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, María Fernanda; Álvarez-Yela, Astrid Catalina; Arcila, Juliana; Hall, Climbiê Ferreira; Barros, Fábio de; Pinheiro, Fábio; Dodsworth, Steven; Chase, Mark W.; Antonelli, Alexandre; Arias, Tatiana

doi:10.1101/774018

Cited by 9 publications

(29 citation statements)

References 87 publications

(162 reference statements)

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“…Another possible explanation, apart from the low coverages, is that the biparental nature of the nuclear genome may be problematic for the inference of phylogenetic relationships (14). Previous studies already suggest that phylogenies based on nrDNA and few selected plastid sequences only weakly support relationships (30). The 18s rRNA gene sequences of representatives of the sections Corollinae and Beta are completely identical containing no phylogenetic signal to separate them.…”

Section: Discussionmentioning

confidence: 99%

“…Previous studies already suggest that phylogenies based on nrDNA and few selected plastid sequences only weakly support relationships (30). The 18s rRNA gene sequences of representatives of the sections Corollinae and Beta are completely identical containing no phylogenetic signal to separate them.…”

Section: Our Proposed Beet Whole-plastome Phylogeny Is Superior To Single Gene Phylogeniesmentioning

confidence: 94%

“…The intergenic regions are significantly less conserved containing more InDels and are therefore more suitable for phylogenies on a lower taxonomic level (22). Among the beet plastomes, ycf1 is the most informative genic region (Figure 1A), which was also detected in other plant groups, such as the Tropaeolaceae, the orchids, and the Malvales (29)(30)(31).…”

Section: Our Proposed Beet Whole-plastome Phylogeny Is Superior To Single Gene Phylogeniesmentioning

confidence: 99%

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Complete pan-plastome sequences enable high resolution phylogenetic classification of sugar beet and closely related crop wild relatives

Sielemann

Pucker

Schmidt

et al. 2021

Preprint

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As the major source of sugar in moderate climates, sugar-producing beets (Beta vulgaris subsp. vulgaris) have a high economic value. However, the low genetic diversity within cultivated beets requires introduction of new traits, for example to increase their tolerance and resistance attributes - traits that often reside in the crop wild relatives. For this, genetic information of wild beet relatives and their phylogenetic placements to each other are crucial. To answer this need, we sequenced and assembled the complete plastome sequences from a broad species spectrum across the beet genera Beta and Patellifolia, both embedded in the Betoideae (order Caryophyllales). This pan-plastome dataset was then used to determine the wild beet phylogeny in high-resolution. We sequenced the plastomes of 18 closely related accessions representing 11 species of the Betoideae subfamily and provide high-quality plastome assemblies which represent an important resource for further studies of beet wild relatives and the diverse plant order Caryophyllales. Their assembly sizes range from 149,723 bp (Beta vulgaris subsp. vulgaris) to 152,816 bp (Beta nana), with most variability in the intergenic sequences. Combining plastome-derived phylogenies with read-based treatments based on mitochondrial information, we were able to suggest a unified and highly confident phylogenetic placement of the investigated Betoideae species. Our results show that the genus Beta can be divided into the two clearly separated sections Beta and Corollinae. Our analysis confirms the affiliation of B. nana with the other Corollinae species, and we argue against a separate placement in the Nanae section. Within the Patellifolia genus, the two diploid species Patellifolia procumbens and Patellifolia webbiana are, regarding the plastome sequences, genetically more similar to each other than to the tetraploid Patellifolia patellaris. Nevertheless, all three Patellifolia species are clearly separated. In conclusion, our wild beet plastome assemblies represent a new resource to understand the molecular base of the beet germplasm. Despite large differences on the phenotypic level, our pan-plastome dataset is highly conserved. For the first time in beets, our whole plastome sequences overcome the low sequence variation in individual genes and provide the molecular backbone for highly resolved beet phylogenomics. Hence, our plastome sequencing strategy can also guide genomic approaches to unravel other closely related taxa.

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Section: Discussionmentioning

confidence: 99%

Section: Our Proposed Beet Whole-plastome Phylogeny Is Superior To Single Gene Phylogeniesmentioning

confidence: 94%

Section: Our Proposed Beet Whole-plastome Phylogeny Is Superior To Single Gene Phylogeniesmentioning

confidence: 99%

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Complete pan-plastome sequences enable high resolution phylogenetic classification of sugar beet and closely related crop wild relatives

Sielemann

Pucker

Schmidt

et al. 2021

Preprint

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“…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; Li, Li, et al, 2019; Serna-sánchez et al, 2020) have relied almost exclusively on plastid datasets. This is because nuclear orchid trees have mostly been inferred from the low-copy Xdh (Górniak et al, 2010) and ribosomal ITS (nrITS) region (Freudenstein and Chase, 2015).…”

Section: Discussionmentioning

confidence: 99%

“…To assess the performance of the Angiosperms353 nuclear loci for resolving orchid relationships and investigate nuclear/plastid gene tree discordance at different taxonomic levels, we utilized the 78-plastid-gene dataset of (Serna-sánchez et al, 2020): 264 species representing 117 genera, 28 subtribes and 18 tribes. The taxon sampling of nuclear and plastid datasets overlaps in 34 genera, 14 tribes and 22 subtribes.…”

Section: Methodsmentioning

confidence: 99%

Hundreds of nuclear and plastid loci yield insights into orchid relationships

Pérez‐Escobar

Dodsworth

Bogarín³

et al. 2020

Preprint

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Premise of the studyEvolutionary relationships in the species-rich Orchidaceae have historically relied on organellar DNA sequences and limited taxon sampling. Previous studies provided a robust plastid-maternal phylogenetic framework, from which multiple hypotheses on the drivers of orchid diversification have been derived. However, the extent to which the maternal evolutionary history of orchids is congruent with that of the nuclear genome has remained uninvestigated.MethodsWe inferred phylogenetic relationships from 294 low-copy nuclear genes sequenced/obtained using the Angiosperms353 universal probe set from 75 species representing 69 genera, 16 tribes and 24 subtribes. To test for topological incongruence between nuclear and plastid genomes, we constructed a tree from 78 plastid genes, representing 117 genera, 18 tribes and 28 subtribes and compared them using a co-phylogenetic approach. The phylogenetic informativeness and support of the Angiosperms353 loci were compared with those of the 78 plastid genes.Key ResultsPhylogenetic inferences of nuclear datasets produced highly congruent and robustly supported orchid relationships. Comparisons of nuclear gene trees and plastid gene trees using the latest co-phylogenetic tools revealed strongly supported phylogenetic incongruence in both shallow and deep time. Phylogenetic informativeness analyses showed that the Angiosperms353 genes were in general more informative than most plastid genes.ConclusionsOur study provides the first robust nuclear phylogenomic framework for Orchidaceae plus 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 documented: nuclear and plastid phylogenetic trees are not fully congruent and therefore should not be considered interchangeable.

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

Cited by 9 publications

References 87 publications

Complete pan-plastome sequences enable high resolution phylogenetic classification of sugar beet and closely related crop wild relatives

Complete pan-plastome sequences enable high resolution phylogenetic classification of sugar beet and closely related crop wild relatives

Hundreds of nuclear and plastid loci yield insights into orchid relationships

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

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