS) region (Freudenstein and Chase, 2015). Historically, nuclear genes have been difficult to sequence due to a combination of factors including inefficient amplification (due to degradation of DNA samples and/or large intronic regions), the need to clone amplified products due to paralogy or allelic diversity, the difficulty of sorting out paralogous sequences from orthologous ones, and lack of universal polymerase chain reaction (PCR) primers (Bailey et al, 2003; Feliner and Rosello, 2007; Sramkó et al, 2014).…”

Section: Discussionmentioning

confidence: 99%

“…The taxon sampling of nuclear and plastid datasets overlaps for 34 genera, 14 tribes, and 22 subtribes (Appendix S1). Detailed information on the completeness of this plastid DNA data set is provided in Serna‐Sánchez et al (2021).…”

Section: Methodsmentioning

confidence: 99%

“…To assess the performance of the Angiosperms353 nuclear loci for resolving orchid relationships and investigating nuclear/plastid gene tree discordance at different taxonomic levels, we utilized the 78-plastid-gene data set of Serna-Sánchez et al (2021; available at https://doi.org/10.6084/m9.figsh are.14068892) for 264 species representing 117 genera, 28 subtribes, and 18 tribes. The taxon sampling of nuclear and plastid datasets overlaps for 34 genera, 14 tribes, and 22 subtribes (Appendix S1).…”

Section: Plastome Phylogenomicsmentioning

confidence: 99%

“…With few exceptions (Bateman et al, 2018;Bogarín et al, 2018;Unruh et al, 2018;Brandrud et al, 2020;Pérez-Escobar et al, 2020), previous orchid studies (Cameron et al, 1999;Salazar et al, 2003;Neubig et al, 2012;Givnish et al, 2015;Y. Li et al, 2019;Serna-Sánchez et al, 2021) have relied on plastid data sets, although some have employed the low-copy nuclear gene Xdh (Górniak et al, 2010) and the nuclear ribosomal ITS (nrITS) region (Freudenstein and FIGURE 2. Species-coalescence tree of the orchid family inferred from 292 maximum likelihood (ML) gene trees.…”

Section: Limitations Of Plastid-only Analysesmentioning

confidence: 99%

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Hundreds of nuclear and plastid loci yield novel insights into orchid relationships

Pérez‐Escobar

Dodsworth

Bogarín

et al. 2021

American J of Botany

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The inference of evolutionary relationships in the species-rich family Orchidaceae has hitherto relied heavily on plastid DNA sequences and limited taxon sampling. Previous studies have provided a robust plastid phylogenetic framework, which was used to classify orchids and investigate the drivers of orchid diversification. However, the extent to which phylogenetic inference based on the plastid genome is congruent with the nuclear genome has been only poorly assessed. METHODS:We inferred higher-level phylogenetic relationships of orchids based on likelihood and ASTRAL analyses of 294 low-copy nuclear genes sequenced using the Angiosperms353 universal probe set for 75 species (representing 69 genera, 16 tribes, 24 subtribes) and a concatenated analysis of 78 plastid genes for 264 species (117 genera, 18 tribes, 28 subtribes). We compared phylogenetic informativeness and support for the nuclear and plastid phylogenetic hypotheses.RESULTS: Phylogenetic inference using nuclear data sets provides well-supported orchid relationships that are highly congruent between analyses. Comparisons of nuclear gene trees and a plastid supermatrix tree showed that the trees are mostly congruent, but revealed instances of strongly supported phylogenetic incongruence in both shallow and deep time. The phylogenetic informativeness of individual Angiosperms353 genes is in general better than that of most plastid genes. CONCLUSIONS:Our study provides the first robust nuclear phylogenomic framework for Orchidaceae and an assessment of intragenomic nuclear discordance, plastid-nuclear tree incongruence, and phylogenetic informativeness across the family. Our results also demonstrate what has long been known but rarely thoroughly documented: nuclear and plastid phylogenetic trees can contain strongly supported discordances, and this incongruence must be reconciled prior to interpretation in evolutionary studies, such as taxonomy, biogeography, and character evolution.

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Section: Are Nuclear and Plastid Evolutionary Histories Broadly Congruent In Orchids?supporting

confidence: 79%

Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Plastome Phylogenomicsmentioning

confidence: 99%

Section: Limitations Of Plastid-only Analysesmentioning

confidence: 99%

See 3 more Smart Citations

Hundreds of nuclear and plastid loci yield novel insights into orchid relationships

Pérez‐Escobar

Dodsworth

Bogarín

et al. 2021

American J of Botany

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Phylogenomics and plastome evolution of a Brazilian mycoheterotrophic orchid, Pogoniopsis schenckii

Klimpert

Mayer

Sarzi

et al. 2022

American J of Botany

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Premise Pogoniopsis likely represents an independent photosynthesis loss in orchids. We use phylogenomic data to better identify the phylogenetic placement of this fully mycoheterotrophic taxon, and investigate its molecular evolution. Methods We performed likelihood analysis of plastid and mitochondrial phylogenomic data to localize the position of Pogoniopsis schenckii in orchid phylogeny, and investigated the evolution of its plastid genome. Results All analyses place Pogoniopsis in subfamily Epidendroideae, with strongest support from mitochondrial data, which also place it near tribe Sobralieae with moderately strong support. Extreme rate elevation in Pogoniopsis plastid genes broadly depresses branch support; in contrast, mitochondrial genes are only mildly rate elevated and display very modest and localized reductions in bootstrap support. Despite considerable genome reduction, including loss of photosynthesis genes and multiple translation apparatus genes, gene order in Pogoniopsis plastomes is identical to related autotrophs, apart from moderately shifted inverted repeat (IR) boundaries. All cis‐spliced introns have been lost in retained genes. Two plastid genes (accD, rpl2) show significant strengthening of purifying selection. A retained plastid tRNA gene (trnE‐UUC) of Pogoniopsis lacks an anticodon; we predict that it no longer functions in translation but retains a secondary role in heme biosynthesis. Conclusions Slowly evolving mitochondrial genes clarify the placement of Pogoniopsis in orchid phylogeny, a strong contrast with analysis of rate‐elevated plastome data. We documented the effects of the novel loss of photosynthesis: for example, despite massive gene loss, its plastome is fully colinear with other orchids, and it displays only moderate shifts in selective pressure in retained genes.

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Systematics and conservation of British and Irish orchids: a "state of the union" assessment to accompany Atlas 2020

Bateman

2022

Kew Bull

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SummaryPrompted by concurrent completion of the latest plant atlas for Britain and Ireland, the orchid flora of these islands is reviewed in detail, focusing on 21st century progress in both systematics research and formal conservation categorisation under IUCN criteria. DNA-based phylogenies consistently circumscribe monophyletic groups that constitute obvious genera, though relationships among those genera remain less certain and resistance to phylogenetic classification persists. Comparison of species circumscription studies in critical groups such as Dactylorhiza, Gymnadenia, Platanthera, Epipactis and Orchis shows that most of the recent progress has been achieved using DNA-based techniques, which have also greatly increased understanding of associated mycorrhizae. Most morphological studies remain disappointingly traditional, squandering opportunities for morphometric studies that identify discontinuities between species, allow comparison of rates of morphological and molecular evolution, and underpin accurate quantitative descriptions designed to aid identification. Possibly only one of the 53 species recognised as native is still viewed as endemic. Conventional views on the significance of both pollinator specificity and quantitative seed output as the preferred measure of fitness are questioned, and mycorrhizae are explored as possibly under-rated ecological filters. Comparison of species distributions in successive Atlases suggests diverse patterns of change that reflect a combination of habitat modification, climate change and, in a few cases, improved identification skills. Ecologically tolerant lowland species such as Ophrys apifera and Dactylorhiza praetermissa are migrating northward rapidly, while the genus Serapias appears to be mounting a cross-Channel invasion. Most formal Red-Listing categorisations, and the underlying IUCN criteria, are supported for decisions made within the British Isles, but unfortunately, they have translated poorly into the equivalent European and Global lists. Within Britain, the Data Deficient category has been employed too frequently and illogically; ironically, it is sometimes used to penalise species for having been the subjects of serious research. Far from being "complete", the present consensus view on the taxonomy and evolution of the glacially impoverished British and Irish flora is judged both parochial and complacent. Reinvigorated UK-based research programmes that integrate quantitative morphological and molecular studies of British and Irish natives in a European context are urgently needed.

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Plastid phylogenomics resolves ambiguous relationships within the orchid family and provides a solid timeframe for biogeography and macroevolution

Cited by 40 publications

References 81 publications

Hundreds of nuclear and plastid loci yield novel insights into orchid relationships

Hundreds of nuclear and plastid loci yield novel insights into orchid relationships

Phylogenomics and plastome evolution of a Brazilian mycoheterotrophic orchid, Pogoniopsis schenckii

Systematics and conservation of British and Irish orchids: a "state of the union" assessment to accompany Atlas 2020

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