Rice CYP703A3, a cytochrome P450 hydroxylase, is essential for development of anther cuticle and pollen exine

Journal of Integrative Plant Biology

Volumn 56, Issue 10, 2014, Pages 979-994

  Yang, Xijia ^a   Wu, Di ^a   Shi, Jianxin ^a   He, Yi ^a   Pinot, Franck ^b   Grausem, Bernard ^b   Yin, Changsong ^a   Zhu, Lu ^a   Chen, Mingjiao ^a   Luo, Zhijing ^a   Liang, Wanqi ^a   Zhang, Dabing ^a  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b UNIVERSITÉ DE STRASBOURG   (France)

Author keywords

7 hydroxylated lauric acid; Anther cuticle; CYP703A3; Cytochrome P450 hydroxylase; Pollen exine

Indexed keywords

BIOCHEMICAL COMPOSITION; GAMETOPHYTE; GENE EXPRESSION; LIPID; POLLEN; POLYMER; RICE;

CUTIN; CYTOCHROME P450; LAURIC ACID; LAURIC ACID DERIVATIVE; MEMBRANE LIPID; VEGETABLE PROTEIN; WAX;

AMINO ACID SEQUENCE; ENZYMOLOGY; FLOWER; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PHENOTYPE; RICE;

AMINO ACID SEQUENCE; BASE SEQUENCE; CYTOCHROME P-450 ENZYME SYSTEM; FLOWERS; LAURIC ACIDS; MEMBRANE LIPIDS; MOLECULAR SEQUENCE DATA; ORYZA SATIVA; PHENOTYPE; PLANT PROTEINS; WAXES;

EID: 84908272689     PISSN: 16729072     EISSN: 17447909     Source Type: Journal    
DOI: 10.1111/jipb.12212     Document Type: Article

References (62)

1. 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
2. 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
3. Ariizumi T, Toriyama K (2007) Pollen exine pattern formation is dependent on three major developmental processes in Arabidopsis thaliana. Int J Plant Dev Biol 1: 106-115
4. Ariizumi T, Toriyama K (2011) Genetic regulation of sporopollenin synthesis and pollen exine development. Annu Rev Plant Biol 62: 437-460
5. 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
6. Bedinger P (1992) The remarkable biology of pollen. Plant Cell 4: 879- 887
7. Blackmore S, Wortley AH, Skvarla JJ, Rowley JR (2007) Pollen wall development in flowering plants. New Phytol 174: 483-498
8. Bonaventure G, Beisson F, Ohlrogge J, PollardM(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
9. Brooks J, Shaw G (1968) Chemical structure of the exine of pollen walls and a new function for carotenoids in nature. Nature 219: 532-533
10. Bubert H, Lambert J, Steuernagel S, Ahlers F, Wiermann R (2002) Continuous decomposition of sporopollenin from pollen of Typha angustifolia L. by acidic methanolysis. Z Naturforsch C 57: 1035-1041
11. Chang HS, Zhang C, Chang YH, Zhu J, Xu XF, Shi ZH, Zhang XL, Xu L, Huang H, Zhang S, Yang ZN (2012) No primexine and plasma membrane undulation is essential for primexine deposition and plasma membrane undulation during microsporogenesis in Arabidopsis. Plant Physiol 158: 264-272
12. Chen L, Chu HW, Yuan Z, Pan AH, Liang WQ, Huang H, Shen MS, Zhang DB, Chen L (2006) Isolation and genetic analysis for rice mutants treated with 6°Co g-Ray. J. Xiamen Univ 45: 82-85
13. Chen WW, Yu XH, Zhang KS, Shi JX, De Oliveira S, Schreiber L, Shanklin J, Zhang DB (2011) Male Sterile2 encodes a plastid-localized fatty acyl carrier protein reductase required for pollen exine development in Arabidopsis. Plant Physiol 157: 842-853
14. 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
15. Dobritsa AA, Lei ZT, Nishikawa S, Urbanczyk-Wochniak E, Huhman DV, Preuss D, Sumner LW(2010) LAP5 and LAP6 encode anther-specific proteins with similarity to chalcone synthase essential for pollen exine development in Arabidopsis. Plant Physiol 153: 937-955
16. 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
17. 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
18. Furness CA, Rudall PJ (1998) The tapetum and systematics in monocotyledons. Bot Rev 64: 201-239
19. 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
20. Grienenberger E, Kim SS, Lallemand B, Geoffroy P, Heintz D, de Azevedo Souza C, Heitz T, Douglas CJ, LegrandM(2010) Analysis of TETRAKETIDE a-PYRONE REDUCTASE function in Arabidopsis thaliana reveals a previously unknown, but conserved, biochemical pathway in sporopollenin monomer biosynthesis. Plant Cell 22: 4067-4083
21. Heredia A (2003) Biophysical and biochemical characteristics of cutin, a plant barrier biopolymer. Biochim Biophys Acta 1620: 1-7
22. 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
23. Humphreys JM, Hemm MR, Chapple C (1999) New routes for lignin biosynthesis defined by biochemical characterization of recombinant ferulate 5-hydroxylase, a multifunctional cytochrome P450- dependent monooxygenase. Proc Nati Acad Sci 96: 10045-10050
24. Huysmans S, El-Ghazaly G, Smets E (1998) Orbicules in Angiosperms: Morphology, function, distribution, and relation with tapetum types. Bot Rev 64: 240-272
25. Jeffree CE (1996) Structure and ontogeny of plant cuticles. Plant Cuticles: An Integrated Functional Approach, Kerstiens, G. BIOS Scientific, Oxford, UK. pp. 33-82
26. 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) Waxdeficient anther1 is involved in cuticle and wax production in rice anther walls and is required for pollen development. Plant Cell 18: 3015-3032
27. Kim SS, Grienenberger E, Lallemand B, Colpitts CC, Kim SY, de Azevedo Souza C, Geoffroy P, Heintz D, Krahn D, Kaiser M, Kombrink E, Heitz T, Suh DY, Legrand M, Douglas CJ (2010) LAP6/POLYKETIDE SYNTHASE A and LAP5/POLYKETIDE SYNTHASE B encode hydroxyalkyl alpha-pyrone synthases required for pollen development and sporopollenin biosynthesis in Arabidopsis thaliana. Plant Cell 22: 4045-4066
28. Kolattukudy PE (2001) Polyesters in higher plants. Adv Biochem Eng Biotechnol 71: 1-49
29. Kunst L, Samuels AL (2003) Biosynthesis and secretion of plant cuticular wax. Prog Lipid Res 42: 51-80
30. Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD, Baud S, Bird D, Debono A, Durrett TP, Franke RB, Graham IA, Katayama K, Kelly AA, Larson T, Markham JE, Miquel M, Molina I, Nishida I, Rowland O, Samuels L, Schmid KM, Wada H, Welti R, Xu C, Zallot R, Ohlrogge J (2013) Acyl-lipid metabolism. Arabidopsis Book 11: e0161
31. 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 vhydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22: 173- 190
32. Li H, Yuan Z, Vizcay-Barrena G, Yang CY, 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
33. Li H, Zhang DB (2010) Biosynthesis of anther cuticle and pollen exine in rice. Plant Signal Behav 5: 1121-1123
34. 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
35. Liu H, Chu H, Li H, Wang H, Wei J, Li N, Ding S, Huang H, Ma H, Huang C (2005) Genetic analysis and mapping of rice (Oryza sativa L.) malesterile (OsMS-L) mutant. Chin Sci Bull 50: 122-125
36. Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56: 393-434
37. McCormick S (1993) Male Gametophyte Development. Plant Cell 5: 1265-1275
38. 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
39. Nawrath C (2002) The biopolymers cutin and suberin. Arabidopsis Book 1: e0021
40. Nawrath C (2006) Unraveling the complex network of cuticular structure and function. Curr Opin Plant Biol 9: 281-287
41. Nelson DR, Schuler MA, Paquette SM, Werck-Reichhart D, Bak S (2004) Comparative genomics of rice and Arabidopsis. Analysis of 727 cytochrome P450 genes and pseudogenes from a monocot and a dicot. Plant Physiol 135: 756-772
42. 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: 710-720
43. Pidkowich MS, Nguyen HT, Heilmann I, Ischebeck T, Shanklin J (2007) Modulating seed b-ketoacyl-acyl carrier protein synthase II level converts the composition of a temperate seed oil to that of a palmlike tropical oil. Proc Nati Acad Sci USA 104: 4742-4747
44. Piffanelli P, Ross JH, Murphy D (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex Plant Reprod 11: 65-80
45. Pollard M, Beisson F, Li YH, Ohlrogge JB (2008) Building lipid barriers: Biosynthesis of cutin and suberin. Trends Plant Sci 13: 236-246
46. Pompon D, Louerat B, Bronine A, Urban P (1996) Yeast expression of animal and plant P450s in optimized redox environments. Methods Enzymol 272: 51-64
47. 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: 138-154
48. Rozema J, Broekman RA, Blokker P, Meijkamp BB, de Bakker N, van de Staaij J, van Beem A, Ariese F, Kars SM (2001) UV-B absorbance and UV-B absorbing compounds (para-coumaric acid) in pollen and sporopollenin: The perspective to track historic UV-B levels. J Photochem Photobiol B 62: 108-117
49. Scott RJ, Spielman M, Dickinson HG (2004) Stamen structure and function. Plant Cell 16 (Suppl): S46-S60
50. 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: 2225-2246
51. Tan HX, Liang WQ, Hu JP, Zhang DB (2012) MTR1 encodes a secretory fasciclin glycoprotein required for male reproductive development in rice. Dev Cell 22: 1127-1137
52. Wang AM, Xia Q, Xie WS, 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
53. Wilson ZA, Zhang DB (2009) From Arabidopsis to rice: Pathways in pollen development. J Exp Bot 60: 1479-1492
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: 91-107
55. Yi B, Zeng FQ, Lei SL, Chen YN, Yao XQ, Zhu Y, Wen J, Shen JX, Ma CZ, Tu JX, Fu TD (2010) Two duplicate CYP704B1-homologous genes BnMs1 and BnMs2 are required for pollen exine formation and tapetal development in Brassica napus. Plant J 63: 925-938
56. 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
57. Zhang DB, Luo X, Zhu L (2011) Cytological analysis and genetic control of rice anther development. J Genet Genomics 38: 379-390
58. Zhang DB, Wilson ZA (2009) Stamen specification and anther development in rice. Chin Sci Bull 54: 2342-2353
59. Zhang DB, Yang L (2014) Specification of tapetum and microsporocyte cells within the anther. Curr Opin Plant Biol 17C: 49-55
60. 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
61. Zhu L, Shi JX, Zhao GC, Zhang DB, LiangWQ(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: 59-68
62. Zinkl GM, Zwiebel BI, Grier DG, Preuss D (1999) Pollen-stigma adhesion in Arabidopsis: A species-specific interaction mediated by lipophilic molecules in the pollen exine. Development 126: 5431-5440