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

Plant Molecular Biology

Volumn 70, Issue 5, 2009, Pages 581-601

  Gibalová, Antónia ^a,b   Reňák, David ^a,c   Matczuk, Katarzyna ^a   Dupl'Áková, Nikoleta ^a   Cháb, David ^a   Twell, David ^d   Honys, David ^a,b  

^a INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

^b CHARLES UNIVERSITY   (Czech Republic)

^c UNIVERSITY OF SOUTH BOHEMIA   (Czech Republic)

^d UNIVERSITY OF LEICESTER   (United Kingdom)

Author keywords

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

Indexed keywords

ARABIDOPSIS PROTEIN; BZIP34 PROTEIN, ARABIDOPSIS; TRANSACTIVATOR PROTEIN;

ARABIDOPSIS; ARTICLE; CELL WALL; FLOWER; FLUORESCENCE MICROSCOPY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; PHYSIOLOGY; POLLEN; POLLEN TUBE; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCANNING ELECTRON MICROSCOPY; TRANSGENIC PLANT; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL WALL; FLOWERS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; GENETIC COMPLEMENTATION TEST; METABOLIC NETWORKS AND PATHWAYS; MICROSCOPY, ELECTRON, SCANNING; MICROSCOPY, ELECTRON, TRANSMISSION; MICROSCOPY, FLUORESCENCE; MUTATION; PLANTS, GENETICALLY MODIFIED; POLLEN; POLLEN TUBE; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TRANS-ACTIVATORS;

ANIMALIA; ARABIDOPSIS; ARABIDOPSIS THALIANA;

EID: 67649205215     PISSN: 01674412     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11103-009-9493-y     Document Type: Article

References (95)

1. MG Aarts R Hodge K Kalantidis D Florack ZA Wilson BJ Mulligan WJ Stiekema R Scott AP Pereira 1997 The Arabidopsis MALE STERILITY 2 protein shares similarity with reductases in elongation/condensation complexes Plant J 12 615 623 10.1046/j.1365-313X.1997.00615.x (Pubitemid 27434040)
2. NN Alder Y Shen JL Brodsky LM Hendershot AE Johnson 2005 The molecular mechanisms underlying BiP-mediated gating of the Sec61 translocon of the endoplasmic reticulum J Cell Biol 168 389 399 10.1083/jcb.200409174
3. RS Allen J Li MI Stahle A Dubroue F Gubler AA Millar 2007 Genetic analysis reveals functional redundancy and the major target genes of the Arabidopsis miR159 family Proc Natl Acad Sci USA 104 16371 16376 10.1073/pnas.0707653104
4. T Ariizumi K Hatakeyama K Hinata S Sato T Kato S Tabata K Toriyama 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 10.1023/B:PLAN.0000009269.97773.70
5. T Ariizumi K Hatakeyama K Hinata R Inatsugi I Nishida S Sato T Kato S Tabata K Toriyama 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 10.1111/j.1365-313X.2004.02118.x
6. T Ariizumi T Kawanabe K Hatakeyama S Sato T Kato S Tabata K Toriyama 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 10.1093/pcp/pcm167
7. R Beckmann D Bubeck R Grassucci P Penczek A Verschoor G Blobel J Frank 1997 Alignment of conduits for the nascent polypeptide chain in the ribosome-Sec61 complex Science 278 2123 2126 10.1126/science.278.5346.2123
8. LC Boavida S [tmp] McCormick 2007 Temperature as a determinant factor for increased and reproducible in vitro pollen germination in Arabidopsis thaliana Plant J 52 570 582 10.1111/j.1365-313X.2007.03248.x
9. KW Bock D Honys JM Ward S Padmanaban EP Nawrocki KD Hirschi D Twell H Sze 2006 Integrating membrane transport with male gametophyte development and function through transcriptomics Plant Physiol 140 1151 1168 10.1104/pp.105.074708
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. YN Chen E Slabaugh F Brandizzi 2008 Membrane-tethered transcription factors in Arabidopsis thaliana: novel regulators in stress response and development Curr Opin Plant Biol 11 695 701 10.1016/j.pbi.2008.10.005
13. H Choi J Hong J Ha J Kang SY Kim 2000 ABFs, a family of ABA-responsive element binding factors J Biol Chem 275 1723 1730 10.1074/jbc.275.3.1723
14. SJ Clough AF Bent 1998 Floral dip: a simplified method for agrobacterium-mediated transformation of Arabidopsis thaliana Plant J 16 735 743 10.1046/j.1365-313x.1998.00343.x
15. CP Cluis CF Mouchel CS Hardtke 2004 The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways Plant J 38 332 347 10.1111/j.1365-313X.2004.02052.x
16. LG Correa DM Riano-Pachon CG Schrago RV dos Santos B Mueller-Roeber M Vincentz 2008 The role of bZIP transcription factors in green plant evolution: adaptive features emerging from four founder genes PLoS ONE 3 e2944 10.1371/journal.pone.0002944
17. GJ Darlington N Wang RW Hanson 1995 C/EBP alpha: a critical regulator of genes governing integrative metabolic processes Curr Opin Genet Dev 5 565 570 10.1016/0959-437X(95)80024-7
18. GJ Darlington SE Ross OA [tmp] MacDougald 1998 The role of C/EBP genes in adipocyte differentiation J Biol Chem 273 30057 30060 10.1074/jbc.273.46.30057
19. CD Deppmann RS Alvania EJ Taparowsky 2006 Cross-species annotation of basic leucine zipper factor interactions: insight into the evolution of closed interaction networks Mol Biol Evol 23 1480 1492 10.1093/molbev/msl022
20. X Dong Z Hong M Sivaramakrishnan M Mahfouz DP Verma 2005 Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis Plant J 42 315 328 10.1111/j.1365-313X.2005. 02379.x
21. N Dupl'áková D Reňák P Hovanec B Honysová D Twell D Honys 2007 Arabidopsis gene family profiler (aGFP)-user-oriented transcriptomic database with easy-to-use graphic interface BMC Plant Biol 7 39 10.1186/1471-2229-7-39
22. A Durbarry I Vizir D Twell 2005 Male germ line development in Arabidopsis. duo pollen mutants reveal gametophytic regulators of generative cell cycle progression Plant Physiol 137 297 307 10.1104/pp.104.053165
23. C Eady K Lindsey D Twell 1995 The significance of microspore division and division symmetry for vegetative cell-specific transcription and generative cell differentiation Plant Cell 7 65 74
24. R Eferl M Sibilia F Hilberg A Fuchsbichler I Kufferath B Guertl R Zenz EF Wagner K Zatloukal 1999 Functions of c-Jun in liver and heart development J Cell Biol 145 1049 1061 10.1083/jcb.145.5.1049
25. A Ehlert F Weltmeier X Wang CS Mayer S Smeekens J Vicente-Carbajosa W Droge-Laser 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 10.1111/j.1365-313X.2006.02731.x
26. RR Finkelstein TJ Lynch 2000 The Arabidopsis abscisic acid response gene ABI5 encodes a basic leucine zipper transcription factor Plant Cell 12 599 609 (Pubitemid 30254875)
27. J Fukazawa T Sakai S Ishida I Yamaguchi Y Kamiya Y Takahashi 2000 Repression of shoot growth, a bZIP transcriptional activator, regulates cell elongation by controlling the level of gibberellins Plant Cell 12 901 915 (Pubitemid 30458036)
28. YF Guan XY Huang J Zhu JF Gao HX Zhang ZN Yang 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 10.1104/pp.108.118026
29. D Honys D Twell 2003 Comparative analysis of the Arabidopsis pollen transcriptome Plant Physiol 132 640 652 10.1104/pp.103.020925
30. D Honys D Twell 2004 Transcriptome analysis of haploid male gametophyte development in Arabidopsis Genome Biol 5 R85 10.1186/gb-2004-5-11-r85
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 76-87
32. T Ito N Nagata Y Yoshiba M Ohme-Takagi H Ma K Shinozaki 2007 Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development Plant Cell 19 3549 3562 10.1105/tpc.107.054536
33. Y Iwata N Koizumi 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 10.1073/pnas.0408941102
34. Y Iwata NV Fedoroff N Koizumi 2008 Arabidopsis bZIP60 is a proteolysis-activated transcription factor involved in the endoplasmic reticulum stress response Plant Cell 20 11 3107 3121
35. M Jakoby B Weisshaar W Droge-Laser J Vicente-Carbajosa J Tiedemann T Kroj F Parcy 2002 bZIP transcription factors in Arabidopsis Trends Plant Sci 7 106 111 10.1016/S1360-1385(01)02223-3
36. M Karimi B De Meyer P Hilson 2005 Modular cloning in plant cells Trends Plant Sci 10 103 105 (Pubitemid 40323292)
37. H Kindl 1993 Fatty acid degradation in plant peroxisomes: function and biosynthesis of the enzymes involved Biochimie 75 225 230 10.1016/0300-9084(93) 90080-C
38. M Leroch HE Neuhaus S Kirchberger S Zimmermann M Melzer J Gerhold J Tjaden 2008 Identification of a novel adenine nucleotide transporter in the endoplasmic reticulum of Arabidopsis Plant Cell 20 438 451 10.1105/tpc.107. 057554
39. C Li WH Wong 2001 Model-based analysis of oligonucleotide arrays: expression index computation and outlier detection Proc Natl Acad Sci USA 98 31 36 10.1073/pnas.011404098
40. C Li WH Wong 2001 Model-based analysis of oligonucleotide arrays: model validation, design issues and standard error application Genome Biol 2 R32
41. JX Liu R Srivastava P Che SH Howell 2007 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 10.1105/tpc.106.050021
42. JX Liu R Srivastava P Che SH Howell 2007 Salt stress responses in Arabidopsis utilize a signal transduction pathway related to endoplasmic reticulum stress signaling Plant J 51 897 909 10.1111/j.1365-313X.2007.03195.x
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, Planta
44. E Martinoia M Klein M Geisler L Bovet C Forestier U Kolukisaoglu B Muller-Rober B Schulz 2002 Multifunctionality of plant ABC transporters-more than just detoxifiers Planta 214 345 355 10.1007/s004250100661
45. McCormick S (2004) Control of male gametophyte development. Plant Cell 16(Suppl):S142-S153. doi: 10.1105/tpc.016659
46. AA Millar F Gubler 2005 The Arabidopsis GAMYB-like genes, MYB33 and MYB65, are microRNA-regulated genes that redundantly facilitate anther development Plant Cell 17 705 721 10.1105/tpc.104.027920
47. DJ Murphy 2001 The biogenesis and functions of lipid bodies in animals, plants and microorganisms Prog Lipid Res 40 325 438 10.1016/S0163-7827(01)00013- 3
48. JR Newman AE Keating 2003 Comprehensive identification of human bZIP interactions with coiled-coil arrays Science 300 2097 2101 10.1126/science. 1084648
49. A Nijhawan M Jain AK Tyagi JP Khurana 2008 Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice Plant Physiol 146 333 350 10.1104/pp.107.112821
50. S Nishikawa GM Zinkl RJ Swanson D Maruyama D Preuss 2005 Callose (beta-1, 3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth BMC Plant Biol 5 22 10.1186/1471-2229-5-22
51. JB Ohlrogge J Browse CR Somerville 1991 The genetics of plant lipids Biochim Biophys Acta 1082 1 26
52. SK Park R Howden D Twell 1998 The Arabidopsis thaliana gametophytic mutation gemini pollen1 disrupts microspore polarity, division asymmetry and pollen cell fate Development 125 3789 3799 (Pubitemid 28488354)
53. DM Paxson-Sowders CH Dodrill HA Owen CA Makaroff 2001 DEX1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis Plant Physiol 127 1739 1749 10.1104/pp.010517 (Pubitemid 34050037)
54. P Piffanelli JHE Ross DJ Murphy 1998 Biogenesis and function of the lipidic structures of pollen grains Sex Plant Reprod 11 65 80 10.1007/s004970050122
55. C Pina F Pinto JA Feijo JD Becker 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 10.1104/pp.104.057935
56. I Pracharoenwattana JE Cornah SM Smith 2007 Arabidopsis peroxisomal malate dehydrogenase functions in beta-oxidation but not in the glyoxylate cycle Plant J 50 381 390 10.1111/j.1365-313X.2007.03055.x
57. C Ringli B Keller 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 10.1023/A:1006030007333
58. N Rotman A Durbarry A Wardle WC Yang A Chaboud JE Faure F Berger D Twell 2005 A novel class of MYB factors controls sperm-cell formation in plants Curr Biol 15 244 248 10.1016/j.cub.2005.01.013
59. R Sanchez-Fernandez TG Davies JO Coleman PA Rea 2001 The Arabidopsis thaliana ABC protein superfamily, a complete inventory J Biol Chem 276 30231 30244 10.1074/jbc.M103104200
60. R Sanchez-Fernandez PA Rea TG Davies JO Coleman 2001 Do plants have more genes than humans? Yes, when it comes to ABC proteins Trends Plant Sci 6 347 348 10.1016/S1360-1385(01)02038-6 (Pubitemid 33141646)
61. S Sanyal DJ Sandstrom CA Hoeffer M Ramaswami 2002 AP-1 functions upstream of CREB to control synaptic plasticity in Drosophila Nature 416 870 874 10.1038/416870a
62. U Schindler AE Menkens H Beckmann JR Ecker AR Cashmore 1992 Heterodimerization between light-regulated and ubiquitously expressed Arabidopsis GBF bZIP proteins EMBO J 11 1261 1273
63. PJ Seo SG Kim CM Park 2008 Membrane-bound transcription factors in plants Trends Plant Sci 13 10 550 556
64. H Shen K Cao X Wang 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 10.1016/j.bbrc.2007.08.026
65. H Shen K Cao X Wang 2008 AtbZIP16 and AtbZIP68, two new members of GBFs, can interact with other G group bZIPs in Arabidopsis thaliana BMB Rep 41 132 138
66. DR Smyth JL Bowman EM Meyerowitz 1990 Early flower development in Arabidopsis Plant Cell 2 755 767 (Pubitemid 120015483)
67. A Svendsen 2000 Lipase protein engineering Biochim Biophys Acta 1543 223 238 (Pubitemid 32063090)
68. H Sze S Padmanaban F Cellier D Honys NH Cheng KW Bock G Conejero X Li D Twell JM Ward KD Hirschi 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 10.1104/pp.104.046003
69. H Tajima Y Iwata M Iwano S Takayama N Koizumi 2008 Identification of an Arabidopsis transmembrane bZIP transcription factor involved in the endoplasmic reticulum stress response Biochem Biophys Res Commun 374 242 247 10.1016/j.bbrc.2008.07.021
70. T Takeda T Toda K Kominami A Kohnosu M Yanagida N Jones 1995 Schizosaccharomyces pombe atf1+ encodes a transcription factor required for sexual development and entry into stationary phase EMBO J 14 6193 6208 (Pubitemid 26007306)
71. T Takeda K Amano MA Ohto K Nakamura S Sato T Kato S Tabata C Ueguchi 2006 RNA interference of the Arabidopsis putative transcription factor TCP16 gene results in abortion of early pollen development Plant Mol Biol 61 165 177 10.1007/s11103-006-6265-9
72. T Takeda R Ozaki Y Onodera Y Takahashi K Yamaguchi T Berberich N Koizumi T Kusano 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 6 603 611
73. JK Teller LA Fahien E Valdivia 1990 Interactions among mitochondrial aspartate aminotransferase, malate dehydrogenase, and the inner mitochondrial membrane from heart, hepatoma, and liver J Biol Chem 265 19486 19494 (Pubitemid 120013890)
74. O Thimm O Blasing Y Gibon A Nagel S Meyer P Kruger J Selbig LA Muller SY Rhee M Stitt 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 10.1111/j.1365-313X.2004.02016.x
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 15-45
76. Y Uno T Furihata H Abe R Yoshida K Shinozaki K Yamaguchi-Shinozaki 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 10.1073/pnas.190309197 (Pubitemid 30780947)
77. AC Van Aelst ES Pierson JL Van Went M Cresti 1993 Ultrastructural changes of Arabidopsis thaliana pollen during final maturation and rehydration Zygote 1 173 179 10.1017/S096719940000143X
78. W Verelst H Saedler T Munster 2007 MIKC*MADS-protein complexes bind motifs enriched in the proximal region of late pollen-specific Arabidopsis promoters Plant Physiol 143 447 460 10.1104/pp.106.089805
79. W Verelst D Twell S de Folter R Immink H Saedler T Munster 2007 MADS-complexes regulate transcriptome dynamics during pollen maturation Genome Biol 8 R249 10.1186/gb-2007-8-11-r249
80. PJ Verrier D Bird B Burla E Dassa C Forestier M Geisler M Klein U Kolukisaoglu Y Lee E Martinoia A Murphy PA Rea L Samuels B Schulz EJ Spalding K Yazaki FL Theodoulou 2008 Plant ABC proteins-a unified nomenclature and updated inventory Trends Plant Sci 13 151 159 10.1016/j.tplants.2008.02.001
81. G Vizcay-Barrena ZA Wilson 2006 Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant J Exp Bot 57 2709 2717 10.1093/jxb/erl032
82. ZQ Wang C Ovitt AE Grigoriadis U Mohle-Steinlein U Ruther EF Wagner 1992 Bone and haematopoietic defects in mice lacking c-fos Nature 360 741 745 10.1038/360741a0
83. Y Watanabe M Yamamoto 1996 Schizosaccharomyces pombe pcr1+ encodes a CREB/ATF protein involved in regulation of gene expression for sexual development Mol Cell Biol 16 704 711
84. Weigel D, Glazebrook J (2002) Arabidopsis. A laboratory handbook. Cold Spring Harbor Laboratory Press, Cold Spring Harbor
85. F Weltmeier F Rahmani A Ehlert K Dietrich K Schutze X Wang C Chaban J Hanson M Teige K Harter J Vicente-Carbajosa S Smeekens W Droge-Laser 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 10.1007/s11103-008-9410-9
86. KW Wirtz 1991 Phospholipid transfer proteins Annu Rev Biochem 60 73 99 10.1146/annurev.bi.60.070191.000445
87. Y Xiang N Tang H Du H Ye L Xiong 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 10.1104/pp.108.128199
88. S Yamaguchi S Mitsui L Yan K Yagita S Miyake H Okamura 2005 Role of DBP in the circadian oscillatory mechanism Mol Cell Biol 20 4773 4781 10.1128/MCB.20.13.4773-4781.2000
89. Y Yamamoto M Nishimura I Hara-Nishimura T Noguchi 2003 Behavior of vacuoles during microspore and pollen development in Arabidopsis thaliana Plant Cell Physiol 44 1192 1201 10.1093/pcp/pcg147
90. C Yang G Vizcay-Barrena K Conner ZA Wilson 2007 MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis Plant Cell 19 3530 3548 10.1105/tpc.107.054981
91. Y Yin Q Zhu S Dai C Lamb RNP Beachy 1997 RF2a, a bZIP transcriptional activator of the phloem-specific rice tungro bacilliform virus promoter, functions in vascular development EMBO J 16 5247 5259 10.1093/emboj/16.17.5247
92. ZB Zhang J Zhu JF Gao C Wang H Li HQ Zhang S Zhang DM Wang QX Wang H Huang HJ Xia ZN Yang 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 10.1111/j.1365-313X.2007.03254.x
93. SL Zhou D Stump CL Kiang LM Isola PD Berk 1995 Mitochondrial aspartate aminotransferase expressed on the surface of 3T3-L1 adipocytes mediates saturable fatty acid uptake Proc Soc Exp Biol Med 208 263 270
94. J Zhu H Chen H Li JF Gao H Jiang C Wang YF Guan ZN Yang 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 10.1111/j.1365-313X.2008.03500.x
95. P Zimmermann L Hennig W Gruissem 2005 Gene-expression analysis and network discovery using Genevestigator Trends Plant Sci 10 407 409 10.1016/j.tplants.2005.07.003