Pollen wall development: The associated enzymes and metabolic pathways

Plant Biology

Volumn 15, Issue 2, 2013, Pages 249-263

  Jiang, J ^a   Zhang, Z ^a,b   Cao, J ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b Taizhou Academy of Agriculture Sciences   (China)

Author keywords

Callose; Cellulose; Exine; Fatty acid; Intine; Metabolism; Pectin; Pollen wall; Primexine; Sporopollenin

Indexed keywords

BIOPOLYMER; CALLOSE; CAROTENOID; GLUCAN; GLUCAN 1,3 BETA GLUCOSIDASE; PECTIN; SPOROPOLLENIN; VEGETABLE PROTEIN; WAX;

CELLULOSE; ENVIRONMENTAL STRESS; ENZYME ACTIVITY; FATTY ACID; GAMETOPHYTE; METABOLISM; POLLEN;

ARABIDOPSIS; BIOSYNTHESIS; CELL WALL; ENZYMOLOGY; GENETIC TRANSCRIPTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; LIPID METABOLISM; METABOLISM; PLANT GENE; POLLEN; PROTEIN DEGRADATION; REVIEW; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; BIOLOGICAL TRANSPORT; BIOPOLYMERS; CAROTENOIDS; CELL WALL; GENES, PLANT; GLUCAN 1,3-BETA-GLUCOSIDASE; GLUCANS; LIPID METABOLISM; PECTINS; PLANT PROTEINS; POLLEN; PROTEOLYSIS; TRANSCRIPTION, GENETIC; WAXES;

EID: 84873475363     PISSN: 14358603     EISSN: 14388677     Source Type: Journal    
DOI: 10.1111/j.1438-8677.2012.00706.x     Document Type: Review

References (101)

1. Aarts M.G., Keijzer C.J., Stiekema W.J., Pereira A. (1995) Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. The Plant Cell, 7, 2115-2127.
2. Aarts M.G., Hodge R., Kalantidis K., Florack D., Wilson Z.A., Mulligan B.J., Stiekema W.J., Scott R., Pereira A. (1997) The Arabidopsis MALE STERILITY 2 protein shares similarity with reductases in elongation/condensation complexes. The Plant Journal, 12, 615-623.
3. Ahlers F., Thom I., Lambert J., Kuckuk R., Wiermann R. (1999) 1H NMR analysis of sporopollenin from Typha angustifolia. Phytochemistry, 50, 1095-1098.
4. Albersheim P., Darvill A., Roberts K., Sederoff R., Staehelin A. (2010) Plant cell walls: from chemistry to biology. Garland Science, New York, NY.
5. Ariizumi T., Toriyama K. (2011) Genetic regulation of sporopollenin synthesis and pollen exine development. Annual Review of Plant Biology, 62, 437-460.
6. 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 Molecular Biology, 53, 107-116.
7. Ariizumi T., Hatakeyama K., Hinata K., Inatsugi R., Nishida I., Sato S., Kat 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. The Plant Journal, 39, 170-181.
8. Arrizumi T., Hatakeyama K., Hinata K., Sato S., Kato T., Tabata S., Toriyama K. (2005) The HKM gene, which is identical to the MS1 gene of Arabidopsis thaliana, is essential for primexine formation and exine pattern formation. Sexual Plant Reproduction, 18, 1-7.
9. 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 Physiololgy, 49, 58-67.
10. Austin M.B., Noel J.P. (2003) The chalcone synthase superfamily of type III polyketide synthases. Natural Product Reports, 20, 79-110.
11. de Azevedo Souza C., Kim S.S., Koch S., Kienow L., Schneider K., McKim S.M., Haughn G.W., Kombrink E., Douglas C.J. (2009) A novel fatty acyl-CoA synthetase is required for pollen development and sporopollenin biosynthesis in Arabidopsis. The Plant Cell, 21, 507-525.
12. Bird D., Beisson F., Brigham A., Shin J., Greer S., Jetter R., Kunst L., Wu X., Yephremov A., Samuels L. (2007) Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. The Plant Journal, 52, 485-498.
13. Blackmore S., Wortley A.H., Skvarla J.J., Rowley J.R. (2007) Pollen wall development in flowering plants. New Phytologist, 174, 483-498.
14. Borg M., Brownfield L., Twell D. (2009) Male gametophyte development: a molecular perspective. Journal of Experimental Botany, 60, 1465-1478.
15. Bourdenx B., Bernard A., Domergue F., Pascal S., Léger A., Roby D., Pervent M., Vile D., Haslam R.P., Napier J.A. (2011a) Overexpression of Arabidopsis CER1 promotes wax VLC-alkane biosynthesis and influences plant response to biotic and abiotic stresses. Plant Physiology, 156, 29-45.
16. Bourdenx B., Bernard A., Domergue F., Pascal S., Léger A., Roby D., Pervent M., Vile D., Haslam R.P., Napier J.A. (2011b) Overexpression of Arabidopsis ECERIFERUM1 promotes wax very-long-chain alkane biosynthesis and influences plant response to biotic and abiotic stresses. Plant Physiology, 156, 29-45.
17. Bucciaglia P.A., Smith A.G. (1994) Cloning and characterization of Tag 1, a tobacco anther β-1, 3-glucanase expressed during tetrad dissolution. Plant Molecular Biology, 24, 903-914.
18. Cao J., Yu X., Ye W., Lu G., Xiang X. (2006) Functional analysis of a novel male fertility CYP86MF gene in Chinese cabbage (Brassica campestris L. ssp. chinensis Makino). Plant Cell Reports, 24, 715-723.
19. Chen W., Yu X.H., Zhang K., Shi J., De Oliveira S., Schreiber L., Shanklin J., Zhang D. (2011) Male Sterile2 encodes a plastid-localized fatty acyl carrier protein reductase required for pollen exine development in Arabidopsis. Plant Physiology, 157, 842-853.
20. Choi H., Jin J.Y., Choi S., Hwang J.U., Kim Y.Y., Suh M.C., Lee Y. (2011) An ABCG/WBC-type ABC transporter is essential for transport of sporopollenin precursors for exine formation in developing pollen. The Plant Journal, 65, 181-193.
21. Costaglioli P., Joubès J., Garcia C., Stef M., Arveiler B., Lessire R., Garbay B. (2005) Profiling candidate genes involved in wax biosynthesis in Arabidopsis thaliana by microarray analysis. Biochimica et Biophysica Acta - Molecular and Cell Biology of Lipids, 1734, 247-258.
22. Doan T.T.P., Carlsson A.S., Hamberg M., Bülow L., Stymne S., Olsson P. (2009) Functional expression of five Arabidopsis fatty acyl-CoA reductase genes in Escherichia coli. Journal of Plant Physiology, 166, 787-796.
23. Dobritsa A.A., Nishikawa S., Preuss D., Urbanczyk-Wochniak E., Sumner L.W., Hammond A., Carlson A.L., Swanson R.J. (2009) LAP3, a novel plant protein required for pollen development, is essential for proper exine formation. Sexual Plant Reproduction, 22, 167-177.
24. Dong X., Hong Z., Sivaramakrishnan M., Mahfouz M., Verma D.P. (2005) Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. The Plant Journal, 42, 315-328.
25. Doxey A.C., Yaish M.W.F., Moffatt B.A., Griffith M., McConkey B.J. (2007) Functional divergence in the Arabidopsis β-1, 3-glucanase gene family inferred by phylogenetic reconstruction of expression states. Molecular Biology and Evolution, 24, 1045-1055.
26. Edlund A.F., Swanson R., Preuss D. (2004) Pollen and stigma structure and function: the role of diversity in pollination. The Plant Cell, 16, S84-S97.
27. EL-Ghazaly G., Huysmans S., Smet E.F. (2001) Pollen development of Rondeletia odorata (Rubiaceae). American Journal of Botany, 88, 14-30.
28. Enns L.C., Kanaoka M.M., Torii K.U., Comai L., Okada K., Cleland R.E. (2005) Two callose synthase, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility. Plant Molecular Biology, 58, 333-349.
29. Fei H., Sawhney V.K. (2001) Ultrastructural characterization of male sterile33 (ms33) mutant in Arabidopsis affected in pollen desiccation and maturation. Canadian Journal of Botany, 79, 118-129.
30. Fei H., Zhang R., Pharis R.P., Sawhney V.K. (2004) Pleiotropic effects of the male sterile33 (ms33) mutation in Arabidopsis are associated with modifications in endogenous gibberellins, indole-3-acetic acid and abscisic acid. Planta, 219, 649-660.
31. Feng X., Dickinson H.G. (2007) Packaging the male germline in plants. Trends in Genetics, 23, 503-510.
32. Francis K.E., Lam S.Y., Copenhaver G.P. (2006) Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiology, 142, 1004-1013.
33. Gibalova A., Renak D., Matczuk K., Duplakova N., Chab D., Twell D., Honys D. (2009) AtbZIP34 is required for Arabidopsis pollen wall patterning and the control of several metabolic pathways in developing pollen. Plant Molecular Biology, 70, 581-601.
34. Goldberg R.B., Beals T.P., Sanders P.M. (1993) Anther development: basic principles and partical applications. The Plant Cell, 5, 1217-1229.
35. Grienenberger E., Kim S.S., Lallemand B., Geoffroy P., Heintz D., de Azevedo Souza C., Heitz T., Douglas C.J., Legrand M. (2010) Analysis of TETRAKETIDE α-PYRONE REDUCTASE function in Arabidopsis thaliana reveals a previously unknown, but conserved, biochemical pathway in sporopollenin monomer biosynthesis. The Plant Cell, 22, 4067-4083.
36. Guan Y.F., Huang X.Y., Zhu J., Gao J.F., Zhang H.X., Yang Z.N. (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 Physiology, 147, 852-863.
37. Hasegawa Y., Nakamura S., Uheda E., Nakamura N. (2000) Immunolocalization and possible roles of pectins during pollen growth and callose plug formation in angiosperms. Grana, 39, 46-55.
38. Heslop-Harrison J. (1968) Pollen wall development. Science, 161, 230-237.
39. Hess M.W. (1993) Cell-wall development in freeze-fixed pollen: intine formation of Ledebouria socialis (Hyacinthaceae). Planta, 189, 139-149.
40. Higginson T., Li S.F., Parish R.W. (2003) AtMYB103 regulates tapetum and trichome development in Arabidopsis thaliana. The Plant Journal, 35, 177-192.
41. Hird D.L., Worrall D., Hodge R., Smartt S., Paul W., Scott R. (1993) The anther-specific protein encoded by the Brassica napus and Arabidopsis thaliana A6 gene displays similarity to β-1, 3-glucanases. The Plant Journal, 4, 1023-1033.
42. Honys D., Twell D. (2003) Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiology, 132, 640-652.
43. Honys D., Twell D. (2004) Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biology, 5, R85.
44. Huang L., Cao J.S., Zhang A.H., Ye Y.Q. (2008) Characterization of a putative pollen-specific arabinogalactan protein gene, BcMF8, from Brassica campestris ssp. chinensis. Molecular Biology Reports, 35, 631-639.
45. Huang L., Cao J., Zhang A., Ye Y., Zhang Y., Liu T. (2009a) The polygalacturonase gene BcMF2 from Brassica campestris is associated with intine development. Journal of Experimental Botany, 60, 301-313.
46. Huang L., Cao J., Zhang A.H., Zhang Y.C., Ye Y.Q. (2009b) Characterisation of BcMF10, a novel gene involved in pollen wall development of Brassica rapa ssp. chinensis. Functional Plant Biology, 35, 1194-1204.
47. Huang L., Liu Y., Yu X., Xiang X., Cao J. (2011) A polygalacturonase inhibitory protein gene (BcMF19) expressed during pollen development in chinese cabbagepak-choi. Molecular Biology Reports, 38, 545-552.
48. 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. The Plant Cell, 19, 3549-3562.
49. Jung K.H., Han M.J., Lee D.Y., Lee Y.S., Schreiber L., Franke R., Faust A., Yephremov A., Saedler H., Kim Y.W. (2006) Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. The Plant Cell, 18, 3015-3032.
50. Kandel S., Sauveplane V., Compagnon V., Franke R., Millet Y., Schreiber L., Werck-Reichhart D., Pinot F. (2007) Characterization of a methyl jasmonate and wounding-responsive cytochrome P450 of Arabidopsis thaliana catalyzing dicarboxylic fatty acid formation in vitro. FEBS Journal, 274, 5116-5127.
51. Kienow L., Schneider K., Bartsch M., Stuible H.P., Weng H., Miersch O., Wasternack C., Kombrink E. (2008) Jasmonates meet fatty acids: functional analysis of a new acyl-coenzyme A synthetase family from Arabidopsis thaliana. Journal of Experimental Botany, 59, 403-419.
52. Kim S.S., Grienenberger E., Lallemand B., Colpitts C.C., Kim S.Y., de Azevedo Souza C., Geoffroy P., Heintz D., Krahn D., Kaiser M. (2010) LAP6/POLYKETIDE SYNTHASE A and LAP5/POLYKETIDE SYNTHASE B encode hydroxyalkyl α-pyrone synthases required for pollen development and sporopollenin biosynthesis in Arabidopsis thaliana. The Plant Cell, 22, 4045-4066.
53. Li H., Zhang D. (2010) Biosynthesis of anther cuticle and pollen exine in rice. Plant Signaling and Behavior, 5, 1121-1123.
54. Li S.F., Higginson T., Parish R.W. (1999) A novel MYB-related gene from Arabidopsis thaliana expressed in development anthers. Plant Cell Physiololgy, 40, 343-347.
55. Li N., Zhang D.S., Liu H.S., Yin C.S., Li X., Liang W., Yuan Z., Xu B., Chu H.W., Wang J., Wen T.Q., Huang H., Luo D., Ma H., Zhang D.B. (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. The Plant Cell, 18, 2999-3014.
56. Li H., Pinot F., Sauveplane V., Werck-Reichhart D., Diehl P., Schreiber L., Franke R., Zhang P., Chen L., Gao Y., Liang W., Zhang D. (2010) Cytochrome P450 family member CYP704B2 catalyzes the {omega}-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. The Plant Cell, 22, 173-190.
57. Li H., Yuan Z., Vizcay-Barrena G., Yang C., Liang W., Zong J., Wilson Z.A., Zhang D. (2011) PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiology, 156, 615-630.
58. Li-Beisson Y., Shorrosh B., Beisson F., Andersson M.X., Arondel V., Bates P.D., Baud S., Bird D., DeBono A., Durrett T.P. (2010) Acyl-lipid metabolism. The Arabidopsis Book/American Society of Plant Biologists, 8, e0133.
59. Liu L.C., Cao J.S., Yu X.L., Xiang X., Fei Y.J. (2006) Expression of an Antisense BcMF3 affects microsporogenesis and pollen tube growth in Arabidopsis. Agricultural Sciences in China, 5, 339-345.
60. McNeil K.J., Smith A.G. (2010) A glycine-rich protein that facilitates exine formation during tomato pollen development. Planta, 231, 793-808.
61. Micheli F. (2001) Pectin methylesterases: cell wall enzymes with important roles in plant physiology. Trends in Plant Science, 6, 414-419.
62. Morant M., Jorgensen K., Schaller H., Pinot F., Moller B.L., Werck-Reichhart D., Bak S. (2007) CYP703 is an ancient cytochrome P450 in land plants catalyzing in-chain hydroxylation of lauric acid to provide building blocks for sporopollenin synthesis in pollen. The Plant Cell, 19, 1473-1487.
63. Nishikawa S., Zinkl G.M., Swanson R.J., Maruyama D., Preuss D. (2005) Callose (beta-1, 3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth. BMC Plant Biology, 5, 22.
64. Otegui M.S., Staehelin L.A. (2004) Electron tomographic analysis of post-meiotic cytokinesis during pollen development in Arabidopsis thaliana. Planta, 218, 501-515.
65. Owen H.A., Markaroff C.A. (1995) Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thanliana (L.) Heynh. ecotype Wassilewskija (Brassicaceae). Protoplasma, 185, 7-21.
66. Palusa S.G., Golovkin M., Shin S.B., Richardson D.N., Reddy A.S. (2007) Organ-specific, development, hormonal and stress regulation of expression of putative pectate lyase genes in Arabidapsis. New phytologist, 174, 537-550.
67. Park S.K., Twell D. (2001) Novel patterns of ectopic cell plate growth and lipid body distribution in the Arabidopsis gemini pollen1 mutant. Plant Physiology, 126, 899-909.
68. Paxson-Sowders D., Owen H., Makaroff C. (1996) A comparative ultrastructural analysis of exine pattern development in wild-type Arabidopsis and a mutant defective in pattern formation. Protoplasma, 198, 53-65.
69. Paxson-Sowders D.M., Owen H.A., Makaroff C.A. (1997) A comparative ultrastructural analysis of exine pattern development in wild-type Arabidopsis and a mutant defective in pattern formation. Protoplasma, 198, 53-65.
70. Paxson-Sowders D.M., Dodrill C.H., Owen H.A., Makaroff C.A. (2001) DEX1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis. Plant Physiology, 127, 1739-1749.
71. Persson S., Paredez A., Carroll A., Palsdottir H., Doblin M., Piondexter P., Khitrov N., Auer M., Somerville C.R. (2007) Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America, 104, 15566-15571.
72. Pina C., Pinto F., Feijó J., Becker J. (2005) Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control, and gene expression regulation. Plant Physiology, 138, 744-756.
73. Preuss D., Lemieux B., Yen G., Davis R. (1993) A conditional sterile mutation eliminates surface components from Arabidopsis pollen and disrupts cell signaling during fertilization. Genes and Development, 7, 974-985.
74. Punt W., Hoen P.P., Blackmore S., Nilsson S., Thomas A.L. (2007) Glossary of pollen and spore terminology. Review of Palaeobotany and Palynology, 143, 1-81.
75. Quilichini T.D., Friedmann M.C., Samuels A.L., Douglas C.J. (2010) ATP-binding cassette transporter G26 is required for male fertility and pollen exine formation in Arabidopsis. Plant Physiology, 154, 678-690.
76. Rhee Y.S., Somerville C.R. (1998) Tetrad pollen formation in quartet mutants of Arabidopsis thaliana is associated with persistence of pectic polysaccharides of the pollen mother cell wall. The Plant Journal, 15, 79-88.
77. Rhee S.Y., Osborne E., Poindexter P.D., Somerville C.R. (2003) Microspore separation in the quartet 3 mutants of Arabidopsis is impaired by a defect in a developmentally regulated polygalacturonase required for pollen mother cell wall degradation. Plant Physiology, 133, 1170-1180.
78. Schmid K.M., Ohlrogge J.B. (2002) Lipid metabolism in plants. In: Vance D.E., Vance J.E. (Eds), Biochemistry of lipids, lipoproteins and membranes. Elsevier, Amsterdam, the Netherlands, pp 93-126.
79. Schnurr J., Shockey J. (2004) The acyl-CoA synthetase encoded by LACS2 is essential for normal cuticle development in Arabidopsis. The Plant Cell, 16, 629-642.
80. Scott R.J., Spielman M., Dickinson H. (2004) Stamen structure and function. The Plant Cell, 16(Suppl. 1), S46-S60.
81. Shi D.Q., Yang W.C. (2011) Ovule development in Arabidopsis: progress and challenge. Current Opinion in Plant Biology, 14, 74-80.
82. Sorensen A.M., Krober S., Unte U.S., Huijser P., Dekker K., Saedler H. (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. The Plant Journal, 33, 413-423.
83. Suárez-Cervera M., Arcalís E., Le Thomas A., Seoane-Camba J.A. (2002) Pectin distribution pattern in the apertural intine of Euphorbia peplus L. (Euphorbiaceae) pollen. Sexual Plant Reproduction, 14, 291-298.
84. Sun L., van Nocker S. (2010) Analysis of promoter activity of members of the PECTATE LYASE-LIKE (PLL) gene family in cell separation in Arabidopsis. BMC Plant Biololgy, 10, 152.
85. Suzuki T., Masaoka K., Nishi M., Nakamura K., Ishiguro S. (2008) Identification of kaonashi mutants showing abnormal pollen exine structure in Arabidopsis thaliana. Plant Cell Physiololgy, 49, 1465-1477.
86. Tang L.K., Chu H., Yip W.K., Yeung E.C., Lo C. (2009) An anther-specific dihydroflavonol 4-reductase-like gene (DRL1) is essential for male fertility in Arabidopsis. New Phytologist, 181, 576-587.
87. Toller A., Brownfield L., Neu C., Twell D., Schulze-Lefert P. (2008) Dual function of Arabidopsis glucan synthae-like genes GSL8 and GSL10 in male gametophyte development and plant growth. The Plant Journal, 54, 911-923.
88. Vizcay-Barrena G., Wilson Z.A. (2006) Altered tapetal PCD and pollen wall development in the Arabidopsis ms1 mutant. Journal of Experimental Botany, 57, 2709-2717.
89. Wan L., Zha W., Cheng X., Liu C., Lv L., Wang Z., Du B., Chen R., Zhu L. (2011) A rice β-1, 3-glucanase gene Osg1 is required for callose degradation in pollen development. Planta, 233, 309-323.
90. Wang Y.Q., Ye W.Z., Cao J., Yu X.L., Xiang X., Lu G. (2005) Cloning and characterization of the microspore development-related gene BcMF2 in Chinese Cabbage Pak-Choi (Brassica campestris L. ssp. chinensis Makino). Journal of Integrative Plant Biology, 47, 863-872.
91. Wilmesmeier S., Wiermann R. (1995) Influence of EPTC (S-Ethyl-Dipropyl-Thiocarbamate) on the Composition of Surface Waxes and Sporopollenin Structure in Zea mays. Journal of Plant Physiology, 146, 22-28.
92. Wilson Z.A., Morroll S.M., Dawson J., Swarup R., Tighe P. (2001) The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. The Plant Journal, 28, 27-39.
93. Xu J., Yang C., Yuan Z., Zhang D., Gondwe M.Y., Ding Z., Liang W., Zhang D., Wilson Z.A. (2010) The ABORTED MICROSPORES regulatory network is required for postmeiotic male reporoductive development in Arabidopsis thaliana. The Plant Cell, 22, 91-107.
94. Yang C., Vizcay-Barrena G., Conner K., Wilson Z.A. (2007) MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis. The Plant Cell, 19, 3530-3548.
95. Yi B., Zeng F., Lei S., Chen Y., Yao X., Zhu Y., Wen J., Shen J., Ma C., Tu J. (2010) Two duplicate CYP704B1-homologous genes BnMs1 and BnMs2 are required for pollen exine formation and tapetal development in Brassica napus. The Plant Journal, 63, 925-938.
96. Zhang W., Sun Y., Timofejeva L., Chen C., Grossniklaus U., Ma H. (2006) Regulation of Arabidopsis tapetum development and function by DYSFUNCTIONAL TAPETUM1 (DYT1) encoding a putative bHLH transcription factor. Development, 133, 3085-3095.
97. Zhang Z.B., Zhu J., Gao J.F., Wang C., Li H., Zhang H.Q., Zhang S., Wang D.M., Wang Q.X., Huang H. (2007) Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis. The Plant Journal, 52, 528-538.
98. Zhang D.S., Liang W.Q., Yuan Z., Li N., Shi J., Wang J., Liu Y.M., Yu W.J., Zhang D.B. (2008a) Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Molecular Plant, 1, 599-610.
99. Zhang Q., Huang L., Liu T., Yu X., Cao J. (2008b) Functional analysis of a pollen-expressed polygalacturonase gene BcMF6 in Chinese cabbage (Brassica campestris L. ssp. chinensis Makino). Plant Cell Reports, 27, 1207-1215.
100. Zhang D.S., Liang W.Q., Yin C., Zong J., Gu F., Zhang D. (2010) OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiology, 154, 149-162.
101. Zhang D., Luo X., Zhu L. (2011) Cytological analysis and genetic control of rice anther development. Journal of Genetics and Genomics, 38, 379-390.