Concomitant loss of NDH complex-related genes within chloroplast and nuclear genomes in some orchids

Choun Sea Lin, Jeremy J.W. Chen, Chi-Chou Chiu, Han C.W. Hsiao, Chen Jui Yang, Xiao Hua Jin, James Leebens-Mack, Claude W. de Pamphilis, Yao Ting Huang, Ling Hung Yang, Wan Jung Chang, Ling Kui, Gane Ka Shu Wong, Jer Ming Hu, Wen Wang, Ming Che Shih

Research output: Contribution to journalArticle

16 Citations (Scopus)

Abstract

The chloroplast NAD(P)H dehydrogenase-like (NDH) complex consists of about 30 subunits from both the nuclear and chloroplast genomes and is ubiquitous across most land plants. In some orchids, such as Phalaenopsis equestris, Dendrobium officinale and Dendrobium catenatum, most of the 11 chloroplast genome-encoded ndh genes (cp-ndh) have been lost. Here we investigated whether functional cp-ndh genes have been completely lost in these orchids or whether they have been transferred and retained in the nuclear genome. Further, we assessed whether both cp-ndh genes and nucleus-encoded NDH-related genes can be lost, resulting in the absence of the NDH complex. Comparative analyses of the genome of Apostasia odorata, an orchid species with a complete complement of cp-ndh genes which represents the sister lineage to all other orchids, and three published orchid genome sequences for P. equestris, D. officinale and D. catenatum, which are all missing cp-ndh genes, indicated that copies of cp-ndh genes are not present in any of these four nuclear genomes. This observation suggests that the NDH complex is not necessary for some plants. Comparative genomic/transcriptomic analyses of currently available plastid genome sequences and nuclear transcriptome data showed that 47 out of 660 photoautotrophic plants and all the heterotrophic plants are missing plastid-encoded cp-ndh genes and exhibit no evidence for maintenance of a functional NDH complex. Our data indicate that the NDH complex can be lost in photoautotrophic plant species. Further, the loss of the NDH complex may increase the probability of transition from a photoautotrophic to a heterotrophic life history.

Original languageEnglish
Pages (from-to)994-1006
Number of pages13
JournalPlant Journal
Volume90
Issue number5
DOIs
Publication statusPublished - 2017 Jun 1

Fingerprint

Chloroplast Genome
Orchidaceae
nuclear genome
Genes
genes
Dendrobium
Genome
Dendrobium officinale
Plastid Genomes
Embryophyta
Phalaenopsis
Plastids
genome
NAD(P)H dehydrogenase (quinone)
chloroplast genome
embryophytes
Chloroplasts
transcriptomics
Transcriptome
transcriptome

All Science Journal Classification (ASJC) codes

  • Genetics
  • Plant Science
  • Cell Biology

Cite this

Lin, C. S., Chen, J. J. W., Chiu, C-C., Hsiao, H. C. W., Yang, C. J., Jin, X. H., ... Shih, M. C. (2017). Concomitant loss of NDH complex-related genes within chloroplast and nuclear genomes in some orchids. Plant Journal, 90(5), 994-1006. https://doi.org/10.1111/tpj.13525
Lin, Choun Sea ; Chen, Jeremy J.W. ; Chiu, Chi-Chou ; Hsiao, Han C.W. ; Yang, Chen Jui ; Jin, Xiao Hua ; Leebens-Mack, James ; de Pamphilis, Claude W. ; Huang, Yao Ting ; Yang, Ling Hung ; Chang, Wan Jung ; Kui, Ling ; Wong, Gane Ka Shu ; Hu, Jer Ming ; Wang, Wen ; Shih, Ming Che. / Concomitant loss of NDH complex-related genes within chloroplast and nuclear genomes in some orchids. In: Plant Journal. 2017 ; Vol. 90, No. 5. pp. 994-1006.
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abstract = "The chloroplast NAD(P)H dehydrogenase-like (NDH) complex consists of about 30 subunits from both the nuclear and chloroplast genomes and is ubiquitous across most land plants. In some orchids, such as Phalaenopsis equestris, Dendrobium officinale and Dendrobium catenatum, most of the 11 chloroplast genome-encoded ndh genes (cp-ndh) have been lost. Here we investigated whether functional cp-ndh genes have been completely lost in these orchids or whether they have been transferred and retained in the nuclear genome. Further, we assessed whether both cp-ndh genes and nucleus-encoded NDH-related genes can be lost, resulting in the absence of the NDH complex. Comparative analyses of the genome of Apostasia odorata, an orchid species with a complete complement of cp-ndh genes which represents the sister lineage to all other orchids, and three published orchid genome sequences for P. equestris, D. officinale and D. catenatum, which are all missing cp-ndh genes, indicated that copies of cp-ndh genes are not present in any of these four nuclear genomes. This observation suggests that the NDH complex is not necessary for some plants. Comparative genomic/transcriptomic analyses of currently available plastid genome sequences and nuclear transcriptome data showed that 47 out of 660 photoautotrophic plants and all the heterotrophic plants are missing plastid-encoded cp-ndh genes and exhibit no evidence for maintenance of a functional NDH complex. Our data indicate that the NDH complex can be lost in photoautotrophic plant species. Further, the loss of the NDH complex may increase the probability of transition from a photoautotrophic to a heterotrophic life history.",
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year = "2017",
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Lin, CS, Chen, JJW, Chiu, C-C, Hsiao, HCW, Yang, CJ, Jin, XH, Leebens-Mack, J, de Pamphilis, CW, Huang, YT, Yang, LH, Chang, WJ, Kui, L, Wong, GKS, Hu, JM, Wang, W & Shih, MC 2017, 'Concomitant loss of NDH complex-related genes within chloroplast and nuclear genomes in some orchids', Plant Journal, vol. 90, no. 5, pp. 994-1006. https://doi.org/10.1111/tpj.13525

Concomitant loss of NDH complex-related genes within chloroplast and nuclear genomes in some orchids. / Lin, Choun Sea; Chen, Jeremy J.W.; Chiu, Chi-Chou; Hsiao, Han C.W.; Yang, Chen Jui; Jin, Xiao Hua; Leebens-Mack, James; de Pamphilis, Claude W.; Huang, Yao Ting; Yang, Ling Hung; Chang, Wan Jung; Kui, Ling; Wong, Gane Ka Shu; Hu, Jer Ming; Wang, Wen; Shih, Ming Che.

In: Plant Journal, Vol. 90, No. 5, 01.06.2017, p. 994-1006.

Research output: Contribution to journalArticle

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T1 - Concomitant loss of NDH complex-related genes within chloroplast and nuclear genomes in some orchids

AU - Lin, Choun Sea

AU - Chen, Jeremy J.W.

AU - Chiu, Chi-Chou

AU - Hsiao, Han C.W.

AU - Yang, Chen Jui

AU - Jin, Xiao Hua

AU - Leebens-Mack, James

AU - de Pamphilis, Claude W.

AU - Huang, Yao Ting

AU - Yang, Ling Hung

AU - Chang, Wan Jung

AU - Kui, Ling

AU - Wong, Gane Ka Shu

AU - Hu, Jer Ming

AU - Wang, Wen

AU - Shih, Ming Che

PY - 2017/6/1

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N2 - The chloroplast NAD(P)H dehydrogenase-like (NDH) complex consists of about 30 subunits from both the nuclear and chloroplast genomes and is ubiquitous across most land plants. In some orchids, such as Phalaenopsis equestris, Dendrobium officinale and Dendrobium catenatum, most of the 11 chloroplast genome-encoded ndh genes (cp-ndh) have been lost. Here we investigated whether functional cp-ndh genes have been completely lost in these orchids or whether they have been transferred and retained in the nuclear genome. Further, we assessed whether both cp-ndh genes and nucleus-encoded NDH-related genes can be lost, resulting in the absence of the NDH complex. Comparative analyses of the genome of Apostasia odorata, an orchid species with a complete complement of cp-ndh genes which represents the sister lineage to all other orchids, and three published orchid genome sequences for P. equestris, D. officinale and D. catenatum, which are all missing cp-ndh genes, indicated that copies of cp-ndh genes are not present in any of these four nuclear genomes. This observation suggests that the NDH complex is not necessary for some plants. Comparative genomic/transcriptomic analyses of currently available plastid genome sequences and nuclear transcriptome data showed that 47 out of 660 photoautotrophic plants and all the heterotrophic plants are missing plastid-encoded cp-ndh genes and exhibit no evidence for maintenance of a functional NDH complex. Our data indicate that the NDH complex can be lost in photoautotrophic plant species. Further, the loss of the NDH complex may increase the probability of transition from a photoautotrophic to a heterotrophic life history.

AB - The chloroplast NAD(P)H dehydrogenase-like (NDH) complex consists of about 30 subunits from both the nuclear and chloroplast genomes and is ubiquitous across most land plants. In some orchids, such as Phalaenopsis equestris, Dendrobium officinale and Dendrobium catenatum, most of the 11 chloroplast genome-encoded ndh genes (cp-ndh) have been lost. Here we investigated whether functional cp-ndh genes have been completely lost in these orchids or whether they have been transferred and retained in the nuclear genome. Further, we assessed whether both cp-ndh genes and nucleus-encoded NDH-related genes can be lost, resulting in the absence of the NDH complex. Comparative analyses of the genome of Apostasia odorata, an orchid species with a complete complement of cp-ndh genes which represents the sister lineage to all other orchids, and three published orchid genome sequences for P. equestris, D. officinale and D. catenatum, which are all missing cp-ndh genes, indicated that copies of cp-ndh genes are not present in any of these four nuclear genomes. This observation suggests that the NDH complex is not necessary for some plants. Comparative genomic/transcriptomic analyses of currently available plastid genome sequences and nuclear transcriptome data showed that 47 out of 660 photoautotrophic plants and all the heterotrophic plants are missing plastid-encoded cp-ndh genes and exhibit no evidence for maintenance of a functional NDH complex. Our data indicate that the NDH complex can be lost in photoautotrophic plant species. Further, the loss of the NDH complex may increase the probability of transition from a photoautotrophic to a heterotrophic life history.

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