Skip to main content

Advertisement

SpringerLink
Log in

A genome-wide analysis of the chloroplast NADH dehydrogenase-like genes in Zostera marina

  • Biology
  • Published:
Journal of Oceanology and Limnology Aims and scope Submit manuscript

Abstract

The chloroplast NADH dehydrogenase-like (NDH) complex, homologous to respiratory complex I, participates in photosystem I cyclic electron flow (PSI-CEF) and chlororespiration in photosynthesis. Phylogenetic analyses indicated that Zostera marina, a widely distributed seagrass, has a complete NDH complex, which is rarely observed in marine macrophytes. We identified all 31 ndh genes necessary for the functional NDH complex, of which ndhB and pnsb3 occurred as duplication events. Secondary structural analyses of antiporter-like subunits showed that the long amphipathic helix of NdhF was lost in Z. marina, which could exhibit an alternative mode in the generation of trans-thylakoid proton gradient. The splicing pattern of ndh exhibited tissue-specific patterns and responded to light stress. RNA editing in Z. marina presented the ancestral pattern with many of the primitive editing sites and types. The partial editing in ndhF reflected the link between light stress and RNA editing. Moreover, the predominant expression in leaves of most ndh genes suggested that their major function is in photosynthesis. The quantitative real time-PCR results show that the expression of ndh was significantly upregulated in response to light stress. Nevertheless, there were two diverse responsive mechanisms of the NDH complex in PSI-CEF and chlororespiration. Overall, the presence of a complete structure, upregulated gene expression level, and multiple post-transcriptional regulations could provide a molecular basis for the powerful NDH complex and enable Z. marina to maintain effective photosynthetic performance.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Data Availability Statement

Individual sequences were submitted to GenBank (https://www.ncbi.nlm.nih.gov/genbank/) and can be retrieved with accession numbers MW051562 and MW051563. The voucher specimen (specimen number: HY202005) is available in the Herbarium of Ocean School of Yantai University, Shandong Province, China.

References

  • Bailey T L, Boden M, Buske F A, Frith M, Grant C E, Clementi L, Ren J Y, Li W W, Noble W L. 2009. MEME Suite: tools for motif discovery and searching. Nucleic Acids Research, 37(S2): W202–W208.

    Article  Google Scholar 

  • Battchikova N, Wei L Z, Du L Y, Bersanini L, Aro E M, Ma W M. 2011. Identification of novel Ssl0352 protein (NdhS), essential for efficient operation of cyclic electron transport around photosystem I, in NADPH: plastoquinone oxidoreductase (NDH-1) complexes of Synechocystis sp. PCC 6803. Journal of Biological Chemistry, 286(42): 36992–37001.

    Article  Google Scholar 

  • Bertelli C M, Unsworth R K F. 2018. Light stress responses by the eelgrass, Zostera marina (L). Frontiers in Environmental Science, 6: 39.

    Article  Google Scholar 

  • Braukmann T W A, Kuzmina M, Stefanović S. 2009. Loss of all plastid NDH genes in Gnetales and conifers: extent and evolutionary significance for the seed plant phylogeny. Current Genetics, 55(3): 323–337.

    Article  Google Scholar 

  • Burrows P A, Sazanov L A, Svab Z, Maliga P, Nixon P J. 1998. Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid NDH genes. The EMBO Journal, 17(4): 868–876.

    Article  Google Scholar 

  • Chateigner-Boutin A L, Small I. 2010. Plant RNA editing. RNA Biology, 7(2): 213–219.

    Article  Google Scholar 

  • Chen C J, Chen H, Zhang Y, Thomas H R, Frank M H, He Y H, Xia R. 2020. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Molecular Plant, 13(8): 1194–1202.

    Article  Google Scholar 

  • Chen H Y, Deng L K, Jiang Y, Lu P, Yu J N. 2011. RNA editing sites exist in protein-coding genes in the chloroplast genome of Cycas taitungensis. Journal of Integrative Plant Biology, 53(12): 961–970.

    Article  Google Scholar 

  • Efremov R G, Baradaran R, Sazanov L A. 2010. The architecture of respiratory complex I. Nature, 465(7297): 441–445.

    Article  Google Scholar 

  • Essemine J, Qu M N, Mi H L, Zhu X G. 2016. Response of chloroplast NAD(P)H dehydrogenase-mediated cyclic electron flow to a shortage or lack in ferredoxin-Quinone oxidoreductase-dependent pathway in rice following short-term heat stress. Frontiers in Plant Science, 7: 383.

    Article  Google Scholar 

  • Fan X Y, Zhang J, Li W J, Peng L W. 2015. The NdhV subunit is required to stabilize the chloroplast NADH dehydrogenase-like complex in Arabidopsis. The Plant Journal: For Cell and Molecular Biology, 82(2): 221–231.

    Article  Google Scholar 

  • Gao F D, Zhao J H, Wang X Z, Qin S, Wei L Z, Ma W M. 2016. NdhV is a subunit of NADPH dehydrogenase essential for cyclic electron transport in Synechocystis sp. Strain PCC 6803. Plant Physiology, 170(2): 752–760.

    Article  Google Scholar 

  • He X, Zhang J. 2005. Gene complexity and gene duplicability. Current Biology Cb, 15(11): 1016–1021.

    Article  Google Scholar 

  • He Z H, Zheng F F, Wu Y Z, Li Q H, Lv J, Fu P C, Mi H L. 2015. NDH-1L interacts with ferredoxin via the subunit NdhS in Thermosynechococcus elongatus. Photosynthesis Research, 126(2–3): 341–349.

    Article  Google Scholar 

  • Hein A, Polsakiewicz M, Knoop V. 2016. Frequent chloroplast RNA editing in early-branching flowering plants: pilot studies on angiosperm-wide coexistence of editing sites and their nuclear specificity factors. BMC Evolutionary Biology, 16(1): 23.

    Article  Google Scholar 

  • Horvath E M, Peter S O, Joët T, Rumeau D, Cournac L, Horváth G V, Kavanagh T A, Schäfer C, Peltier G, Medgyesy P. 2000. Targeted inactivation of the plastid ndhB gene in tobacco results in an enhanced sensitivity of photosynthesis to moderate stomatal closure. Plant Physiology, 123(4): 1337–1350.

    Article  Google Scholar 

  • Ifuku K, Endo T, Shikanai T, Aro E M. 2011. Structure of the chloroplast NADH dehydrogenase-like complex: nomenclature for nuclear-encoded subunits. Plant & Cell Physiology, 52(9): 1560–1568.

    Article  Google Scholar 

  • Iles W J D, Smith S Y, Graham S W. 2013. A well-supported phylogenetic framework for the monocot order Alismatales reveals multiple losses of the plastid NADH dehydrogenase complex and a strong long-branch effect. In: Wilkin P, Mayo S J eds. Early Events in Monocot Evolution. Cambridge: Cambridge University Press.

    Google Scholar 

  • Ishikawa N, Takabayashi A, Ishida S, Hano Y, Endo T, Sato F. 2008. NDF6: a thylakoid protein specific to terrestrial plants is essential for activity of chloroplastic NAD(P)H dehydrogenase in Arabidopsis. Plant and Cell Physiology, 49(7): 1066–1073.

    Article  Google Scholar 

  • Jobson R W, Qiu Y L. 2008. Did RNA editing in plant organellar genomes originate under natural selection or through genetic drift? Biology Direct, 3(1): 43.

    Article  Google Scholar 

  • Kim H T, Chase M W. 2017. Independent degradation in genes of the plastid ndh gene family in species of the orchid genus Cymbidium (Orchidaceae; Epidendroideae). PLoS One, 12(11): e0187318.

    Article  Google Scholar 

  • Kofer W, Koop H U, Wanner G, Steinmüller K. 1998. Mutagenesis of the genes encoding subunits A, C, H, I, J and K of the plastid NAD(P)H-plastoquinone-oxidoreductase in tobacco by polyethylene glycolmediated plastome transformation. Molecular and General Genetics MGG, 258(1–2): 166–173.

    Article  Google Scholar 

  • Krogh A, Larsson B, Von Heijne G, Sonnhammer E L L. 2001. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology, 305(3): 567–580.

    Article  Google Scholar 

  • Larkin M A, Blackshields G, Brown N P, Chenna R, McGettigan P A, McWilliam H, Valentin F, Wallace I M, Wilm A, Lopez R, Thompson J D, Gibson T J, Higgins D G. 2007. Clustal W and Clustal X version 2.0. Bioinformatics, 23(21): 2947–2948.

    Article  Google Scholar 

  • Larkum A W D, Davey P A, Kuo J, Ralph P J, Raven J A. 2017. Carbon-concentrating mechanisms in seagrasses. Journal of Experimental Botany, 68(14): 3773–3784.

    Article  Google Scholar 

  • Lee H T, Golicz A A, Bayer P E, Severn-Ellis A A, Chan C K K, Batley J, Kendrick G A, Edwards D. 2018. Genomic comparison of two independent seagrass lineages reveals habitat-driven convergent evolution. Journal of Experimental Botany, 69(15): 3689–3702.

    Article  Google Scholar 

  • Lemieux C, Otis C, Turmel M. 2000. Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution. Nature, 403(6770): 649–652.

    Article  Google Scholar 

  • Les D H, Cleland M A, Waycott M. 1997. Phylogenetic studies in Alismatidae, II: evolution of marine angiosperms (seagrasses) and hydrophily. Systematic Botany, 22(3): 443–463.

    Article  Google Scholar 

  • Li X G, Duan W, Meng Q W, Zou Q, Zhao S J. 2004. The function of chloroplastic NAD(P)H dehydrogenase in tobacco during chilling stress under low irradiance. Plant and Cell Physiology, 45(1): 103–108.

    Article  Google Scholar 

  • Lin C S, Chen J J W, Chiu C C, Hsiao H C W, Yang C J, Jin X H, Leebens-Mack J, De Pamphilis C W, Huang Y T, Yang L H, Chang W J, Kui L, Wong G K S, Hu J M, Wang W, Shih M C. 2017. Concomitant loss of NDH complex-related genes within chloroplast and nuclear genomes in some orchids. The Plant Journal, 90(5): 994–1006.

    Article  Google Scholar 

  • Maier R M, Neckermann K, Igloi G L, Kössel H. 1995. Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. Journal of Molecular Biology, 251(5): 614–628.

    Article  Google Scholar 

  • Matsubayashi T, Wakasugi T, Shinozaki K, Yamaguchi-Shinozaki K, Zaita N, Hidaka T, Meng B Y, Ohto C, Tanaka M, Kato A, Maruyama T, Sugiura M. 1987. Six chloroplast genes (ndhA-F) homologous to human mitochondrial genes encoding components of the respiratory chain NADH dehydrogenase are actively expressed: determination of the splice sites in ndhA and ndhB pre-mRNAs. Molecular and General Genetics MGG, 210(3): 385–393.

    Article  Google Scholar 

  • Munekage Y, Hashimoto M, Miyake C, Tomizawa K I, Endo T, Tasaka M, Shikanai T. 2004. Cyclic electron flow around photosystem I is essential for photosynthesis. Nature, 429(6991): 579–582.

    Article  Google Scholar 

  • Ogawa T. 1991. A gene homologous to the subunit-2 gene of NADH dehydrogenase is essential to inorganic carbon transport of Synechocystis PCC6803. Proceedings of the National Academy of Sciences of the United States of America, 88(10): 4275–4279.

    Article  Google Scholar 

  • Ohyama K, Fukuzawa H, Kohchi T, Shirai H, Sano T, Sano S, Umesono K, Shiki Y, Takeuchi M, Chang Z, Aota S I, Inokuchi H, Ozeki H. 1986. Chloroplast gene organization deduced from complete sequence of liverwort Marchantia polymorpha chloroplast DNA. Nature, 322(6079): 572–574.

    Article  Google Scholar 

  • Okegawa Y, Kagawa Y, Kobayashi Y, Shikanai T. 2008. Characterization of factors affecting the activity of photosystem I Cyclic electron transport in chloroplasts. Plant and Cell Physiology, 49(5): 825–834.

    Article  Google Scholar 

  • Olsen J L, Rouzé P, Verhelst B, Lin Y C, Bayer T, Collen J, Dattolo E, De Paoli E, Dittami S, Maumus F, Michel G, Kersting A, Lauritano C, Lohaus R, Töpel M, Tonon T, Vanneste K, Amirebrahimi M, Brakel J, Boström C, Chovatia M, Grimwood J, Jenkins J W, Jueterbock A, Mraz A, Stam W T, Tice H, Bornberg-Bauer E, Green P J, Pearson G A, Procaccini G, Duarte C M, Schmutz J, Reusch T B H, Van De Peer Y. 2016. The genome of the seagrass Zostera marina reveals angiosperm adaptation to the sea. Nature, 530(7590): 331–335.

    Article  Google Scholar 

  • Pan X W, Cao D F, Xie F, Xu F, Su X D, Mi H L, Zhang X Z, Li M. 2020. Structural basis for electron transport mechanism of complex I-like photosynthetic NAD(P)H dehydrogenase. Nature Communications, 11(1): 610.

    Article  Google Scholar 

  • Peltier G, Cournac L. 2002. Chlororespiration. Annual Review of Plant Biology, 53: 523–550.

    Article  Google Scholar 

  • Peng L W, Yamamoto H, Shikanai T. 2011. Structure and biogenesis of the chloroplast NAD(P)H dehydrogenase complex. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1807(8): 945–953.

    Article  Google Scholar 

  • Peredo E L, King U M, Les D H. 2013. The plastid genome of Najas flexilis: adaptation to submersed environments is accompanied by the complete loss of the NDH complex in an aquatic angiosperm. PLoS One, 8(7): e68591.

    Article  Google Scholar 

  • Qiao X, Li Q H, Yin H, Qi K J, Li L T, Wang R Z, Zhang S L, Paterson A H. 2019. Gene duplication and evolution in recurring polyploidization-diploidization cycles in plants. Genome Biology, 20(1): 38.

    Article  Google Scholar 

  • Reddy A S N, Marquez Y, Kalyna M, Barta A. 2013. Complexity of the alternative splicing landscape in plants. The Plant Cell, 25(10): 3657–3683.

    Article  Google Scholar 

  • Robert X, Gouet P. 2014. Deciphering key features in protein structures with the new ENDscript server. Nucleic Acids Research, 42(1): 320–324.

    Article  Google Scholar 

  • Romano P, Gray J, Horton P, Luan S. 2005. Plant immunophilins: functional versatility beyond protein maturation. New Phytologist, 166(3): 753–769.

    Article  Google Scholar 

  • Ruhlman T A, Chang W J, Chen J J W, Huang Y T, Chan M T, Zhang J, Liao D C, Blazier J C, Jin X H, Shih M C, Jansen R K, Lin C S. 2015. NDH expression marks major transitions in plant evolution and reveals coordinate intracellular gene loss. BMC Plant Biology, 15(1): 100.

    Article  Google Scholar 

  • Rumeau D, Becuwe-Linka N, Beyly A, Louwagie M, Garin J, Peltier G. 2005. New subunits NDH-M, -N, and-O, encoded by nuclear genes, are essential for plastid NDH complex functioning in higher plants. The Plant Cell, 17(1): 219–232.

    Article  Google Scholar 

  • Schubert N, Colombo-Pallota M F, Enríquez S. 2015. Leaf and canopy scale characterization of the photoprotective response to high-light stress of the seagrass Thalassia testudinum. Limnologyand Oceanography, 60(1): 286–302.

    Article  Google Scholar 

  • Shikanai T. 2007. Cyclic electron transport around photosystem I: genetic approaches. Annual Review of Plant Biology, 58: 199–217.

    Article  Google Scholar 

  • Shikanai T. 2016. Chloroplast NDH: a different enzyme with a structure similar to that of respiratory NADH dehydrogenase. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1857(7): 1015–1022.

    Article  Google Scholar 

  • Shikanai T, Endo T, Hashimoto T, Yamada Y, Asada K, Yokota A. 1998. Directed disruption of the tobacco ndhB gene impairs cyclic electron flow around photosystem I. Proceedings of the National Academy of Sciences of the United States of America, 95(16): 9705–9709.

    Article  Google Scholar 

  • Shimizu H, Peng L W, Myouga F, Motohashi R, Shinozaki K, Shikanai T. 2008. CRR23/NdhL is a subunit of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant and Cell Physiology, 49(5): 835–842.

    Article  Google Scholar 

  • Shinozaki K, Ohme M, Tanaka M, Wakasugi T, Hayshida N, Matsubayasha T, Zaita N, Chunwongse J, Obokata J, Yamaguchi-Shinozaki K, Ohto C, Torazawa K, Meng B Y, Sugita M, Deno H, Kamogashira T, Yamada K, Kusuda J, Takaiwa F, Kata A, Tohdoh N, Shimada H, Sugiura M. 1986. The complete nucleotide sequence of the tobacco chloroplast genome. Plant Molecular Biology Reporter, 4(3): 111–148.

    Article  Google Scholar 

  • Sirpiö S, Holmström M, Battchikova N, Aro E M. 2009. AtCYP20-2 is an auxiliary protein of the chloroplast NAD(P)H dehydrogenase complex. FEBS Letters, 583(14): 2355–2358.

    Article  Google Scholar 

  • Staudt A C, Wenkel S. 2011. Regulation of protein function by ‘microProteins’. EMBO Reports, 12(1): 35–42.

    Article  Google Scholar 

  • Suorsa M, Sirpiö S, Aro E M. 2009. Towards characterization of the chloroplast NAD(P)H dehydrogenase complex. Molecular Plant, 2(6): 1127–1140.

    Article  Google Scholar 

  • Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S. 2011. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution, 28(10): 2731–2739.

    Article  Google Scholar 

  • Tan Y, Zhang Q S, Zhao W, Liu Z, Ma M Y, Zhong M Y, Wang M X. 2020a. The highly efficient NDH-dependent photosystem I cyclic electron flow pathway in the marine angiosperm Zostera marina. Photosynthesis Research, 144(1): 49–62.

    Article  Google Scholar 

  • Tan Y, Zhang Q S, Zhao W, Liu Z, Ma M Y, Zhong M Y, Wang M X, Xu B. 2020b. Chlororespiration serves as photoprotection for the photo-inactivated oxygen-evolving complex in Zostera marina, a marine angiosperm. Plant and Cell Physiology, 61(8): 1517–1529.

    Article  Google Scholar 

  • Tillich M, Funk H T, Schmitz-Linneweber C, Poltnigg P, Sabater B, Martin M, Maier R M. 2005. Editing of plastid RNA in Arabidopsis thaliana ecotypes. The Plant Journal, 43(5): 708–715.

    Article  Google Scholar 

  • Turmel M, Otis C, Lemieux C. 1999. The complete chloroplast DNA sequence of the green alga Nephroselmis olivacea: insights into the architecture of ancestral chloroplast genomes. Proceedings of the National Academy of Sciences of the United States of America, 96(18): 10248–10253.

    Article  Google Scholar 

  • Ueda M, Kuniyoshi T, Yamamoto H, Sugimoto K, Ishizaki K, Kohchi T, Nishimura Y, Shikanai T. 2012. Composition and physiological function of the chloroplast NADH dehydrogenase-like complex in Marchantia polymorpha. The Plant Journal: for Cell and Molecular Biology, 72(4): 683–693.

    Article  Google Scholar 

  • Uthaipaisanwong P, Chanprasert J, Shearman J R, Sangsrakru D, Yoocha T, Jomchai N, Jantasuriyarat C, Tragoonrung S, Tangphatsornruang S. 2012. Characterization of the chloroplast genome sequence of oil palm (Elaeis guineensis Jacq.). Gene, 500(2): 172–180.

    Article  Google Scholar 

  • Wang P, Ye J Y, Shen Y G, Mi H L. 2006. The role of chloroplast NAD(P)H dehydrogenase in protection of tobacco plant against heat stress. Science in China Series C: Life Sciences, 49(4): 311–321.

    Article  Google Scholar 

  • Wang W, Zhang W, Wu Y, Maliga P, Messing J. 2015. RNA Editing in chloroplasts of Spirodela polyrhiza, an aquatic monocotelydonous species. PLoS One, 10(10): e0140285.

    Article  Google Scholar 

  • Waycott M, Duarte C M, Carruthers T J B, Orth R J, Dennison W C, Olyarnik S, Calladine A, Fourqurean J W, Heck K L J, Hughes A R, Kendrick G A, Kenworthy W J, Short F T, Williams S L. 2009. Accelerating loss of seagrasses across the globe threatens coastal ecosystems. Proceedings of the National Academy of Sciences of the United States of America, 106(30): 12377–12381.

    Article  Google Scholar 

  • Weng M L, Blazier J C, Govindu M, Jansen R K. 2014. Reconstruction of the ancestral plastid genome in Geraniaceae reveals a correlation between genome rearrangements, repeats, and nucleotide substitution rates. Molecular Biology and Evolution, 31(3): 645–659.

    Article  Google Scholar 

  • Wu C S, Wang Y N, Liu S M, Chaw S M. 2007. Chloroplast genome (cpDNA) of Cycas taitungensis and 56 cp protein-coding genes of Gnetum parvifolium: insights into cpDNA evolution and phylogeny of extant seed plants. Molecular Biology and Evolution, 24(6): 1366–1379.

    Article  Google Scholar 

  • Xing Q K, Guo J. 2018. Characterization of the complete chloroplast genome of the seagrass Zostera marina using Illumina sequencing technology. Conservation Genetics Resources, 10(3): 419–422.

    Article  Google Scholar 

  • Xiong A S, Peng R H, Zhuang J, Gao F, Zhu B, Fu X Y, Xue Y, Jin X F, Tian Y S, Zhao W, Yao Q H. 2009. Gene duplication, transfer, and evolution in the chloroplast genome. Biotechnology Advances, 27(4): 340–347.

    Article  Google Scholar 

  • Yang X Q, Zhang Q S, Zhang D, Sheng Z T. 2017. Light intensity dependent photosynthetic electron transport in eelgrass (Zostera marina L.). Plant Physiology and Biochemistry, 113: 168–176.

    Article  Google Scholar 

  • Zhang P P, Battchikova N, Paakkarinen V, Katoh H, Iwai M, Ikeuchi M, Pakrasi H B, Ogawa T, Aro E M. 2005. Isolation, subunit composition and interaction of the NDH-1 complexes from Thermosynechococcus elongatus BP-1. The Biochemical Journal, 390(2): 513–520.

    Article  Google Scholar 

  • Zhang Y Y, Li B B, Xu Y Y, Li H, Li S S, Zhang D J, Mao Z W, Guo S Y, Yang C H, Weng Y X, Chong K. 2013. The cyclophilin CYP20-2 modulates the conformation of brassinazole-resistant1, which binds the promoter of flowering locus D to regulate flowering in Arabidopsis. The Plant Cell, 25(7): 2504–2521.

    Article  Google Scholar 

  • Zhang Y Z, Ma J, Yang B X, Li R Y, Zhu W, Sun L L, Tian J K, Zhang L. 2014. The complete chloroplast genome sequence of Taxus chinensis var. mairei (Taxaceae): loss of an inverted repeat region and comparative analysis with related species. Gene, 540(2): 201–209.

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Ocean School, Yantai University, Yantai, 264005, China

    Mingyu Ma, Mingyu Zhong, Quansheng Zhang, Wei Zhao, Mengxin Wang, Chengying Luo & Bin Xu

Authors
  1. Mingyu Ma
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mingyu Zhong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Quansheng Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Wei Zhao
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mengxin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Chengying Luo
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Bin Xu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Quansheng Zhang.

Additional information

Supported by the National Natural Science Foundation of China (No.41376154) and the Yantai Municipal Key Research and Development Project (No. 2019XDHZ096)

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ma, M., Zhong, M., Zhang, Q. et al. A genome-wide analysis of the chloroplast NADH dehydrogenase-like genes in Zostera marina. J. Ocean. Limnol. 40, 656–677 (2022). https://doi.org/10.1007/s00343-021-0027-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00343-021-0027-z

Keyword

Search

Navigation