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Roles of the nuclear-encoded chloroplast SMR domain-containing PPR protein SVR7 in photosynthesis and oxidative stress tolerance in Arabidopsis

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Abstract

The mutations of the plastid SMR domaincontaining PPR protein SVR7 were previously reported to cause a specific reduction in the chloroplast ATP synthase levels. Here, we isolated a new mutant allele of SVR7, named svr7-4, in which T-DNA is inserted into the initiation codon of SVR7. The rosette leaves of svr7-4, especially in the juvenile stage, showed a pale green phenotype as a result of a reduction in the chlorophyll levels. The values of P700 and Fv/Fm indicated that the photosynthetic capacities of both PSI and PSII were damaged in svr7-4. Furthermore, we found that the svr7-4 accumulated more reactive oxygen species (ROS) and showed lower photo-oxidative stress tolerance by histochemical staining and hydrogen peroxide bleaching experiments, respectively. The leaves of svr7-4 also had increased anthocyanins accumulation compared to that of wild-type (WT) when floated on water under light. Finally, we found that the expression levels of four abiotic stress-responsive genes including ZAT10, AtAPX1, CAT1 and AtGPX2 were up-regulated in svr7-4. SVR7 was expressed ubiquitously during plant development. These results indicate that SVR7 is important for normal photosynthesis and photo-oxidative stress responses in chloroplasts.

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References

  • Adibhatla RM, Hatcher JF (2010) Lipid oxidation and peroxidation in cns health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 12:125–169

    Article  PubMed  CAS  Google Scholar 

  • Aronsson H, Schottler MA, Kelly AA, Sundqvist C, Dormann P, Karim S, Jarvis P (2008) Monogalactosyldiacylglycerol deficiency in Arabidopsis thaliana affects pigment composition in the prolamellar body and impairs thylakoid membrane energization and photoprotection in leaves. Plant Physiol 148:580–592

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Asada K (1999) The water-water cycle in chloroplasts: scavenging of active oxygen and dissipation of excess photons. Annu Rev Plant Physiol Plant Mol Biol 50:601–639

    Article  PubMed  CAS  Google Scholar 

  • Asada K (2000) The water-water cycle as alternative photon and electron sinks. Philos Trans R Soc Lond B Biol Sci 355:1419–1431

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Asada K (2006) Production and scavenging of reactive oxygen species in chloroplasts and their functions. Plant Physiol 141:391–396

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Aubourg S, Boudet N, Kreis M, Lecharny A (2000) In Arabidopsis thaliana, 1% of the genome codes for a novel protein family unique to plants. Plant Mol Biol 42:603–613

    Article  PubMed  CAS  Google Scholar 

  • Bochkov VN, Oskolkova OV, Birukov KG, Levonen AL, Binder CJ, Stöckl J (2010) Generation and biological activities of oxidized phospholipids. Antioxid Redox Signal 12:1009–1059

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Bowler C, van Camp W, van Montagu M, Inzé D (1994) Superoxide dismutases in plants. Crit Rev Plant Sci 13:199–218

    Article  CAS  Google Scholar 

  • Chateigner-Boutin AL, Ramos-Vega M, Guevara-Garcia A, Andres C, de la Luz Gutierrez-Nava M, Cantero A, Delannoy E, Jimenez LF, Lurin C, Small I, Leon P (2008) CLB19, a pentatricopeptide repeat protein required for editing of rpoA and clpP chloroplast transcripts. Plant J 56:590–602

    Article  PubMed  CAS  Google Scholar 

  • Chen M, Choi Y, Voytas DF, Rodermel S (2000) Mutations in the Arabidopsis VAR2 locus cause leaf variegation due to the loss of a chloroplast FtsH protease. Plant J 22:303–313

    Article  PubMed  Google Scholar 

  • Cottage A, Mott EK, Kempster JA, Gray JC (2010) The Arabidopsis plastid-signalling mutant gun1 (genomes uncoupled1) shows altered sensitivity to sucrose and abscisic acid and alterations in early seedling development. J Exp Bot 61:3773–3786

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein Zat12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139:847–856

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Delannoy E, Stanley WA, Bond CS, Small ID (2007) Pentatricopeptide repeat (PPR) proteins as sequencespecificity factors in posttranscriptional processes in organelles. Biochem Soc Trans 35:1643–1647

    Article  PubMed  CAS  Google Scholar 

  • Díaz-Vivancos P, Clemente-Moreno MJ, Rubio M, Olmos E, García JA, Martínez-Gómez P, Hernández JA (2008) Alteration in the chloroplastic metabolism leads to ROS accumulation in pea plants in response to plum pox virus. J Exp Bot 59:2147–2160

    Article  PubMed  PubMed Central  Google Scholar 

  • Fukui K, Kuramitsu S (2011) Structure and function of the small MutS-related domain. Mol Biol Int 2011:691735

    Article  PubMed  PubMed Central  Google Scholar 

  • Fukui K, Nakagawa N, Kitamura Y, Nishida Y, Masui R, Kuramitsu S (2008) Crystal structure of Muts2 endonuclease domain and the mechanism of homologous recombination suppression. J Biol Chem 283:33417–33427

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Hricová A, Quesada V, Micol JL (2006) The SCABRA3 nuclear gene encodes the plastid RpoTp RNA polymerase, which is required for chloroplast biogenesis and mesophyll cell proliferation in Arabidopsis. Plant Physiol 141:942–956

    Article  PubMed  PubMed Central  Google Scholar 

  • Kang J, Huang S, Blaser MJ (2005) Structural and functional divergence of MutS2 from bacterial MutS1 and eukaryotic MSH4-MSH5 homologst. J Biol Chem 187:3528–3537

    CAS  Google Scholar 

  • Kotera E, Tasaka M, Shikanai T (2005) A pentatricopeptide repeat protein is essential for RNA editing in chloroplasts. Nature 433:326–330

    Article  PubMed  CAS  Google Scholar 

  • Koussevitzky S, Nott A, Mockler TC, Hong F, Sachetto-Martins G, Surpin M, Lim J, Mittler R, Chory J (2007) Signals from chloroplasts converge to regulate nuclear gene expression. Science 316:715–719

    Article  PubMed  CAS  Google Scholar 

  • Lahmy S, Barnèche F, Derancourt J, Filipowicz W, Delseny M, Echeverria M (2000) A chloroplastic RNA-binding protein is a new member of the PPR family. FEBS Letters 480:255–260

    Article  PubMed  CAS  Google Scholar 

  • Leister D (2003) Chloroplast research in the genomic age. Trends Genet 19:47–56

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler HK, Wellburn AR (1983) Determination of total carotenoids and chlorophylls a and b of leaf extracts in different solvents. Biochem Soc Trans 11:591–592

    CAS  Google Scholar 

  • Liu X, Yu F, Rodermel S (2010) An Arabidopsis pentatricopeptide repeat protein, SUPPRESSOR OF VARIEGATION7, is required for FtsH-mediated chloroplast biogenesis. Plant Physiol 154:1588–1601

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Liu YG, Mitsukawa N, Oosumi T, Whittier RF (1995) Efficient isolation and mapping of Arabidopsis thaliana T-DNA insert junctions by thermal asymmetric interlaced PCR. Plant J 8:457–463

    Article  PubMed  CAS  Google Scholar 

  • Lopez-Juez E, Pyke KA (2005) Plastids unleashed: their development and their integration in plant development. Int J Dev Biol 49:557–577

    Article  PubMed  CAS  Google Scholar 

  • Lurin C, Andrés C, Aubourg S, Bellaoui M, Bitton F, Bruyère 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  PubMed  CAS  PubMed Central  Google Scholar 

  • Manfield IW, Jen CH, Pinney JW, Michalopoulos I, Bradford JR, Gilmartin PM, Westhead DR (2006) Arabidopsis Co-expression Tool (ACT): web server tools for microarray-based gene expression analysis. Nucleic Acids Res 34 (Web Server issue):W504–W509

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Martin W, Herrmann RG (1998) Gene transfer from organelles to the nucleus: how much, what happens, and why? Plant Physiol 118:9–17

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Merzlyak MN, Chivkunova OB (2000) Light-stress-induced pigment changes and evidence for anthocyanin photoprotection in apples. J Photochem Photobiol B 55:155–163

    Article  PubMed  CAS  Google Scholar 

  • Meurer J, Meierhoff K, Westhoff P (1996) Isolation of highchlorophyllfluorescence mutants of Arabidopsis thaliana and their characterization by spectroscopy, immunoblotting and Northern hybridization. Planta 198:385–396

    Article  PubMed  CAS  Google Scholar 

  • Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410

    Article  PubMed  CAS  Google Scholar 

  • Moreira D, Philippe H (1999) Smr: a bacterial and eukaryotic homologue of the C-terminal region of the MutS2 family. Trends Biochem Sci 24:298–300

    Article  PubMed  CAS  Google Scholar 

  • Mylona PV, Polidoros AN (2010) ROS Regulation of Antioxidant Genes. In: S. Dutta Gupta (ed), Reactive oxygen species and antioxidants in higher plants, Science Publishers, USA, pp:101–127

    Chapter  Google Scholar 

  • Myouga F, Hosoda C, Umezawa T, Iizumi H, Kuromori T, Motohashi P, Shono Y, Nagata N, Ikeuchi M, Shinozaki K (2008) A heterocomplex of iron superoxide dismutases defends chloroplast nucleoids against oxidative stress and is essential for chloroplast development in Arabidopsis. Plant Cell 20:3148–3162

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Næsted H, Holm A, Jenkins T, Nielsen HB, Harris CA, Beale MH, Andersen M, Mant A, Scheller H, Camara B, Mattsson O, Mundy J (2004) Arabidopsis VARIEGATED 3 encodes a chloroplasttargeted, zinc-finger protein required for chloroplast and palisade cell development. J Cell Sci 117:4807–4818

    Article  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  PubMed  CAS  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  PubMed  CAS  PubMed Central  Google Scholar 

  • Pfalz J, Liere K, Kandlbinder A, Dietz KJ, Oelmüller R (2006) pTAC2,-6, and-12 are components of the transcriptionally active plastid chromosome that are required for plastid gene expression. Plant Cell 18:176–197

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Pinto AV, Mathieu A, Marsin S, Veaute X, Ielpi L, Labigne A, Radicella JP (2005) Suppression of homologous and homeologous recombination by the bacterial MutS2 protein. Mol Cell 17:113–120

    Article  PubMed  CAS  Google Scholar 

  • Qin G, Kang D, Dong Y, Shen Y, Zhang L, Deng X, Zhang Y, Li S, Chen N, Niu W, Chen C, Liu P, Chen H, Li J, Ren Y, Gu H, Deng XW, Qu LJ, Chen Z (2003) Obtaining and analysis of flanking sequences from T-DNA transformants of Arabidopsis. Plant Sci 165:941–949

    Article  CAS  Google Scholar 

  • Schmitz-Linneweber C, Williams-Carrier RE, Williams-Voelker PM, Kroeger TS, Vichas A, Barkan A (2006) A pentatricopeptide repeat protein facilitates the trans-splicing of the maize chloroplast rps12 pre-mRNA. Plant Cell 18:2650–2663

    Article  PubMed  CAS  PubMed Central  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  PubMed  CAS  Google Scholar 

  • Sedelnikova OA, Redon CE, Dickey JS, Nakamura AJ, Georgakilas AG., Bonner WM (2010) Role of oxidatively induced DNA lesions in human pathogenesis. Mutat Res 704:152–159

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Small ID, Peeters N (2000) The PPR motif-a TPR-related motif prevalent in plant organellar proteins. Trends Biochem Sci 25:46–47

    Article  PubMed  CAS  Google Scholar 

  • Smillie RM, Hetherington SE (1999) Photoabatement by anthocyanin shields photosynthetic systems from light stress. Photosynthetica 36:451–463

    Article  CAS  Google Scholar 

  • Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  PubMed  CAS  Google Scholar 

  • Takechi K, Sodmergen Murata M, Motoyoshi F, Sakamoto W (2000) The YELLOW VARIEGATED (VAR2) locus encodes a homologue of FtsH, an ATP-dependent protease in Arabidopsis. Plant Cell Physiol 41:1334–1346

    Article  PubMed  CAS  Google Scholar 

  • Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  PubMed  CAS  PubMed Central  Google Scholar 

  • Timmis JN, Ayliffe MA, Huang CY, Martin W (2004) Endosymbiotic gene transfer: organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135

    Article  PubMed  CAS  Google Scholar 

  • Weigel D, Glazebrook J (2002) Arabidopsis: A Laboratory Manual, Cold Spring Harbor Laboratory Press, New York, pp:243–245

    Google Scholar 

  • Yu QB, Jiang Y, Chong K, Yang ZN (2009) AtECB2, a pentatricopeptide repeat protein, is required for chloroplast transcript accD RNA editing and early chloroplast biogenesis in Arabidopsis thaliana. Plant J 59:1011–1023

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Fujita K, Sakai K (2005) Oxidative stress in plant cell culture: a role in production of beta-thujaplicin by Cupresssus lusitanica suspension culture. Biotechnol Bioeng 90:621–631

    Article  PubMed  CAS  Google Scholar 

  • Zhou W, Cheng Y, Yap A, Chateigner-Boutin AL, Delannoy E, Hammani K, Small I, Huang JR (2008) The Arabidopsis gene YS1 encoding a DYW protein is required for editing of rpoB transcripts and the rapid development of chloroplasts during early growth. Plant J 58:82–96

    Article  PubMed  Google Scholar 

  • Zoschke R, Kroeger T, Belcher S, Schottler MA, Barkan A, Schmitz-Linneweber C (2012) The pentatricopeptide repeat-SMR protein ATP4 promotes translation of the chloroplast atpB/E mRNA. Plant J 77:547–558

    Article  Google Scholar 

  • Zoschke R, Qu YJ, Zubo YO, Börner T, Schmitz-Linneweber C (2013) Mutation of the pentatricopeptide repeat-SMR protein SVR7 impairs accumulation and translation of chloroplast ATP synthase subunits in Arabidopsis thaliana. J Plant Res 126:403–414

    Article  PubMed  CAS  Google Scholar 

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Authors and Affiliations

  1. School of Biotechnology, Tianjin University of Science & Technology, Tianjin, 300457, China

    He-Xin Lv

  2. Institute of Cell Biology, School of Life Sciences, Lanzhou University, 222 South Tianshui Road, Lanzhou, 730000, China

    He-Xin Lv & Guang-Qin Guo

  3. College of Life and Environmental Sciences, Shanghai Normal University, 100 Guilin Road, Shanghai, 200234, China

    Chao Huang & Zhong-Nan Yang

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  1. He-Xin Lv
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  2. Chao Huang
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Correspondence to Zhong-Nan Yang.

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Lv, HX., Huang, C., Guo, GQ. et al. Roles of the nuclear-encoded chloroplast SMR domain-containing PPR protein SVR7 in photosynthesis and oxidative stress tolerance in Arabidopsis . J. Plant Biol. 57, 291–301 (2014). https://doi.org/10.1007/s12374-014-0041-1

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