Multiple BiP genes of arabidopsis thaliana are required for male gametogenesis and pollen competitiveness

Plant and Cell Physiology

Volumn 55, Issue 4, 2014, Pages 801-810

  Maruyama, Daisuke ^a   Sugiyama, Tomoyuki ^b   Endo, Toshiya ^a   Nishikawa, Shuh Ichi ^a,b  

^a NAGOYA UNIVERSITY   (Japan)

^b NIIGATA UNIVERSITY   (Japan)

Author keywords

Arabidopsis thaliana; Endoplasmic reticulum; Male gametogenesis; Molecular chaperone; Pollen tube

Indexed keywords

ARABIDOPSIS PROTEIN; BIP1 PROTEIN, ARABIDOPSIS; BIP2 PROTEIN, ARABIDOPSIS; BIP3 PROTEIN, ARABIDOPSIS; CHAPERONE;

ARABIDOPSIS; CHROMOSOME SEGREGATION; ENDOPLASMIC RETICULUM; GENETICS; GERMINATION; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MITOSIS; MUTATION; PHYSIOLOGY; PLANT GAMETOGENESIS; PLANT GENE; POLLEN; POLLEN TUBE; PROMOTER REGION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CHROMOSOME SEGREGATION; ENDOPLASMIC RETICULUM; GAMETOGENESIS, PLANT; GENES, PLANT; GERMINATION; MITOSIS; MOLECULAR CHAPERONES; MUTATION; POLLEN; POLLEN TUBE; PROMOTER REGIONS, GENETIC;

EID: 84898870660     PISSN: 00320781     EISSN: 14719053     Source Type: Journal    
DOI: 10.1093/pcp/pcu018     Document Type: Article

References (36)

1. Alexander, M.P. (1969) Differential staining of aborted and nona-borted pollen. Stain Technol. 44: 117-122.
2. Anelli, T. and Sitia, R. (2008) Protein quality control in the early secretory pathway. EMBO J. 27: 315-327.
3. Bedinger, P. (1992) The remarkable biology of pollen. Plant Cell 4: 879-887.
4. Boavida, L.C. and McCormick, S. (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J. 52: 570-582.
5. Bukau, B., Weissman, J.S. and Horwich, A.L. (2006) Molecular chaper-ones and protein quality control. Cell 125: 443-451.
6. Buzeli, R.A., Cascardo, J.C., Rodrigues, L.A., Andrade, M.O., Almeida, R.S., Loureiro, M.E. et al. (2002) Tissue-specific regulation of BiP genes: a cis-acting regulatory domain is required for BiP promoter activity in plant meristems. Plant Mol. Biol. 50: 757-771.
7. Cheung, A.Y., Chen, C.Y.-H., Glaven, R.H., de Graaf, B.H.J., Vidali, L., Hepler, P.K. et al. (2002) Rab2 GTPase regulates vesicle trafficking between the endoplasmic reticulum and the Golgi bodies and is important to pollen tube growth. Plant Cell 14: 945-962.
8. Christensen, C.A., King, E.J., Jordan, J. and Drews, G.N. (1997) Megagametogenesis in Arabidopsis wild type and the Gf mutant. Sex. Plant Reprod. 10: 49-64.
9. Clough, S.J. and Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16: 735-743.
10. Cole, R.A., Synek, L., Zarsky, V. and Fowler, J.E. (2005) SEC8, a subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth. Plant Physiol. 138: 2005-2018.
11. Copenhaver, G.P., Keith, K.C. and Preuss, D. (2000) Tetrad analysis in higher plants. A budding technology. Plant Physiol. 124: 7-16.
12. Honys, D. and Twell, D. (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol. 5: R85.
13. Johnson, M.A., von Besser, K., Zhou, Q., Smith, E., Aux, G., Patton, D. et al. (2004) Arabidopsis hapless mutations define essential gam-etophytic functions. Genetics 168: 971-982.
14. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
15. Luo, S., Mao, C., Lee, B. and Lee, A.S. (2006) GRP78/BiP is required for cell proliferation and protecting the inner cell mass from apoptosis during early mouse embryonic development. Mol. Cell. Biol. 26: 5688-5697.
16. Maruyama, D., Endo, T. and Nishikawa, S. (2010) BiP-mediated polar nuclei fusion is essential for the regulation of endosperm nuclei proliferation in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 107: 1684-1689.
17. McCormick, S. (2004) Control of male gametophyte development. Plant Cell 16 Suppl. S142-S153.
18. Nishikawa, S., Brodsky, J.L. and Nakatsukasa, K. (2005a) Roles of molecular chaperones in endoplasmic reticulum (ER) quality control and ER-associated degradation (ERAD). J. Biochem. 137: 551-555.
19. Nishikawa, S., Zinkl, G.M., Swanson, R.J., Maruyama, D. and Preuss, D. (2005b) Callose (beta-1, 3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth. BMC Plant Biol. 5: 22.
20. Noh, S.-J., Kwon, C.-S., Oh, D.-H., Moon, J.S. and Chung, W.-I. (2003) Expression of an evolutionarily distinct novel BiP gene during the unfolded protein response in Arabidopsis thaliana. Gene 311: 81-91.
21. Normington, K., Kohno, K., Kozutsumi, Y., Gething, M.J. and Sambrook, J.F. (1989) S. cerevisiae encodes an essential protein homologous in sequence and function to mammalian BiP. Cell 57: 1223-1236.
22. Peng, J., Ilarslan, H., Wurtele, E.S. and Bassham, D.C. (2011) AtRabD2b and AtRabD2c have overlapping functions in pollen development and pollen tube growth. BMC Plant Biol. 11: 25.
23. Preuss, D., Rhee, S.Y. and Davis, R.W. (1994) Tetrad analysis possible in Arabidopsis with mutation of the QUARTET (QRT) genes. Science 264: 1458-1460.
24. Qin, Y., Leydon, A.R., Manziello, A., Pandey, R., Mount, D., Denic, S. et al. (2009) Penetration of the stigma and style elicits a novel transcriptome in pollen tubes, pointing to genes critical for growth in a pistil. PLoS Genet. 5: e1000621.
25. Rose, M.D., Misra, L.M. and Vogel, J.P. (1989) KAR2, a karyogamy gene, is the yeast homolog of the mammalian BiP/GRP78 gene. Cell 57: 1211-1221.
26. Samaj, J., Müller, J., Beck, M., Böhm, N. and Menzel, D. (2006) Vesicular trafficking, cytoskeleton and signalling in root hairs and pollen tubes. Trends Plant Sci. 11: 594-600.
27. Sarkar, N.K., Kundnani, P. and Grover, A. (2013) Functional analysis of Hsp70 superfamily proteins of rice (Oryza sativa). Cell Stress Chaperones 18: 427-437.
28. Sessions, A., Burke, E., Presting, G., Aux, G., McElver, J.A., Patton, D.A. et al. (2002) A high-throughput Arabidopsis reverse genetics system. Plant Cell 14: 2985-2994.
29. Sherman, F. and Wakem, P. (1991) Mapping yeast genes. Methods Enzymol. 194: 38-57.
30. Sung, D.Y., Vierling, E. and Guy, C.L. (2001) Comprehensive expression profile analysis of the Arabidopsis Hsp70 gene family. Plant Physiol. 126: 789-800.
31. Szumlanski, A.L. and Nielsen, E. (2009) The Rab GTPase RabA4d regulates pollen tube tip growth in Arabidopsis thaliana. Plant Cell 21: 526-544.
32. Towbin, H., Staehelin, T. and Gordon, J. (1979) Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc. Natl Acad. Sci. USA 76: 4350-4354.
33. Tuskan, G.A., Difazio, S., Jansson, S., Bohlmann, J., Grigoriev, I., Hellsten, U. et al. (2006) The genome of black cottonwood, Populus trichocarpa (Torr. and Gray). Science 313: 1596-1604.
34. Twell, D., Yamaguchi, J. and McCormick, S. (1990) Pollen-specific gene expression in transgenic plants: coordinate regulation of two different tomato gene promoters during microsporogenesis. Development 109: 705-713.
35. Velasco, R., Zharkikh, A., Troggio, M., Cartwright, D.A., Cestaro, A., Pruss, D. et al. (2007) A high quality draft consensus sequence of the genome of a heterozygous grapevine variety. PLoS One 2: e1326.
36. Yamamoto, M., Maruyama, D., Endo, T. and Nishikawa, S. (2008) Arabidopsis thaliana has a set of J proteins in the endoplasmic reticulum that are conserved from yeast to animals and plants. Plant Cell Physiol. 49: 1547-1562.