YAO is a Nucleolar WD40-repeat Protein Critical for Embryogenesis and Gametogenesis in Arabidopsis

Overview

Journal BMC Plant Biol

Publisher Biomed Central

Specialty Biology

Date 2010 Aug 12

PMID 20699009

Citations 23

Authors

Hong-Ju Li

Nai-you Liu

Dong-Qiao Shi

Jie Liu

Wei-Cai Yang

Affiliations

Soon will be listed here.

Abstract

Background: In flowering plants, gametogenesis generates multicellular male and female gametophytes. In the model system Arabidopsis, the male gametophyte or pollen grain contains two sperm cells and a vegetative cell. The female gametophyte or embryo sac contains seven cells, namely one egg, two synergids, one central cell and three antipodal cells. Double fertilization of the central cell and egg produces respectively a triploid endosperm and a diploid zygote that develops further into an embryo. The genetic control of the early embryo patterning, especially the initiation of the first zygotic division and the positioning of the cell plate, is largely unknown.

Results: Here we report the characterization of a mutation, yaozhe (yao), that causes zygote arrest and misplacement of cell plate of the zygote, leading to early embryo lethality. In addition, gametophyte development is partially impaired. A small portion of the mutant embryo sacs are arrested at four-nucleate stage with aberrant nuclear positioning. Furthermore, the competence of male gametophytes is also compromised. YAO encodes a nucleolar protein with seven WD-repeats. Its homologues in human and yeast have been shown to be components of the U3 snoRNP complex and function in 18S rRNA processing. YAO is expressed ubiquitously, with high level of expression in tissues under active cell divisions, including embryo sacs, pollen, embryos, endosperms and root tips.

Conclusions: Phenotypic analysis indicated that YAO is required for the correct positioning of the first zygotic division plane and plays a critical role in gametogenesis in Arabidopsis. Since YAO is a nucleolar protein and its counterparts in yeast and human are components of the U3 snoRNP complex, we therefore postulate that YAO is most likely involved in rRNA processing in plants as well.

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References

Liu M, Yuan L, Liu N, Shi D, Liu J, Yang W . GAMETOPHYTIC FACTOR 1, involved in pre-mRNA splicing, is essential for megagametogenesis and embryogenesis in Arabidopsis. J Integr Plant Biol. 2009; 51(3):261-71. DOI: 10.1111/j.1744-7909.2008.00783.x. View

Lam Y, Trinkle-Mulcahy L, Lamond A . The nucleolus. J Cell Sci. 2005; 118(Pt 7):1335-7. DOI: 10.1242/jcs.01736. View

Tzafrir I, Pena-Muralla R, Dickerman A, Berg M, Rogers R, Hutchens S . Identification of genes required for embryo development in Arabidopsis. Plant Physiol. 2004; 135(3):1206-20. PMC: 519041. DOI: 10.1104/pp.104.045179. View

Shevell D, Leu W, Gillmor C, Xia G, Feldmann K, Chua N . EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7. Cell. 1994; 77(7):1051-62. DOI: 10.1016/0092-8674(94)90444-8. View

Steinborn K, Maulbetsch C, Priester B, Trautmann S, Pacher T, Geiges B . The Arabidopsis PILZ group genes encode tubulin-folding cofactor orthologs required for cell division but not cell growth. Genes Dev. 2002; 16(8):959-71. PMC: 152350. DOI: 10.1101/gad.221702. View

Visintin R, Hwang E, Amon A . Cfi1 prevents premature exit from mitosis by anchoring Cdc14 phosphatase in the nucleolus. Nature. 1999; 398(6730):818-23. DOI: 10.1038/19775. View

Xu J, Zhang H, Xie C, Xue H, Dijkhuis P, Liu C . EMBRYONIC FACTOR 1 encodes an AMP deaminase and is essential for the zygote to embryo transition in Arabidopsis. Plant J. 2005; 42(5):743-56. DOI: 10.1111/j.1365-313X.2005.02411.x. View

Olson M, Hingorani K, Szebeni A . Conventional and nonconventional roles of the nucleolus. Int Rev Cytol. 2002; 219:199-266. PMC: 7133188. DOI: 10.1016/s0074-7696(02)19014-0. View

Smyth D, Bowman J, Meyerowitz E . Early flower development in Arabidopsis. Plant Cell. 1990; 2(8):755-67. PMC: 159928. DOI: 10.1105/tpc.2.8.755. View

10.

Meinke D, Muralla R, Sweeney C, Dickerman A . Identifying essential genes in Arabidopsis thaliana. Trends Plant Sci. 2008; 13(9):483-91. DOI: 10.1016/j.tplants.2008.06.003. View

11.

Griffith M, Mayer U, Capron A, Ngo Q, Surendrarao A, McClinton R . The TORMOZ gene encodes a nucleolar protein required for regulated division planes and embryo development in Arabidopsis. Plant Cell. 2007; 19(7):2246-63. PMC: 1955705. DOI: 10.1105/tpc.106.042697. View

12.

Hernandez-Verdun D . The nucleolus: a model for the organization of nuclear functions. Histochem Cell Biol. 2006; 126(2):135-48. DOI: 10.1007/s00418-006-0212-3. View

13.

Pagnussat G, Yu H, Ngo Q, Rajani S, Mayalagu S, Johnson C . Genetic and molecular identification of genes required for female gametophyte development and function in Arabidopsis. Development. 2005; 132(3):603-14. DOI: 10.1242/dev.01595. View

14.

Shi D, Liu J, Xiang Y, Ye D, Sundaresan V, Yang W . SLOW WALKER1, essential for gametogenesis in Arabidopsis, encodes a WD40 protein involved in 18S ribosomal RNA biogenesis. Plant Cell. 2005; 17(8):2340-54. PMC: 1182493. DOI: 10.1105/tpc.105.033563. View

15.

Venema J, Vos H, Faber A, van Venrooij W, Raue H . Yeast Rrp9p is an evolutionarily conserved U3 snoRNP protein essential for early pre-rRNA processing cleavages and requires box C for its association. RNA. 2000; 6(11):1660-71. PMC: 1370034. DOI: 10.1017/s1355838200001369. View

16.

Clough S, Bent A . Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 1999; 16(6):735-43. DOI: 10.1046/j.1365-313x.1998.00343.x. View

17.

Moll C, von Lyncker L, Zimmermann S, Kagi C, Baumann N, Twell D . CLO/GFA1 and ATO are novel regulators of gametic cell fate in plants. Plant J. 2008; 56(6):913-21. DOI: 10.1111/j.1365-313X.2008.03650.x. View

18.

Lukowiak A, Granneman S, Mattox S, Speckmann W, Jones K, Pluk H . Interaction of the U3-55k protein with U3 snoRNA is mediated by the box B/C motif of U3 and the WD repeats of U3-55k. Nucleic Acids Res. 2000; 28(18):3462-71. PMC: 110750. DOI: 10.1093/nar/28.18.3462. View

19.

Fleurdepine S, Deragon J, Devic M, Guilleminot J, Bousquet-Antonelli C . A bona fide La protein is required for embryogenesis in Arabidopsis thaliana. Nucleic Acids Res. 2007; 35(10):3306-21. PMC: 1904278. DOI: 10.1093/nar/gkm200. View

20.

Jurgens G . Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development. 1994; 120(10):2967-78. DOI: 10.1242/dev.120.10.2967. View