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Molecular cloning and characterization of OsCHR4, a rice chromatin-remodeling factor required for early chloroplast development in adaxial mesophyll

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Abstract

Mi-2 protein, the central component of the NuRD nucleosome remodeling and histone deacetylase complex, plays a role in transcriptional repression in animals. Mi-2-like genes have been reported in Arabidopsis, though their function in monocots remains largely unknown. In the present study, a rice Mi-2-like gene, OsCHR4 (Oryza sativa Chromatin Remodeling 4, LOC_Os07g03450), was cloned from a rice mutant with adaxial albino leaves. The Oschr4 mutant exhibited defective chloroplasts in adaxial mesophyll, but not in abaxial mesophyll. Ultrastructural observations indicated that proplastid growth and/or thylakoid membrane formation in adaxial mesophyll cells was blocked in the Oschr4 mutant. Subcellular localization revealed that OsCHR4::GFP fusion protein was targeted to the nuclei. OsCHR4 was mainly expressed in the root meristem, flower, vascular bundle, and mesophyll cells by promoter::GUS analysis in transgenic rice. The transcripts of some nuclear- and plastid-encoded genes required for early chloroplast development and photosynthesis were decreased in the adaxial albino mesophyll of the Oschr4 mutant. These observations provide evidence that OsCHR4, the rice Mi-2-like protein, plays an important role in early chloroplast development in adaxial mesophyll cells. The results increase our understanding of the molecular mechanism underlying tissue-specific chloroplast development in plants.

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Abbreviations

CC:

Chloroplast-containing

CHD:

Chromodomain helicase DNA-binding

EMS:

Ethyl methanesulfonate

GFP:

Green fluorescent protein

LCM:

Laser capture microdissection

Mi-2/NuRD:

Multi-subunit chromatin remodeling complex

NCC:

No chloroplast-containing

NEP:

Nuclear encoded RNA polymerase

ORF:

Open reading frame

OsCHR4:

Oryza sativa chromatin remodeling 4

PEP:

Plastid encoded RNA polymerase

qRT-PCR:

Quantitative real-time PCR

RT-PCR:

Reverse transcription PCR

STS:

Sequence tagged site

TEM:

Transmission electron microscopy

WT:

Wild type

References

  • Baumgartner BJ, Rapp JC, Mullet JE (1989) Plastid transcription activity and DNA copy number increase early in barley chloroplast development. Plant Physiol 89:1011–1018

    Article  PubMed  CAS  Google Scholar 

  • Bowman JL, Eshed Y, Baum SF (2002) Establishment of polarity in angiosperm lateral organs. Trends Genet 18:134–141

    Article  PubMed  CAS  Google Scholar 

  • Chen SY, Jin WZ, Wang MY, Zhang F, Zhou J, Jia QJ, Wu YR, Liu FY, Wu P (2003) Distribution and characterization of over 1000 T-DNA tags in rice genome. Plant J 36:105–113

    Article  PubMed  CAS  Google Scholar 

  • Chory J (1991) Light signals in leaf and chloroplast development: photoreceptors and downstream responses in search of a transduction pathway. New Biol 3:538–548

    PubMed  CAS  Google Scholar 

  • Eshed Y, Baum SF, Bowman JL (1999) Distinct mechanisms promote polarity establishment in carpels of Arabidopsis. Cell 99:199–209

    Article  PubMed  CAS  Google Scholar 

  • Fahn A (1990) Plant anatomy, 4th edn. Pergramon, New York

    Google Scholar 

  • Hanley-Bowdoin L, Chua NH (1989) Transcriptional interaction between the promoters of the maize chloroplast genes which encode the beta subunit of ATP synthase and the large subunit of ribulose 1,5-bisphosphate carboxylase. Mol Gen Genet 215:217–224

    Article  PubMed  CAS  Google Scholar 

  • Hedtke B, Börner T, Weihe A (1997) Mitochondrial and chloroplast phagetype RNA polymerases in Arabidopsis. Science 277:809–811

    Article  PubMed  CAS  Google Scholar 

  • Hibara K, Obara M, Hayashida E, Abe M, Ishimaru T, Satoh H, Itoh J, Nagato Y (2009) The ADAXIALIZED LEAF1 gene functions in leaf and embryonic pattern formation in rice. Dev Biol 334:345–354

    Article  PubMed  CAS  Google Scholar 

  • Inada H, Kusumi K, Nishimura M, Iba K (1996) Specific expression of the chloroplast gene for RNA polymerase (rpoB) at an early stage of leaf development in rice. Plant Cell Physiol 37:229–232

    Article  PubMed  CAS  Google Scholar 

  • Inada N, Sakai A, Kuroiwa H, Kuroiwa T (1998) Three-dimensional analysis of the senescence program in rice (Oryza sativa L.) coleoptiles. Investigations of tissues and cells by fluorescence microscopy. Planta 205:153–164

    Article  PubMed  CAS  Google Scholar 

  • Jia L, Zhang B, Mao C, Li J, Wu Y, Wu P, Wu Z (2008) OsCYT-INV1 for alkaline/neutral invertase is involved in root cell development and reproductivity in rice (Oryza sativa L.). Planta 228:51–59

    Article  PubMed  CAS  Google Scholar 

  • Kapoor S, Suzuki JY, Sugiura M (1997) Identification and functional significance of a new class of non-consensus-type plastid promoters. Plant J 11:327–337

    Article  PubMed  CAS  Google Scholar 

  • Kehle J, Beuchle D, Treuheit S, Christen B, Kennison JA, Bienz M, Muller J (1998) dMi-2, a hunchback-interacting protein that functions in polycomb repression. Science 282:1897–1900

    Article  PubMed  CAS  Google Scholar 

  • Kusumi K, Mizutani A, Nishimura M, Iba K (1997) A virescent gene V 1 determines the expression timing of plastid genes for transcription/translation apparatus during early leaf development in rice. Plant J 12:1241–1250

    Article  CAS  Google Scholar 

  • Leutwiler LS, Meyerowitz EM, Tobin EM (1986) Structure and expression of three light-harvesting chlorophyll a/b-binding protein genes in Arabidopsis thaliana. Nucleic Acids Res 14:4051–4064

    Article  PubMed  CAS  Google Scholar 

  • Li L, Shi ZY, Li L, Shen GZ, Wang XQ, An LS, Zhang JL (2010) Overexpression of ACL1 (abaxially curled leaf 1) increased bulliform cells and induced abaxial curling of leaf blades in rice. Mol Plant 3:807–817

    Article  PubMed  CAS  Google Scholar 

  • Lichtenthaler FW (1987) Karl Freudenberg, Burckhardt Helferich, Hermann O. L. Fischer: a centennial tribute. Carbohydr Res 164:1–22

    Article  PubMed  CAS  Google Scholar 

  • Liere K, Maliga P (1999) In vitro characterization of the tobacco rpoB promoter reveals a core sequence motif conserved between phage-type plastid and plant mitochondrial promoters. EMBO J 18:249–257

    Article  PubMed  CAS  Google Scholar 

  • Liere K, Kestermann M, Muller U, Link G (1995) Identification and characterization of the Arabidopsis thaliana chloroplast DNA region containing the genes psbA, trnH and rps19′. Curr Genet 28:128–130

    Article  PubMed  CAS  Google Scholar 

  • Liu H, Wang S, Yu X, Yu J, He X, Zhang S, Shou H, Wu P (2005) ARL1, a LOB-domain protein required for adventitious root formation in rice. Plant J 43:47–56

    Article  PubMed  Google Scholar 

  • Mandel MA, Feldmann KA, HerreraEstrella L, RochaSosa M, Leon P (1996) CLA1, a novel gene required for chloroplast development, is highly conserved in evolution. Plant J 9:649–658

    Article  PubMed  CAS  Google Scholar 

  • McConnell JR, Barton MK (1998) Leaf polarity and meristem formation in Arabidopsis. Development 125:2935–2942

    PubMed  CAS  Google Scholar 

  • Mullet JE (1988) Chloroplast development and gene expression. Annu Rev Plant Physiol Plant Mol Biol 39:475–502

    Article  CAS  Google Scholar 

  • Mullet JE (1993) Dynamic regulation of chloroplast transcription. Plant Physiol 103:309–313

    Article  PubMed  CAS  Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  PubMed  CAS  Google Scholar 

  • Nelson JM, Lane B, Freeling M (2002) Expression of a mutant maize gene in the ventral leaf epidermis is sufficient to signal a switch of the leaf’s dorsoventral axis. Development 129:4581–4589

    PubMed  CAS  Google Scholar 

  • Nilasena DS, Trieu EP, Targoff IN (1995) Analysis of the mi-2 autoantigen of dermatomyositis. Arthritis Rheum 38:123–128

    Article  PubMed  CAS  Google Scholar 

  • Ogas J, Cheng JC, Sung ZR, Somerville C (1997) Cellular differentiation regulated by gibberellin in the Arabidopsis thaliana pickle mutant. Science 277:91–94

    Article  PubMed  CAS  Google Scholar 

  • Ogas J, Kaufmann S, Henderson J, Somerville C (1999) PICKLE is a CHD3 chromatin-remodeling factor that regulates the transition from embryonic to vegetative development in Arabidopsis. Proc Natl Acad Sci USA 96:13839–13844

    Article  PubMed  CAS  Google Scholar 

  • Scimone ML, Meisel J, Reddien PW (2010) The Mi-2-like Smed-CHD4 gene is required for stem cell differentiation in the planarian Schmidtea mediterranea. Development 137:1231–1241

    Article  PubMed  CAS  Google Scholar 

  • Seelig HP, Moosbrugger I, Ehrfeld H, Fink T, Renz M, Genth E (1995) The major dermatomyositis-specific mi-2 autoantigen is a presumed helicase involved in transcriptional activation. Arthritis Rheum 38:1389–1399

    Article  PubMed  CAS  Google Scholar 

  • Shaked H, Avivi-Ragolsky N, Levy AA (2006) Involvement of the Arabidopsis SWI2/SNF2 chromatin remodeling gene family in DNA damage response and recombination. Genetics 173:985–994

    Article  PubMed  CAS  Google Scholar 

  • von Zelewsky T, Palladino F, Brunschwig K, Tobler H, Hajnal A, Muller F (2000) The C. elegans Mi-2 chromatin-remodelling proteins function in vulval cell fate determination. Development 127:5277–5284

    Google Scholar 

  • Vothknecht UC, Westhoff P (2001) Biogenesis and origin of thylakoid membranes. Biochim Biophys Acta 1541:91–101

    Article  PubMed  CAS  Google Scholar 

  • Wade PA, Gegonne A, Jones PL, Ballestar E, Aubry F, Wolffe AP (1999) Mi-2 complex couples DNA methylation to chromatin remodelling and histone deacetylation. Nat Genet 23:62–66

    PubMed  CAS  Google Scholar 

  • Woodage T, Basrai MA, Baxevanis AD, Hieter P, Collins FS (1997) Characterization of the CHD family of proteins. Proc Natl Acad Sci USA 94:11472–11477

    Article  PubMed  CAS  Google Scholar 

  • Xue Y, Wong J, Moreno GT, Young MK, Cote J, Wang W (1998) NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell 2:851–861

    Article  PubMed  CAS  Google Scholar 

  • Yamasaki Y, Nishida Y (2006) Mi-2 chromatin remodeling factor functions in sensory organ development through proneural gene repression in Drosophila. Dev Growth Differ 48:411–418

    Article  PubMed  CAS  Google Scholar 

  • Yoshida S, Forno DA, Cock JH, Gomez KA (1976) Laboratory manual for physiological studies of rice, 3rd edn. The International Rice Research Institute, The Philippines

    Google Scholar 

  • Yue R, Wang X, Chen J, Ma X, Zhang H, Mao C, Wu P (2010) A rice stromal processing peptidase regulates chloroplast and root development. Plant Cell Physiol 51:475–485

    Article  PubMed  CAS  Google Scholar 

  • Zhang GH, Xu Q, Zhu XD, Qian Q, Xue HW (2009) SHALLOT-LIKE1 is a KANADI transcription factor that modulates rice leaf rolling by regulating leaf abaxial cell development. Plant Cell 21:719–735

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was financially supported by the National Basic Research and Development Program of China (2011CB100300), the Ministry of Agriculture of China (2011ZX08009-003-005) and the National Natural Science Foundation (30971703, 30971742).

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Correspondence to Ping Wu.

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Zhao, C., Xu, J., Chen, Y. et al. Molecular cloning and characterization of OsCHR4, a rice chromatin-remodeling factor required for early chloroplast development in adaxial mesophyll. Planta 236, 1165–1176 (2012). https://doi.org/10.1007/s00425-012-1667-1

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  • DOI: https://doi.org/10.1007/s00425-012-1667-1

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