OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice

Plant Physiology

Volumn 154, Issue 1, 2010, Pages 149-162

  Zhang, Dasheng ^a   Liang, Wanqi ^a   Yin, Changsong ^a   Zong, Jie ^a   Gu, Fangwei ^a   Zhang, Dabing ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DICOTYLEDONEAE; LILIOPSIDA; ORYZA SATIVA;

EID: 77956708669     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.110.158865     Document Type: Article

References (89)

1. Aarts MG, Hodge R, Kalantidis K, Florack D, Wilson ZA, Mulligan BJ, Stiekema WJ, Scott R, Pereira A (1997) The Arabidopsis MALE STERILITY 2 protein shares similarity with reductases in elongation/condensation complexes. Plant J 12: 615-623
2. Ahlers F, Bubert H, Steuernagel S, Wiermann R (2000) The nature of oxygen in sporopollenin from the pollen of Typha angustifolia L. Z Naturforsch C 55: 129-136
3. Ahlers F, Lambert J, Wiermann R (2003) Acetylation and silylation of piperidine solubilized sporopollenin from pollen of Typha angustifolia L. Z Naturforsch C 58: 807-811
4. 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
5. 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 acetolysissensitive exine. Plant Mol Biol 53: 107-116
6. Aya K, Ueguchi-Tanaka M, Kondo M, Hamada K, Yano K, Nishimura M, Matsuoka M (2009) Gibberellin modulates anther development in rice via the transcriptional regulation of GAMYB. Plant Cell 21: 1453-1472
7. Bedinger P (1992) The remarkable biology of pollen. Plant Cell 4: 879-887
8. Blackmore S (2007) Pollen and spores: microscopic keys to understanding the earth's biodiversity. Plant Syst Evol 263: 3-12
9. Blein JP, Coutos-Thevenot P,Marion D, PonchetM(2002) From elicitins to lipid-transfer proteins: a new insight in cell signalling involved in plant defence mechanisms. Trends Plant Sci 7: 293-296
10. Boavida LC, Shuai B, Yu HJ, Pagnussat GC, Sundaresan V, McCormick S (2009) A collection of Ds insertional mutants associated with defects in male gametophyte development and function in Arabidopsis thaliana. Genetics 181: 1369-1385
11. Boutrot F, Chantret N, Gautier MF (2008) Genome-wide analysis of the rice and Arabidopsis non-specific lipid transfer protein (nsLtp) gene families and identification of wheat nsLtp genes by EST data mining. BMC Genomics 9: 86
12. Brooks J, Shaw G (1978) Sporopollenin: a review of its chemistry, palaeochemistry and geochemistry. Grana 17: 91-97
13. Carvalho AO, Gomes VM (2007) Role of plant lipid transfer proteins in plant cell physiology: a concise review. Peptides 28: 1144-1153
14. Carvalho AO, Teodoro CES, Da Cunha M, Okorokova-Facanha AL, Okorokov LA, Fernandes KVS, Gomes VM (2004) Intracellular localization of a lipid transfer protein in Vigna unguiculata seeds. Physiol Plant 122: 328-336
15. Castro MS, Gerhardt IR, Orru S, Pucci P, Bloch C Jr (2003) Purification and characterization of a small (7.3 kDa) putative lipid transfer protein from maize seeds. J Chromatogr B Analyt Technol Biomed Life Sci 794: 109-114
16. Charvolin D, Douliez JP, Marion D, Cohen-Addad C, Pebay-Peyroula E (1999) The crystal structure of a wheat nonspecific lipid transfer protein (ns-LTP1) complexed with two molecules of phospholipid at 2.1 A resolution. Eur J Biochem 264: 562-568
17. Chen ZK, Wang FH, Zhou F (1988) On the origin, development and ultrastructure of the orbicules and pollenkitt in the tapetum of Anemarrhena asphodeloides (Liliaceae). Grana 27: 273-282
18. Cheng HC, Cheng PT, Peng P, Lyu PC, Sun YJ (2004) Lipid binding in rice nonspecific lipid transfer protein-1 complexes from Oryza sativa. Protein Sci 13: 2304-2315
19. Clark AM, Bohnert HJ (1999) Cell-specific expression of genes of the lipid transfer protein family from Arabidopsis thaliana. Plant Cell Physiol 40: 69-76
20. Dai S, Chen T, Chong K, Xue Y, Liu S, Wang T (2007) Proteomics identification of differentially expressed proteins associated with pollen germination and tube growth reveals characteristics of germinated Oryza sativa pollen. Mol Cell Proteomics 6: 207-230
21. de Azevedo Souza C, Kim SS, Koch S, Kienow L, Schneider K, McKim SM, Haughn GW, Kombrink E, Douglas CJ (2009) A novel Fatty Acyl- CoA Synthetase is required for pollen development and sporopollenin biosynthesis in Arabidopsis. Plant Cell 21: 507-525
22. Deng ZY, Wang T (2007) OsDMC1 is required for homologous pairing in Oryza sativa. Plant Mol Biol 65: 31-42
23. Dobritsa AA, Shrestha J, Morant M, Pinot F, Matsuno M, Swanson R, Moller BL, Preuss D (2009) CYP704B1 is a long-chain fatty acid v-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis. Plant Physiol 151: 574-589
24. Douliez JP, Michon T, Elmorjani K,Marian D (2000) Structure, biological and technological functions of lipid transfer proteins and indolines, the major lipid binding proteins from cereal kernels. J Cereal Sci 32: 1-20
25. Douliez JP, Pato C, Rabesona H, Molle D,Marion D (2001) Disulfide bond assignment, lipid transfer activity and secondary structure of a 7-kDa plant lipid transfer protein, LTP2. Eur J Biochem 268: 1400-1403
26. Echlin P, Godwin H (1968) The ultrastructure and ontogeny of pollen in Helleborus foetidus L. I. The development of the tapetum and Ubisch bodies. J Cell Sci 3: 161-174
27. Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797
28. El-Ghazaly G, Jensen WA (1986) Studies of the development of wheat (Triticum aestivum) pollen. Grana 25: 1-29
29. Ge X, Chen J, Li N, Lin Y, Sun C, Cao K (2003) Resistance function of rice lipid transfer protein LTP110. J Biochem Mol Biol 36: 603-607
30. Goldberg RB, Sanders PM, Beals TP (1995) A novel cell-ablation strategy for studying plant development. Philos Trans R Soc Lond B Biol Sci 350: 5-17
31. Gonzalez A, Zhao M, Leavitt JM, Lloyd AM (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. Plant J 53: 814-827
32. Hamilton JA (2004) Fatty acid interactions with proteins: what X-ray crystal and NMR solution structures tell us. Prog Lipid Res 43: 177-199
33. Han GW, Lee JY, Song HK, Chang C, Min K, Moon J, Shin DH, Kopka ML, Sawaya MR, Yuan HS, et al (2001) Structural basis of non-specific lipid binding in maize lipid-transfer protein complexes revealed by high-resolution x-ray crystallography. J Mol Biol 308: 263-278
34. Hiei Y, Ohta S, Komari T, Kumashiro T (1994) Efficient transformation of rice (Oryza sativa L.) mediated by Agrobacterium and sequence analysis of the boundaries of the T-DNA. Plant J 6: 271-282
35. Hihara Y, Hara C, Uchimiya H (1996) Isolation and characterization of two cDNA clones for mRNAs that are abundantly expressed in immature anthers of rice (Oryza sativa L.). Plant Mol Biol 30: 1181-1193
36. Huang AH (1996) Oleosins and oil bodies in seeds and other organs. Plant Physiol 110: 1055-1061
37. Huang MD, Wei FJ, Wu CC, Hsing YI, Huang AH (2009) Analyses of advanced rice anther transcriptomes reveal global tapetum secretory functions and potential proteins for lipid exine formation. Plant Physiol 149: 694-707
38. Huang Y, Liang W, Pan A, Zhou Z, Huang C, Chen J, Zhang D (2003) Production of FaeG, the major subunit of K88 fimbriae, in transgenic tobacco plants and its immunogenicity in mice. Infect Immun 71: 5436-5439
39. Huysmans S, El-Ghazaly G, Smets E (1998) Orbicules in angiosperms: morphology, function, distribution, and relation with tapetum types. Bot Rev 64: 240-272
40. Jose-Estanyol M, Gomis-Ruth FX, Puigdomenech P (2004) The eightcysteine motif, a versatile structure in plant proteins. Plant Physiol Biochem 42: 355-365
41. Jung KH, Han MJ, Lee DY, Lee YS, Schreiber L, Franke R, Faust A, Yephremov A, Saedler H, Kim YW, et al (2006) Wax-deficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18: 3015-3032
42. Kader JC (1975) Proteins and the intracellular exchange of lipids. I. Stimulation of phospholipid exchange between mitochondria and microsomal fractions by proteins isolated from potato tuber. Biochim Biophys Acta 380: 31-44
43. Kaneko M, Inukai Y, Ueguchi-Tanaka M, Itoh H, Izawa T, Kobayashi Y, Hattori T, Miyao A, Hirochika H, Ashikari M, et al (2004) Loss-offunction mutations of the rice GAMYB gene impair a-amylase expression in aleurone and flower development. Plant Cell 16: 33-44
44. Kim TH, Park JH, Kim MC, Cho SH (2008) Cutin monomer induces expression of the rice OsLTP5 lipid transfer protein gene. J Plant Physiol 165: 345-349
45. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinform 5: 150-163
46. Lauga B, Charbonnel-Campaa L, Combes D (2000) Characterization of MZm3-3, a Zea mays tapetum-specific transcript. Plant Sci 157: 65-75
47. Lee JY, Min K, Cha H, Shin DH, Hwang KY, Suh SW (1998) Rice nonspecific lipid transfer protein: the 1.6 Å crystal structure in the unliganded state reveals a small hydrophobic cavity. J Mol Biol 276: 437-448
48. Lee SB, Go YS, Bae HJ, Park JH, Cho SH, Cho HJ, Lee DS, Park OK, Hwang I, Suh MC (2009) Disruption of glycosylphosphatidylinositolanchored lipid transfer protein gene altered cuticular lipid composition, increased plastoglobules, and enhanced susceptibility to infection by the fungal pathogen Alternaria brassicicola. Plant Physiol 150: 42-54
49. Lerche MH, Kragelund BB, Bech LM, Poulsen FM (1997) Barley lipidtransfer protein complexed with palmitoyl CoA: the structure reveals a hydrophobic binding site that can expand to fit both large and small lipid-like ligands. Structure 5: 291-306
50. Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao Y, et al (2010) Cytochrome P450 family member CYP704B2 catalyzes the v-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22: 173-190
51. Li N, Zhang DS, Liu HS, Yin CS, Li XX, LiangWQ, Yuan Z, Xu B, Chu HW, Wang J, et al (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18: 2999-3014
52. Liu YJ, Samuel D, Lin CH, Lyu PC (2002) Purification and characterization of a novel 7-kDa non-specific lipid transfer protein-2 from rice (Oryza sativa). Biochem Biophys Res Commun 294: 535-540
53. Liu ZH, Bao WJ, Liang WQ, Yin JY, Zhang DB (2010) Identification of gamyb-4 and analysis of the regulatory role of GAMYB in rice anther development. J Integr Plant Biol 52: 670-678
54. Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56: 393-434
55. Maldonado AM, Doerner P, Dixon RA, Lamb CJ, Cameron RK (2002) A putative lipid transfer protein involved in systemic resistance signalling in Arabidopsis. Nature 419: 399-403
56. Mao J, Zhang YC, Sang Y, Li QH, Yang HQ (2005) A role for Arabidopsis cryptochromes and COP1 in the regulation of stomatal opening. Proc Natl Acad Sci USA 102: 12270-12275
57. Matsuhira H, Shinada H, Yui-Kurino R, Hamato N, Umeda M, Mikami T, Kubo T, Almeida J (2007) An anther-specific lipid transfer protein gene in sugar beet: its expression is strongly reduced in male-sterile plants with Owen cytoplasm. Physiol Plant 129: 407-414
58. McCormick S (1993) Male gametophyte development. Plant Cell 5: 1265-1275
59. Morant M, Jorgensen K, Schaller H, Pinot F, Moller BL, 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. Plant Cell 19: 1473-1487
60. Murphy DJ (2001) The biogenesis and functions of lipid bodies in animals, plants and microorganisms. Prog Lipid Res 40: 325-438
61. Nelson T, Harpster MH, Mayfield SP, Taylor WC (1984) Light-regulated gene expression during maize leaf development. J Cell Biol 98: 558-564
62. Ouyang YD, Chen JJ, Ding JH, Zhang QF (2009) Advances in the understanding of inter-subspecific hybrid sterility and wide-compatibility in rice. Chin Sci Bull 54: 2332-2341
63. 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
64. Piffanelli P, Ross JHE, Murphy DJ (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex Plant Reprod 11: 65-80
65. Pyee J, Yu H, Kolattukudy PE (1994) Identification of a lipid transfer protein as the major protein in the surface wax of broccoli (Brassica oleracea) leaves. Arch Biochem Biophys 311: 460-468
66. Ramsay NA, Glover BJ (2005) MYB-bHLH-WD40 protein complex and the evolution of cellular diversity. Trends Plant Sci 10: 63-70
67. Roberts MR, Hodge R, Ross JH, Sorensen A, Murphy DJ, Draper J, Scott R (1993) Characterization of a new class of oleosins suggests a male gametophyte-specific lipid storage pathway. Plant J 3: 629-636
68. RobertsMR, Hodge R, Scott R (1995) Brassica napus pollen oleosins possess a characteristic C-terminal domain. Planta 195: 469-470
69. Roberts MR, Robson F, Foster GD, Draper J, Scott RJ (1991) A Brassica napus mRNA expressed specifically in developing microspores. Plant Mol Biol 17: 295-299
70. Samuel D, Liu YJ, Cheng CS, Lyu PC (2002) Solution structure of plant nonspecific lipid transfer protein-2 from rice (Oryza sativa). J Biol Chem 277: 35267-35273
71. Sarowar S, Kim YJ, Kim KD, Hwang BK, Ok SH, Shin JS (2009) Overexpression of lipid transfer protein (LTP) genes enhances resistance to plant pathogens and LTP functions in long-distance systemic signaling in tobacco. Plant Cell Rep 28: 419-427
72. Sodano P, Caille A, Sy D, de Person G, Marion D, PtakM(1997) 1H NMR and fluorescence studies of the complexation of DMPG by wheat non-specific lipid transfer protein: global fold of the complex. FEBS Lett 416: 130-134
73. Suarez-Cervera M, Marquez J, Seoane-Camba J (1995) Pollen grain and Ubisch body development in Platanus acerifolia. Rev Palaeobot Palynol 85: 63-84
74. Suen DF, Huang AH (2007) Maize pollen coat xylanase facilitates pollen tube penetration into silk during sexual reproduction. J Biol Chem 282: 625-636
75. Suwabe K, Suzuki G, Takahashi H, Shiono K, Endo M, Yano K, Fujita M, Masuko H, Saito H, Fujioka T, et al (2008) Separated transcriptomes of male gametophyte and tapetum in rice: validity of a laser microdissection (LM) microarray. Plant Cell Physiol 49: 1407-1416
76. Thoma S, Hecht U, Kippers A, Botella J, De Vries S, Somerville C (1994) Tissue-specific expression of a gene encoding a cell wall-localized lipid transfer protein from Arabidopsis. Plant Physiol 105: 35-45
77. Thoma S, Kaneko Y, Somerville C (1993) A non-specific lipid transfer protein from Arabidopsis is a cell wall protein. Plant J 3: 427-436
78. Tsuboi S, Osafune T, Tsugeki R, Nishimura M, Yamada M (1992) Nonspecific lipid transfer protein in castor bean cotyledon cells: subcellular localization and a possible role in lipid metabolism. J Biochem 111: 500-508
79. Tsuchiya T, Toriyama K, Ejiri S, Hinata K (1994) Molecular characterization of rice genes specifically expressed in the anther tapetum. PlantMol Biol 26: 1737-1746
80. Tsuchiya T, Toriyama K, Nasrallah ME, Ejiri S (1992) Isolation of genes abundantly expressed in rice anthers at the microspore stage. Plant Mol Biol 20: 1189-1193
81. Wang A, Xia Q, Xie W, Datla R, Selvaraj G (2003) The classical Ubisch bodies carry a sporophytically produced structural protein (RAFTIN) that is essential for pollen development. Proc Natl Acad Sci USA 100: 14487-14492
82. Willemsen V, Wolkenfelt H, de Vrieze G, Weisbeek P, Scheres B (1998) The HOBBIT gene is required for formation of the root meristem in the Arabidopsis embryo. Development 125: 521-531
83. Wilson ZA, Zhang DB (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60: 1479-1492
84. Xu SX, Liu GS, Chen RD (2006) Characterization of an anther- and tapetum-specific gene and its highly specific promoter isolated from tomato. Plant Cell Rep 25: 231-240
85. Yeats TH, Rose JK (2008) The biochemistry and biology of extracellular plant lipid-transfer proteins (LTPs). Protein Sci 17: 191-198
86. Zachowski A, Guerbette F, Grosbois M, Jolliot-Croquin A, Kader JC (1998) Characterisation of acyl binding by a plant lipid-transfer protein. Eur J Biochem 257: 443-448
87. Zhang DB, Wilson ZA (2009) Stamen specification and anther development in rice. Chin Sci Bull 54: 2342-2353
88. Zhang DS, Liang WQ, Yuan Z, Li N, Shi J, Wang J, Liu YM, Yu WJ, Zhang DB (2008) Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development.Mol Plant 1: 599-610
89. Zhang L, Tao J, Wang S, Chong K, Wang T (2006) The rice OsRad21-4, an orthologue of yeast Rec8 protein, is required for efficient meiosis. Plant Mol Biol 60: 533-554