Skip to main content
SpringerLink
Log in

OsNDUFA9 encoding a mitochondrial complex I subunit is essential for embryo development and starch synthesis in rice

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Abstract

Key message

Loss of function of a mitochondrial complex I subunit (OsNDUFA9) causes abnormal embryo development and affects starch synthesis by altering the expression of starch synthesis-related genes and proteins.

Abstract

Proton-pumping NADH: ubiquinone oxidoreductase (also called complex I) is thought to be the largest and most complicated enzyme of the mitochondrial respiratory chain. Mutations of complex I subunits have been revealed to link with a number of growth inhibitions in plants. However, the function of complex I subunits in rice remains unclear. Here, we isolated a rice floury endosperm mutant (named flo13) that was embryonic lethal and failed to germinate. Semi-thin sectioning analysis showed that compound starch grain development in the mutant was greatly impaired, leading to significantly compromised starch biosynthesis and decreased 1000-grain weight relative to the wild type. Map-based cloning revealed that FLO13 encodes an accessory subunit of complex I protein (designated as OsNDUFA9). A single nucleotide substitution (G18A) occurred in the first exon of OsNDUFA9, introducing a premature stop codon in the flo13 mutant gene. OsNDUFA9 was ubiquitously expressed in various tissues and the OsNDUFA9 protein was localized to the mitochondria. Quantitative RT-PCR and protein blotting indicated loss of function of OsNDUFA9 altered gene expression and protein accumulation associated with respiratory electron chain complex in the mitochondria. Moreover, transmission electron microscopic analysis showed that the mutant lacked obvious mitochondrial cristae structure in the mitochondria of endosperm cell. Our results demonstrate that the OsNDUFA9 subunit of complex I is essential for embryo development and starch synthesis in rice endosperm.

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

Access this article

Log in via an institution

Price includes VAT (France)

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

AOX:

Alternative oxidase

DAF:

Days after flowering

dCAPS:

Derived cleaved amplified polymorphic sequence

EMS:

Ethyl methane sulfonate

ETC:

Electron transfer chain

GFP:

Green fluorescent protein

InDel:

Insertion–deletion

nad:

NADH dehydrogenase subunit

NDUFA9:

Mitochondrial NADH dehydrogenase [ubiquinone] 1 alpha subcomplex subunit 9

ORF:

Open reading frame

OXPHOS:

Oxidative phosphorylation

SEM:

Scanning electron microscope

TTC:

2,3,5-Triphenyltetrazolium chloride

TEM:

Transmission electron microscope

RT-PCR:

Real-time PCR

References

  • Abdrakhmanova A, Zwicker K, Kerscher S, Zickermann V, Brandt U (2006) Tight binding of NADPH to the 39-kDa subunit of complex I is not required for catalytic activity but stabilizes the multiprotein complex. Biochem Biophys Acta 1757:1676–1682

    CAS  PubMed  Google Scholar 

  • Ahn BH, Kim HS, Song S, Lee IH, Liu J, Vassilopoulos A, Deng CX, Finkel T (2008) A role for the mitochondrial deacetylase Sirt3 in regulating energy homeostasis. Proc Natl Acad Sci USA 105:14447–14452

    Article  CAS  Google Scholar 

  • Angerer H, Zwicker K, Wumaier Z, Sokolova L, Heide H, Steger M, Kaiser S, Nubel E, Brutschy B, Radermacher M, Brandt U, Zickermann V (2011) A scaffold of accessory subunits links the peripheral arm and the distal proton-pumping module of mitochondrial complex I. Biochem J 437:279–288

    Article  CAS  Google Scholar 

  • Babot M, Labarbuta P, Birch A, Kee S, Fuszard M, Botting CH, Wittig I, Heide H, Galkin A (2014) ND3, ND1 and 39 kDa subunits are more exposed in the de-active form of bovine mitochondrial complex I. Biochim Biophys Acta 1837(6):929–939

    Article  CAS  Google Scholar 

  • Baertling F, Sánchez-Caballero L, Van MA, Fung CW, Chan SH (2018a) NDUFA9 point mutations cause a variable mitochondrial complex I assembly defect. Clin Genet 93:111–118

    Article  CAS  Google Scholar 

  • Baertling F, Sánchez-Caballero L, van den Brand M, Distelmaier F, Janssen M, Rodenburg R, Smeitink J, Nijtmans L (2018b) A heterozygous NDUFV1 variant aggravates mitochondrial Complex I deficiency in a family with a homoplasmic ND1 variant. J Pediatr 196:309–313

    Article  CAS  Google Scholar 

  • Brangeon J, Sabar M, Gutierres S, Combettes B, Bove J, Gendy C, Chétrit P, Des Francs-Small CC, Pla M, Vedel F, De Paepe R (2000) Defective splicing of the first nad4 intron is associated with lack of several complex I subunits in the Nicotiana sylvestris NMS1 nuclear mutant. Plant J 21(3):269–280

    Article  CAS  Google Scholar 

  • Bridges HR, Fearnley IM, Hirst J (2010) The subunit composition of mitochondrial NADH: ubiquinone oxidoreductase (complex I) from Pichia pastoris. Mol Cell Proteomics 9(10):2318–2326

    Article  CAS  Google Scholar 

  • Cai M, Li S, Sun F, Sun Q, Zhao H, Ren X, Zhao Y, Tan BC, Zhang Z, Qiu F (2017) Emp10 encodes a mitochondrial PPR protein that affects the cis-splicing of nad2 intron 1 and seed development in maize. Plant J 91:132–144

    Article  CAS  Google Scholar 

  • Cardol P (2011) Mitochondrial NADH: ubiquinone oxidoreductase (complex I) in eukaryotes: a highly conserved subunit composition highlighted by mining of protein databases. Biochem Biophys Acta 1807:1390–1397

    CAS  PubMed  Google Scholar 

  • Chen S, Tao L, Zeng L, Vega-Sanchez ME, Umemura K, Wang GL (2006) A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice. Mol Plant Pathol 7:417–427

    Article  CAS  Google Scholar 

  • Chen X, Feng F, Qi W, Xu L, Yao D, Wang Q, Song R (2017) Dek35 encodes a PPR protein that affects cis-splicing of mitochondrial nad4 intron 1 and seed development in maize. Mol Plant 10:427–441

    Article  CAS  Google Scholar 

  • Chistiakov DA, Shkurat TP, Melnichenko AA, Grechko AV, Orekhov AN (2018) The role of mitochondrial dysfunction in cardiovascular disease: a brief review. Ann Med 50:121–127

    Article  CAS  Google Scholar 

  • Chiu W, Niwa Y, Zeng W, Hirano T, Kobayashi H, Sheen J (1996) Engineered GFP as a vital reporter in plants. Curr Biol 6:325–330

    Article  CAS  Google Scholar 

  • Ciano M, Fuszard M, Heide H, Botting CH, Galkin A (2013) Conformation-specific crosslinking of mitochondrial complex I. FEBS Lett 587:867–872

    Article  CAS  Google Scholar 

  • Cohen S, Zmudjak M, Colas Des Francs-Small C, Malik S, Shaya F, Keren I, Belausov E, Many Y, Brown GG, Small I, Ostersetzer-Biran O (2014) nMAT4, a maturase factor required for nad1 pre-mRNA processing and maturation, is essential for holocomplex I biogenesis in Arabidopsis mitochondria. Plant J 78:253–268

    Article  CAS  Google Scholar 

  • de Longevialle AF, Meyer EH, Andrés C, Taylor NL, Lurin C, Millar AH, Small ID (2007) The pentatricopeptide repeat gene OTP43 is required for trans-splicing of the mitochondrial nad1 Intron 1 in Arabidopsis thaliana. Plant Cell 19:3256–3265

    Article  Google Scholar 

  • Deng Y, Zou W, Li G, Zhao J (2014) TRANSLOCASE OF THE INNER MEMBRANE9 and 10 are essential for maintaining mitochondrial function during early embryo cell and endosperm free nucleus divisions in Arabidopsis. Plant Physiol 166:853–868

    Article  Google Scholar 

  • Dudkina NV, Heinemeyer J, Sunderhaus S, Boekema EJ, Braun HP (2006) Respiratory chain supercomplexes in the plant mitochondrial membrane. Trends Plant Sci 11:232–240

    Article  CAS  Google Scholar 

  • Galletti R, Ingram GC (2015) Communication is key: reducing DEK1 activity reveals a link between cell-cell contacts and epidermal cell differentiation status. Commun Integr Biol 8:e1059979

    Article  Google Scholar 

  • Gellerich FN, Trumbeckaite S, Muller T, Deschauer M, Chen Y, Gizatullina Z, Zierz S (2004) Energetic depression caused by mitochondrial dysfunction. Mol Cell Biochem 256–257(1–2):391–405

    Article  Google Scholar 

  • Gilkerson RW, Margineantu DH, Capaldi RA, Selker JM (2000) Mitochondrial DNA depletion causes morphological changes in the mitochondrial reticulum of cultured human cells. FEBS Lett 474:1–4

    Article  CAS  Google Scholar 

  • Gutierres S, Sabar M, Lelandais C, Chétrit P, Diolez P, Degand H, Boutry M, Vedel F, DeKouchkovsky Y, DePaepe R (1997) Lack of mitochondrial and nuclear-encoded subunits of complex I and alteration of the respiratory chain in Nicotiana sylvestris mitochondrial deletion mutants. Proc Natl Acad Sci USA 94:3436–3441

    Article  CAS  Google Scholar 

  • Gutierres S, Combettes B, De Paepe R, Mirande M, Lelandais C, Vedel F, Chétrit P (1999) In the Nicotiana sylvestris CMSII mutant, a recombination-mediated change 5′ to the first exon of the mitochondrial nad1 gene is associated with lack of the NADH: ubiquinone oxidoreductase (complex I) NAD1 subunit. Eur J Biochem 261:361–370

    Article  CAS  Google Scholar 

  • Hammani K, des Francs-Small CC, Takenaka M, Tanz SK, Okuda K, Shikanai T, Brennicke A, Small I (2011) The pentatricopeptide repeat protein OTP87 is essential for RNA editing of nad7 and atp1 transcripts in Arabidopsis mitochondria. J Biol Chem 286:21361–21371

    Article  CAS  Google Scholar 

  • Han X, Wang Y, Liu X, Jiang L, Ren Y, Liu F, Peng C, Li J, Jin X, Wu F, Wang J, Guo X, Zhang X, Cheng Z, Wan J (2012) The failure to express a protein disulphide isomerase-like protein results in a floury endosperm and an endoplasmic reticulum stress response in rice. J Exp Bot 63:121–130

    Article  CAS  Google Scholar 

  • Heazlewood JL (2004) Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 16:241–256

    Article  CAS  Google Scholar 

  • Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6:271–282

    Article  CAS  Google Scholar 

  • Hsieh W, Liao J, Chang C, Harrison T, Boucher C, Hsieh M (2015) The SLOW GROWTH3 pentatricopeptide repeat protein is required for the splicing of mitochondrial NADH Dehydrogenase Subunit7 intron 2 in Arabidopsis. Plant Physiol 168:490–501

    Article  CAS  Google Scholar 

  • Kang H, Park S, Matsuoka M, An G (2005) White-core endosperm floury endosperm-4 in rice is generated by knockout mutations in the C4-type pyruvate orthophosphate dikinase gene (OsPPDKB). Plant J 42:901–911

    Article  CAS  Google Scholar 

  • Karpova OV, Newton KJ (1999) A partially assembled complex I in NAD4-deficient mitochondria of maize. Plant J 17:511–521

    Article  CAS  Google Scholar 

  • Keren I, Bezawork-Geleta A, Kolton M, Maayan I, Belausov E, Levy M, Mett A, Gidoni D, Shaya F, Ostersetzer-Biran O (2009) AtnMat2, a nuclear-encoded maturase required for splicing of group-II introns in Arabidopsis mitochondria. RNA 15:2299–2311

    Article  CAS  Google Scholar 

  • Keren I, Tal L, des Francs-Small CC, Araújo WL, Shevtsov S, Shaya F, Fernie AR, Small I, Ostersetzer-Biran O (2012) nMAT1, a nuclear-encoded maturase involved in the trans-splicing of nad1 intron 1, is essential for mitochondrial complex I assembly and function. Plant J 71:413–426

    CAS  PubMed  Google Scholar 

  • Kmita K, Zickermann V (2013) Accessory subunits of mitochondrial complex I. Biochem Soc Trans 41:1272–1279

    Article  CAS  Google Scholar 

  • Kühn K, Obata T, Feher K, Bock R, Fernie AR, Meyer EH (2015) Complete mitochondrial complex I deficiency induces an up-regulation of respiratory fluxes that is abolished by traces of functional complex I. Plant Physiol 168:1537–1549

    Article  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    Article  CAS  Google Scholar 

  • Lazarou M, Thorburn DR, Ryan MT, McKenzie M (2009) Assembly of mitochondrial complex I and defects in disease. Biochim Biophys Acta 1793:78–88

    Article  CAS  Google Scholar 

  • Li X, Zhang Y, Hou M, Sun F, Shen Y, Xiu Z, Wang X, Chen Z, Sun SSM, Small I, Tan B (2014) Small kernel 1 encodes a pentatricopeptide repeat protein required for mitochondrial nad7 transcript editing and seed development in maize (Zea mays) and rice (Oryza sativa). Plant J 79:797–809

    Article  CAS  Google Scholar 

  • Liu YJ, Xiu ZH, Meeley R, Tan BC (2013) Empty pericarp5 encodes a pentatricopeptide repeat protein that is required for mitochondrial RNA editing and seed development in maize. Plant Cell 25:868–883

    Article  CAS  Google Scholar 

  • Logan DC (2006) The mitochondrial compartment. J Exp Bot 57:1225–1243

    Article  CAS  Google Scholar 

  • Mannella CA, Lederer WJ, Jafri MS (2013) The connection between inner membrane topology and mitochondrial function. J Mol Cell Cardiol 62:51–57

    Article  CAS  Google Scholar 

  • Marienfeld JR, Newton KJ (1994) The maize NCS2 abnormal growth mutant has a chimeric nad4-nad7 mitochondrial gene and is associated with reduced complex I function. Genetics 138:855–863

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meyer EH, Tomaz T, Carroll AJ, Estavillo G, Delannoy E, Tanz SK, Small ID, Pogson BJ, Millar AH (2009) Remodeled respiration in ndufs4 with low phosphorylation efficiency suppresses Arabidopsis germination and growth and alters control of metabolism at night. Plant Physiol 151:603–619

    Article  CAS  Google Scholar 

  • Nakagawa N, Sakurai N (2006) A mutation in At-nMat1a, which encodes a nuclear gene having high similarity to group II intron maturase, causes impaired splicing of mitochondrial NAD4 transcript and altered carbon metabolism in Arabidopsis thaliana. Plant Cell Physiol 47:772–783

    Article  CAS  Google Scholar 

  • Ortigoza-Escobar JD, Oyarzabal A, Montero R, Artuch R, Jou C, Jiménez C, Gort L, Briones P, Muchart J, López-Gallardo E, Emperador S, Pesini ER, Montoya J, Pérez B, Rodríguez-Pombo P, Pérez-Dueñas B (2016) Ndufs4 related Leigh syndrome: a case report and review of the literature. Mitochondrion 28:73–78

    Article  CAS  Google Scholar 

  • Peng C, Wang Y, Liu F, Ren Y, Zhou K, Lv J, Zheng M, Zhao S, Zhang L, Wang C, Jiang L, Zhang X, Guo X, Bao Y, Wan J (2014) FLOURY ENDOSPERM6 encodes a CBM48 domain-containing protein involved in compound granule formation and starch synthesis in rice endosperm. Plant J 77:917–930

    Article  CAS  Google Scholar 

  • Pineau B, Mathieu C, Gérard-Hirne C, De Paepe R, Chétrit P (2005) Targeting the NAD7 subunit to mitochondria restores a functional complex I and a wild type phenotype in the Nicotiana sylvestris CMSII mutant lacking nad. J Biol Chem 280:25994–26001

    Article  CAS  Google Scholar 

  • Pla M, Mathieu C, De Paepe R, Chétrit P, Vedel F (1995) Deletion of the last two exons of the mitochondrial nad7 gene results in lack of the NAD7 polypeptide in a Nicotiana sylvestris CMS mutant. Mol Gen Genet 248:79–88

    Article  CAS  Google Scholar 

  • Sabar M, De Paepe R, de Kouchkovsky Y (2000) Complex I impairment, respiratory compensations, and photosynthetic decrease in nuclear and mitochondrial male sterile mutants of Nicotiana sylvestris. Plant Physiol 124:1239–1250

    Article  CAS  Google Scholar 

  • Siedow JN, Umbach AL (2000) The mitochondrial cyanide-resistant oxidase: structural conservation amid regulatory diversity. Biochim Biophys Acta 1459:432–439

    Article  CAS  Google Scholar 

  • Sofou K, de Coo I, Ostergaard E, Isohanni P, Naess K, De Meirleir L, Tzoulis C, Uusimaa J, Lonnqvist T, Bindoff LA, Tulinius M, Darin N (2018) Phenotype-genotype correlations in Leigh syndrome: new insights from a multicentre study of 96 patients. J Med Genet 55:21–27

    Article  Google Scholar 

  • Sosso D, Mbelo S, Vernoud V, Gendrot G, Dedieu A, Chambrier P, Dauzat M, Heurtevin L, Guyon V, Takenaka M, Rogowsky PM (2012) PPR2263, a DYW-subgroup pentatricopeptide repeat protein, is required for mitochondrial nad5 and cob transcript editing, mitochondrion biogenesis, and maize growth. Plant Cell 24:676–691

    Article  CAS  Google Scholar 

  • Stroud DA, Surgenor EE, Formosa LE, Reljic B, Frazier AE, Dibley MG, Osellame LD, Stait T, Beilharz TH, Thorburn DR, Salim A, Ryan MT (2016) Accessory subunits are integral for assembly and function of human mitochondrial complex I. Nature 538:123–126

    Article  CAS  Google Scholar 

  • Toda T, Fujii S, Noguchi K, Kazama T, Toriyama K (2012) Rice MPR25 encodes a pentatricopeptide repeat protein and is essential for RNA editing of nad5 transcripts in mitochondria. Plant J 72:450–460

    Article  CAS  Google Scholar 

  • Towill LE, Mazur P (1975) Studies on the reduction of 2,3,5-triphenyl-tetrazolium chloride as a viability assay for plant tissue cultures. Can J Bot 53:1097–1102

    Article  Google Scholar 

  • Ugalde C, Vogel R, Huijbens R, Van Den Heuvel B, Smeitink J, Nijtmans L (2004) Human mitochondrial complex I assembles through the combination of evolutionary conserved modules: a framework to interpret complex I deficiencies. Hum Mol Genet 13:2461–2472

    Article  CAS  Google Scholar 

  • Vandecasteele G, Szabadkai G, Rizzuto R (2001) Mitochondrial calcium homeostasis: mechanisms and molecules. IUBMB life 52:213–219

    Article  CAS  Google Scholar 

  • Vanlerberghe G (2013) Alternative oxidase: a mitochondrial respiratory pathway to maintain metabolic and signaling homeostasis during abiotic and biotic stress in plants. Int J Mol Sci 14:6805–6847

    Article  CAS  Google Scholar 

  • Wang Y, Wang C, Zheng M, Lyu J, Xu Y, Li X, Niu M, Long W, Wang D, Wang H, Terzaghi W, Wang Y, Wan J (2016) WHITE PANICLE1, a Val-tRNA synthetase regulating chloroplast ribosome biogenesis in rice, is essential for early chloroplast development. Plant Physiol 170:2110–2123

    Article  CAS  Google Scholar 

  • Wirth C, Brandt U, Hunte C, Zickermann V (2016) Structure and function of mitochondrial complex I. Biochem Biophys Acta 1857:902–914

    CAS  PubMed  Google Scholar 

  • Wu JJ, Peng XB, Li WW, He R, Xin HP, Sun MX (2012) Mitochondrial GCD1 dysfunction reveals reciprocal cell-to-cell signaling during the maturation of Arabidopsis female gametes. Dev Cell 23:1043–1058

    Article  CAS  Google Scholar 

  • Wydro MM, Sharma P, Foster JM, Bych K, Meyer EH, Balk J (2013) The evolutionarily conserved iron-sulfur protein INDH is required for complex I assembly and mitochondrial translation in Arabidopsis. Plant Cell 25:4014–4027

    Article  CAS  Google Scholar 

  • Xiu Z, Sun F, Shen Y, Zhang X, Jiang R, Bonnard G, Zhang J, Tan BC (2016) EMPTY PERICARP16 is required for mitochondrial nad2 intron 4 cis-splicing, complex I assembly and seed development in maize. Plant J 85:507–519

    Article  CAS  Google Scholar 

  • Yang Y, Ding S, Wang H, Sun F, Huang W, Song S, Xu C, Tan B (2017) The pentatricopeptide repeat protein EMP9 is required for mitochondrial ccmB and rps4 transcript editing, mitochondrial complex biogenesis and seed development in maize. New Phytol 214:782–795

    Article  CAS  Google Scholar 

  • Youle RJ, Karbowski M (2005) Mitochondrial fission in apoptosis. Nat Rev Mol Cell Biol 6:657–663

    Article  CAS  Google Scholar 

  • Zhang L, Ren Y, Lu B et al (2016) FLOURY ENDOSPERM7 encodes a regulator of starch synthesis and amyloplast development essential for peripheral endosperm development in rice. J Exp Bot 67(3):633–647

    Article  CAS  Google Scholar 

Download references

Acknowledgements

This research was supported by the Key Laboratory of Biology, Genetics and Breeding of Japonica Rice in Mid-lower Yangtze River, Ministry of Agriculture of China, The Yangtze River Valley Hybrid Rice Collaboration Innovation Center, Jiangsu Collaborative Innovation Center for Modern Crop Production, and the grants from The National Key Research and Development Program of China (2017YFD0100400), a project (2016ZX08001006) from the Ministry of Agriculture of China for transgenic research, Jiangsu Science and Technology Development Program (BE2015355-1), and Jiangsu Province Self-Innovation Program [CX(16)1029]. This work was also supported by the Fundamental Research Funds for the Central Universities (KYTZ201601).

Author information

Author notes

  1. Tingting Hu and Yunlu Tian contributed equally to this work.

Authors and Affiliations

  1. State Key Laboratory of Crop Genetics and Germplasm Enhancement, Jiangsu Plant Gene Engineering Research Center, Nanjing Agricultural University, Nanjing, 210095, China

    Tingting Hu, Yunlu Tian, Jianping Zhu, Yunlong Wang, Ruonan Jing, Jie Lei, Yinglun Sun, Yanfang Yu, Jingfang Li, Xiaoli Chen, Xiaopin Zhu, Yuanyuan Hao, Linglong Liu, Yihua Wang & Jianmin Wan

  2. National Key Facility for Crop Gene Resources and Genetic Improvement, Institute of Crop Science, Chinese Academy of Agricultural Sciences, Beijing, 100081, China

    Jianmin Wan

  3. Xuzhou Institute of Agricultural Sciences in Jiangsu Xuhuai Area, Xuzhou, 221131, China

    Tingting Hu

Authors
  1. Tingting Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Yunlu Tian
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Jianping Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yunlong Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Ruonan Jing
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Jie Lei
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Yinglun Sun
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Yanfang Yu
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Jingfang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Xiaoli Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Xiaopin Zhu
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Yuanyuan Hao
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Linglong Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Yihua Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Jianmin Wan
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Yihua Wang or Jianmin Wan.

Ethics declarations

Conflict of interest

These authors declare that they have no conflict of interest.

Additional information

Communicated by Kang Chong.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOCX 1151 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hu, T., Tian, Y., Zhu, J. et al. OsNDUFA9 encoding a mitochondrial complex I subunit is essential for embryo development and starch synthesis in rice. Plant Cell Rep 37, 1667–1679 (2018). https://doi.org/10.1007/s00299-018-2338-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-018-2338-x

Keywords

Search

Navigation