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Severe Plastid Genome Size Reduction in a Mycoheterotrophic Orchid, Danxiaorchis singchiana, Reveals Heavy Gene Loss and Gene Relocations.

ABSTRACT: 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 and a small single copy (SSC) region of 17,831 bp. When compared to its sister taxa, Cremastra appendiculata and Corallorhiza striata var. involuta, D. singchiana showed an inverted gene block in the LSC and SSC regions. A total of 61 genes were predicted, including 21 tRNA, 4 rRNA, and 36 protein-coding genes. While most of the housekeeping genes were still intact and seem to be protein-coding, only four photosynthesis-related genes appeared presumably intact. The majority of the presumably intact protein-coding genes seem to have undergone purifying selection (dN/dS < 1), and only the psaC gene was positively selected (dN/dS > 1) when compared to that in Cr. appendiculata. Phylogenetic analysis of 26 complete plastome sequences from 24 species of the tribe Epidendreae had revealed that D. singchiana diverged after Cr. appendiculata and is sister to the genus Corallorhiza with strong bootstrap support (100%).

SUBMITTER: Lee SY

PROVIDER: S-EPMC7238169 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Severe Plastid Genome Size Reduction in a Mycoheterotrophic Orchid, Danxiaorchis singchiana, Reveals Heavy Gene Loss and Gene Relocations.

Lee Shiou Yih SY Meng Kaikai K Wang Haowei H Zhou Renchao R Liao Wenbo W Chen Fang F Zhang Shouzhou S Fan Qiang Q

Plants (Basel, Switzerland) 20200417 4

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 and a small single copy (SSC) region of 17,831 bp. When compared to its sister taxa, Cremastra appendiculata and Corallorhiza s ...[more]

PMID: 32316476

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Project description:Background and aimsDespite their significant capacity to propagate vegetatively, most orchids reproduce via seeds. Sexual reproduction via seed is commonly reported, in contrast to apomixis, whereby seeds are clones of the mother. Although insect pollination and autonomous self-pollination exist in mycoheterotrophic plants, the reproductive embryology of these plants remains under-studied. This paper provides evidence for the co-occurrence of both sexual and apomictic reproduction in a population of mycoheterotrophic plants - Epipogium aphyllum We investigated seed formation via open pollination, induced autogamy, autogamy sensu stricto and autonomous apomixis.MethodsThe study was performed on a population of E. aphyllum located in northern Poland. The research included studies of the micromorphology, histochemistry and embryology of four types of reproductive systems. Scanning, fluorescence and light microscopy accompanied by graphical and statistical analyses were employed.Key resultsWe observed gametophyte development, from the one-nucleate stage to maturity, in unpollinated flower buds. The lack of zygotes in flower buds indicated that fertilization did not occur at this stage. Manual self-pollination led to a zygote, followed by embryo formation. Fertilization and embryo development derived from embryogenesis via open pollination is delayed compared with hand pollination. Isolation from external pollination resulted only in structures resembling zygotes that may originate either sexually or independent of fertilization. Parthenogenetic structures that resembled zygotes were observed in flowers that were emasculated and isolated from pollination. Zygotes formed at significantly higher frequencies via open pollination and induced autogamy in comparison to the parthenogenetic structures formed in other treatments.ConclusionsWe showed the absence of pre-zygotic barriers for autogamy in E. aphyllum Self-pollination and self-fertilization are possible; however, natural self-pollination is unlikely or rare due to the position of the pollinia. Incidental parthenogenesis in E. aphyllum is very likely, given the biology of ovule development of this mycoheterotrophic orchid. This species therefore has the potential to produce seeds via both sexual and asexual means, although the contribution of apomixis to this process appears largely negligible.

Project description:BackgroundChloroplasts of most plants are responsible for photosynthesis and contain a conserved set of about 110 genes that encode components of housekeeping gene expression machinery and photosynthesis-related functions. Heterotrophic plants obtaining nutrients from other organisms and their plastid genomes represent model systems in which to study the effects of relaxed selective pressure on photosynthetic function. The most evident is a reduction in the size and gene content of the plastome, which correlates with the loss of genes encoding photosynthetic machinery which become unnecessary. Transition to a non-photosynthetic lifestyle is expected also to relax the selective pressure on photosynthetic machinery in the nuclear genome, however, the corresponding changes are less known.ResultsHere we report the complete sequence of the plastid genome of Monotropa hypopitys, an achlorophyllous obligately mycoheterotrophic plant belonging to the family Ericaceae. The plastome of M. hypopitys is greatly reduced in size (35,336 bp) and lacks the typical quadripartite structure with two single-copy regions and an inverted repeat. Only 45 genes remained presumably intact- those encoding ribosomal proteins, ribosomal and transfer RNA and housekeeping genes infA, matK, accD and clpP. The clpP and accD genes probably remain functional, although their sequences are highly diverged. The sets of genes for ribosomal protein and transfer RNA are incomplete relative to chloroplasts of a photosynthetic plant. Comparison of the plastid genomes of two subspecies-level isolates of M. hypopitys revealed major structural rearrangements associated with repeat-driven recombination and the presence of isolate-specific tRNA genes. Analysis of the M. hypopitys transcriptome by RNA-Seq showed the absence of expression of nuclear-encoded components of photosystem I and II reaction center proteins, components of cytochrome b6f complex, ATP synthase, ribulose bisphosphate carboxylase components, as well as chlorophyll from protoporphyrin IX biosynthesis pathway.ConclusionsWith the complete loss of genes related to photosynthesis, NADH dehydrogenase, plastid-encoded RNA polymerase and ATP synthase, the M. hypopitys plastid genome is among the most functionally reduced ones characteristic of obligate non-photosynthetic parasitic species. Analysis of the M. hypopitys transcriptome revealed coordinated evolution of the nuclear and plastome genomes and the loss of photosynthesis-related functions in both genomes.

Dataset Information

Severe Plastid Genome Size Reduction in a Mycoheterotrophic Orchid, Danxiaorchis singchiana, Reveals Heavy Gene Loss and Gene Relocations.

Publications

Severe Plastid Genome Size Reduction in a Mycoheterotrophic Orchid, <i>Danxiaorchis singchiana</i>, Reveals Heavy Gene Loss and Gene Relocations.

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