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Heterotrophic plants are evolutionary experiments in genomic, morphological, and physiological change. Yet, genomic sampling gaps exist among independently derived heterotrophic lineages, leaving unanswered questions about the process of genome modification. Here, we have sequenced complete plastid genomes for all species of the leafless orchid gen...
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... quantified the numbers of putatively functional coding genes, pseudogenes, and wholescale gene losses to summarize the structural evolutionary consequences of relaxed selection pressure on each plastid gene system and genome structure overall. Figure 3 and supplementary figure S4, Supplementary Material online, summarize the number of putatively functional genes, pseudogenes, and physical gene losses among Bletia, Basiphyllaea, and Hexalectris. All plastid genes are putatively functional in Bletia and Basiphyllaea, as evidenced by intact reading frames. ...Context 2
... as compared with a negative constraint in which they are nonmonophyletic (mean ln L monophyly ¼ À129,194.1, mean ln L nonmonophyly ¼ À124,795.9, and Bayes Maximum likelihood reconstruction of photosynthetic loss under a model restricting photosynthetic gains (i.e., a loss-only model) reveals four to five losses of photosynthesis in Hexalectris ( fig. 4). Ancestral states for photosynthetic losses in H. warnockii and H. brevicaulis are unequivocal at >0.99 for a photosynthetic ancestor for both the LCB and CDS matrices. The ancestral state for the H. spicata-nitida complex is nonphotosynthetic, though with a probability of 0.63 for the LCB tree and 0.61 for the CDS matrix. For the LCB ...Similar publications
Danxiaorchis singchiana (Orchidaceae) is a leafless mycoheterotrophic orchid in the subfamily Epidendroideae. We sequenced the complete plastome of D. singchiana. The plastome has a reduced size of 87,931 bp, which includes a pair of inverted repeat (IR) regions of 13,762 bp each that are separated by a large single copy (LSC) region of 42,575 bp a...
Citations
... Heterotrophic plants-plants that rely on other organisms for energy and nutrients-are remarkable survivors, exhibiting often curious morphological, physical, or genomic modifications, reflecting evolutionary relaxed selective pressure on photosynthetic function (Graham et al., 2017;Barrett et al., 2019). Advances in nextgeneration sequencing and bioinformatic pipelines have vastly accelerated the characterisation of plastid genomes (plastomes), including heterotrophic plants, providing new insights into plastome evolution. ...
... Advances in nextgeneration sequencing and bioinformatic pipelines have vastly accelerated the characterisation of plastid genomes (plastomes), including heterotrophic plants, providing new insights into plastome evolution. Plastomes of heterotrophic plants often exhibit greatly altered structure and gene content due to photosynthesis-related genes that are no longer required (Delannoy et al., 2011;Barrett et al., 2014;Lam et al., 2015;Braukmann et al., 2017;Graham et al., 2017;Barrett et al., 2018;Wicke and Naumann, 2018;Barrett et al., 2019;Qu et al., 2019;Klimpert et al., 2022;Peng et al., 2022;Wen et al., 2022). Hence, heterotrophic plants offer excellent opportunities to gain insight into plastome evolution under relaxed selection. ...
... Thus far, most phylogenetic comparative studies included plastomes of taxa scattered across families, tribes, or genera (e.g., Kim et al., 2015;Feng et al., 2016;Niu et al., 2017;Lallemand et al., 2019;Kim et al., 2020;Li et al., 2020;Tu et al., 2021;Kim et al., 2023). Nevertheless, phylogenetic, comparative approaches at the infrageneric level are still scarce (e.g., Barrett et al., 2018Barrett et al., , 2019. ...
The orchid genus Dipodium R.Br. (Epidendroideae) comprises leafy autotrophic and leafless mycoheterotrophic species, with the latter confined to sect. Dipodium. This study examined plastome degeneration in Dipodium in a phylogenomic and temporal context. Whole plastomes were reconstructed and annotated for 24 Dipodium samples representing 14 species and two putatively new species, encompassing over 80% of species diversity in sect. Dipodium. Phylogenomic analysis based on 68 plastid loci including a broad outgroup sampling across Orchidaceae found that sect. Leopardanthus is the sister lineage to sect. Dipodium. Dipodium ensifolium, the only leafy autotrophic species in sect. Dipodium, was found to be a sister to all leafless, mycoheterotrophic species, supporting a single evolutionary origin of mycoheterotrophy in the genus. Divergence-time estimations found that Dipodium arose ca. 33.3 Ma near the lower boundary of the Oligocene and that crown diversification commenced in the late Miocene, ca. 11.3 Ma. Mycoheterotrophy in the genus was estimated to have evolved in the late Miocene, ca. 7.3 Ma, in sect. Dipodium. The comparative assessment of plastome structure and gene degradation in Dipodium revealed that plastid ndh genes were pseudogenised or physically lost in all Dipodium species, including in leafy autotrophic species of both Dipodium sections. Levels of plastid ndh gene degradation were found to vary among species as well as within species, providing evidence of relaxed selection for retention of the NADH dehydrogenase complex within the genus. Dipodium exhibits an early stage of plastid genome degradation, as all species were found to have retained a full set of functional photosynthesis-related genes and housekeeping genes. This study provides important insights into plastid genome degradation along the transition from autotrophy to mycoheterotrophy in a phylogenomic and temporal context.
... To achieve this, we performed next-generation sequencing using genome skimming (Dodsworth 2015), and obtained whole-plastome sequence and nuclear ribosomal DNA (rDNA) repeat sequence data for all six Yoania taxa currently recognized. Such a molecular approach has proven helpful in the phylogenomic reconstruction of Orchidaceae (Kim et al. 2020, Li et al. 2020, Serna-Sánchez et al. 2021, and has been successfully applied to Corallorhiza, a mycoheterotrophic lineage within Calypsoinae Davis 2012, Barrett et al. 2018), as well as for other unrelated mycoheterotrophic orchids (Kim et al. 2015, Barrett et al. 2019. We assembled and characterized the whole plastome and partial nuclear rDNA gene unit of Yoania to uncover its evolutionary history and the evolution of its plastome. ...
Subtribe Calypsoinae (Epidendroideae, Orchidaceae) comprises several fully mycoheterotrophic species. Phylogenetic analysis indicates that full mycoheterotrophy has evolved independently at least four times within this group, including the Yoania clade. The taxonomic classification of Yoania species has been challenging. Therefore, to understand the plastomic degeneration during the evolution of mycoheterotrophy and to uncover the phylogenetic relationship within Yoania, we conducted a phylogenetic analysis using eight specimens representing all six recognized Yoania taxa from the complete plastome and partial ribosomal DNA (rDNA) operon sequence (ETS–18S–ITS1–5.8S–ITS2–26S). Among the Calypsoinae taxa examined, Yoania possessed the shortest plastome, ranging from 43 998 to 44 940 bp. Comparative analysis of the plastomes revealed a relatively conserved gene structure, content, and order, with species-level sequence variation (in the form of indels) primarily observed in the intergenic spacer regions. Plastomic gene-block inversions were observed between Yoania and Danxiaorchis singchiana, but not between Yoania and other related genera. Phylogenetic analyses based on the plastome and rDNA data strongly supported the monophyletic placement of Yoania within Calypsoinae, and indicated substantial molecular divergence between Yoania and other Calypsoinae taxa. Yoania can thus be considered genetically isolated from the other Calypsoinae taxa.
... Parasitic plants consist of 292 genera and 4750 species across 12 lineages of flowering plants and have evolved independently 12 or 13 times (Westwood et al. 2010;Nickrent 2020). The transition from autotrophy to heterotrophy usually involves structural and functional variations in the plastome (Krause 2008;Wicke et al. 2016), making the parasitic plant as an important system to investigate plastome evolution under relaxed selective pressures and adaptation of plants to lifestyle changes (Young and dePamphilis 2005;McNeal et al. 2007; Barrett et al. 2019). ...
... It is believed that the lifestyle change from autotrophy to parasitism is the main factor and triggers genomic structure instability via functional relaxation (Wicke et al. 2013;Wicke and Naumann 2018). Several genes in the inversed fragments (the region 2, 3, 7, 9 10, and 12) showed significant relaxed selection with lower GC content ( Fig. 2; Supplementary Fig. S10), indicating that genes from organellar and nuclear genomes involved in repairing DNA breaks, mis-incorporated bases, and illegitimate recombinants during coevolution may also undergo relaxed selection (Barrett et al. 2019;Zhang et al. 2018). Therefore, the relaxed selection is likely the driving force behind these fragment variations through introducing unstable factors, such as large repeats, low GC content, and DNA breaks in Cuscuta. ...
... Grammica and proposed a refined model specific to Cuscuta, but the subtle gene reduction of the evolutionary model in C. subgen. Grammica remains unclear due to insufficient sampling coverage at species level to better understand the lineage-specific evolution of plastome reduction, thus, calling for broad and comprehensive taxon samplings of the whole genus of Cuscuta (Barrett et al. 2019). Moreover, rpl32 and rps16 genes were frequently lost in other heterotrophic lineages (Barrett et al. 2014;Cusimano and Wicke 2016;Chen et al. 2020) and they are essential components of the plastid translation apparatus, suggesting that they were likely transferred to nuclear or replaced by nuclear gene copies (Fleischmann et al. 2011;Park et al. 2015;Shrestha et al. 2020). ...
Parasitic lifestyle can often relax the constraint on the plastome, leading to gene pseudogenization and loss, and resulting in diverse genomic structures and rampant genome degradation. Although several plastomes of parasitic Cuscuta have been reported, the evolution of parasitism in the family Convolvulaceae which is linked to structural variations and reduction of plastome has not been well investigated. In this study, we assembled and collected 40 plastid genomes belonging to 23 species representing four subgenera of Cuscuta and ten species of autotrophic Convolvulaceae. Our findings revealed nine types of structural variations and six types of inverted repeat (IR) boundary variations in the plastome of Convolvulaceae spp. These structural variations were associated with the shift of parasitic lifestyle, and IR boundary shift, as well as the abundance of long repeats. Overall, the degradation of Cuscuta plastome proceeded gradually, with one clade exhibiting an accelerated degradation rate. We observed five stages of gene loss in Cuscuta, including NAD(P)H complex → PEP complex → Photosynthesis-related → Ribosomal protein subunits → ATP synthase complex. Based on our results, we speculated that the shift of parasitic lifestyle in early divergent time promoted relaxed selection on plastomes, leading to the accumulation of microvariations, which ultimately resulted in the plastome reduction. This study provides new evidence towards a better understanding of plastomic evolution, variation, and reduction in the genus Cuscuta.
... It is made available under a preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in The copyright holder for this this version posted February 6, 2024. ; https://doi.org/10.1101/2024.02.05.578113 doi: bioRxiv preprint not be essential anymore (e.g., Barrett et al., 2019). One reason for this may be that they are 773 less exposed to photooxidative stress (e.g., Feng et al., 2016;Barrett et al., 2019). ...
... ; https://doi.org/10.1101/2024.02.05.578113 doi: bioRxiv preprint not be essential anymore (e.g., Barrett et al., 2019). One reason for this may be that they are 773 less exposed to photooxidative stress (e.g., Feng et al., 2016;Barrett et al., 2019). However, 774 the NDH complex is composed of 11 chloroplast encoded subunits and additional subunits 775 encoded by the nucleus (e.g., Peltier et al., 2016). ...
The orchid genus Dipodium R.Br. (Epidendroideae) comprises leafy autotrophic and leafless mycoheterotrophic species, the latter confined to sect. Dipodium . This study examined plastome degeneration in Dipodium in a phylogenomic and temporal context. Whole plastomes were reconstructed and annotated for 24 Dipodium samples representing 14 species and two putatively new species, encompassing over 80% of species diversity in sect. Dipodium . Phylogenomic analysis based on 68 plastid loci including a broad outgroup sampling across Orchidaceae found sect. Leopardanthus as sister lineage to sect. Dipodium . Dipodium ensifolium , the only leafy autotrophic species in sect. Dipodium was found sister to all leafless, mycoheterotrophic species, supporting a single evolutionary origin of mycoheterotrophy in the genus. Divergence time estimations found that Dipodium arose ca. 33.3 Ma near the lower boundary of the Oligocene and crown diversification commenced in the late Miocene, ca. 11.3 Ma. Mycoheterotrophy in the genus was estimated to have evolved in the late Miocene, ca. 7.3 Ma, in sect. Dipodium . The comparative assessment of plastome structure and gene degradation in Dipodium revealed that plastid ndh genes were pseudogenised or physically lost in all Dipodium species, including in leafy autotrophic species of both Dipodium sections. Levels of plastid ndh gene degradation were found to vary among species as well as within species, providing evidence of relaxed selection for retention of the NADH dehydrogenase complex within the genus. Dipodium exhibits an early stage of plastid genome degradation as all species were found to have retained a full set of functional photosynthesis-related genes and housekeeping genes. This study provides important insights into plastid genome degradation along the transition from autotrophy to mycoheterotrophy in a phylogenomic and temporal context.
... Elevation of molecular evolutionary rates in parts of the genome may relate to relaxed selection [26]. It may also be that fully and some mixotrophic heterotrophic plants "ramp up" their metabolic rates to compensate for carbon deficits, resulting from the loss of photosynthesis, which may cause an increase in reactive free radicals and associated oxidative stress, known to be linked to increased DNA damage [69,70]. As preyderived organic carbon use and increased respiration rates were reported in some carnivorous plants [24,25,68], we hypothesize that some but not all carnivorous plants undergo a similar process as heterotrophic lineages, as discussed previously for Lentibulariaceae [26]. ...
Background
Independent origins of carnivory in multiple angiosperm families are fabulous examples of convergent evolution using a diverse array of life forms and habitats. Previous studies have indicated that carnivorous plants have distinct evolutionary trajectories of plastid genome (plastome) compared to their non-carnivorous relatives, yet the extent and general characteristics remain elusive.
Results
We compared plastomes from 9 out of 13 carnivorous families and their non-carnivorous relatives to assess carnivory-associated evolutionary patterns. We identified inversions in all sampled Droseraceae species and four species of Utricularia, Pinguicula, Darlingtonia and Triphyophyllum. A few carnivores showed distinct shifts in inverted repeat boundaries and the overall repeat contents. Many ndh genes, along with some other genes, were independently lost in several carnivorous lineages. We detected significant substitution rate variations in most sampled carnivorous lineages. A significant overall substitution rate acceleration characterizes the two largest carnivorous lineages of Droseraceae and Lentibulariaceae. We also observe moderate substitution rates acceleration in many genes of Cephalotus follicularis, Roridula gorgonias, and Drosophyllum lusitanicum. However, only a few genes exhibit significant relaxed selection.
Conclusion
Our results indicate that the carnivory of plants have different effects on plastome evolution across carnivorous lineages. The complex mechanism under carnivorous habitats may have resulted in distinctive plastome evolution with conserved plastome in the Brocchinia hechtioides to strongly reconfigured plastomes structures in Droseraceae. Organic carbon obtained from prey and the efficiency of utilizing prey-derived nutrients might constitute possible explanation.
... Plastome data have been used to resolve the phylogenetic relationships of tribes, subtribes and genera in Orchidaceae [3,24,[38][39][40][41][42][43], which further indicates that the plastomes are useful for phylogenetic relationship reconstruction. Moreover, plastomes have also been used to investigate the evolution of mycoheterotrophic orchid genomes suffering extreme gene loss and structural variation [43][44][45][46][47]. However, plastome analysis has yet to be Conclusion This study was the first to analyse the plastome characteristics of the genus Chiloschista in Orchidaceae, and the results showed that Chiloschista plastomes have conserved plastome structures. ...
Background
Chiloschista (Orchidaceae, Aeridinae) is an epiphytic leafless orchid that is mainly distributed in tropical or subtropical forest canopies. This rare and threatened orchid lacks molecular resources for phylogenetic and barcoding analysis. Therefore, we sequenced and assembled seven complete plastomes of Chiloschista to analyse the plastome characteristics and phylogenetic relationships and conduct a barcoding investigation.
Results
We are the first to publish seven Chiloschista plastomes, which possessed the typical quadripartite structure and ranged from 143,233 bp to 145,463 bp in size. The plastomes all contained 120 genes, consisting of 74 protein-coding genes, 38 tRNA genes and eight rRNA genes. The ndh genes were pseudogenes or lost in the genus, and the genes petG and psbF were under positive selection. The seven Chiloschista plastomes displayed stable plastome structures with no large inversions or rearrangements. A total of 14 small inversions (SIs) were identified in the seven Chiloschista plastomes but were all similar within the genus. Six noncoding mutational hotspots (trnNGUU–rpl32 > rpoB–trnCGCA > psbK–psbI > psaC–rps15 > trnEUUC–trnTGGU > accD–psaI) and five coding sequences (ycf1 > rps15 > matK > psbK > ccsA) were selected as potential barcodes based on nucleotide diversity and species discrimination analysis, which suggested that the potential barcode ycf1 was most suitable for species discrimination. A total of 47–56 SSRs and 11–14 long repeats (> 20 bp) were identified in Chiloschista plastomes, and they were mostly located in the large single copy intergenic region. Phylogenetic analysis indicated that Chiloschista was monophyletic. It was clustered with Phalaenopsis and formed the basic clade of the subtribe Aeridinae with a moderate support value. The results also showed that seven Chiloschista species were divided into three major clades with full support.
Conclusion
This study was the first to analyse the plastome characteristics of the genus Chiloschista in Orchidaceae, and the results showed that Chiloschista plastomes have conserved plastome structures. Based on the plastome hotspots of nucleotide diversity, several genes and noncoding regions are suitable for phylogenetic and population studies. Chiloschista may provide an ideal system to investigate the dynamics of plastome evolution and DNA barcoding investigation for orchid studies.
... In Hechtioideae, the most recently diverged species of Hechtia are the ones presenting most cases of ndh family gene loss and/or potential pseudogenization, particularly in clade F (Fig. 3). However, potential pseudogenization or loss of the ndh genes appears to occur independently across the Hechtioideae phylogenetic tree, as has been reported for several land plant lineages (Martín & Sabater, 2010;Barrett et al., 2019;Strand et al., 2019;Yang et al., 2022). Future studies aimed at obtaining transcriptomic data could help to assess whether the genes of the ndh family identified as potential pseudogenes in Hechtioideae species are indeed not expressed. ...
... Plastid ndh genes, together with a set of nuclear loci, encode a subunit of the plastome NDH (NADH dehydrogenase-like) complex involved in cyclic electron flow (CEF) in photosynthesis (Martín & Sabater, 2010;Strand et al., 2019). In general, significant ndh gene losses have been commonly reported for parasitic plants (Ruhlman et al., 2015), mycoheterotrophs (e.g., Orchidaceae; Barrett et al., 2019), and carnivorous plants (Yao et al., 2019), associated to reduction or absence of photosynthetic activity. However, multiple losses have been reported in fully photosynthetic plant lineages such as gymnosperms (e.g., Pinaceae; Strand et al., 2019), aquatic plants (e.g., Littorella uniflora (L.) Asch.; Mower et al., 2021), and xerophytic species (e.g., Yao et al., 2019). ...
Full plastomes have recently proven to be a valuable data source for resolving recalcitrant phylogenetic relationships in the flowering plant family Bromeliaceae. The study of complete plastomes has additionally led to the discovery of new structural rearrangements and advanced our understanding of bromeliad plastome diversity and evolution. Here, we focus on the study of full plastomes of the bromeliad subfamily Hechtioideae to assess phylogenetic relationships, marker informativeness, and plastome structure and evolution. Using whole‐genome sequencing data, we de novo assembled and annotated new plastid genomes of 19 Hechtioideae species plus one representative each from the Pitcairnioideae and Puyoideae subfamilies and compared them with four additional available plastomes from other bromeliad subfamilies. Our phylogenetic analysis using complete plastome sequences not only recovered the three currently recognized genera of Hechtioideae as monophyletic, strongly supporting Mesoamerantha as sister of Bakerantha and Hechtia , but also improved statistical support at different phylogenetic depths within the subfamily. We identified a set of highly informative loci, some of them explored for the first time in Hechtioideae. Structural rearrangements, including expansions and contractions of the inverted repeats, large inversions, and gene loss and potential pseudogenization were detected mainly within the genus Hechtia . Evolutionary trait rate shifts were associated with the size and guanine–cytosine content of the small single copy and inverted repeats.
... This includes holoparasites (Epifagus Nutt., dePamphilis and Palmer 1990; Cytinus L., Roquet et al. 2016;Hydnora Thunb., Naumann et al. 2016; Cuscuta L., Braukmann et al. 2013;Cistanche Hoffmans. & Link, Li et al. 2013; Pilostyles Guill., Bellot and Renner 2016;Rhopalocnemis Jungh., Schelkunov et al. 2019; Parasitaxus de Laub., Qu et al. 2019), hemiparasites (Viscum L., Petersen et al. 2015), and mycoheterotrophs (Corrallorhiza Gagnebin, Barrett et al. 2019; Rhizanthella R.S.Rogers, Delannoy et al. 2011;Neottia Jacq., Logacheva et al. 2011;Epipogium R.Br., Schelkunov et al. 2015; Corsia dispar D.L.Jones & B.Gray, Bodin et al. 2016; Sciaphila Blume, Lam et al. 2015;Orobanchaceae Vent., Frailey et al. 2018; Burmannia L., Li et al. 2019;Epirixanthes Blume, Petersen et al. 2019; Monotropa L., Gruzdev et al. 2016). The ultimate state of degradation of plastome function in heterotrophic plants is exemplified by an apparent complete loss of the plastome in several holoparasitic taxa (Rafflesia R.Br., Molina et al. 2014; Schoepfia Schreb., Su and Hu 2016). ...
... For example, even the very reduced plastomes of Epipogeum (~11 kb) are thought to be functional in some way as they contain a high proportion of coding DNA, an absence of nonsynonymous mutations in protein-coding genes, and apparently functional tRNAs (Schelkunov et al. 2015). Studies with dense sampling of mycoheterotrophs and related autotrophs have found significant plastome sequence variation at even very fine taxonomic scales (including within species variation) and rapid degradation of plastid genomes associated with a transition to heterotrophy (Barrett et al. , 2019Schneider et al. 2018). Conversely, examples where a photosynthetic species and an apparent (facultative) heterotroph have similar plastomes are rare in the literature (but see Kim et al. 2020). ...
... Perhaps the most well-studied transition to full mycoheterotrophy and loss of photosynthetic capability in orchids is in Corallorhiza. Extensive studies in the genus have found that fully mycoheterotrophic species have degradation in a suite of key photosynthetic genes (including pet, psa, rpo complexes and ccsA, cemA and rbcL, as well as ndh complex), and phylogenetic reconstruction of gene loss in the genus identified several independent losses of photosynthetic genes (Barrett et al. 2019). However, mycoheterotrophs did not necessarily have reduced plastome sizes , leaflessness was not correlated with plastome degradation, and some mycoheterotrophs have detectable levels of chlorophyll (10-fold less than autotrophs; Barrett et al. 2014). ...
Context Giving up photosynthetic function is a bold evolutionary step for a plant, yet the evolutionary transition from autotrophy to mycoheterotrophy has occurred dozens of times. Comparing plastome sequences of mycoheterotrophs and autotrophs has identified recurring patterns of gene loss throughout a range of land plants, though more comparisons are required to see how broadly these patterns apply across the diversity of terrestrial plants. Mycoheterotrophy is especially common in Orchidaceae, with more than 40 transitions from autotrophy to mycoheterotrophy in the family. Aims We sought to test generalised patterns of plastome degradation seen in other mycoheterotrophs by comparing two species in the genus Dipodium (Orchidaceae); one species is photosynthetic and the other appears to be a facultative mycoheterotroph species. Methods We sequenced and assembled the plastomes of two Dipodium species and compared the two genomes to identify gene degradation or loss. Results The two plastomes were nearly identical, with no degradation of photosynthesis genes in the putative mycoheterotroph, and both species have undergone loss or pseudogenisation of all plastid ndh (nicotinamide adenine dinucleotide + hydrogen specific dehydrogenase) genes. Conclusions These results contrast with most other comparisons between photosynthetic and likely mycoheterotrophic relatives, where rapid degradation in mycoheterotroph plastome genes is common, and may suggest the leafless Dipodium species are capable of photosynthesis and may be in the early stages of transitioning to a fully heterotrophic lifestyle. Implications Further investigation of trophic transitions in Dipodium, including sequencing more plastomes and measuring photosynthetic capability of the putative heterotrophs, will yield insights into the evolution of plant lineages that lose the ability to photosynthesise.
... Mycoheterotrophs commonly undergo loss or pseudogenization of photosynthesis-related genes due to relaxed selective constraints, further leading to dramatic plastid genome (plastome) reductions and structural rearrangements [1,4,[7][8][9][10][11][12][13][14]. Moreover, there are repeated plastome-based phylogenetic changes during trophic transitions from autotrophy, via partial mycoheterotrophy (mixotrophy), to holomycotrophy [15,16]. ...
... The loss of plastid-encoded genes coinciding with or following the evolution of parasitic plants has been extensively explored [1,12,[16][17][18][19]. Recently, an increasing number of studies revealed more and more evolution details by incorporating dense sampling of plastomes across higher taxonomic levels (e.g. ...
... Recently, an increasing number of studies revealed more and more evolution details by incorporating dense sampling of plastomes across higher taxonomic levels (e.g. genera, families or tribes) containing parasitic plants, from the phylogenetic-comparative perspective [8,15,16,[19][20][21][22][23][24][25]. Plastomes of parasitic plants are characterized by elevated substitution rates, gene pseudogenization and loss. ...
Background
Mycoheterotrophs, acquiring organic carbon and other nutrients from mycorrhizal fungi, have evolved repeatedly with substantial plastid genome (plastome) variations. To date, the fine-scale evolution of mycoheterotrophic plastomes at the intraspecific level is not well-characterized. A few studies have revealed unexpected plastome divergence among species complex members, possibly driven by various biotic/abiotic factors. To illustrate evolutionary mechanisms underlying such divergence, we analyzed plastome features and molecular evolution of 15 plastomes of Neottia listeroides complex from different forest habitats.
Results
These 15 samples of Neottia listeroides complex split into three clades according to their habitats approximately 6 million years ago: Pine Clade, including ten samples from pine-broadleaf mixed forests, Fir Clade, including four samples from alpine fir forests and Fir-willow Clade with one sample. Compared with those of Pine Clade members, plastomes of Fir Clade members show smaller size and higher substitution rates. Plastome size, substitution rates, loss and retention of plastid-encoded genes are clade-specific. We propose to recognized six species in N. listeroides complex and slightly modify the path of plastome degradation.
Conclusions
Our results provide insight into the evolutionary dynamics and discrepancy of closely related mycoheterotrophic orchid lineages at a high phylogenetic resolution.
... Alternatively, it is also possible that Gastrodieae and the subtribe Epipogiinae independently gained the fully mycoheterotrophic habit. Additionally, previous studies revealed that the fully mycoheterotrophic species have evolved in parallel among closely related species within the same genus (Barrett et al., 2019;Li et al., 2020), indicating that the gain of the fully mycoheterotrophic habit could happen in different taxonomic ranks and might be frequent in the evolution history of Orchidaceae. ...
... In addition, epiphytism and mycoheterotrophic habit likely originated multiple times within some orchid genera. For example, mycoheterotrophs have originated several times in Oreorchis and Hexalectris (Barrett et al., 2019;Li et al., 2020b). Hence, the transition times of growth forms in Orchidaceae detected here are probably underestimated because character states were coded at the genus, not species, level in this study. ...
Orchidaceae (with >28,000 orchid species) are one of the two largest plant families, with economically and ecologically important species, and occupy global and diverse niches with primary distribution in rainforests. Among orchids, 70% grow on other plants as epiphytes; epiphytes contribute up to ~50% of the plant diversity in rainforests and provide food and shelter for diverse animals and microbes, thereby contributing to the health of these ecosystems. Orchids account for over two‐thirds of vascular epiphytes and provide an excellent model for studying evolution of epiphytism. Extensive phylogenetic studies of Orchidaceae and subgroups have ;been crucial for understanding relationships among many orchid lineages, although some uncertainties remain. For example, in the largest subfamily Epidendroideae with nearly all epiphytic orchids, relationships among some tribes and many subtribes are still controversial, hampering evolutionary analyses of epiphytism. Here we obtained 1,450 low‐copy nuclear genes from 610 orchid species, including 431 with newly generated transcriptomes, and used them for the reconstruction of robust Orchidaceae phylogenetic trees with highly supported placements of tribes and subtribes. We also provide generally well‐supported phylogenetic placements of 131 genera and 437 species that were not sampled by previous plastid and nuclear phylogenomic studies. Molecular clock analyses estimated the Orchidaceae origin at ~132 million years ago (Ma) and divergences of most subtribes from 52 to 29 Ma. Character reconstruction supports at least 14 parallel origins of epiphytism; one such origin was placed at the most recent common ancestor of ~95% of epiphytic orchids and linked to modern rainforests. Ten occurrences of rapid increase in the diversification rate were detected within Epidendroideae near and after the K‐Pg boundary, contributing to ~80% of the Orchidaceae diversity. This study provides a robust and the largest family‐wide Orchidaceae nuclear phylogenetic tree thus far and new insights into the evolution of epiphytism in vascular plants.
