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Genetic mapping and isolation of two arc3 alleles in Arabidopsis

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Abstract

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Two new alleles of arc3 in Arabidopsis thaliana, arc3-4 and arc3-5, were isolated in the Columbia-0 ecotype. The mutants were characterized in detail using microscopy and molecular techniques.

Abstract

Chloroplasts are essential organelles for photosynthesis in plant cells. Division of chloroplasts is coordinated by the internal division machinery (mainly the tubulin-like FtsZ ring) and the external division machinery (mainly the dynamin-like ARC5 ring). Accumulation and replication of chloroplasts3 (ARC3) is important for the correct positioning of chloroplast division machinery. During evolution, ARC3 has probably replaced minicellC (MinC), an important factor involved in positioning of the division site in bacteria. However, the working mechanism of ARC3 is still unclear. Using forward genetic approaches, we isolated two new alleles of arc3 in Arabidopsis thaliana, arc3-4 and arc3-5, in which mutant loci differed from those of previously reported arc3 mutants. Microscopy analyses showed more detailed, and some new, phenotypes of arc3 mutants. Reverse-transcription polymerase chain reaction (RT-PCR) and real-time quantitative RT-PCR (qRT-PCR) results indicated that the mRNA of the ARC3 gene was unstable in arc3-4 and arc3-5 mutant plants. Also, RNA secondary structures of the ARC3 gene were predicted to differ between these two arc3 mutants and wild type. Our studies increase our understanding of the function of ARC3 in chloroplast division.

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References

  • Aldridge C, Maple J, Moller SG (2005) The molecular biology of plastid division in higher plants. J Exp Bot 56:1061–1077

    Article  PubMed  CAS  Google Scholar 

  • Brodskii LI, Ivanov VV, Kalaidzidis Ia L, Leontovich AM, Nikolaev VK, Feranchuk SI, Drachev VA (1995) GeneBee-NET: an internet based server for biopolymer structure analysis. Biokhimiia 60:1221–1230

    PubMed  CAS  Google Scholar 

  • Chang YF, Imam JS, Wilkinson MF (2007) The nonsense-mediated decay RNA surveillance pathway. Annu Rev Biochem 76:51–74

    Article  PubMed  CAS  Google Scholar 

  • Cho YH, Kim GD, Yoo SD (2012) Giant chloroplast development in ethylene response1-1 is caused by a second mutation in ACCUMULATION AND REPLICATION OF CHLOROPLAST3 in Arabidopsis. Mol Cells 33:99–103

    Article  PubMed  CAS  Google Scholar 

  • Colletti KS, Tattersall EA, Pyke KA, Froelich JE, Stokes KD, Osteryoung KW (2000) A homologue of the bacterial cell division site-determining factor MinD mediates placement of the chloroplast division apparatus. Curr Biol 10:507–516

    Article  PubMed  CAS  Google Scholar 

  • Fujiwara MT, Nakamura A, Itoh R, Shimada Y, Yoshida S, Moller SG (2004) Chloroplast division site placement requires dimerization of the ARC11/AtMinD1 protein in Arabidopsis. J Cell Sci 117:2399–2410

    Article  PubMed  CAS  Google Scholar 

  • Fujiwara MT, Hashimoto H, Kazama Y, Abe T, Yoshida S, Sato N, Itoh RD (2008) The assembly of the FtsZ ring at the mid-chloroplast division site depends on a balance between the activities of AtMinE1 and ARC11/AtMinD1. Plant Cell Physiol 49:345–361

    Article  PubMed  CAS  Google Scholar 

  • Gao H, Kadirjan-Kalbach D, Froehlich JE, Osteryoung KW (2003) ARC5, a cytosolic dynamin-like protein from plants, is part of the chloroplast division machinery. Proc Natl Acad Sci USA 100:4328–4333

    Article  PubMed  CAS  Google Scholar 

  • Glynn JM, Miyagishima SY, Yoder DW, Osteryoung KW, Vitha S (2007) Chloroplast division. Traffic 8:451–461

    Article  PubMed  CAS  Google Scholar 

  • Glynn JM, Froehlich JE, Osteryoung KW (2008) Arabidopsis ARC6 coordinates the division machineries of the inner and outer chloroplast membranes through interaction with PDV2 in the intermembrane space. Plant Cell 20:2460–2470

    Article  PubMed  CAS  Google Scholar 

  • Glynn JM, Yang Y, Vitha S, Schmitz AJ, Hemmes M, Miyagishima SY, Osteryoung KW (2009) PARC6, a novel chloroplast division factor, influences FtsZ assembly and is required for recruitment of PDV1 during chloroplast division in Arabidopsis. Plant J 59:700–711

    Article  PubMed  CAS  Google Scholar 

  • Hu Z, Lutkenhaus J (2000) Analysis of MinC reveals two independent domains involved in interaction with MinD and FtsZ. J Bacteriol 182:3965–3971

    Article  PubMed  CAS  Google Scholar 

  • Li W, Wu J, Weng S, Zhang D, Zhang Y, Shi C (2010) Characterization and fine mapping of the glabrous leaf and hull mutants (gl1) in rice (Oryza sativa L.). Plant Cell Rep 29:617–627

    Article  PubMed  CAS  Google Scholar 

  • Ma H, Lou Y, Lin WH, Xue HW (2006) MORN motifs in plant PIPKs are involved in the regulation of subcellular localization and phospholipid binding. Cell Res 16:466–478

    Article  PubMed  CAS  Google Scholar 

  • Maple J, Moller SG (2007a) Interdependency of formation and localisation of the Min complex controls symmetric plastid division. J Cell Sci 120:3446–3456

    Article  PubMed  CAS  Google Scholar 

  • Maple J, Moller SG (2007b) Plastid division: evolution, mechanism and complexity. Ann Bot 99:565–579

    Article  PubMed  CAS  Google Scholar 

  • Maple J, Chua NH, Moller SG (2002) The topological specificity factor AtMinE1 is essential for correct plastid division site placement in Arabidopsis. Plant J 31:269–277

    Article  PubMed  CAS  Google Scholar 

  • Maple J, Vojta L, Soll J, Moller SG (2007) ARC3 is a stromal Z-ring accessory protein essential for plastid division. EMBO Rep 8:293–299

    Article  PubMed  CAS  Google Scholar 

  • Maple J, Winge P, Tveitaskog AE, Gargano D, Bones AM, Moller SG (2011) Genome-wide gene expression profiles in response to plastid division perturbations. Planta 234:1055–1063

    Article  PubMed  CAS  Google Scholar 

  • Marrison JL, Rutherford SM, Robertson EJ, Lister C, Dean C, Leech RM (1999) The distinctive roles of five different ARC genes in the chloroplast division process in Arabidopsis. Plant J 18:651–662

    Article  PubMed  CAS  Google Scholar 

  • McAndrew RS, Olson BJ, Kadirjan-Kalbach DK, Chi-Ham CL, Vitha S, Froehlich JE, Osteryoung KW (2008) In vivo quantitative relationship between plastid division proteins FtsZ1 and FtsZ2 and identification of ARC6 and ARC3 in a native FtsZ complex. Biochem J 412:367–378

    Article  PubMed  CAS  Google Scholar 

  • Miyagishima SY, Froehlich JE, Osteryoung KW (2006) PDV1 and PDV2 mediate recruitment of the dynamin-related protein ARC5 to the plastid division site. Plant Cell 18:2517–2530

    Article  PubMed  CAS  Google Scholar 

  • Osteryoung KW, Pyke KA (1998) Plastid division: evidence for a prokaryotically derived mechanism. Curr Opin Plant Biol 1:475–479

    Article  PubMed  CAS  Google Scholar 

  • Osteryoung KW, Stokes KD, Rutherford SM, Percival AL, Lee WY (1998) Chloroplast division in higher plants requires members of two functionally divergent gene families with homology to bacterial ftsZ. Plant Cell 10:1991–2004

    PubMed  CAS  Google Scholar 

  • Pyke KA, Leech RM (1991) Rapid image analysis screening procedure for identifying chloroplast number mutants in mesophyll cells of Arabidopsis thaliana (L.) Heynh. Plant Physiol 96:1193–1195

    Article  PubMed  CAS  Google Scholar 

  • Pyke KA, Leech RM (1992) Chloroplast division and expansion is radically altered by nuclear mutations in Arabidopsis thaliana. Plant Physiol 99:1005–1008

    Article  PubMed  CAS  Google Scholar 

  • Pyke KA, Leech RM (1994) A genetic analysis of chloroplast division and expansion in Arabidopsis thaliana. Plant Physiol 104:201–207

    PubMed  CAS  Google Scholar 

  • Robertson EJ, Rutherford SM, Leech RM (1996) Characterization of chloroplast division using the Arabidopsis mutant arc5. Plant Physiol 112:149–159

    Article  PubMed  CAS  Google Scholar 

  • Rothfield L, Taghbalout A, Shih YL (2005) Spatial control of bacterial division-site placement. Nat Rev Microbiol 3:959–968

    Article  PubMed  CAS  Google Scholar 

  • Schmitz AJ, Glynn JM, Olson BJ, Stokes KD, Osteryoung KW (2009) Arabidopsis FtsZ2-1 and FtsZ2-2 are functionally redundant, but FtsZ-based plastid division is not essential for chloroplast partitioning or plant growth and development. Mol Plant 2:1211–1222

    Article  PubMed  CAS  Google Scholar 

  • Shimada H, Koizumi M, Kuroki K, Mochizuki M, Fujimoto H, Ohta H, Masuda T, Takamiya K (2004) ARC3, a chloroplast division factor, is a chimera of prokaryotic FtsZ and part of eukaryotic phosphatidylinositol-4-phosphate 5-kinase. Plant Cell Physiol 45:960–967

    Article  PubMed  CAS  Google Scholar 

  • Vitha S, McAndrew RS, Osteryoung KW (2001) FtsZ ring formation at the chloroplast division site in plants. J Cell Biol 153:111–120

    Article  PubMed  CAS  Google Scholar 

  • Vitha S, Froehlich JE, Koksharova O, Pyke KA, van Erp H, Osteryoung KW (2003) ARC6 is a J-domain plastid division protein and an evolutionary descendant of the cyanobacterial cell division protein Ftn2. Plant Cell 15:1918–1933

    Article  PubMed  CAS  Google Scholar 

  • Yang Y, Glynn JM, Olson BJ, Schmitz AJ, Osteryoung KW (2008) Plastid division: across time and space. Curr Opin Plant Biol 11:577–584

    Article  PubMed  CAS  Google Scholar 

  • Yoder DW, Kadirjan-Kalbach D, Olson BJ, Miyagishima SY, Deblasio SL, Hangarter RP, Osteryoung KW (2007) Effects of mutations in Arabidopsis FtsZ1 on plastid division, FtsZ ring formation and positioning, and FtsZ filament morphology in vivo. Plant Cell Physiol 48:775–791

    Article  PubMed  CAS  Google Scholar 

  • Zhang M, Hu Y, Jia J, Li D, Zhang R, Gao H, He Y (2009) CDP1, a novel component of chloroplast division site positioning system in Arabidopsis. Cell Res 19:877–886

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by grants from the Natural Science Foundation of China (No. 31070162) and the Fundamental Research Funds for the Central Universities.

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Authors and Affiliations

  1. College of Biological Sciences and Biotechnology, Beijing Forestry University, Haidian, Beijing, 100083, China

    Deng Pan, Yuhong Shi, Xia Liu, Yuefang Gao, Zhonghua Liu & Hongbo Gao

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  1. Deng Pan
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  2. Yuhong Shi
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  3. Xia Liu
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  4. Yuefang Gao
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  5. Zhonghua Liu
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  6. Hongbo Gao
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Corresponding author

Correspondence to Hongbo Gao.

Additional information

Communicated by R. Rose.

D. Pan and Y. Shi contributed equally to this work.

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Pan, D., Shi, Y., Liu, X. et al. Genetic mapping and isolation of two arc3 alleles in Arabidopsis . Plant Cell Rep 32, 173–182 (2013). https://doi.org/10.1007/s00299-012-1352-7

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  • DOI: https://doi.org/10.1007/s00299-012-1352-7

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