OsABCG15 encodes a membrane protein that plays an important role in anther cuticle and pollen exine formation in rice
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  • 作者:Lina Wu (1)
    Yusheng Guan (1)
    Zigang Wu (1)
    Kun Yang (1) (2)
    Jun Lv (1) (2)
    Richard Converse (3)
    Yuanxin Huang (1) (2)
    Jinxiong Mao (4)
    Yong Zhao (1) (2)
    Zhongwei Wang (1)
    Hengqi Min (1)
    Dongyang Kan (1)
    Yi Zhang (1) (2)
  • 关键词:ABC transporter ; Rice ; Anther cuticle ; Pollen exine ; Pollen development
  • 刊名:Plant Cell Reports
  • 出版年:2014
  • 出版时间:November 2014
  • 年:2014
  • 卷:33
  • 期:11
  • 页码:1881-1899
  • 全文大小:9,955 KB
  • 参考文献:1. Aarts MGM, 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鈥?23. doi:10.1046/j.1365-313X.1997.00615.x CrossRef
    2. Ahlers F, Thom I, Lambert J, Kuckuk R, Wiermann R (1999) H-1 NMR analysis of sporopollenin from / Typha angustifolia. Phytochemistry 50:1095鈥?098. doi:10.1016/S0031-9422(98)00225-8 CrossRef
    3. Ariizumi T, Toriyama K (2011) Genetic regulation of sporopollenin synthesis and pollen exine development. Annu Rev Plant Biol 62:437鈥?60. doi:10.1146/annurev-arplant-042809-112312 CrossRef
    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鈥?16. doi:10.1023/B:Plan.0000009269.97773.70 CrossRef
    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鈥?81. doi:10.1111/j.1365-313X.2004.02118.x CrossRef
    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鈥?472. doi:10.1105/tpc.108.062935 CrossRef
    7. Bessire M, Borel S, Fabre G, Carraca L, Efremova N, Yephremov A, Cao Y, Jetter R, Jacquat AC, Metraux JP, Nawrath C (2011) A member of the PLEIOTROPIC DRUG RESISTANCE family of ATP binding cassette transporters is required for the formation of a functional cuticle in Arabidopsis. Plant Cell 23:1958鈥?970. doi:10.1105/tpc.111.083121 CrossRef
    8. Bird D, Beisson F, Brigham A, Shin J, Greer S, Jetter R, Kunst L, Wu XW, Yephremov A, Samuels L (2007) Characterization of Arabidopsis ABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J 52:485鈥?98. doi:10.1111/j.1365-313X.2007.03252.x CrossRef
    9. Bolte S, Talbot C, Boutte Y, Catrice O, Read ND, Satiat-Jeunemaitre B (2004) FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells. J Microsc 214:159鈥?73. doi:10.1111/j.0022-2720.2004.01348.x CrossRef
    10. Borowski E, Bontemps-Gracz MM, Piwkowska A (2005) Strategies for overcoming ABC-transporters-mediated multidrug resistance (MDR) of tumor cells. Acta Biochim Pol 52:609鈥?27
    11. Carvalho AD, Gomes VM (2007) Role of plant lipid transfer proteins in plant cell physiology鈥攁 concise review. Peptides 28:1144鈥?153. doi:10.1016/j.peptides.2007.03.004 CrossRef
    12. Chen GX, Komatsuda T, Ma JF, Nawrath C, Pourkheirandish M, Tagiri A, Hu YG, Sameri M, Li XR, Zhao X, Liu YB, Li C, Ma XY, Wang AD, Nair S, Wang N, Miyao A, Sakuma S, Yamaji N, Zheng XT, Nevo E (2011) An ATP-binding cassette subfamily G full transporter is essential for the retention of leaf water in both wild barley and rice. Proc Natl Acad of Sci USA 108:12354鈥?2359. doi:10.1073/pnas.1108444108 CrossRef
    13. Choi H, Jin JY, Choi S, Hwang JU, Kim YY, Suh MC, Lee Y (2011) An ABCG/WBC-type ABC transporter is essential for transport of sporopollenin precursors for exine formation in developing pollen. Plant J 65:181鈥?93. doi:10.1111/j.1365-313X.2010.04412.x CrossRef
    14. Dou XY, Yang KZ, Zhang Y, Wang W, Liu XL, Chen LQ, Zhang XQ, Ye D (2011) WBC27, an adenosine tri-phosphate-binding cassette protein, controls pollen wall formation and patterning in Arabidopsis. J Integr Plant Biol 53:74鈥?8. doi:10.1111/j.1744-7909.2010.01010.x CrossRef
    15. 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鈥?63. doi:10.1104/pp.108.118026 CrossRef
    16. Guilford WJ, Schneider DM, Labovitz J, Opella SJ (1988) High-resolution solid-state C-13 NMR-spectroscopy of sporopollenins from different plant taxa. Plant Physiol 86:134鈥?36. doi:10.1104/Pp.86.1.134 CrossRef
    17. Heredia A (2003) Biophysical and biochemical characteristics of cutin, a plant barrier biopolymer. Biochim Biophys Acta 1620:1鈥? CrossRef
    18. Huysmans S, El-Ghazaly G, Smets E (1998) Orbicules in angiosperms: morphology, function, distribution, and relation with tapetum types. Bot Rev 64:240鈥?72. doi:10.1007/Bf02856566 CrossRef
    19. Jung KH, Han MJ, Lee DY, Lee YS, Schreiber L, Franke R, Faust A, Yephremov A, Saedler H, Kim YW, Hwang I, An G (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鈥?032. doi:10.1105/tpc.106.042044 CrossRef
    20. Kandel S, Sauveplane V, Olry A, Diss L, Benveniste I, Pinot F (2006) Cytochrome P450-dependent fatty acid hydroxylases in plants. Phytochem Rev 5:359鈥?72 CrossRef
    21. Keijzer CJ, LeferinkTenKlooster HB, Reinders MC (1996) The mechanics of the grass flower: anther dehiscence and pollen shedding in maize. Ann Bot 78:15鈥?1. doi:10.1006/anbo.1996.0089 CrossRef
    22. Kerstiens G (1996) Plant cuticles: an integrated function approach. Environmental plant biology series. BIOS Scientific, Oxford
    23. Kolattukudy PE (2001) Polyesters in higher plants. Adv Biochem Eng Biotechnol 71:1鈥?9
    24. Kunst L, Samuels AL (2003) Biosynthesis and secretion of plant cuticular wax. Prog Lipid Res 42:51鈥?0 CrossRef
    25. Kuromori T, Shinozaki K (2010) ABA transport factors found in Arabidopsis ABC transporters. Plant Signal Behav 5:1124鈥?126 CrossRef
    26. Kuromori T, Miyaji T, Yabuuchi H, Shimizu H, Sugimoto E, Kamiya A, Moriyama Y, Shinozaki K (2010) ABC transporter AtABCG25 is involved in abscisic acid transport and responses. Proc Natl Acad Sci USA 107:2361鈥?366. doi:10.1073/pnas.0912516107 CrossRef
    27. Li H, Zhang D (2010) Biosynthesis of anther cuticle and pollen exine in rice. Plant Signal Behav 5:1121鈥?123. doi:10.4161/psb.5.9.12562 CrossRef
    28. Li N, Zhang DS, Liu HS, Yin CS, Li XX, Liang WQ, Yuan Z, Xu B, Chu HW, Wang J, Wen TQ, Huang H, Luo D, Ma H, Zhang DB (2006) The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999鈥?014. doi:10.1105/tpc.106.044107 CrossRef
    29. Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao YW, Liang WQ, Zhang DB (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. Plant Cell 22:173鈥?90. doi:10.1105/tpc.109.070326 CrossRef
    30. Mentewab A, Stewart CN (2005) Overexpression of an / Arabidopsis thaliana ABC transporter confers kanamycin resistance to transgenic plants. Nat Biotechnol 23:1177 CrossRef
    31. Meuter-Gerhards A, Riegert S, Wiermann R (1999) Studies on sporopollenin biosynthesis in / Cucurbita maxima (DUCH.)鈥擨I. The involvement of aliphatic metabolism. J Plant Physiol 154:431鈥?36 CrossRef
    32. 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鈥?487. doi:10.1105/tpc.106.045948 CrossRef
    33. Nawrath C (2006) Unraveling the complex network of cuticular structure and function. Curr Opin Plant Biol 9:281鈥?87. doi:10.1016/j.pbi.2006.03.001 CrossRef
    34. Niu BX, He FR, He M, Ren D, Chen LT, Liu YG (2013) The ATP-binding cassette transporter OsABCG15 is required for anther development and pollen fertility in rice. J Integr Plant Biol 55:710鈥?20. doi:10.1111/jipb.12053 CrossRef
    35. Pacini E, Franchi GG, Hesse M (1985) The tapetum鈥攊ts form, function, and possible phylogeny in embryophyta. Plant Syst Evol 149:155鈥?85. doi:10.1007/Bf00983304 CrossRef
    36. Panikashvili D, Savaldi-Goldstein S, Mandel T, Yifhar T, Franke RB, Hofer R, Schreiber L, Chory J, Aharoni A (2007) The Arabidopsis DESPERADO/AtWBC11 transporter is required for cutin and wax secretion. Plant Physiol 145:1345鈥?360. doi:10.1104/pp.107.105676 CrossRef
    37. Panikashvili D, Shi JX, Schreiber L, Aharoni A (2011) The Arabidopsis ABCG13 transporter is required for flower cuticle secretion and patterning of the petal epidermis. New Phytol 190:113鈥?24. doi:10.1111/j.1469-8137.2010.03608.x CrossRef
    38. 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鈥?749. doi:10.1104/Pp.010517 CrossRef
    39. Pighin JA, Zheng HQ, Balakshin LJ, Goodman IP, Western TL, Jetter R, Kunst L, Samuels AL (2004) Plant cuticular lipid export requires an ABC transporter. Science 306:702鈥?04. doi:10.1126/science.1102331 CrossRef
    40. Qin P, Tu B, Wang YP, Deng LC, Quilichini TD, Li T, Wang H, Ma BT, Li SG (2013) ABCG15 encodes an ABC transporter protein, and is essential for post-meiotic anther and pollen exine development in rice. Plant Cell Physiol 54:138鈥?54. doi:10.1093/Pcp/Pcs162 CrossRef
    41. Quilichini TD, Friedmann MC, Samuels AL, Douglas CJ (2010) ATP-binding cassette transporter G26 is required for male fertility and pollen exine formation in arabidopsis. Plant Physiol 154:678鈥?90. doi:10.1104/pp.110.161968 CrossRef
    42. Riederer M, Muller C (2006) Biology of the plant cuticle. Annual plant reviews, vol 23. Blackwell Pub, Oxford CrossRef
    43. Saitou N, Nei M (1987) The neighbor-joining method鈥攁 new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406鈥?25
    44. Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu Rev Plant Biol 59:683鈥?07. doi:10.1146/annurev.arplant.59.103006.093219 CrossRef
    45. Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16:S46鈥揝60. doi:10.1105/Tpc.017012 CrossRef
    46. Shi J, Tan HX, Yu XH, Liu YY, Liang WQ, Ranathunge K, Franke RB, Schreiber L, Wang YJ, Kai GY, Shanklin J, Ma H, Zhang DB (2011) Defective pollen wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase. Plant Cell 23:2225鈥?246. doi:10.1105/tpc.111.087528 CrossRef
    47. Shivanna KR, Cresti M, Ciampolini F (1997) Pollen development and pollen-pistil interaction. In: Pollen biotechnology for crop production and improvement. Cambridge University Press, Cambridge
    48. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S (2011) MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28:2731鈥?739. doi:10.1093/molbev/msr121 CrossRef
    49. Ukitsu H, Kuromori T, Toyooka K, Goto Y, Matsuoka K, Sakuradani E, Shimizu S, Kamiya A, Imura Y, Yuguchi M, Wada T, Hirayama T, Shinozaki K (2007) Cytological and biochemical analysis of COF1, an Arabidopsis mutant of an ABC transporter gene. Plant Cell Physiol 48:1524鈥?533. doi:10.1093/Pcp/Pcm139 CrossRef
    50. Verrier PJ, Bird D, Buria B, Dassa E, Forestier C, Geisler M, Klein M, Kolukisaoglu U, Lee Y, Martinoia E, Murphy A, Rea PA, Samuels L, Schulz B, Spalding EP, Yazaki K, Theodoulou FL (2008) Plant ABC proteins鈥攁 unified nomenclature and updated inventory. Trends Plant Sci 13:151鈥?59. doi:10.1016/j.tplants.2008.02.001 CrossRef
    51. Voinnet O, Rivas S, Mestre P, Baulcombe D (2003) An enhanced transient expression system in plants based on suppression of gene silencing by the p19 protein of tomato bushy stunt virus. Plant J 33:949鈥?56. doi:10.1046/j.1365-313X.2003.01676.x CrossRef
    52. Wiermann R, Ahlers F, Schmitz-Thom I (2001) Sporopollenin. In: Stenbuchel A, Hofrichter M (eds) Biopolymers, vol 1. Wiley-VCH, Weinheim
    53. Xiao H, Tang JF, Li YF, Wang WM, Li XB, Jin L, Xie R, Luo HF, Zhao XF, Meng Z, He GH, Zhu LH (2009) STAMENLESS 1, encoding a single C2H2 zinc finger protein, regulates floral organ identity in rice. Plant J 59:789鈥?01. doi:10.1111/j.1365-313X.2009.03913.x CrossRef
    54. Xu J, Yang CY, Yuan Z, Zhang DS, Gondwe MY, Ding ZW, Liang WQ, Zhang DB, Wilson ZA (2010) The ABORTED MICROSPORES regulatory network is required for postmeiotic male reproductive development in / Arabidopsis thaliana. Plant Cell 22:91鈥?07. doi:10.1105/tpc.109.071803 CrossRef
    55. Xue YB, Collin S, Davies DR, Thomas CM (1994) Differential screening of mitochondrial cDNA libraries from male-fertile and cytoplasmic male-sterile sugar-beet reveals genome rearrangements at Atp6 and Atpa loci. Plant Mol Biol 25:91鈥?03. doi:10.1007/Bf00024201 CrossRef
    56. Yeats TH, Rose JKC (2008) The biochemistry and biology of extracellular plant lipid-transfer proteins (LTPs). Protein Sci 17:191鈥?98. doi:10.1110/Ps.073300108 CrossRef
    57. Zhang DS, Liang WQ, Yuan Z, Li N, Shi J, Wang J, Liu YM, Yu WJ, Zhang DB (2008a) Tapetum degeneration retardation is critical for aliphatic metabolism and gene regulation during rice pollen development. Mol Plant 1:599鈥?10. doi:10.1093/Mp/Ssn028 CrossRef
    58. Zhang Y, Mao JX, Yang K, Li YF, Zhang J, Huang YX, Shen FC, Zhang CD (2008b) Characterization and mapping of a male-sterility mutant, tapetum desquamation (t), in rice. Genome 51:368鈥?74. doi:10.1139/G08-013 CrossRef
    59. Zhang DS, Liang WQ, Yin CS, Zong J, Gu FW, Zhang DB (2010) OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol 154:149鈥?62. doi:10.1104/pp.110.158865 CrossRef
    60. Zhang D, Luo X, Zhu L (2011) Cytological analysis and genetic control of rice anther development. J Genet Genomics 38:379鈥?90. doi:10.1016/j.jgg.2011.08.001 CrossRef
    61. Zhu L, Shi JX, Zhao GC, Zhang DB, Liang WQ (2013) Post-meiotic deficient anther1 (PDA1) encodes an ABC transporter required for the development of anther cuticle and pollen exine in rice. J Plant Biol 56:59鈥?8. doi:10.1007/s12374-013-0902-z CrossRef
  • 作者单位:Lina Wu (1)
    Yusheng Guan (1)
    Zigang Wu (1)
    Kun Yang (1) (2)
    Jun Lv (1) (2)
    Richard Converse (3)
    Yuanxin Huang (1) (2)
    Jinxiong Mao (4)
    Yong Zhao (1) (2)
    Zhongwei Wang (1)
    Hengqi Min (1)
    Dongyang Kan (1)
    Yi Zhang (1) (2)

    1. College of Agronomy and Biotechnology, Southwest University, Chongqing, 400715, China
    2. Engineering Research Center of South Upland Agriculture, Ministry of Education, Southwest University, Chongqing, 400715, China
    3. Cincinnati State Technical and Community College, 3520 Central Parkway, Cincinnati, OH, 45223, USA
    4. Nanchong Academy of Agricultural Sciences, Nanchong, 637000, Sichuan, China
  • ISSN:1432-203X
文摘
Key message An ABC transporter gene ( OsABCG15 ) was proven to be involved in pollen development in rice. The corresponding protein was localized on the plasma membrane using subcellular localization. Abstract Wax, cutin, and sporopollenin are important for normal development of the anther cuticle and pollen exine, respectively. Their lipid soluble precursors, which are produced in the tapetum, are then secreted and transferred to the anther and microspore surface for polymerization. However, little is known about the mechanisms underlying the transport of these precursors. Here, we identified and characterized a member of the G subfamily of ATP-binding cassette (ABC) transporters, OsABCG15, which is required for the secretion of these lipid-soluble precursors in rice. Using map-based cloning, we found a spontaneous A-to-C transition in the fourth exon of OsABCG15 that caused an amino acid substitution of Thr-to-Pro in the predicted ATP-binding domain of the protein sequence. This osabcg15 mutant failed to produce any viable pollen and was completely male sterile. Histological analysis indicated that osabcg15 exhibited an undeveloped anther cuticle, enlarged middle layer, abnormal Ubisch body development, tapetum degeneration with a falling apart style, and collapsed pollen grains without detectable exine. OsABCG15 was expressed preferentially in the tapetum, and the fused GFP-OsABCG15 protein was localized to the plasma membrane. Our results suggested that OsABCG15 played an essential role in the formation of the rice anther cuticle and pollen exine. This role may include the secretion of the lipid precursors from the tapetum to facilitate the transfer of precursors to the surface of the anther epidermis as well as to microspores.

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