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The expression of Orysa;CycB1;1 is essential for endosperm formation and causes embryo enlargement in rice

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Abstract

The cell cycle is an important process during seed development in plants and its progression is driven by a number of core regulators such as the cyclins. Currently, however, little is known regarding the role of the cyclins in embryo and endosperm development in cereals. In our current study, we show that the knockdown of Orysa;CycB1;1 in rice results in the production of abnormal seeds, which at maturity contain only an enlarged embryo. It was further found that a delayed and abnormal cellularization occurred in the endosperm in these knockdown seeds which eventually became abortive. Moreover, the observed development of the enlarged embryo was also morphologically abnormal and found to be caused by an enlarged cell size rather than an increased cell number. Expression analysis showed that Orysa;CycB1;1 transcripts were localized in the endosperm and embryo. Genome-wide transcriptional profiling further indicated that a large number of genes are responsible for the phenotype of the enlarged embryo. The results of the knockdown of Orysa;CycB1;1 via an endosperm or an embryo-specific promoter also suggest that the enlarged embryo may be correlated to the abortive endosperm. Our results suggest that Orysa;CycB1;1 expression is critical for endosperm formation via the regulation of mitotic division, and that the endosperm plays an important role in maintenance of embryo development in rice.

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Abbreviations

CDK:

Cyclin-dependent kinase

enl1 :

Endospermless1

EXS:

Extra sporogenous cells

ge-2 :

Giant embryo-2

GUS :

Beta-glucuronidase

MPF:

M-phase-promoting factor

qRT-PCR:

Real-time quantitative PCR

Rb:

Retinoblastoma protein

RT-PCR:

Reverse transcriptase polymerase chain reaction

SDS:

SOLO DANCERS

XTH:

Xyloglucan endotransglucosylase/hydrolase

References

  • Alexander MP (1969) Differential staining of aborted and nonaborted pollen. Stain Technol 44:117–122

    CAS  PubMed  Google Scholar 

  • Azumi Y, Liu D, Li W, Wang G, Hu Y, Ma H (2002) Homolog interaction during meiotic prophase I in Arabidopsis requires the SOLO DANCERS gene encoding a novel cyclin-like protein. EMBO J 21:3081–3095

    Article  CAS  PubMed  Google Scholar 

  • Barrôco RM, Peres A, Droual AM, De Veylder L, Nguyen le SL, De Wolf J, Mironov V, Peerbolte R, Beemster GT, Inźe D, Broekaert WF, Frankard V (2006) The cyclin-dependent kinase inhibitor Orysa;KRP1 plays an important role in seed development of rice. Plant Physiol 142:1053–1064

    Article  PubMed  Google Scholar 

  • Berger F, Grini PE, Schnittger A (2006) Endosperm an integrator of seed growth and development. Curr Opin Plant Biol 9:664–670

    Article  CAS  PubMed  Google Scholar 

  • Booher RN, Holman PS, Fattaey A (1997) Human myt1 is a cell cycle-regulated kinase that inhibits cdc2 but not cdk2 activity. J Biol Chem 272:22300–22306

    Article  CAS  PubMed  Google Scholar 

  • Brown RC, Lemmon BE (2007) The developmental biology of cereal endosperm. Plant Cell Biol Monogr 8:1–20

    Article  Google Scholar 

  • Canales C, Bhatt AM, Scott R, Dickinson H (2002) EXS, a putative LRR receptor kinase, regulates male germline cell number and tapetal identity and promotes seed development in Arabidopsis. Curr Biol 12:1718–1727

    Article  CAS  PubMed  Google Scholar 

  • Chang L, Ma H, Xue HW (2009) Functional conservation of the meiotic genes SDS and RCK in male meiosis in the monocot rice. Cell Res 19:768–782

    Article  CAS  PubMed  Google Scholar 

  • Cosgrove DJ (2000) Expansive growth of plant cell walls. Plant Physiol Biochem 38:109–124

    Article  CAS  PubMed  Google Scholar 

  • Dewitte W, Riou-Khamlichi C, Scofield S, Healy JM, Jacqmard A, Kilby NJ, Murray JA (2003) Altered cell cycle distribution, hyperplasia, and inhibited differentiation in Arabidopsis caused by the D-type cyclin CYCD3. Plant Cell 15:79–92

    Article  CAS  PubMed  Google Scholar 

  • Doerner P, Jorgensen JE, You R, Steppuhn J, Lamb C (1996) Control of root growth and development by cyclin expression. Nature 380:520–523

    Article  CAS  PubMed  Google Scholar 

  • Donnelly PM, Bonetta D, Tsukaya H, Dengler RE, Dengler NG (1999) Cell cycling and cell enlargement in developing leaves of Arabidopsis. Dev Biol 215:407–419

    Article  CAS  PubMed  Google Scholar 

  • Ferreira PC, Hemerly AS, Engler JD, van Montagu M, Engler G, Inźe D (1994) Developmental expression of the Arabidopsis cyclin gene cyc1At. Plant Cell 6:1763–1774

    Article  CAS  PubMed  Google Scholar 

  • Fuerst RA, Soni R, Murray JA, Lindsey K (1996) Modulation of cyclin transcript levels in cultured cells of Arabidopsis thaliana. Plant Physiol 112:1023–1033

    Article  CAS  PubMed  Google Scholar 

  • Genschik P, Criqui MC, Parmentier Y, Derevier A, Fleck J (1998) Cell cycle-dependent proteolysis in plants: identification of the destruction box pathway and metaphase arrest produced by the proteasome inhibitor mg132. Plant Cell 10:2063–2076

    Article  CAS  PubMed  Google Scholar 

  • Grafi G, Larkins BA (1995) Endoreduplication in maize endosperm-involvement of M-phase promoting factor inhibition and induction of S-phase-related kinases. Science 269:1262–1264

    Article  CAS  PubMed  Google Scholar 

  • Guo J, Song J, Wang F, Zhang XS (2007) Genome-wide identification and expression analysis of rice cell cycle genes. Plant Mol Biol 64:349–360

    Article  CAS  PubMed  Google Scholar 

  • Hong SK, Kitano H, Satoh H, Nagato Y (1996) How is embryo size genetically regulated in rice? Development 122:2051–2058

    CAS  PubMed  Google Scholar 

  • Ito M, Criqui M-C, Sakabe M, Ohno T, Hata S, Kouchi H, Hashimoto J, Fukuda H, Komamine A, Watanabe A (1997) Cell-cycle regulated transcription of A- and B-type plant cyclin genes in synchronous cultures. Plant J 11:983–992

    Article  CAS  PubMed  Google Scholar 

  • Jang I-C, Nahm BH, Kim J-K (1999) Subcellular targeting of green fluorescent protein to plastids in transgenic rice plants provides a high-level expression system. Mol Breed 5:453–461

    Article  CAS  Google Scholar 

  • Kageyama Y, Fukuoka H, Yamamoto K, Takeda G (1991) The rice plant bearing endospermless grains: a novel mutant induced by gamma-irradiation of tetraploid rice (Oryza sativa L.). J Breed 41:341–345

    Google Scholar 

  • Lee J, Das A, Yamaguchi M, Hashimoto J, Tsutsumi N, Uchimiya H, Umeda M (2003) Cell cycle function of a rice B2-type cyclin interacting with a B-type cyclin-dependent kinase. Plant J 34:417–425

    Article  CAS  PubMed  Google Scholar 

  • Lopes MA, Larkins BA (1993) Endosperm origin, development, and function. Plant Cell 5:1383–1399

    Article  CAS  PubMed  Google Scholar 

  • Minshull J, Blow JJ, Hunt T (1989) Translation of cyclin mRNA is necessary for extracts of activated Xenopus eggs to enter mitosis. Cell 56:947–956

    Article  CAS  PubMed  Google Scholar 

  • Nowack MK, Grini PE, Jakoby MJ, Lafos M, Koncz C, Schnittger A (2006) A positive signal from the fertilization of the egg cell sets off endosperm proliferation in angiosperm embryogenesis. Nat Genet 38:63–67

    Article  CAS  PubMed  Google Scholar 

  • Peters JM (1998) SCF and APC: the Yin and Yang of cell cycle regulated proteolysis. Curr Opin Cell Biol 10:759–768

    Article  CAS  PubMed  Google Scholar 

  • Pines J (1999) Four-dimensional control of the cell cycle. Nat Cell Biol 1:73–79

    Article  Google Scholar 

  • Qu LQ, Xing YP, Liu WX, Xu XP, Song YR (2008) Expression pattern and activity of six glutelin gene promoters in transgenic rice. J Exp Bot 59:2417–2424

    Article  CAS  Google Scholar 

  • Reichheld JP, Chaubet N, Shen WH, Renaudin JP, Gigot C (1996) Multiple A-type cyclins express sequentially during the cell cycle in Nicotiana tabacum BY2 cells. Proc Natl Acad Sci USA 93:13819–13824

    Article  CAS  PubMed  Google Scholar 

  • Renaudin JP, Doonan JH, Freeman D, Hashimoto J, Hirt H, Inźe D, Jacobs T, Kouchi H, Rouze P, Sauter M, Savoure A, Sorrell DA, Sundaresan V, Murray JA (1996) Plant cyclins: a unified nomenclature for plant A-, B- and D-type cyclins based on sequence organization. Plant Mol Biol 32:1003–1018

    Article  CAS  PubMed  Google Scholar 

  • Sauter M, von Wiegen P, Lörz H, Kranz E (1998) Cell cycle regulatory genes from maize are differentially controlled during fertilization and first embryonic cell cycle. Sex Plant Reprod 11:41–48

    Article  CAS  Google Scholar 

  • Schnittger A, Schöbinger U, Stierhof YD, Hülskamp M (2002) Ectopic B-type cyclin expression induces mitotic cycles in endoreduplicating Arabidopsis trichomes. Curr Biol 12:415–420

    Article  CAS  PubMed  Google Scholar 

  • Setiady YY, Sekine M, Hariguchi N, Yamamoto T, Kouchi H, Shinmyo A (1995) Tobacco mitotic cyclins: cloning, characterization, gene expression and functional assay. Plant J 8:949–957

    CAS  PubMed  Google Scholar 

  • Soni DV, Sramkoski RM, Lam M, Stefan T, Jacobberger JW (2008) Cyclin B1 is rate limiting but not essential for mitotic entry and progression in mammalian somatic cells. Cell Cycle 7:1285–1300

    CAS  PubMed  Google Scholar 

  • Sun Y, Dilkes BP, Zhang C, Dante RA, Carneiro NP, Lowe KS, Jung R, Gordon-Kamm WJ, Larkins BA (1999a) Characterization of maize (Zea mays L.) Wee1 and its activity in developing endosperm. Proc Natl Acad Sci USA 96:4180–4185

    Article  CAS  PubMed  Google Scholar 

  • Sun Y, Flannigan BA, Setter TL (1999b) Regulation of endoreduplication in maize (Zea mays L.) endosperm. Isolation of a novel B1-type cyclin and its quantitative analysis. Plant Mol Biol 41:245–258

    Article  CAS  PubMed  Google Scholar 

  • Torres Acosta JA, De Almeida Engler J, Raes J, Magyar Z, De Groodt R, Inzé D, De Veylder L (2004) Molecular characterization of Arabidopsis PHO80-like proteins, a novel class of CDKA;1-interacting cyclins. Cell Mol Life Sci 61:1485–1497

    Article  CAS  PubMed  Google Scholar 

  • Wang G, Kong H, Sun Y, Zhang X, Zhang W, Altman N, DePamphilis CW, Ma H (2004) Genome-wide analysis of the cyclin family in Arabidopsis and comparative phylogenetic analysis of plant cyclin-like proteins. Plant Physiol 135:1084–1099

    Article  CAS  PubMed  Google Scholar 

  • Wang F, Huo SN, Guo J, Zhang XS (2006) Wheat D-Type cyclin Triae;CYCD2;1 regulate development of transgenic Arabidopsis plants. Planta 224:1129–1140

    Article  CAS  PubMed  Google Scholar 

  • Watanabe N, Broome M, Hunter T (1995) Regulation of the human WEE1Hu CDK tyrosine 15-kinase during the cell cycle. EMBO J 14:1878–1891

    CAS  PubMed  Google Scholar 

  • Yoshida K, Wada T, Koyama H, Mizobuchi-Fukuoka R, Naito S (1999) Temporal and spatial patterns of accumulation of the transcript of Myo-inositol-1-phosphate synthase and phytin-containing particles during seed development in rice. Plant Physiol 119:65–72

    Article  CAS  PubMed  Google Scholar 

  • Zhao W, Su HY, Song J, Zhao XY, Zhang XS (2006) Ectopic expression of TaYAB1, a member of YABBY gene family in wheat, causes the partial abaxialization of the adaxial epidermises of leaves and arrests the development of shoot apical meristem in Arabidopsis. Plant Sci 170:364–371

    Article  CAS  Google Scholar 

  • Zheng Q, Wang XJ (2008) GOEAST: a Web-based software toolkit for Gene Ontology enrichment analysis. Nucleic Acids Res 36:W358–W363

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Dr. LQ, Qu (Institute of Botany, Chinese Academy of Sciences, Beijing 100093, China) for generously providing the endosperm-specific GluA-1 gene promoter, and Dr. K. Chong for his kindly supplying the vector pTCK303 (Institute of Botany, Chinese Academy of Sicences, Beijing 100093, China). This research was supported by the Major State Basic Research Program of the People’s Republic of China (2005CB120803).

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  1. Jing Guo

    Present address: College of Life Sciences, Northeast Forestry University, 150040, Harbin, Heilongjiang, China

  2. Jian Song

    Present address: Department of Biology, Dezhou University, 253023, Dezhou, Shandong, China

Authors and Affiliations

  1. State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, 271018, Taian, Shandong, China

    Fang Wang, Wei Sun & Xian Sheng Zhang

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  1. Jing Guo
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Correspondence to Xian Sheng Zhang.

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Guo, J., Wang, F., Song, J. et al. The expression of Orysa;CycB1;1 is essential for endosperm formation and causes embryo enlargement in rice. Planta 231, 293–303 (2010). https://doi.org/10.1007/s00425-009-1051-y

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