Skip to main content
SpringerLink
Log in

Functional analysis for domains of maize PPR protein EMP5 in RNA editing and plant development in Arabidopsis

  • Original paper
  • Published:
Plant Growth Regulation Aims and scope Submit manuscript

Abstract

EMP5 and OTP72 are PPR proteins involved in mitochondrial same site RNA editing of rpl16 in maize and Arabidopsis, respectively. Besides rpl16, EMP5 also affects the editing efficiency of some editing sites in other mitochondrial transcripts. Loss of function of EMP5 causes arrested embryogenesis and endosperm development in maize, but no discernable defective phenotype is observed in Arabidopsis otp72 mutant plants. We here report that EMP5 can completely complement Arabidopsis otp72 for Ararpl16-440 editing, and E domain can’t be disrupted for normal function of EMP5. An interesting finding was that overexpression of a set of truncated EMP5s in Col-0 resulted in delayed bolting phenotypes and smaller plants. It seems some truncated EMP5s, such as EMP5-C and EMP5-D, have yet unknown functions, are not responsible for Ararpl16-440 editing any more. The phylogenetic analysis indicated that the functions of most EMP5 orthologs may be conserved, but EMP5 ortholog proteins from Nicotiana and Solanum can’t be found, and the C to U editing of Zmrpl16-458 site was not needed any more in the two species. Therefore, these two primary orthologs maybe already evolve new functions and change to different new proteins during evolutionary history. Overall, our studies revealed that E domain is crucial for mitochondrial RNA editing function of EMP5, and a set of truncated EMP5s still have functions for Arabidopsis normal growth and development, providing new insights into investigating the functions of EMP5 protein.

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.

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

Similar content being viewed by others

References

  • Barkan A, Small I (2014) Pentatricopeptide repeat proteins in plants. Annu Rev Plant Biol 65:415–442

    Article  CAS  PubMed  Google Scholar 

  • Bentolila S, Heller WP, Sun T, Babina AM, Friso G, van Wijk KJ, Hanson MR (2012) RIP1, a member of an Arabidopsis protein family, interacts with the protein RARE1 and broadly affects RNA editing. Proc Natl Acad Sci USA 109:E1453–E1461

    Article  PubMed  PubMed Central  Google Scholar 

  • Boussardon C, Avon A, Kindgren P, Bond CS, Challenor M, Lurin C, Small I (2014) The cytidine deaminase signature HxE(x)(n)CxxC of DYW1 binds zinc and is necessary for RNA editing of ndhD-1. New Phytol 203:1090–1095

    Article  CAS  PubMed  Google Scholar 

  • Chateigner-Boutin AL, Small I (2010) Plant RNA editing. RNA Biol 7:213–219

    Article  CAS  PubMed  Google Scholar 

  • Chateigner-Boutin AL, Colas des Francs-Small C, Fujii S, Okuda K, Tanz SK, Small I (2013) The E domains of pentatricopeptide repeat proteins from different organelles are not functionally equivalent for RNA editing. Plant J 74:935–945

    Article  CAS  PubMed  Google Scholar 

  • Cheng SF, Gutmann B, Zhong X, Ye YT, Fisher MF, Bai FQ, Castleden I, Song Y, Song B, Huang JY, Liu X, Xu X, Lim BL, Bond CS, Yiu SM, Small I (2016) Redefining the structural motifs that determine RNA binding and RNA editing by pentatricopeptide repeat proteins in land plants. Plant J 85:532–547

    Article  CAS  PubMed  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • de Longevialle AF, Meyer EH, Andres 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Fujii S, Small I (2011) The evolution of RNA editing and pentatricopeptide repeat genes. New Phytol 191:37–47

    Article  CAS  PubMed  Google Scholar 

  • Giege P, Brennicke A (1999) RNA editing in Arabidopsis mitochondria effects 441 C to U changes in ORFs. Proc Natl Acad Sci USA 96:15324–15329

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Glass F, Hartel B, Zehrmann A, Verbitskiy D, Takenaka M (2015) MEF13 requires MORF3 and MORF8 for RNA editing at eight targets in mitochondrial mRNAs in Arabidopsis thaliana. Mol Plant 8:1466–1477

    Article  CAS  PubMed  Google Scholar 

  • Gomez-Casati DF, Busi MV, Gonzalez-Schain N, Mouras A, Zabaleta EJ, Araya A (2002) A mitochondrial dysfunction induces the expression of nuclear-encoded complex I genes in engineered male sterile Arabidopsis thaliana. FEBS Lett 532:70–74

    Article  CAS  PubMed  Google Scholar 

  • Gray MW, Burger G, Lang BF (2001) The origin and early evolution of mitochondria. Genome Biol 2:REVIEWS1018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grennan AK (2011) To thy proteins be true: RNA editing in plants. Plant Physiol 156:453–454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Haag S, Schindler M, Berndt L, Brennicke A, Takenaka M, Weber G (2017) Crystal structures of the Arabidopsis thaliana organellar RNA editing factors MORF1 and MORF9. Nucleic Acids Res 45:4915–4928

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jia F, Wan X, Zhu W, Sun D, Zheng C, Liu P, Huang J (2015) Overexpression of mitochondrial phosphate transporter 3 severely hampers plant development through regulating mitochondrial function in Arabidopsis. PLoS ONE 10:e0129717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kuhn K, Carrie C, Giraud E, Wang Y, Meyer EH, Narsai R, des Francs-Small CC, Zhang B, Murcha MW, Whelan J (2011) The RCC1 family protein RUG3 is required for splicing of nad2 and complex I biogenesis in mitochondria of Arabidopsis thaliana. Plant J 67:1067–1080

    Article  CAS  PubMed  Google Scholar 

  • Kuhn 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  CAS  PubMed  PubMed Central  Google Scholar 

  • Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23:2947–2948

    Article  CAS  PubMed  Google Scholar 

  • Li LG, Sokolov LN, Yang YH, Li DP, Ting J, Pandy GK, Luan S (2008) A mitochondrial magnesium transporter functions in Arabidopsis pollen development. Mol Plant 1:675–685

    Article  CAS  PubMed  Google Scholar 

  • Liu ZC, Butow RA (2006) Mitochondrial retrograde signaling. Annu Rev Genet 40:159–185

    Article  CAS  PubMed  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  PubMed  PubMed Central  Google Scholar 

  • Lurin C, Andres C, Aubourg S, Bellaoui M, Bitton F, Bruyere C, Caboche M, Debast C, Gualberto J, Hoffmann B, Lecharny A, Le Ret M, Martin-Magniette ML, Mireau H, Peeters N, Renou JP, Szurek B, Taconnat L, Small I (2004) Genome-wide analysis of Arabidopsis pentatricopeptide repeat proteins reveals their essential role in organelle biogenesis. Plant Cell 16:2089–2103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Marechal A, Parent JS, Sabar M, Veronneau-Lafortune F, Abou-Rached C, Brisson N (2008) Overexpression of mtDNA-associated AtWhy2 compromises mitochondrial function. BMC Plant Biol 8:42

    Article  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  PubMed  PubMed Central  Google Scholar 

  • Meyer EH, Solheim C, Tanz SK, Bonnard G, Millar AH (2011) Insights into the composition and assembly of the membrane arm of plant complex I through analysis of subcomplexes in Arabidopsis mutant lines. J Biol Chem 286:26081–26092

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura T, Sugita M (2008) A conserved DYW domain of the pentatricopeptide repeat protein possesses a novel endoribonuclease activity. FEBS Lett 582:4163–4168

    Article  CAS  PubMed  Google Scholar 

  • O’Toole N, Hattori M, Andres C, Iida K, Lurin C, Schmitz-Linneweber C, Sugita M, Small I (2008) On the expansion of the pentatricopeptide repeat gene family in plants. Mol Biol Evol 25:1120–1128

    Article  CAS  PubMed  Google Scholar 

  • Okuda K, Myouga F, Motohashi R, Shinozaki K, Shikanai T (2007) Conserved domain structure of pentatricopeptide repeat proteins involved in chloroplast RNA editing. Proc Natl Acad Sci USA 104:8178–8183

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okuda K, Chateigner-Boutin AL, Nakamura T, Delannoy E, Sugita M, Myouga F, Motohashi R, Shinozaki K, Small I, Shikanai T (2009) Pentatricopeptide repeat proteins with the DYW motif have distinct molecular functions in RNA editing and RNA cleavage in Arabidopsis chloroplasts. Plant Cell 21:146–156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Okuda K, Hammani K, Tanz SK, Peng L, Fukao Y, Myouga F, Motohashi R, Shinozaki K, Small I, Shikanai T (2010) The pentatricopeptide repeat protein OTP82 is required for RNA editing of plastid ndhB and ndhG transcripts. Plant J 61:339–349

    Article  CAS  PubMed  Google Scholar 

  • Ramos-Vega M, Guevara-Garcia A, Llamas E, Sanchez-Leon N, Olmedo-Monfil V, Vielle-Calzada JP, Leon P (2015) Functional analysis of the Arabidopsis thaliana CHLOROPLAST BIOGENESIS 19 pentatricopeptide repeat editing protein. New Phytol 208:430–441

    Article  CAS  PubMed  Google Scholar 

  • Salone V, Rudinger M, Polsakiewicz M, Hoffmann B, Groth-Malonek M, Szurek B, Small I, Knoop V, Lurin C (2007) A hypothesis on the identification of the editing enzyme in plant organelles. FEBS Lett 581:4132–4138

    Article  CAS  PubMed  Google Scholar 

  • Schmitz-Linneweber C, Small I (2008) Pentatricopeptide repeat proteins: a socket set for organelle gene expression. Trends Plant Sci 13:663–670

    Article  CAS  PubMed  Google Scholar 

  • Shikanai T (2006) RNA editing in plant organelles: machinery, physiological function and evolution. Cell Mol Life Sci 63:698–708

    Article  CAS  PubMed  Google Scholar 

  • Takenaka M (2010) MEF9, an E-subclass pentatricopeptide repeat protein, is required for an RNA editing event in the nad7 transcript in mitochondria of Arabidopsis. Plant Physiol 152:939–947

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Takenaka M, Zehrmann A, Verbitskiy D, Kugelmann M, Hartel B, Brennicke A (2012) Multiple organellar RNA editing factor (MORF) family proteins are required for RNA editing in mitochondria and plastids of plants. Proc Natl Acad Sci USA 109:10606–10606

    Article  Google Scholar 

  • Tamura K, Stecher G, Peterson D, Filipski A, Kumar S (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Mol Biol Evol 30:2725–2729

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Verbitskiy D, van der Merwe JA, Zehrmann A, Hartel B, Takenaka M (2012) The E-class PPR protein MEF3 of Arabidopsis thaliana can also function in mitochondrial RNA editing with an additional DYW domain. Plant Cell Physiol 53:358–367

    Article  CAS  PubMed  Google Scholar 

  • Wagoner JA, Sun T, Lin L, Hanson MR (2015) Cytidine deaminase motifs within the DYW domain of two pentatricopeptide repeat-containing proteins are required for site-specific chloroplast RNA editing. J Biol Chem 290:2957–2968

    Article  CAS  PubMed  Google Scholar 

  • Wang XM, Chang N, Bi YR, Tan BC (2015) Measurement of mitochondrial respiration rate in maize (Zea mays) leaves. Bio Protoc 5(10):e1483

    Article  Google Scholar 

  • Wang Y, Yan J, Zhang Q, Ma X, Zhang J, Su M, Wang X, Huang Y (2017) The Schizosaccharomyces pombe PPR protein Ppr10 associates with a novel protein Mpa1 and acts as a mitochondrial translational activator. Nucleic Acids Res 45:3323–3340

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wu W, Liu S, Ruwe H, Zhang D, Melonek J, Zhu Y, Hu X, Gusewski S, Yin P, Small ID, Howell KA, Huang J (2016) SOT1, a pentatricopeptide repeat protein with a small MutS-related domain, is required for correct processing of plastid 23S-4.5S rRNA precursors in Arabidopsis thaliana. Plant J 85:607–621

    Article  CAS  PubMed  Google Scholar 

  • Xiao H, Zhang Q, Qin X, Xu Y, Ni C, Huang J, Zhu L, Zhong F, Liu W, Yao G, Zhu Y, Hu J (2018) Rice PPS1 encodes a DYW motif-containing pentatricopeptide repeat protein required for five consecutive RNA-editing sites of nad3 in mitochondria. New Phytol. https://doi.org/10.1111/nph.15347

    Article  PubMed  Google Scholar 

  • Xin B, Tao F, Wang Y, Liu H, Ma C, Xu P (2017) Coordination of metabolic pathways: enhanced carbon conservation in 1,3-propanediol production by coupling with optically pure lactate biosynthesis. Metab Eng 41:102–114

    Article  CAS  PubMed  Google Scholar 

  • Xiu ZH, Sun F, Shen Y, Zhang XY, Jiang RC, Bonnard G, Zhang JH, 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  PubMed  Google Scholar 

  • Yang YZ, Ding S, Wang HC, Sun F, Huang WL, Song S, Xu C, Tan BC (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  PubMed  Google Scholar 

  • Zehrmann A, Verbitskiy D, van der Merwe JA, Brennicke A, Takenaka M (2009) A DYW domain-containing pentatricopeptide repeat protein is required for RNA editing at multiple sites in mitochondria of Arabidopsis thaliana. Plant Cell 21:558–567

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang YF, Suzuki M, Sun F, Tan BC (2017) The mitochondrion-targeted PENTATRICOPEPTIDE REPEAT78 protein is required for nad5 mature mRNA stability and seed development in maize. Mol Plant 10:1321–1333

    Article  CAS  PubMed  Google Scholar 

  • Zoschke R, Watkins KP, Miranda RG, Barkan A (2016) The PPR-SMR protein PPR53 enhances the stability and translation of specific chloroplast RNAs in maize. Plant J 85:594–606

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We thank Tsuyoshi Nakagawa (Shimane University, Japan) for the pGWB vectors. This work was supported by funds from the National Natural Science Foundation of China (Project No. 31501375) and China Postdoctoral Science Foundation Funded Project (Project No. 2016M590542).

Author information

Authors and Affiliations

  1. Institute of Crop Science, College of Agriculture and Biotechnology, Zhejiang University, Hangzhou, 310058, People’s Republic of China

    Peng Zheng, Jumin Tu & Yu-Jun Liu

  2. State Key Lab of Agrobiotechnology, School of Life Science, The Chinese University of Hong Kong, Shatin, New Territories, Hong Kong, People’s Republic of China

    Jianhua Zhang

  3. School of Life Sciences, Lanzhou University, Lanzhou, 730000, People’s Republic of China

    Qiang He & Xiaomin Wang

Authors
  1. Peng Zheng
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Qiang He
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaomin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jumin Tu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Jianhua Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Yu-Jun Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yu-Jun Liu.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (PDF 2113 KB)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Zheng, P., He, Q., Wang, X. et al. Functional analysis for domains of maize PPR protein EMP5 in RNA editing and plant development in Arabidopsis. Plant Growth Regul 87, 19–27 (2019). https://doi.org/10.1007/s10725-018-0447-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10725-018-0447-8

Keywords

Search

Navigation