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Comparative analysis of plastid genomes of non-photosynthetic Ericaceae and their photosynthetic relatives.

ABSTRACT: Although plastid genomes of flowering plants are typically highly conserved regarding their size, gene content and order, there are some exceptions. Ericaceae, a large and diverse family of flowering plants, warrants special attention within the context of plastid genome evolution because it includes both non-photosynthetic and photosynthetic species with rearranged plastomes and putative losses of "essential" genes. We characterized plastid genomes of three species of Ericaceae, non-photosynthetic Monotropa uniflora and Hypopitys monotropa and photosynthetic Pyrola rotundifolia, using high-throughput sequencing. As expected for non-photosynthetic plants, M. uniflora and H. monotropa have small plastid genomes (46?kb and 35?kb, respectively) lacking genes related to photosynthesis, whereas P. rotundifolia has a larger genome (169?kb) with a gene set similar to other photosynthetic plants. The examined genomes contain an unusually high number of repeats and translocations. Comparative analysis of the expanded set of Ericaceae plastomes suggests that the genes clpP and accD that are present in the plastid genomes of almost all plants have not been lost in this family (as was previously thought) but rather persist in these genomes in unusual forms. Also we found a new gene in P. rotundifolia that emerged as a result of duplication of rps4 gene.

SUBMITTER: Logacheva MD

PROVIDER: S-EPMC4958920 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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Comparative analysis of plastid genomes of non-photosynthetic Ericaceae and their photosynthetic relatives.

Logacheva Maria D MD Schelkunov Mikhail I MI Shtratnikova Victoria Y VY Matveeva Maria V MV Penin Aleksey A AA

Scientific reports 20160725

Although plastid genomes of flowering plants are typically highly conserved regarding their size, gene content and order, there are some exceptions. Ericaceae, a large and diverse family of flowering plants, warrants special attention within the context of plastid genome evolution because it includes both non-photosynthetic and photosynthetic species with rearranged plastomes and putative losses of "essential" genes. We characterized plastid genomes of three species of Ericaceae, non-photosynthe ...[more]

PMID: 27452401

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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.

Project description:Plastids are actively involved in numerous plant processes critical to growth, development and adaptation. They play a primary role in photosynthesis, pigment and monoterpene synthesis, gravity sensing, starch and fatty acid synthesis, as well as oil, and protein storage. We applied two complementary methods to analyze the recently published apple genome (Malus × domestica) to identify putative plastid-targeted proteins, the first using TargetP and the second using a custom workflow utilizing a set of predictive programs. Apple shares roughly 40% of its 10,492 putative plastid-targeted proteins with that of the Arabidopsis (Arabidopsis thaliana) plastid-targeted proteome as identified by the Chloroplast 2010 project and ∼57% of its entire proteome with Arabidopsis. This suggests that the plastid-targeted proteomes between apple and Arabidopsis are different, and interestingly alludes to the presence of differential targeting of homologs between the two species. Co-expression analysis of 2,224 genes encoding putative plastid-targeted apple proteins suggests that they play a role in plant developmental and intermediary metabolism. Further, an inter-specific comparison of Arabidopsis, Prunus persica (Peach), Malus × domestica (Apple), Populus trichocarpa (Black cottonwood), Fragaria vesca (Woodland Strawberry), Solanum lycopersicum (Tomato) and Vitis vinifera (Grapevine) also identified a large number of novel species-specific plastid-targeted proteins. This analysis also revealed the presence of alternatively targeted homologs across species. Two separate analyses revealed that a small subset of proteins, one representing 289 protein clusters and the other 737 unique protein sequences, are conserved between seven plastid-targeted angiosperm proteomes. Majority of the novel proteins were annotated to play roles in stress response, transport, catabolic processes, and cellular component organization. Our results suggest that the current state of knowledge regarding plastid biology, preferentially based on model systems is deficient. New plant genomes are expected to enable the identification of potentially new plastid-targeted proteins that will aid in studying novel roles of plastids.

Project description:Owing to its attractive flower shape and color, Renanthera (Orchidaceae), comprising about 19 species, has significant ornamental value as a houseplant, in floral design and in landscape gardens. Two species of Renanthera are categorized as endangered and critically endangered in China's Red List and international trade in these orchids is currently strictly monitored by the Convention on International Trade in Endangered Species of Wild Fauna and Flora (CITES). This paper reports on the de novo assembled and annotated plastome of four species of Renanthera; R. citrina, R. coccinea, R. imschootiana, and R. philippinensis. The length of the plastome sequences ranged from 144,673 bp (R. imschootiana) to 149,007 bp (R. coccinea) with GC content of 36.6-36.7%. The plastomes showed a typical quadripartite structure, including a large single-copy (84,241-86,404 bp), a small single-copy (11,468-12,167 bp), and a pair of inverted repeats (24,482-25,715 bp) regions. Of the 120 genes detected, 74 were protein coding, 38 were tRNA, and eight were rRNA genes. The plastome of Renanthera is rather conserved, but nucleotide variations that could distinguish them apart are noticeable-the total number of tandem repeats ranged from 62 (in R. imschootiana) to 74 (in R. citrina); while the number of long repeats ranged from 21 (in R. imschootiana and R. philippinensis) to 43 (in R. citrina). Three hypervariable regions (psbI-trnS-GCU, trnG-GCC, rpl32) were identified. Phylogenetic analyses based on the CDS using maximum likelihood (ML) and Bayesian inference (BI) revealed that Renanthera is closely related to Holcoglossum, Neofinetia, Pendulorchis, and Vanda. The relationship between the four species of Renanthera was fully resolved; a monophyletic clade was formed and R. coccinea was recorded as the first to diverge from the rest. The genetic data obtained from this study could serve as a useful resource for species identification in Renanthera as well as contribute to future research on the phylogenomics of Orchidaceae.

Dataset Information

Comparative analysis of plastid genomes of non-photosynthetic Ericaceae and their photosynthetic relatives.

Publications

Comparative analysis of plastid genomes of non-photosynthetic Ericaceae and their photosynthetic relatives.

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