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Plant Molecular Biology

, Volume 70, Issue 5, pp 581–601 | Cite as

AtbZIP34 is required for Arabidopsis pollen wall patterning and the control of several metabolic pathways in developing pollen

  • Antónia Gibalová
  • David Reňák
  • Katarzyna Matczuk
  • Nikoleta Dupl’áková
  • David Cháb
  • David Twell
  • David Honys
Article

Abstract

Sexual plant reproduction depends on the production and differentiation of functional gametes by the haploid gametophyte generation. Currently, we have a limited understanding of the regulatory mechanisms that have evolved to specify the gametophytic developmental programs. To unravel such mechanisms, it is necessary to identify transcription factors (TF) that are part of such haploid regulatory networks. Here we focus on bZIP TFs that have critical roles in plants, animals and other kingdoms. We report the functional characterization of Arabidopsis thaliana AtbZIP34 that is expressed in both gametophytic and surrounding sporophytic tissues during flower development. T-DNA insertion mutants in AtbZIP34 show pollen morphological defects that result in reduced pollen germination efficiency and slower pollen tube growth both in vitro and in vivo. Light and fluorescence microscopy revealed misshapen and misplaced nuclei with large lipid inclusions in the cytoplasm of atbzip34 pollen. Scanning and transmission electron microscopy revealed defects in exine shape and micropatterning and a reduced endomembrane system. Several lines of evidence, including the AtbZIP34 expression pattern and the phenotypic defects observed, suggest a complex role in male reproductive development that involves a sporophytic role in exine patterning, and a sporophytic and/or gametophytic mode of action of AtbZIP34 in several metabolic pathways, namely regulation of lipid metabolism and/or cellular transport.

Keywords

bZIP transcription factor AtbZIP34 Male gametophyte development Lipid metabolism Cellular transport Cell wall formation Transcriptomics 

Notes

Acknowledgments

Authors thank Dr Milada Čiamporová (Institute of Botany, Slovak Academy of Sciences) and Dr Aleš Soukup (Department of Plant Physiology, Charles University in Prague) for their expertise with evaluation of transmission electron micrographs. Authors gratefully acknowledge financial support from Grant Agency of the Czech Republic (GACR grants 522/06/0896 and 522/09/0858) and Ministry of Education of the Czech Republic (MSMT grant LC06004). DT acknowledges support from the Biotechnology and Biological Sciences Research Council (BBSRC) and the University of Leicester.

Supplementary material

11103_2009_9493_MOESM1_ESM.pdf (52 kb)
Supplementary material 1 (PDF 51 kb)
11103_2009_9493_MOESM2_ESM.xls (42 kb)
Supplementary Table 2 Expression of AtbZIP transcription factors in various tissues and cell types according to aGFP database (Duplakova et al., 2007). (XLS 42 kb)
11103_2009_9493_MOESM3_ESM.xls (322 kb)
Supplementary Table 3 List of genes at least two-fold downregulated in atbzip34 pollen (XLS 322 kb)
11103_2009_9493_MOESM4_ESM.xls (500 kb)
Supplementary Table 4 List of genes at least two-fold upregulated in atbzip34 pollen (XLS 500 kb)
11103_2009_9493_MOESM5_ESM.xls (57 kb)
Supplementary table 5 List of genes showing late male gametophytic expression profile and at least two-fold downregulated in atbzip34 pollen (XLS 57 kb)
11103_2009_9493_MOESM6_ESM.xls (24 kb)
Supplementary Table 6 List of genes showing late male gametophytic expression profile and at least two-fold upregulated in atbzip34 pollen (XLS 23 kb)
11103_2009_9493_MOESM7_ESM.pdf (65 kb)
Supplementary material 7 (PDF 65 kb)
11103_2009_9493_MOESM8_ESM.pdf (3 mb)
Supplementary Fig. 1 Transmission electron micrographs of cross-sections of developing male gametophyte from tetrad stage to bicellular pollen. wild type (A, C, E, G, I, K) and atbzip34 (B, D, F, H, J, L). Size bar corresponds to 2 µm (A, B, E-H, J-L) and 5 µm (C, D, I). Tetrad stage (A-D). Tetrads of haploid microspores are surrounded by callose wall and deposits of sporopollenin are visible on surface of outer callose wall in wt (A). Primexine forms characteristic undulations in wt, while the atbzip34 tetrads (B) seem to be younger with smooth plasma membrane and thinner callose wall with no sporopollenin deposits on the outher callosic wall. The structure of tapetum was similar in wt (C) and mutant (D). Uninucleate microspore stage (E-H). Microspores of wt (E) and mutant (F) looked similar with large nucleus and smooth cytoplasm. On the contrary, mutant tapetal cells (H) were less vacuolated than wt (G) and contained clusters of electron-dense granules along the locule wall. Late bicellular stage (I-L). Unlike wt (I), vegetative cell of atbzip34 bicellular pollen (J) was highly vacuolated and was enclosed in characteristic wrinkled intine On the contrary, there were no apparent ultrastructural differences in wt (K) and atbzip34 (L) tapetum; in both genotypes elaioplasts were fully developed. BA, baculae; C, callose wall; E, endothecium; EL, elaioplast; ER, endoplasmic reticulum; GC, generative cell; I, electron-dense inclusions; IN, intine; LO, anther locule; M, middle layer; MS, microspore; N, nucleus; P, plastid; S, starch; T, tapetum; TC, tectum; V, vacuole; VC vegetative cell (PDF 3107 kb)
11103_2009_9493_MOESM9_ESM.pdf (582 kb)
Supplementary Fig. 2 MapMan visualization of genes with altered expression in atbzip34 pollen. General transporters (A), genes involved in development and cell wall and lipid metabolism (B), stress-response genes (C) and metabolic pathways leading to cell wall precursors (C) are shown. Logarithmic scale; downregulated genes in blue, upregulated genes in red (PDF 581 kb)
11103_2009_9493_MOESM10_ESM.pdf (246 kb)
Supplementary Fig. 3 MapMan visualization of transcription factor genes with altered expression in atbzip34 pollen. Logarithmic scale; downregulated genes in blue, upregulated genes in red (PDF 245 kb)

References

  1. Aarts MG, Hodge R, Kalantidis K, Florack D, Wilson ZA, Mulligan BJ, Stiekema WJ, Scott R, Pereira AP (1997) The Arabidopsis MALE STERILITY 2 protein shares similarity with reductases in elongation/condensation complexes. Plant J 12:615–623. doi: 10.1046/j.1365-313X.1997.00615.x PubMedCrossRefGoogle Scholar
  2. Alder NN, Shen Y, Brodsky JL, Hendershot LM, Johnson AE (2005) The molecular mechanisms underlying BiP-mediated gating of the Sec61 translocon of the endoplasmic reticulum. J Cell Biol 168:389–399. doi: 10.1083/jcb.200409174 PubMedCrossRefGoogle Scholar
  3. Allen RS, Li J, Stahle MI, Dubroue A, Gubler F, Millar AA (2007) Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family. Proc Natl Acad Sci USA 104:16371–16376. doi: 10.1073/pnas.0707653104 PubMedCrossRefGoogle Scholar
  4. Ariizumi T, Hatakeyama K, Hinata K, Sato S, Kato T, Tabata S, Toriyama K (2003) A novel male-sterile mutant of Arabidopsis thaliana, faceless pollen-1, produces pollen with a smooth surface and an acetolysis-sensitive exine. Plant Mol Biol 53:107–116. doi: 10.1023/B:PLAN.0000009269.97773.70 PubMedCrossRefGoogle Scholar
  5. Ariizumi T, Hatakeyama K, Hinata K, Inatsugi R, Nishida I, Sato S, Kato T, Tabata S, Toriyama K (2004) Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana. Plant J 39:170–181. doi: 10.1111/j.1365-313X.2004.02118.x PubMedCrossRefGoogle Scholar
  6. Ariizumi T, Kawanabe T, Hatakeyama K, Sato S, Kato T, Tabata S, Toriyama K (2008) Ultrastructural characterization of exine development of the transient defective exine 1 mutant suggests the existence of a factor involved in constructing reticulate exine architecture from sporopollenin aggregates. Plant Cell Physiol 49:58–67. doi: 10.1093/pcp/pcm167 PubMedCrossRefGoogle Scholar
  7. Beckmann R, Bubeck D, Grassucci R, Penczek P, Verschoor A, Blobel G, Frank J (1997) Alignment of conduits for the nascent polypeptide chain in the ribosome-Sec61 complex. Science 278:2123–2126. doi: 10.1126/science.278.5346.2123 PubMedCrossRefGoogle Scholar
  8. Boavida LC, McCormick S (2007) Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana. Plant J 52:570–582. doi: 10.1111/j.1365-313X.2007.03248.x PubMedCrossRefGoogle Scholar
  9. Bock KW, Honys D, Ward JM, Padmanaban S, Nawrocki EP, Hirschi KD, Twell D, Sze H (2006) Integrating membrane transport with male gametophyte development and function through transcriptomics. Plant Physiol 140:1151–1168. doi: 10.1104/pp.105.074708 PubMedCrossRefGoogle Scholar
  10. Borg M, Brownfield L, Twell D (2009) Male gametophyte development: a molecular perspective. J Exp Bot. doi: 10.1093/jxb/ern355
  11. Brownfield L, Hafidh S, Borg M, Sidorova A, Mori T, Twell D (2009) A plant germ cell-specific integrator of cell cycle progression and sperm specification. PLoS Genet 5 doi: 10.1371/journal.pgen.1000430
  12. Chen YN, Slabaugh E, Brandizzi F (2008) Membrane-tethered transcription factors in Arabidopsis thaliana: novel regulators in stress response and development. Curr Opin Plant Biol 11:695–701. doi: 10.1016/j.pbi.2008.10.005 PubMedCrossRefGoogle Scholar
  13. Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730. doi: 10.1074/jbc.275.3.1723 PubMedCrossRefGoogle Scholar
  14. Clough SJ, Bent AF (1998) Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743. doi: 10.1046/j.1365-313x.1998.00343.x PubMedCrossRefGoogle Scholar
  15. Cluis CP, Mouchel CF, Hardtke CS (2004) The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant J 38:332–347. doi: 10.1111/j.1365-313X.2004.02052.x PubMedCrossRefGoogle Scholar
  16. Correa LG, Riano-Pachon DM, Schrago CG, dos Santos RV, Mueller-Roeber B, Vincentz M (2008) The role of bZIP transcription factors in green plant evolution: adaptive features emerging from four founder genes. PLoS ONE 3:e2944. doi: 10.1371/journal.pone.0002944 PubMedCrossRefGoogle Scholar
  17. Darlington GJ, Wang N, Hanson RW (1995) C/EBP alpha: a critical regulator of genes governing integrative metabolic processes. Curr Opin Genet Dev 5:565–570. doi: 10.1016/0959-437X(95)80024-7 PubMedCrossRefGoogle Scholar
  18. Darlington GJ, Ross SE, MacDougald OA (1998) The role of C/EBP genes in adipocyte differentiation. J Biol Chem 273:30057–30060. doi: 10.1074/jbc.273.46.30057 PubMedCrossRefGoogle Scholar
  19. Deppmann CD, Alvania RS, Taparowsky EJ (2006) Cross-species annotation of basic leucine zipper factor interactions: insight into the evolution of closed interaction networks. Mol Biol Evol 23:1480–1492. doi: 10.1093/molbev/msl022 PubMedCrossRefGoogle Scholar
  20. Dong X, Hong Z, Sivaramakrishnan M, Mahfouz M, Verma DP (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J 42:315–328. doi: 10.1111/j.1365-313X.2005.02379.x PubMedCrossRefGoogle Scholar
  21. Dupl’áková N, Reňák D, Hovanec P, Honysová B, Twell D, Honys D (2007) Arabidopsis gene family profiler (aGFP)—user-oriented transcriptomic database with easy-to-use graphic interface. BMC Plant Biol 7:39. doi: 10.1186/1471-2229-7-39 PubMedCrossRefGoogle Scholar
  22. Durbarry A, Vizir I, Twell D (2005) Male germ line development in Arabidopsis. duo pollen mutants reveal gametophytic regulators of generative cell cycle progression. Plant Physiol 137:297–307. doi: 10.1104/pp.104.053165 PubMedCrossRefGoogle Scholar
  23. Eady C, Lindsey K, Twell D (1995) The significance of microspore division and division symmetry for vegetative cell-specific transcription and generative cell differentiation. Plant Cell 7:65–74PubMedCrossRefGoogle Scholar
  24. Eferl R, Sibilia M, Hilberg F, Fuchsbichler A, Kufferath I, Guertl B, Zenz R, Wagner EF, Zatloukal K (1999) Functions of c-Jun in liver and heart development. J Cell Biol 145:1049–1061. doi: 10.1083/jcb.145.5.1049 PubMedCrossRefGoogle Scholar
  25. Ehlert A, Weltmeier F, Wang X, Mayer CS, Smeekens S, Vicente-Carbajosa J, Droge-Laser W (2006) Two-hybrid protein–protein interaction analysis in Arabidopsis protoplasts: establishment of a heterodimerization map of group C and group S bZIP transcription factors. Plant J 46:890–900. doi: 10.1111/j.1365-313X.2006.02731.x PubMedCrossRefGoogle Scholar
  26. Finkelstein RR, Lynch TJ (2000) The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor. Plant Cell 12:599–609PubMedCrossRefGoogle Scholar
  27. Fukazawa J, Sakai T, Ishida S, Yamaguchi I, Kamiya Y, Takahashi Y (2000) Repression of shoot growth, a bZIP transcriptional activator, regulates cell elongation by controlling the level of gibberellins. Plant Cell 12:901–915PubMedCrossRefGoogle Scholar
  28. Guan YF, Huang XY, Zhu J, Gao JF, Zhang HX, Yang ZN (2008) RUPTURED POLLEN GRAIN1, a member of the MtN3/saliva gene family, is crucial for exine pattern formation and cell integrity of microspores in Arabidopsis. Plant Physiol 147:852–863. doi: 10.1104/pp.108.118026 PubMedCrossRefGoogle Scholar
  29. Honys D, Twell D (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiol 132:640–652. doi: 10.1104/pp.103.020925 PubMedCrossRefGoogle Scholar
  30. Honys D, Twell D (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biol 5:R85. doi: 10.1186/gb-2004-5-11-r85 PubMedCrossRefGoogle Scholar
  31. Honys D, Reňák D, Twell D (2006) Male gametophyte development and function. In: Teixeira da Silva J (ed) Floriculture, ornamental and plant biotechnology: advances and topical issues, 1st edn. Global Science Books, London, pp 76–87Google Scholar
  32. Ito T, Nagata N, Yoshiba Y, Ohme-Takagi M, Ma H, Shinozaki K (2007) Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development. Plant Cell 19:3549–3562. doi: 10.1105/tpc.107.054536 PubMedCrossRefGoogle Scholar
  33. Iwata Y, Koizumi N (2005) An Arabidopsis transcription factor, AtbZIP60, regulates the endoplasmic reticulum stress response in a manner unique to plants. Proc Natl Acad Sci USA 102:5280–5285. doi: 10.1073/pnas.0408941102 PubMedCrossRefGoogle Scholar
  34. Iwata Y, Fedoroff NV, Koizumi N (2008) Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response. Plant Cell 20(11):3107–3121PubMedCrossRefGoogle Scholar
  35. Jakoby M, Weisshaar B, Droge-Laser W, Vicente-Carbajosa J, Tiedemann J, Kroj T, Parcy F (2002) bZIP transcription factors in Arabidopsis. Trends Plant Sci 7:106–111. doi: 10.1016/S1360-1385(01)02223-3 PubMedCrossRefGoogle Scholar
  36. Karimi M, De Meyer B, Hilson P (2005) Modular cloning in plant cells. Trends Plant Sci 10:103–105PubMedGoogle Scholar
  37. Kindl H (1993) Fatty acid degradation in plant peroxisomes: function and biosynthesis of the enzymes involved. Biochimie 75:225–230. doi: 10.1016/0300-9084(93)90080-C PubMedCrossRefGoogle Scholar
  38. Leroch M, Neuhaus HE, Kirchberger S, Zimmermann S, Melzer M, Gerhold J, Tjaden J (2008) Identification of a novel adenine nucleotide transporter in the endoplasmic reticulum of Arabidopsis. Plant Cell 20:438–451. doi: 10.1105/tpc.107.057554 PubMedCrossRefGoogle Scholar
  39. Li C, Wong WH (2001a) Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection. Proc Natl Acad Sci USA 98:31–36. doi: 10.1073/pnas.011404098 PubMedCrossRefGoogle Scholar
  40. Li C, Wong WH (2001b) Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application. Genome Biol 2:R32Google Scholar
  41. Liu JX, Srivastava R, Che P, Howell SH (2007a) An endoplasmic reticulum stress response in Arabidopsis is mediated by proteolytic processing and nuclear relocation of a membrane-associated transcription factor, bZIP28. Plant Cell 19:4111–4119. doi: 10.1105/tpc.106.050021 PubMedCrossRefGoogle Scholar
  42. Liu JX, Srivastava R, Che P, Howell SH (2007b) Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling. Plant J 51:897–909. doi: 10.1111/j.1365-313X.2007.03195.x PubMedCrossRefGoogle Scholar
  43. Lu G, Gao C, Zheng X, Han B (2008) Identification of OsbZIP72 as a positive regulator of ABA response and drought tolerance in rice. Epub ahead of print, PlantaGoogle Scholar
  44. Martinoia E, Klein M, Geisler M, Bovet L, Forestier C, Kolukisaoglu U, Muller-Rober B, Schulz B (2002) Multifunctionality of plant ABC transporters—more than just detoxifiers. Planta 214:345–355. doi: 10.1007/s004250100661 PubMedCrossRefGoogle Scholar
  45. McCormick S (2004) Control of male gametophyte development. Plant Cell 16(Suppl):S142–S153. doi: 10.1105/tpc.016659 Google Scholar
  46. Millar AA, Gubler F (2005) The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development. Plant Cell 17:705–721. doi: 10.1105/tpc.104.027920 PubMedCrossRefGoogle Scholar
  47. Murphy DJ (2001) The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog Lipid Res 40:325–438. doi: 10.1016/S0163-7827(01)00013-3 PubMedCrossRefGoogle Scholar
  48. Newman JR, Keating AE (2003) Comprehensive identification of human bZIP interactions with coiled-coil arrays. Science 300:2097–2101. doi: 10.1126/science.1084648 PubMedCrossRefGoogle Scholar
  49. Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008) Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice. Plant Physiol 146:333–350. doi: 10.1104/pp.107.112821 PubMedCrossRefGoogle Scholar
  50. Nishikawa S, Zinkl GM, Swanson RJ, Maruyama D, Preuss D (2005) Callose (beta-1, 3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth. BMC Plant Biol 5:22. doi: 10.1186/1471-2229-5-22 PubMedCrossRefGoogle Scholar
  51. Ohlrogge JB, Browse J, Somerville CR (1991) The genetics of plant lipids. Biochim Biophys Acta 1082:1–26PubMedGoogle Scholar
  52. Park SK, Howden R, Twell D (1998) The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate. Development 125:3789–3799PubMedGoogle Scholar
  53. Paxson-Sowders DM, Dodrill CH, Owen HA, Makaroff CA (2001) DEX1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis. Plant Physiol 127:1739–1749. doi: 10.1104/pp.010517 PubMedCrossRefGoogle Scholar
  54. Piffanelli P, Ross JHE, Murphy DJ (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex Plant Reprod 11:65–80. doi: 10.1007/s004970050122 CrossRefGoogle Scholar
  55. Pina C, Pinto F, Feijo JA, Becker JD (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiol 138:744–756. doi: 10.1104/pp.104.057935 PubMedCrossRefGoogle Scholar
  56. Pracharoenwattana I, Cornah JE, Smith SM (2007) Arabidopsis peroxisomal malate dehydrogenase functions in beta-oxidation but not in the glyoxylate cycle. Plant J 50:381–390. doi: 10.1111/j.1365-313X.2007.03055.x PubMedCrossRefGoogle Scholar
  57. Ringli C, Keller B (1998) Specific interaction of the tomato bZIP transcription factor VSF-1 with a non-palindromic DNA sequence that controls vascular gene expression. Plant Mol Biol 37:977–988. doi: 10.1023/A:1006030007333 PubMedCrossRefGoogle Scholar
  58. Rotman N, Durbarry A, Wardle A, Yang WC, Chaboud A, Faure JE, Berger F, Twell D (2005) A novel class of MYB factors controls sperm-cell formation in plants. Curr Biol 15:244–248. doi: 10.1016/j.cub.2005.01.013 PubMedCrossRefGoogle Scholar
  59. Sanchez-Fernandez R, Davies TG, Coleman JO, Rea PA (2001a) The Arabidopsis thaliana ABC protein superfamily, a complete inventory. J Biol Chem 276:30231–30244. doi: 10.1074/jbc.M103104200 PubMedCrossRefGoogle Scholar
  60. Sanchez-Fernandez R, Rea PA, Davies TG, Coleman JO (2001b) Do plants have more genes than humans? Yes, when it comes to ABC proteins. Trends Plant Sci 6:347–348. doi: 10.1016/S1360-1385(01)02038-6 PubMedCrossRefGoogle Scholar
  61. Sanyal S, Sandstrom DJ, Hoeffer CA, Ramaswami M (2002) AP-1 functions upstream of CREB to control synaptic plasticity in Drosophila. Nature 416:870–874. doi: 10.1038/416870a PubMedCrossRefGoogle Scholar
  62. Schindler U, Menkens AE, Beckmann H, Ecker JR, Cashmore AR (1992) Heterodimerization between light-regulated and ubiquitously expressed Arabidopsis GBF bZIP proteins. EMBO J 11:1261–1273PubMedGoogle Scholar
  63. Seo PJ, Kim SG, Park CM (2008) Membrane-bound transcription factors in plants. Trends Plant Sci 13(10):550–556PubMedCrossRefGoogle Scholar
  64. Shen H, Cao K, Wang X (2007) A conserved proline residue in the leucine zipper region of AtbZIP34 and AtbZIP61 in Arabidopsis thaliana interferes with the formation of homodimer. Biochem Biophys Res Commun 362:425–430. doi: 10.1016/j.bbrc.2007.08.026 PubMedCrossRefGoogle Scholar
  65. Shen H, Cao K, Wang X (2008) AtbZIP16 and AtbZIP68, two new members of GBFs, can interact with other G group bZIPs in Arabidopsis thaliana. BMB Rep 41:132–138PubMedGoogle Scholar
  66. Smyth DR, Bowman JL, Meyerowitz EM (1990) Early flower development in Arabidopsis. Plant Cell 2:755–767PubMedCrossRefGoogle Scholar
  67. Svendsen A (2000) Lipase protein engineering. Biochim Biophys Acta 1543:223–238PubMedGoogle Scholar
  68. Sze H, Padmanaban S, Cellier F, Honys D, Cheng NH, Bock KW, Conejero G, Li X, Twell D, Ward JM, Hirschi KD (2004) Expression patterns of a novel AtCHX gene family highlight potential roles in osmotic adjustment and K+ homeostasis in pollen development. Plant Physiol 136:2532–2547. doi: 10.1104/pp.104.046003 PubMedCrossRefGoogle Scholar
  69. Tajima H, Iwata Y, Iwano M, Takayama S, Koizumi N (2008) Identification of an Arabidopsis transmembrane bZIP transcription factor involved in the endoplasmic reticulum stress response. Biochem Biophys Res Commun 374:242–247. doi: 10.1016/j.bbrc.2008.07.021 PubMedCrossRefGoogle Scholar
  70. Takeda T, Toda T, Kominami K, Kohnosu A, Yanagida M, Jones N (1995) Schizosaccharomyces pombe atf1+ encodes a transcription factor required for sexual development and entry into stationary phase. EMBO J 14:6193–6208PubMedGoogle Scholar
  71. Takeda T, Amano K, Ohto MA, Nakamura K, Sato S, Kato T, Tabata S, Ueguchi C (2006) RNA interference of the Arabidopsis putative transcription factor TCP16 gene results in abortion of early pollen development. Plant Mol Biol 61:165–177. doi: 10.1007/s11103-006-6265-9 PubMedCrossRefGoogle Scholar
  72. Tateda C, Ozaki R, Onodera Y, Takahashi Y, Yamaguchi K, Berberich T, Koizumi N, Kusano T (2008) NtbZIP60, an endoplasmic reticulum-localized transcription factor, plays a role in the defense response against bacterial pathogens in Nicotiana tabacum. J Plant Res 121(6):603–611CrossRefGoogle Scholar
  73. Teller JK, Fahien LA, Valdivia E (1990) Interactions among mitochondrial aspartate aminotransferase, malate dehydrogenase, and the inner mitochondrial membrane from heart, hepatoma, and liver. J Biol Chem 265:19486–19494PubMedGoogle Scholar
  74. Thimm O, Blasing O, Gibon Y, Nagel A, Meyer S, Kruger P, Selbig J, Muller LA, Rhee SY, Stitt M (2004) MAPMAN: a user-driven tool to display genomics data sets onto diagrams of metabolic pathways and other biological processes. Plant J 37:914–939. doi: 10.1111/j.1365-313X.2004.02016.x PubMedCrossRefGoogle Scholar
  75. Twell D, Oh S-A, Honys D (2006) Pollen development, a genetic and transcriptomic view. In: Malho R (ed) The pollen tube, vol 3. Springer–Verlag, Berlin, Heidelberg, pp 15–45CrossRefGoogle Scholar
  76. Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637. doi: 10.1073/pnas.190309197 PubMedCrossRefGoogle Scholar
  77. Van Aelst AC, Pierson ES, Van Went JL, Cresti M (1993) Ultrastructural changes of Arabidopsis thaliana pollen during final maturation and rehydration. Zygote 1:173–179. doi: 10.1017/S096719940000143X PubMedGoogle Scholar
  78. Verelst W, Saedler H, Munster T (2007a) MIKC* MADS-protein complexes bind motifs enriched in the proximal region of late pollen-specific Arabidopsis promoters. Plant Physiol 143:447–460. doi: 10.1104/pp.106.089805 PubMedCrossRefGoogle Scholar
  79. Verelst W, Twell D, de Folter S, Immink R, Saedler H, Munster T (2007b) MADS-complexes regulate transcriptome dynamics during pollen maturation. Genome Biol 8:R249. doi: 10.1186/gb-2007-8-11-r249 PubMedCrossRefGoogle Scholar
  80. Verrier PJ, Bird D, Burla B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E, Murphy A, Rea PA, Samuels L, Schulz B, Spalding EJ, Yazaki K, Theodoulou FL (2008) Plant ABC proteins—a unified nomenclature and updated inventory. Trends Plant Sci 13:151–159. doi: 10.1016/j.tplants.2008.02.001 PubMedCrossRefGoogle Scholar
  81. Vizcay-Barrena G, Wilson ZA (2006) Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant. J Exp Bot 57:2709–2717. doi: 10.1093/jxb/erl032 PubMedCrossRefGoogle Scholar
  82. Wang ZQ, Ovitt C, Grigoriadis AE, Mohle-Steinlein U, Ruther U, Wagner EF (1992) Bone and haematopoietic defects in mice lacking c-fos. Nature 360:741–745. doi: 10.1038/360741a0 PubMedCrossRefGoogle Scholar
  83. Watanabe Y, Yamamoto M (1996) Schizosaccharomyces pombe pcr1+ encodes a CREB/ATF protein involved in regulation of gene expression for sexual development. Mol Cell Biol 16:704–711PubMedGoogle Scholar
  84. Weigel D, Glazebrook J (2002) Arabidopsis. A laboratory handbook. Cold Spring Harbor Laboratory Press, Cold Spring HarborGoogle Scholar
  85. Weltmeier F, Rahmani F, Ehlert A, Dietrich K, Schutze K, Wang X, Chaban C, Hanson J, Teige M, Harter K, Vicente-Carbajosa J, Smeekens S, Droge-Laser W (2009) Expression patterns within the Arabidopsis C/S1 bZIP transcription factor network: availability of heterodimerization partners controls gene expression during stress response and development. Plant Mol Biol 69:107–119. doi: 10.1007/s11103-008-9410-9 PubMedCrossRefGoogle Scholar
  86. Wirtz KW (1991) Phospholipid transfer proteins. Annu Rev Biochem 60:73–99. doi: 10.1146/annurev.bi.60.070191.000445 PubMedCrossRefGoogle Scholar
  87. Xiang Y, Tang N, Du H, Ye H, Xiong L (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952. doi: 10.1104/pp.108.128199 PubMedCrossRefGoogle Scholar
  88. Yamaguchi S, Mitsui S, Yan L, Yagita K, Miyake S, Okamura H (2005) Role of DBP in the circadian oscillatory mechanism. Mol Cell Biol 20:4773–4781. doi: 10.1128/MCB.20.13.4773-4781.2000 CrossRefGoogle Scholar
  89. Yamamoto Y, Nishimura M, Hara-Nishimura I, Noguchi T (2003) Behavior of vacuoles during microspore and pollen development in Arabidopsis thaliana. Plant Cell Physiol 44:1192–1201. doi: 10.1093/pcp/pcg147 PubMedCrossRefGoogle Scholar
  90. Yang C, Vizcay-Barrena G, Conner K, Wilson ZA (2007) MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis. Plant Cell 19:3530–3548. doi: 10.1105/tpc.107.054981 PubMedCrossRefGoogle Scholar
  91. Yin Y, Zhu Q, Dai S, Lamb C, Beachy RNP (1997) RF2a, a bZIP transcriptional activator of the phloem-specific rice tungro bacilliform virus promoter, functions in vascular development. EMBO J 16:5247–5259. doi: 10.1093/emboj/16.17.5247 PubMedCrossRefGoogle Scholar
  92. Zhang ZB, Zhu J, Gao JF, Wang C, Li H, Zhang HQ, Zhang S, Wang DM, Wang QX, Huang H, Xia HJ, Yang ZN (2007) Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. Plant J 52:528–538. doi: 10.1111/j.1365-313X.2007.03254.x PubMedCrossRefGoogle Scholar
  93. Zhou SL, Stump D, Kiang CL, Isola LM, Berk PD (1995) Mitochondrial aspartate aminotransferase expressed on the surface of 3T3–L1 adipocytes mediates saturable fatty acid uptake. Proc Soc Exp Biol Med 208:263–270PubMedGoogle Scholar
  94. Zhu J, Chen H, Li H, Gao JF, Jiang H, Wang C, Guan YF, Yang ZN (2008) Defective in Tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J 55:266–277. doi: 10.1111/j.1365-313X.2008.03500.x PubMedCrossRefGoogle Scholar
  95. Zimmermann P, Hennig L, Gruissem W (2005) Gene-expression analysis and network discovery using Genevestigator. Trends Plant Sci 10:407–409. doi: 10.1016/j.tplants.2005.07.003 PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2009

Authors and Affiliations

  • Antónia Gibalová
    • 1
    • 2
  • David Reňák
    • 1
    • 3
  • Katarzyna Matczuk
    • 1
  • Nikoleta Dupl’áková
    • 1
  • David Cháb
    • 4
  • David Twell
    • 5
  • David Honys
    • 1
    • 2
  1. 1.Laboratory of Pollen BiologyInstitute of Experimental Botany ASCRPraha 6Czech Republic
  2. 2.Department of Plant Physiology, Faculty of ScienceCharles University in PraguePraha 2Czech Republic
  3. 3.Faculty of Biological Sciences, Department of Plant Physiology and AnatomyUniversity of South BohemiaCeske BudejoviceCzech Republic
  4. 4.Plant Reproduction LabInstitute of Experimental Botany ASCRPraha 6Czech Republic
  5. 5.Department of BiologyUniversity of LeicesterLeicesterUK

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