Abstract
The tapetum of the anther locule encloses the male reproductive cells and plays a supportive role for normal pollen development. However, the underlying mechanism remains less understood. Previously, we identified a complete recessive male sterile mutant, post-meiotic deficient anther1 (pda1), with abnormal postmeiotic tapetal development. In this study we comprehensively characterized pda1. Chemical analysis uncovered that pda1 anther had significant lower levels of cutin monomers and cuticular waxes. PDA1 gene encodes an ATP-binding cassette (ABC) half-transporter, namely OsABCG15, which is conserved from algae to higher plants. In situ RNA hybridization assay showed that PDA1 is strongly expressed in tapetal cells, and weakly in microspores during the anther development. Additionally, the expression of two pollen exine biosynthetic genes CYP704B2 and CYP703A3 was dramatically reduced in pda1 mutant anthers. Altogether, these observations suggest that the tapetum-expressed ABC transporter PDA1 plays a crucial role in secreting lipidic precursors from the tapetum to developing microspores and the anther epidermis.
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References
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
Ariizumi T, Toriyama K (2011) Genetic regulation of sporopollenin synthesis and pollen exine development. Annu Rev Plant Biol 62:437–460
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
Bedinger P (1992) The remarkable biology of pollen. Plant Cell 4: 879–887
Beisson F, Li-Beisson YH, Pollard M (2012) Solving the puzzles of cutin and suberin polymer biosynthesis. Curr Opin Plant Biol 15:329–337
Bird D, Beisson F, Brigham A, Shin J, Greer S, Jetter R, Kunst L, Wu XW, Yephremov A, Samuels L (2007) Characterization of ArabidopsisABCG11/WBC11, an ATP binding cassette (ABC) transporter that is required for cuticular lipid secretion. Plant J 52:485–498
Blackmore S, Wortley AH, Skvarla JJ, Rowley JR (2007) Pollen wall development in flowering plants. New Phytol 174:483–498
Bonaventure G, Beisson F, Ohlrogge J, Pollard M (2004) Analysis of the aliphatic monomer composition of polyesters associated with Arabidopsis epidermis: occurrence of octadeca-cis-6, cis-9-diene-1,18-dioate as the major component. Plant J 40:920–930
Brooks J, Shaw G (1978) Sporopollenin: a review of its chemistry, palaeochemistry and geochemistry. Taylor & Francis 17:91–97
Chen WW, Yu XH, Zhang KS, Shi JX, De Oliveira S, Schreiber L, Shanklin J, Zhang DB (2011) Male Sterile2 encodes a plastidlocalized fatty acyl carrier protein reductase required for pollen exine development in Arabidopsis. Plant Physiol 157:842–853
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 65:181–193
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 53:74–88
Edgar RC (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792–1797
Franke R, Briesen I, Wojciechowski T, Faust A, Yephremov A, Nawrath C, Schreiber L (2005) Apoplastic polyesters in Arabidopsis surface tissues—a typical suberin and a particular cutin. Phytochemistry 66:2643–2658
Goldberg RB, Beals TP, Sanders PM (1993) Anther development: basic principles and practical applications. Plant Cell 5:1217–1229
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
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
Higgins CF (1992) ABC transporters: from microorganisms to man. Annu Rev Cell Biol 8:67–113
Hu LF, Tan HX, Liang WQ, Zhang DB (2010) The Post-meiotic Deficicent Anther1 (PDA1) gene is required for post-meiotic anther development in rice. J Genet Genomics 37:37–46
Huang CF, Yamaji N, Chen Z, Ma JF (2012) A tonoplast-localized half-size ABC transporter is required for internal detoxification of aluminum in rice. Plant J 69:857–867
Huang CF, Yamaji N, Mitani N, Yano M, Nagamura Y, Ma JF (2009) A bacterial-type ABC transporter is involved in aluminum tolerance in rice. Plant Cell 21: 655–67
Huysmans S, El-Ghazaly G, Smets E (1998) Orbicules in angiosperms: morphology, function, distribution, and relation with tapetum types. Bot Rev 64:240–272
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 18:3015–3032
Kouchi H, Hata S (1993) Isolation and characterization of novel nodulin cDNAs representing genes expressed at early stages of soybean nodule development. Mol Gen Genet 238:106–119
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 107:2361–2366
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 22:173–190
Li H, Yuan Z, Vizcay-Barrena G, Yang CS, Liang WQ, Zong J, Wilson ZA, Zhang DB (2011) PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 156:615–630
Li H, Zhang DB (2010) Biosynthesis of anther cuticle and pollen exine in rice. Plant Signal Behav 5:1121–1123
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 18:2999–3014
Liu YG and Whittier RF (1995) Thermal asymmetric interlaced PCR: automatable amplification and sequencing of insert end fragments from P1 and YAC clones for chromosome walking. Genomics 25:674–681
Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434
McCormick S (1993) Male gametophyte development. Plant Cell 5: 1265–1275
Mentewab A, Stewart CN (2005) Overexpression of an Arabidopsis thaliana ABC transporter confers kanamycin resistance to transgenic plants. Nat Biotechnol 23:1177–1180
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
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 145:1345–1360
Panikashvili D, Shi JX, Schreiber L, and Aharoni A (2011) The Arabidopsis ABCG13 transporter is required for ower cuticle secretion and patterning of the petal epidermis. New Phytol 190: 113–124
Piffanelli P, Ross JHE, Murphy DJ (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex Plant Reprod 11:65–80
Pighin JA, Zheng H, Balakshin LJ, Goodman IP, Western TL, Jetter R, Kunst L, Samuels AL (2004) Plant cuticular lipid export requires an ABC transporter. Science 306:702–704
Pollard M, Beisson F, Li YH, Ohlrogge JB (2008) Building lipid barriers: biosynthesis of cutin and suberin. Trends in Plant Science 13:236–246
Qin P, Tu B, Wang YP, Deng LC, Quilichini TD, Li T, Wang H, Ma BT and Li SG (2012) ABCG15 encodes an ABC transporter protein, and is essential for post-meiotic anther and pollen exine development in Rice. Plant Cell Physiol first published online December 5, 2012 doi:10.1093/pcp/pcs162
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 154:678–690
Rea PA (2007) Plant ATP-binding cassette transporters. Annu Rev Plant Biol 58:347–375
Samuels L, Kunst L, Jetter R (2008) Sealing plant surfaces: cuticular wax formation by epidermal cells. Annu Rev Plant Biol 59:683–707
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
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
Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16Suppl, S46–60
Schulz B and Kolukisaoglu HU (2006) Genomics of plant ABC transporters: The alphabet of photosynthetic life forms or just holes in membranes? FEBS letters 580:1010–1016
Shi J, Tan HX, Yu XH, Liu YY, Liang WQ, Ranathunge K, Franke RB, Schreiber L, Wang Y, Kai G, 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 23:2225–2246
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 48:1524–1533
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
Wang A, Xia Q, Xie W, Dumonceaux T, Zou J, Datla R, Selvaraj G (2002) Male gametophyte development in bread wheat (Triticum aestivum L.): molecular, cellular, and biochemical analyses of a sporophytic contribution to pollen wall ontogeny. Plant J 30: 613–623
Wilson ZA, Zhang DB (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60:1479–1492
Xu J, Yang CS, 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 22:91–107
Yuan L (2004) Hybrid rice technology for food security in the world. Crop Res 4:185–186
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 154:149–162
Zhang DB, Luo X, Zhu L (2011) Cytological analysis and genetic control of rice anther development. J Genet Genomics 38:379–390
Zhang DS, Liang WQ, Yuan Z, Li N, Shi J, Wang J, Liu YM, Yu WJ, Zhang DB (2008) Tapetum Degeneration Retardationis critical for aliphatic metabolism and gene regulation during rice pollen development. Mol Plant 1:599–610
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Zhu, L., Shi, J., Zhao, G. et al. 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, 59–68 (2013). https://doi.org/10.1007/s12374-013-0902-z
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DOI: https://doi.org/10.1007/s12374-013-0902-z