The complete plastid genome sequence and the photosynthetic activity of the putative mycoheterotrophic orchid Limodorum abortivum

in Israel Journal of Plant Sciences
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The sparsely distributed Limodorum abortivum is a European-Mediterranean orchid species, which grows on decomposing plant material. Although some chlorophyll-pigmentation is observed in the degenerated scales-shaped leaf and stems regions of the plant, its photosynthetic capacity is assumed to be insufficient to support the full energy requirements of an adult plant. In Israel, L. abortivum shows a patchy distribution patterns in the Galilee, Golan, Carmel and Judean regions. To gain more insights into the physiology and photosynthetic activity of L. abortivum, we analyzed the organellar morphologies, photosynthetic activities the chloroplast-DNA sequence by Illumina-HTS. Microscopic analyses indicated to the presence of mature chloroplasts with well-organized grana-thylakoids in the leaves and stems of L. abortivum. However, the numbers of chloroplasts per cell and the grana ultrastructure density within the organelles were notably lower than those of model plant species and fully photosynthetically-active orchids. The cpDNA of L. abortivum (154,954 bp) encodes 60 proteins, 34 tRNAs and 4 rRNAs. The coding-regions of 24 genes are interrupted by 26 group-II intron-sequences. While many genes related to photosynthesis (RuBisCo, PSI, PSII and cytochrome b 6 /f subunits) have remained intact in the cpDNA, the majority of the NADH-dehydrogenase (ndh) subunits were either lost or became nonfunctional (i.e. pseudogenized). In agreement with previous reports, the photosynthetic-rates of adult Limodorum plants were found to be very low, further indicating that carbon-assimilation activity is insufficient to support the energy requirements of an adult plant, and may suggest that L. abortivum have adopted nutritional strategies similar to that of mycoheterotrophic orchid species.

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Figures
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    Morphology and habitat of Limodorum abortivum plants in Israel. Limodorum abortivum is a relatively rare orchid species that is found in large parts of Europe and the Middle-East regions. Panel A – a typical flower of Limodorum abortivum (from the N. Golan, Mas'ade Forest region); B – A schematic diagram of Limodorum abortivum shoots, roots flowers and seeds (Source – Polunin 1989). C – Limodorum abortivum plants in their native habitat (i.e. N. Golan, Mas'ade Forest region); D – In Israel, L. abortivum has a patchy growth pattern in the Galilee and Judean mountain regions. We would like to thank Prof. Avi Shmida for his kind assistance and permission to use the material in the figure.

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    Electron micrograph images of leaf and stem tissues from L. abortivum and C. longifolia plants. Thin sections obtained from leaf (panels A, B, E and F) and stem (C, D, G and H) tissues obtained from field-grown C. longifolia (panels A–D) and L. abortivum (E-H) plants were stained with uranyl acetate and lead citrate and examined in a transmission electron microscope. Image scale of × 1450 (panels A, C, E and G) and enlarged images (i.e. × 9,700, panels B, D, F and H). Nucleus (“N”), Mitochondria (“M”), Chloroplasts (“C”), Grana stacking (“G”) and starch granules (“S”) are indicated on the micrograph images.

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    Circular map of L. abortivum plastome sequence (MH685741). Boxes on the inside and outside of the outer circle represent genes transcribed clockwise and anti-clockwise, respectively, as also indicated by arrows within the figure. Gene colors correspond to the functional categories listed in the legend, while regions indicate group II intron regions, as indicated in the figure layout (see Table 3). The figure was created using OGDraw v1.2 (Lohse et al. 2013).

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    Phylogenetic analysis of different orchids. Phylogeny tree was constructed using the MAFFT (version 7) multiple sequence alignment server (Katoh et al. 2017), using the complete cpDNA sequences of 106 different orchid species (see Supplementary Fig. S4) (bootstrap values for 1000 bootstrap replicates). The resulting tree file was then returned for visualization in the Archaeopteryx tree viewer (Zmasek and Eddy 2001).

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    Protein-coding genes in L. abortivum and various other orchids of the Neottieae tribe. Figure was modified from (Feng et al. 2016). Intact genes per species are indicated by black boxes, whereas white and striped boxes mark functional and or physical losses, respectively.

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    tRNA-coding genes in L. abortivum and various other orchids of the Neottieae tribe. Figure was modified from (Feng et al. 2016). Intact genes per species are indicated by black boxes, whereas white boxes mark functional and or physical losses, respectively.

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    Schematic view of the photosynthetic complexes within the chloroplasts of L. abortivum and N. nidus-avis. The photosynthetic complexes photosystem I (PSI), photosystem II (PSII), the cytochrome b6f, ATP synthase and the NAD(P)H dehydrogenase complexes are shown in the figure The figure was modified from Allen et al. (2011) and Casano et al. (2004).

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