scholarly journals Plastome Reduction in the Only Parasitic Gymnosperm Parasitaxus Is Due to Losses of Photosynthesis but Not Housekeeping Genes and Apparently Involves the Secondary Gain of a Large Inverted Repeat

2019 ◽  
Vol 11 (10) ◽  
pp. 2789-2796 ◽  
Author(s):  
Xiao-Jian Qu ◽  
Shou-Jin Fan ◽  
Susann Wicke ◽  
Ting-Shuang Yi
Keyword(s):  
Inverted Repeat ◽  
Chlorophyll Biosynthesis ◽  
Housekeeping Genes ◽  
Parasitic Plants ◽  
Structural Features ◽  
Regulation System ◽  
Biosynthesis Pathway ◽  
Plastid Genomes ◽  
Plastome Evolution ◽  
Selection For

Abstract Plastid genomes (plastomes) of parasitic plants undergo dramatic reductions as the need for photosynthesis relaxes. Here, we report the plastome of the only known heterotrophic gymnosperm Parasitaxus usta (Podocarpaceae). With 68 unique genes, of which 33 encode proteins, 31 tRNAs, and four rRNAs in a plastome of 85.3-kb length, Parasitaxus has both the smallest and the functionally least capable plastid genome of gymnosperms. Although the heterotroph retains chlorophyll, all genes for photosynthesis are physically or functionally lost, making photosynthetic energy gain impossible. The pseudogenization of the three plastome-encoded light-independent chlorophyll biosynthesis genes chlB, chlL, and chlN implies that Parasitaxus relies on either only the light-dependent chlorophyll biosynthesis pathway or another regulation system. Nesting within a group of gymnosperms known for the absence of the large inverted repeat regions (IRs), another unusual feature of the Parasitaxus plastome is the existence of a 9,256-bp long IR. Its short length and a gene composition that completely differs from those of IR-containing gymnosperms together suggest a regain of this critical, plastome structure-stabilizing feature. In sum, our findings highlight the particular path of lifestyle-associated reductive plastome evolution, where structural features might provide additional cues of a continued selection for plastome maintenance.

scholarly journals Mycoheterotrophic Epirixanthes (Polygalaceae) has a typical angiosperm mitogenome but unorthodox plastid genomes

2019 ◽  
Vol 124 (5) ◽  
pp. 791-807 ◽  
Author(s):  
G Petersen ◽  
H Darby ◽  
V K Y Lam ◽  
H Æ Pedersen ◽  
V S F T Merckx ◽  
...  
Keyword(s):  
Mitochondrial Genome ◽  
Housekeeping Genes ◽  
Structural Rearrangements ◽  
Substitution Rates ◽  
Organellar Genomes ◽  
Genome Data ◽  
Plastid Genomes ◽  
Plastome Evolution ◽  
Mycoheterotrophic Plants ◽  
Mitochondrial Genome Evolution

Abstract Background and Aims Fully mycoheterotrophic plants derive carbon and other nutrients from root-associated fungi and have lost the ability to photosynthesize. While mycoheterotroph plastomes are often degraded compared with green plants, the effect of this unusual symbiosis on mitochondrial genome evolution is unknown. By providing the first complete organelle genome data from Polygalaceae, one of only three eudicot families that developed mycoheterotrophy, we explore how both organellar genomes evolved after loss of photosynthesis. Methods We sequenced and assembled four complete plastid genomes and a mitochondrial genome from species of Polygalaceae, focusing on non-photosynthetic Epirixanthes. We compared these genomes with those of other mycoheterotroph and parasitic plant lineages, and assessed whether organelle genes in Epirixanthes experienced relaxed or intensified selection compared with autotrophic relatives. Key Results Plastomes of two species of Epirixanthes have become substantially degraded compared with that of autotrophic Polygala. Although the lack of photosynthesis is presumably homologous in the genus, the surveyed Epirixanthes species have marked differences in terms of plastome size, structural rearrangements, gene content and substitution rates. Remarkably, both apparently replaced a canonical plastid inverted repeat with large directly repeated sequences. The mitogenome of E. elongata incorporated a considerable number of fossilized plastid genes, by intracellular transfer from an ancestor with a less degraded plastome. Both plastid and mitochondrial genes in E. elongata have increased substitution rates, but the plastid genes of E. pallida do not. Despite this, both species have similar selection patterns operating on plastid housekeeping genes. Conclusions Plastome evolution largely fits with patterns of gene degradation seen in other heterotrophic plants, but includes highly unusual directly duplicated regions. The causes of rate elevation in the sequenced Epirixanthes mitogenome and of rate differences in plastomes of related mycoheterotrophic species are not currently understood.

scholarly journals The chicken or the egg? Plastome evolution and a novel loss of the inverted repeat in papilionoid legumes

2021 ◽  
Author(s):  
Chaehee Lee ◽  
In-Su Choi ◽  
Domingos Cardoso ◽  
Haroldo C. de Lima ◽  
Luciano P. de Queiroz ◽  
...  
Keyword(s):  
Inverted Repeat ◽  
Structural Changes ◽  
Structural Evolution ◽  
Comparative Genomic ◽  
Independent Events ◽  
Plastid Genomes ◽  
Plastome Evolution ◽  
The Family ◽  
History Of

AbstractThe plastid genome (plastome), while surprisingly constant in gene order and content across most photosynthetic angiosperms, exhibits variability in several unrelated lineages. During the diversification history of the legume family Fabaceae, plastomes have undergone many rearrangements, including inversions, expansion, contraction and loss of the typical inverted repeat (IR), gene loss and repeat accumulation in both shared and independent events. While legume plastomes have been the subject of study for some time, most work has focused on agricultural species in the IR-lacking clade (IRLC) and the plant model Medicago truncatula. The subfamily Papilionoideae, which contains virtually all of the agricultural legume species, also comprises most of the plastome variation detected thus far in the family. In this study 33 newly sequenced plastomes of papilionoid legumes and outgroups were evaluated, along with 34 publicly available sequences, to assess plastome structural evolution in the subfamily. In an effort to examine plastome variation across the subfamily, just ∼20% of the sampling represents the IRLC with the remainder selected to represent the early-branching papilionoid clades. A number of IR-related and repeat-mediated changes were identified and examined in a phylogenetic context. Recombination between direct repeats associated with ycf2 resulted in intraindividual plastome heteroplasmy. Although loss of the inverted repeat has not been reported in legumes outside of the IRLC, one genistoid taxon was found to completely lack the typical plastome IR. The role of the IR and non-IR repeats in driving plastome change is discussed.Significance statementComparative genomic approaches employing plastid genomes (plastomes) have revealed that they are more variable across angiosperms than previously suggested. This study examined 64 species of Fabaceae and outgroups, including 33 newly sequenced taxa, to explore plastome structural evolution of the subfamily Papilionoideae in a phylogenetic context. Several unusual features of the inverted repeat highlight the importance of recombination in plastomic structural changes within and between individuals and species.

scholarly journals The chloroplast genome evolution of Venus slipper (Paphiopedilum): IR expansion, SSC contraction, and highly rearranged SSC regions

2021 ◽  
Vol 21 (1) ◽  
Author(s):  
Yan-Yan Guo ◽  
Jia-Xing Yang ◽  
Ming-Zhu Bai ◽  
Guo-Qiang Zhang ◽  
Zhong-Jian Liu
Keyword(s):  
Gene Order ◽  
Inverted Repeat ◽  
Single Copy ◽  
Gene Content ◽  
Comparative Genomic ◽  
Substitution Rates ◽  
Plastome Evolution ◽  
Chloroplast Genomes ◽  
Ideal System ◽  
Small Single Copy

Abstract Background Paphiopedilum is the largest genus of slipper orchids. Previous studies showed that the phylogenetic relationships of this genus are not well resolved, and sparse taxon sampling documented inverted repeat (IR) expansion and small single copy (SSC) contraction of the chloroplast genomes of Paphiopedilum. Results Here, we sequenced, assembled, and annotated 77 plastomes of Paphiopedilum species (size range of 152,130 – 164,092 bp). The phylogeny based on the plastome resolved the relationships of the genus except for the phylogenetic position of two unstable species. We used phylogenetic and comparative genomic approaches to elucidate the plastome evolution of Paphiopedilum. The plastomes of Paphiopedilum have a conserved genome structure and gene content except in the SSC region. The large single copy/inverted repeat (LSC/IR) boundaries are relatively stable, while the boundaries of the inverted repeat and small single copy region (IR/SSC) varied among species. Corresponding to the IR/SSC boundary shifts, the chloroplast genomes of the genus experienced IR expansion and SSC contraction. The IR region incorporated one to six genes of the SSC region. Unexpectedly, great variation in the size, gene order, and gene content of the SSC regions was found, especially in the subg. Parvisepalum. Furthermore, Paphiopedilum provides evidence for the ongoing degradation of the ndh genes in the photoautotrophic plants. The estimated substitution rates of the protein coding genes show accelerated rates of evolution in clpP, psbH, and psbZ. Genes transferred to the IR region due to the boundary shift also have higher substitution rates. Conclusions We found IR expansion and SSC contraction in the chloroplast genomes of Paphiopedilum with dense sampling, and the genus shows variation in the size, gene order, and gene content of the SSC region. This genus provides an ideal system to investigate the dynamics of plastome evolution.

scholarly journals The Complete Chloroplast Genome of the Vulnerable Oreocharis esquirolii (Gesneriaceae): Structural Features, Comparative and Phylogenetic Analysis

Plants ◽  
2020 ◽  
Vol 9 (12) ◽  
pp. 1692
Author(s):  
Li Gu ◽  
Ting Su ◽  
Ming-Tai An ◽  
Guo-Xiong Hu
Keyword(s):  
Phylogenetic Analysis ◽  
Sequence Similarity ◽  
Single Copy ◽  
Structural Features ◽  
Rrna Genes ◽  
Trna Genes ◽  
Sequencing Data ◽  
High Sequence Similarity ◽  
Plastid Genomes ◽  
Cp Genome

Oreocharis esquirolii, a member of Gesneriaceae, is known as Thamnocharis esquirolii, which has been regarded a synonym of the former. The species is endemic to Guizhou, southwestern China, and is evaluated as vulnerable (VU) under the International Union for Conservation of Nature (IUCN) criteria. Until now, the sequence and genome information of O. esquirolii remains unknown. In this study, we assembled and characterized the complete chloroplast (cp) genome of O. esquirolii using Illumina sequencing data for the first time. The total length of the cp genome was 154,069 bp with a typical quadripartite structure consisting of a pair of inverted repeats (IRs) of 25,392 bp separated by a large single copy region (LSC) of 85,156 bp and a small single copy region (SSC) of18,129 bp. The genome comprised 114 unique genes with 80 protein-coding genes, 30 tRNA genes, and four rRNA genes. Thirty-one repeat sequences and 74 simple sequence repeats (SSRs) were identified. Genome alignment across five plastid genomes of Gesneriaceae indicated a high sequence similarity. Four highly variable sites (rps16-trnQ, trnS-trnG, ndhF-rpl32, and ycf 1) were identified. Phylogenetic analysis indicated that O. esquirolii grouped together with O. mileensis, supporting resurrection of the name Oreocharis esquirolii from Thamnocharisesquirolii. The complete cp genome sequence will contribute to further studies in molecular identification, genetic diversity, and phylogeny.

scholarly journals Complete Chloroplast Genome of Paphiopedilum delenatii and Phylogenetic Relationships among Orchidaceae

Plants ◽  
2020 ◽  
Vol 9 (1) ◽  
pp. 61 ◽  
Author(s):  
Huyen-Trang Vu ◽  
Ngan Tran ◽  
Thanh-Diem Nguyen ◽  
Quoc-Luan Vu ◽  
My-Huyen Bui ◽  
...  
Keyword(s):  
Chloroplast Genome ◽  
Inverted Repeat ◽  
Gc Content ◽  
Single Copy ◽  
Rrna Genes ◽  
Trna Genes ◽  
Complete Chloroplast Genome ◽  
Critically Endangered Species ◽  
Plastid Genomes ◽  
Chloroplast Genomes

Paphiopedilum delenatii is a native orchid of Vietnam with highly attractive floral traits. Unfortunately, it is now listed as a critically endangered species with a few hundred individuals remaining in nature. In this study, we performed next-generation sequencing of P. delenatii and assembled its complete chloroplast genome. The whole chloroplast genome of P. delenatii was 160,955 bp in size, 35.6% of which was GC content, and exhibited typical quadripartite structure of plastid genomes with four distinct regions, including the large and small single-copy regions and a pair of inverted repeat regions. There were, in total, 130 genes annotated in the genome: 77 coding genes, 39 tRNA genes, 8 rRNA genes, and 6 pseudogenes. The loss of ndh genes and variation in inverted repeat (IR) boundaries as well as data of simple sequence repeats (SSRs) and divergent hotspots provided useful information for identification applications and phylogenetic studies of Paphiopedilum species. Whole chloroplast genomes could be used as an effective super barcode for species identification or for developing other identification markers, which subsequently serves the conservation of Paphiopedilum species.

scholarly journals Unprecedented Parallel Photosynthetic Losses in a Heterotrophic Orchid Genus

2019 ◽  
Vol 36 (9) ◽  
pp. 1884-1901 ◽  
Author(s):  
Craig F Barrett ◽  
Brandon T Sinn ◽  
Aaron H Kennedy
Keyword(s):  
Genome Evolution ◽  
Gene Loss ◽  
Photosynthetic Apparatus ◽  
Housekeeping Genes ◽  
Genomic Rearrangements ◽  
Model Organisms ◽  
Plastid Genomes ◽  
Genome Modification ◽  
Single Genus ◽  
Genome Degradation

AbstractHeterotrophic 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 genus Hexalectris, including multiple individuals for most, and leafy relatives Basiphyllaea and Bletia. Our objectives are to determine the number of independent losses of photosynthesis and to test hypotheses on the process of genome degradation as a result of relaxed selection. We demonstrate four to five independent losses of photosynthesis in Hexalectris based on degradation of the photosynthetic apparatus, with all but two species displaying evidence of losses, and variation in gene loss extending below the species level. Degradation in the atp complex is advanced in Hexalectris warnockii, whereas only minimal degradation (i.e., physical loss) has occurred among some “housekeeping” genes. We find genomic rearrangements, shifts in Inverted Repeat boundaries including complete loss in one accession of H. arizonica, and correlations among substitutional and genomic attributes. Our unprecedented finding of multiple, independent transitions to a fully mycoheterotrophic lifestyle in a single genus reveals that the number of such transitions among land plants is likely underestimated. This study underscores the importance of dense taxon sampling, which is highly informative for advancing models of genome evolution in heterotrophs. Mycoheterotrophs such as Hexalectris provide forward-genetic opportunities to study the consequences of radical genome evolution beyond what is possible with mutational studies in model organisms alone.

scholarly journals Extensive plastome reduction and loss of photosynthesis genes in Diphelypaea coccinea, a holoparasitic plant of the family Orobanchaceae

PeerJ ◽  
2019 ◽  
Vol 7 ◽  
pp. e7830 ◽  
Author(s):  
Eugeny V. Gruzdev ◽  
Vitaly V. Kadnikov ◽  
Alexey V. Beletsky ◽  
Andrey V. Mardanov ◽  
Nikolai V. Ravin
Keyword(s):  
Genome Evolution ◽  
Plastid Genome ◽  
Housekeeping Genes ◽  
Parasitic Plants ◽  
Rrna Genes ◽  
Phylogenetic Position ◽  
Trna Genes ◽  
Protein Coding ◽  
The Family ◽  
Plastid Genome Evolution

Background Parasitic plants have the ability to obtain nutrients from their hosts and are less dependent on their own photosynthesis or completely lose this capacity. The reduction in plastid genome size and gene content in parasitic plants predominantly results from loss of photosynthetic genes. Plants from the family Orobanchaceae are used as models for studying plastid genome evolution in the transition from an autotrophic to parasitic lifestyle. Diphelypaea is a poorly studied genus of the Orobanchaceae, comprising two species of non-photosynthetic root holoparasites. In this study, we sequenced the plastid genome of Diphelypaea coccinea and compared it with other Orobanchaceae, to elucidate patterns of plastid genome evolution. In addition, we used plastid genome data to define the phylogenetic position of Diphelypaea spp. Methods The complete nucleotide sequence of the plastid genome of D. coccinea was obtained from total plant DNA, using pyrosequencing technology. Results The D. coccinea plastome is only 66,616 bp in length, and is highly rearranged; however, it retains a quadripartite structure. It contains only four rRNA genes, 25 tRNA genes and 25 protein-coding genes, being one of the most highly reduced plastomes among the parasitic Orobanchaceae. All genes related to photosynthesis, including the ATP synthase genes, had been lost, whereas most housekeeping genes remain intact. The plastome contains two divergent, but probably intact clpP genes. Intron loss had occurred in some protein-coding and tRNA genes. Phylogenetic analysis yielded a fully resolved tree for the Orobanchaceae, with Diphelypaea being a sister group to Orobanche sect. Orobanche.

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