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  • Review Article
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Biosynthesis and transport of pollen coat precursors in angiosperms

Abstract

The pollen coat is a hydrophobic mixture on the pollen grain surface, which plays an important role in protecting male gametes from various environmental stresses and microorganism attacks, and in pollen–stigma interactions during pollination in angiosperms. An abnormal pollen coat can result in humidity-sensitive genic male sterility (HGMS), which can be used in two-line hybrid crop breeding. Despite the crucial functions of the pollen coat and the application prospect of its mutants, few studies have focused on pollen coat formation. In this Review, the morphology, composition and function of different types of pollen coat are assessed. On the basis of the ultrastructure and development process of the anther wall and exine found in rice and Arabidopsis, the genes and proteins involved in the biosynthesis of pollen coat precursors and the possible transport and regulation process are sorted. Additionally, current challenges and future perspectives, including potential strategies utilizing HGMS genes in heterosis and plant molecular breeding, are highlighted.

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Fig. 1: Ultrastructural diagrams and visualization of tapetum and pollen wall.
Fig. 2: Biosynthesis and transport of pollen coat formation enzymes/transporters in monocotyledons and dicotyledons.
Fig. 3: Transport of pollen coat precursors with specialized organelles in tapetum development.

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References

  1. Ariizumi, T. & Toriyama, K. Genetic regulation of sporopollenin synthesis and pollen exine development. Annu. Rev. Plant Biol. 62, 437–460 (2011).

    CAS  PubMed  Google Scholar 

  2. Jiang, J., Zhang, Z. & Cao, J. Pollen wall development: the associated enzymes and metabolic pathways. Plant Biol. 15, 249–263 (2013).

    CAS  PubMed  Google Scholar 

  3. Shi, J., Cui, M., Yang, L., Kim, Y. J. & Zhang, D. Genetic and biochemical mechanisms of pollen wall development. Trends Plant Sci. 20, 741–753 (2015).

    CAS  PubMed  Google Scholar 

  4. Preuss, D., Lemieux, B., Yen, G. & Davis, R. W. A conditional sterile mutation eliminates surface components from Arabidopsis pollen and disrupts cell signaling during fertilization. Genes Dev. 7, 974–985 (1993).

    CAS  PubMed  Google Scholar 

  5. Aarts, M. G., Keijzer, C. J., Stiekema, W. J. & Pereira, A. Molecular characterization of the CER1 gene of Arabidopsis involved in epicuticular wax biosynthesis and pollen fertility. Plant Cell 7, 2115–2127 (1995).

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Ariizumi, T. et al. 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, 107–116 (2003).

    CAS  PubMed  Google Scholar 

  7. Xue, Z. et al. Deficiency of a triterpene pathway results in humidity-sensitive genic male sterility in rice. Nat. Commun. 9, 604 (2018).

    PubMed  PubMed Central  Google Scholar 

  8. Yu, B., Liu, L. & Wang, T. Deficiency of very long chain alkanes biosynthesis causes humidity-sensitive male sterility via affecting pollen adhesion and hydration in rice. Plant Cell Environ. 42, 3340–3354 (2019).

    CAS  PubMed  Google Scholar 

  9. Chen, H. et al. HMS1 interacts with HMS1I to regulate very-long-chain fatty acid biosynthesis and the humidity-sensitive genic male sterility in rice (Oryza sativa). New Phytol. 225, 2077–2093 (2020).

    CAS  PubMed  Google Scholar 

  10. Quilichini, T. D., Grienenberger, E. & Douglas, C. J. The biosynthesis, composition and assembly of the outer pollen wall: a tough case to crack. Phytochemistry 113, 170–182 (2015).

    CAS  PubMed  Google Scholar 

  11. Song, Y., Tang, Y., Liu, L., Xu, Y. & Wang, T. The methyl-CpG-binding domain family member PEM1 is essential for Ubisch body formation and pollen exine development in rice. Plant J. 111, 1283–1295 (2022).

    CAS  PubMed  Google Scholar 

  12. Zhu, J. et al. Slowing development restores the fertility of thermo-sensitive male-sterile plant lines. Nat. Plants 6, 360–367 (2020).

    CAS  PubMed  Google Scholar 

  13. Shi, Q. S. et al. A cellular mechanism underlying the restoration of thermo/photoperiod-sensitive genic male sterility. Mol. Plant 14, 2104–2114 (2021).

    CAS  PubMed  Google Scholar 

  14. Xu, D. et al. Defective Pollen Wall 2 (DPW2) encodes an acyl transferase required for rice pollen development. Plant Physiol. 173, 240–255 (2017).

    CAS  PubMed  Google Scholar 

  15. Zhang, D., Luo, X. & Zhu, L. Cytological analysis and genetic control of rice anther development. J. Genet. Genom. 38, 379–390 (2011).

    CAS  Google Scholar 

  16. Pacini, E. & Hesse, M. Pollenkitt-its composition, forms and functions. Flora 200, 399–415 (2005).

    Google Scholar 

  17. Thien, L. B. et al. Pollination biology of basal angiosperms (ANITA grade). Am. J. Bot. 96, 166–182 (2009).

    PubMed  Google Scholar 

  18. Ishiguro, S. et al. The Arabidopsis FLAKY POLLEN1 gene encodes a 3-hydroxy-3-methylglutaryl-coenzyme A synthase required for development of tapetum-specific organelles and fertility of pollen grains. Plant Cell Physiol. 51, 896–911 (2010).

    CAS  PubMed  Google Scholar 

  19. Choi, H. et al. An ABCG/WBC-type ABC transporter is essential for transport of sporopollenin precursors for exine formation in developing pollen. Plant J. 65, 181–193 (2011).

    CAS  PubMed  Google Scholar 

  20. Cui, Y. et al. MONENSIN SENSITIVITY1 (MON1)/CALCIUM CAFFEINE ZINC SENSITIVITY1 (CCZ1)-mediated Rab7 activation regulates tapetal programmed cell death and pollen development. Plant Physiol. 173, 206–218 (2017).

    CAS  PubMed  Google Scholar 

  21. Aboulela, M., Nakagawa, T., Oshima, A., Nishimura, K. & Tanaka, Y. The Arabidopsis COPII components, AtSEC23A and AtSEC23D, are essential for pollen wall development and exine patterning. J. Exp. Bot. 69, 1615–1633 (2018).

    CAS  PubMed  PubMed Central  Google Scholar 

  22. Kobayashi, K., Suzuki, M., Muranaka, T. & Nagata, N. The mevalonate pathway but not the methylerythritol phosphate pathway is critical for elaioplast and pollen coat development in Arabidopsis. Plant Biotechnol. J. 35, 381–385 (2018).

    CAS  Google Scholar 

  23. Wang, A., Xia, Q., Xie, W., Datla, R. & Selvaraj, G. 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 (2003).

    CAS  PubMed  PubMed Central  Google Scholar 

  24. Li, N. et al. The rice tapetum degeneration retardation gene is required for tapetum degradation and anther development. Plant Cell 18, 2999–3014 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Sharma, A., Singh, M. B. & Bhalla, P. L. Ultrastructure of microsporogenesis and microgametogenesis in Brachypodium distachyon. Protoplasma 252, 1575–1586 (2015).

    CAS  PubMed  Google Scholar 

  26. Wang, S. et al. Cytological and transcriptomic analyses reveal important roles of CLE19 in pollen exine formation. Plant Physiol. 175, 1186–1202 (2017).

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Doughty, J. et al. PCP-A1, a defensin-like Brassica pollen coat protein that binds the S locus glycoprotein, is the product of gametophytic gene expression. Plant Cell 10, 1333–1347 (1998).

    CAS  PubMed  PubMed Central  Google Scholar 

  28. Fellenberg, C. & Vogt, T. Evolutionarily conserved phenylpropanoid pattern on angiosperm pollen. Trends Plant Sci. 20, 212–218 (2015).

    CAS  PubMed  Google Scholar 

  29. RejĂłn, J. D. et al. The pollen coat proteome: at the cutting edge of plant reproduction. Proteomes 4, 5 (2016).

    PubMed  PubMed Central  Google Scholar 

  30. Wang, L. et al. PCP-B class pollen coat proteins are key regulators of the hydration checkpoint in Arabidopsis thaliana pollen-stigma interactions. New Phytol. 213, 764–777 (2017).

    CAS  PubMed  Google Scholar 

  31. Jia, X. L. et al. A dye combination for the staining of pollen coat and pollen wall. Plant Reprod. 34, 91–101 (2021).

    CAS  PubMed  Google Scholar 

  32. Takayama, S. et al. Isolation and characterization of pollen coat proteins of Brassica campestris that interact with S locus-related glycoprotein 1 involved in pollen-stigma adhesion. Proc. Natl Acad. Sci. USA 97, 3765–3770 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  33. Shiba, H. et al. A pollen coat protein, SP11/SCR, determines the pollen S-specificity in the self-incompatibility of Brassica species. Plant Physiol. 125, 2095–2103 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  34. Liu, C. et al. Pollen PCP-B peptides unlock a stigma peptide-receptor kinase gating mechanism for pollination. Science 372, 171–175 (2021).

    CAS  PubMed  Google Scholar 

  35. Mayfield, J. A., Fiebig, A., Johnstone, S. E. & Preuss, D. Gene families from the Arabidopsis thaliana pollen coat proteome. Science 292, 2482–2485 (2001).

    CAS  PubMed  Google Scholar 

  36. Murphy, D. J. The extracellular pollen coat in members of the Brassicaceae: composition, biosynthesis, and functions in pollination. Protoplasma 228, 31–39 (2006).

    CAS  PubMed  Google Scholar 

  37. Zienkiewicz, K. et al. Identification and localization of a caleosin in olive (Olea europaea L.) pollen during in vitro germination. J. Exp. Bot. 61, 1537–1546 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Chen, J. C., Tsai, C. C. & Tzen, J. T. Cloning and secondary structure analysis of caleosin, a unique calcium-binding protein in oil bodies of plant seeds. Plant Cell Physiol. 40, 1079–1086 (1999).

    CAS  PubMed  Google Scholar 

  39. Mayfield, J. A. & Preuss, D. Rapid initiation of Arabidopsis pollination requires the oleosin-domain protein GRP17. Nat. Cell Biol. 2, 128–130 (2000).

    CAS  PubMed  Google Scholar 

  40. Updegraff, E. P., Zhao, F. & Preuss, D. The extracellular lipase EXL4 is required for efficient hydration of Arabidopsis pollen. Sex. Plant Reprod. 22, 197–204 (2009).

    CAS  PubMed  Google Scholar 

  41. Upton, C. & Buckley, J. T. A new family of lipolytic enzymes? Trends Plant Sci. 20, 178–179 (1995).

    CAS  Google Scholar 

  42. Yang, C., Vizcay-Barrena, G., Conner, K. & Wilson, Z. A. MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis. Plant Cell 19, 3530–3548 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Lévesque-Lemay, M. et al. Tapetal oleosins play an essential role in tapetosome formation and protein relocation to the pollen coat. New Phytol. 209, 691–704 (2016).

    PubMed  Google Scholar 

  44. Hiscock, S. J. & Allen, A. M. Diverse cell signalling pathways regulate pollen-stigma interactions: the search for consensus. New Phytol. 179, 286–317 (2008).

    CAS  PubMed  Google Scholar 

  45. Haslam, T. M. et al. ECERIFERUM2-LIKE proteins have unique biochemical and physiological functions in very-long-chain fatty acid elongation. Plant Physiol. 167, 682–692 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  46. Ni, E. et al. OsCER1 regulates humidity-sensitive genic male sterility through very-long-chain (VLC) alkane metabolism of tryphine in rice. Funct. Plant Biol. 48, 461–468 (2021).

    CAS  PubMed  Google Scholar 

  47. Agati, G. et al. Functional roles of flavonoids in photoprotection: new evidence, lessons from the past. Plant Physiol. Biochem. 72, 35–45 (2013).

    CAS  PubMed  Google Scholar 

  48. Walters, D., Meurer-Grimes, B. & Rovira, I. Antifungal activity of three spermidine conjugates. FEMS Microbiol. Lett. 201, 255–258 (2001).

    CAS  PubMed  Google Scholar 

  49. Piffanelli, P., Ross, J. & Murphy, D. Biogenesis and function of the lipidic structures of pollen grains. Sex. Plant Reprod. 11, 65–80 (1998).

    CAS  Google Scholar 

  50. Thimmappa, R., Geisler, K., Louveau, T., O’Maille, P. & Osbourn, A. Triterpene biosynthesis in plants. Annu. Rev. Plant Biol. 65, 225–257 (2014).

    CAS  PubMed  Google Scholar 

  51. Vranová, E., Coman, D. & Gruissem, W. Structure and dynamics of the isoprenoid pathway network. Mol. Plant 5, 318–333 (2012).

    PubMed  Google Scholar 

  52. Vranová, E., Coman, D. & Gruissem, W. Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu. Rev. Plant Biol. 64, 665–700 (2013).

    PubMed  Google Scholar 

  53. Suzuki, M. et al. Complete blockage of the mevalonate pathway results in male gametophyte lethality. J. Exp. Bot. 60, 2055–2064 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  54. Okada, K. et al. Genetic evidence for the role of isopentenyl diphosphate isomerases in the mevalonate pathway and plant development in Arabidopsis. Plant Cell Environ. 49, 604–616 (2008).

    CAS  Google Scholar 

  55. Li, H. & Zhang, D. Biosynthesis of anther cuticle and pollen exine in rice. Plant Signal. Behav. 5, 1121–1123 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  56. Burton, M., Rose, T. M., Faergeman, N. J. & Knudsen, J. Evolution of the acyl-CoA binding protein (ACBP). Biochem. J. 392, 299–307 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  57. Chen, Q. F., Xiao, S. & Chye, M. L. Overexpression of the Arabidopsis 10-kilodalton acyl-coenzyme A-binding protein ACBP6 enhances freezing tolerance. Plant Physiol. 148, 304–315 (2008).

    CAS  PubMed  PubMed Central  Google Scholar 

  58. Jessen, D. et al. Combined activity of LACS1 and LACS4 is required for proper pollen coat formation in Arabidopsis. Plant J. 68, 715–726 (2011).

    CAS  PubMed  Google Scholar 

  59. Shockey, J. M., Fulda, M. S. & Browse, J. A. Arabidopsis contains nine long-chain acyl-coenzyme A synthetase genes that participate in fatty acid and glycerolipid metabolism. Plant Physiol. 129, 1710–1722 (2002).

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Lü, S. et al. Arabidopsis CER8 encodes LONG-CHAIN ACYL-COA SYNTHETASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. Plant J. 59, 553–564 (2009).

    PubMed  Google Scholar 

  61. Hsiao, A. S., Yeung, E. C., Ye, Z. W. & Chye, M. L. The Arabidopsis cytosolic Acyl-CoA-binding proteins play combinatory roles in pollen development. Plant Cell Physiol. 56, 322–333 (2015).

    CAS  PubMed  Google Scholar 

  62. Hsiao, A. S. et al. Arabidopsis cytosolic acyl-CoA-binding proteins ACBP4, ACBP5 and ACBP6 have overlapping but distinct roles in seed development. Biosci. Rep. 34, e00165 (2014).

    PubMed  PubMed Central  Google Scholar 

  63. Bourdenx, B. et al. Overexpression of Arabidopsis ECERIFERUM1 promotes wax very-long-chain alkane biosynthesis and influences plant response to biotic and abiotic stresses. Plant Physiol. 156, 29–45 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  64. Haslam, T. M., Mañas-Fernández, A., Zhao, L. & Kunst, L. Arabidopsis ECERIFERUM2 is a component of the fatty acid elongation machinery required for fatty acid extension to exceptional lengths. Plant Physiol. 160, 1164–1174 (2012).

    CAS  PubMed  PubMed Central  Google Scholar 

  65. Zhan, H., Xiong, H., Wang, S. & Yang, Z. N. Anther endothecium-derived very-long-chain fatty acids facilitate pollen hydration in Arabidopsis. Mol. Plant 11, 1101–1104 (2018).

    CAS  PubMed  Google Scholar 

  66. Rowland, O., Lee, R., Franke, R., Schreiber, L. & Kunst, L. The CER3 wax biosynthetic gene from Arabidopsis thaliana is allelic to WAX2/YRE/FLP1. FEBS Lett. 581, 3538–3544 (2007).

    CAS  PubMed  Google Scholar 

  67. Xu, F., Zheng, L., Yang, Z. & Zhang, S. Arabidopsis ECERIFERUM3 (CER3) functions to maintain hydration for pollen–stigma recognition during fertilization. J. Plant Biol. 6, 347–359 (2020).

    Google Scholar 

  68. Fiebig, A. et al. Alterations in CER6, a gene identical to CUT1, differentially affect long-chain lipid content on the surface of pollen and stems. Plant Cell 12, 2001–2008 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  69. Jung, K. H. et al. 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 (2006).

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Ni, E. et al. OsCER1 plays a pivotal role in very-long-chain alkane biosynthesis and affects plastid development and programmed cell death of tapetum in rice (Oryza sativa L.). Front. Plant Sci. 9, 1217 (2018).

    PubMed  PubMed Central  Google Scholar 

  71. Fellenberg, C., Böttcher, C. & Vogt, T. Phenylpropanoid polyamine conjugate biosynthesis in Arabidopsis thaliana flower buds. Phytochemistry 70, 1392–1400 (2009).

    CAS  PubMed  Google Scholar 

  72. Grienenberger, E. et al. A BAHD acyltransferase is expressed in the tapetum of Arabidopsis anthers and is involved in the synthesis of hydroxycinnamoyl spermidines. Plant J. 58, 246–259 (2009).

    CAS  PubMed  Google Scholar 

  73. Yonekura-Sakakibara, K. et al. A flavonoid 3-O-glucoside:2′-O-glucosyltransferase responsible for terminal modification of pollen-specific flavonols in Arabidopsis thaliana. Plant J. 79, 769–782 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Winkel-Shirley, B. Flavonoid biosynthesis. A colorful model for genetics, biochemistry, cell biology, and biotechnology. Plant Physiol. 126, 485–493 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Skirycz, A. et al. Transcription factor AtDOF4;2 affects phenylpropanoid metabolism in Arabidopsis thaliana. New Phytol. 175, 425–438 (2007).

    CAS  PubMed  Google Scholar 

  76. Yang, J., Wu, J., Romanovicz, D., Clark, G. & Roux, S. J. Co-regulation of exine wall patterning, pollen fertility and anther dehiscence by Arabidopsis apyrases 6 and 7. Plant Physiol. Biochem. 69, 62–73 (2013).

    CAS  PubMed  Google Scholar 

  77. Chiu, T. Y. et al. Biochemical characterization of Arabidopsis APYRASE family reveals their roles in regulating endomembrane NDP/NMP homoeostasis. Biochem. J. 472, 43–54 (2015).

    CAS  PubMed  Google Scholar 

  78. Jiang, J. et al. PECTATE LYASE-LIKE 9 from Brassica campestris is associated with intine formation. Plant Sci. 229, 66–75 (2014a).

    CAS  PubMed  Google Scholar 

  79. Jiang, J. et al. PECTATE LYASE-LIKE10 is associated with pollen wall development in Brassica campestris. J. Integr. Plant Biol. 56, 1095–1105 (2014b).

    CAS  PubMed  Google Scholar 

  80. Mizelle, M. B., Sethi, R., Ashton, M. E. & Jensen, W. A. Development of the pollen grain and tapetum of wheat (Triticum aestivum) in untreated plants and plants treated with chemical hybridizing agent RH0007. Sex. Plant Reprod. 2, 231–253 (1989).

    Google Scholar 

  81. Sanders, P. et al. Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex. Plant Reprod. 11, 297–322 (1999).

    CAS  Google Scholar 

  82. Wilson, Z. A. & Zhang, D. B. From Arabidopsis to rice: pathways in pollen development. J. Exp. Bot. 60, 1479–1492 (2009).

    CAS  PubMed  Google Scholar 

  83. Fernández Gómez, J. & Wilson, Z. A. A barley PHD finger transcription factor that confers male sterility by affecting tapetal development. Plant Biotechnol. J. 12, 765–777 (2014).

    PubMed  Google Scholar 

  84. Zheng, S. et al. OsAGO2 controls ROS production and the initiation of tapetal PCD by epigenetically regulating OsHXK1 expression in rice anthers. Proc. Natl Acad. Sci. USA 116, 7549–7558 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Goldberg, R. B., Beals, T. P. & Sanders, P. M. Anther development: basic principles and practical applications. Plant Cell 5, 1217–1229 (1993).

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Xu, Y., Iacuone, S., Li, S. F. & Parish, R. W. MYB80 homologues in Arabidopsis, cotton and Brassica: regulation and functional conservation in tapetal and pollen development. BMC Plant Biol. 14, 278 (2014).

    PubMed  PubMed Central  Google Scholar 

  87. Gao, C. et al. A cytological study of anther and pollen development in Camellia oleifera. Genet. Mol. Res. 14, 8755–8765 (2015).

    CAS  PubMed  Google Scholar 

  88. Field, S. & Thompson, B. Analysis of the maize dicer-like1 mutant, fuzzy tassel, implicates microRNAs in anther maturation and dehiscence. PLoS ONE 11, e0146534 (2016).

    PubMed  PubMed Central  Google Scholar 

  89. Kim, Y. J. et al. Cytological characterization of anther development in Panax ginseng Meyer. Protoplasma 253, 1111–1124 (2016).

    PubMed  Google Scholar 

  90. Browne, R. G., Iacuone, S., Li, S. F., Dolferus, R. & Parish, R. W. Anther morphological development and stage determination in Triticum aestivum. Front. Plant Sci. 9, 228 (2018).

    PubMed  PubMed Central  Google Scholar 

  91. Zhang, D. et al. Histological and cytological characterization of anther and appendage development in Asian Lotus (Nelumbo nucifera Gaertn.). Int. J. Mol. Sci. 20, 1015 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  92. Li, N. et al. FAX1, a novel membrane protein mediating plastid fatty acid export. PLoS Biol. 13, e1002053 (2015).

    PubMed  PubMed Central  Google Scholar 

  93. Ariizumi, T. et al. 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 (2004).

    CAS  PubMed  Google Scholar 

  94. Schekman, R. & Orci, L. Coat proteins and vesicle budding. Science 271, 1526–1533 (1996).

    CAS  PubMed  Google Scholar 

  95. Zhao, B. et al. Secretory COPII protein SEC31B is required for pollen wall development. Plant Physiol. 172, 1625–1642 (2016).

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Huang, M. D., Chen, T. L. & Huang, A. H. Abundant type III lipid transfer proteins in Arabidopsis tapetum are secreted to the locule and become a constituent of the pollen exine. Plant Physiol. 163, 1218–1229 (2013).

    CAS  PubMed  PubMed Central  Google Scholar 

  97. Zhang, D. et al. OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol. 154, 149–162 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  98. Chen, L. et al. OsLTP47 may function in a lipid transfer relay essential for pollen wall development in rice. J. Genet. Genom. 49, 481–491 (2022).

    Google Scholar 

  99. Choi, H. et al. The role of Arabidopsis ABCG9 and ABCG31 ATP binding cassette transporters in pollen fitness and the deposition of steryl glycosides on the pollen coat. Plant Cell 26, 310–324 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  100. Grunewald, S. et al. The tapetal major facilitator NPF2.8 is required for accumulation of flavonol glycosides on the pollen surface in Arabidopsis thaliana. Plant Cell 32, 1727–1748 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  101. Hsieh, K. & Huang, A. H. Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum-derived flavonoids and alkanes for delivery to the pollen surface. Plant Cell 19, 582–596 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  102. Quilichini, T. D., Samuels, A. L. & Douglas, C. J. ABCG26-mediated polyketide trafficking and hydroxycinnamoyl spermidines contribute to pollen wall exine formation in Arabidopsis. Plant Cell 26, 4483–4498 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  103. Zhu, L., Shi, J., Zhao, G., Zhang, D. & Liang, W. 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).

    CAS  Google Scholar 

  104. Yim, S. et al. Postmeiotic development of pollen surface layers requires two Arabidopsis ABCG-type transporters. Plant Cell Rep. 35, 1863–1873 (2016).

    CAS  PubMed  Google Scholar 

  105. Zhao, G. et al. Two ATP binding cassette G transporters, rice ATP binding cassette G26 and ATP binding cassette G15, collaboratively regulate rice male reproduction. Plant Physiol. 169, 2064–2079 (2015).

    CAS  PubMed  PubMed Central  Google Scholar 

  106. Fei, H. & Sawhney, V. K. Ultrastructural characterization of male sterile33 (ms33) mutant in Arabidopsis affected in pollen desiccation and maturation. Botany 79, 118–129 (2001).

    Google Scholar 

  107. Cascales-Miñana, B. et al. The phosphorylated pathway of serine biosynthesis is essential both for male gametophyte and embryo development and for root growth in Arabidopsis. Plant Cell 25, 2084–2101 (2013).

    PubMed  PubMed Central  Google Scholar 

  108. Flores-Tornero, M., Anoman, A. D., Rosa-Téllez, S. & Ros, R. Lack of phosphoserine phosphatase activity alters pollen and tapetum development in Arabidopsis thaliana. Plant Sci. 235, 81–88 (2015).

    CAS  PubMed  Google Scholar 

  109. Chen, P. Y., Wu, C. C., Lin, C. C., Jane, W. N. & Suen, D. F. 3D imaging of tapetal mitochondria suggests the importance of mitochondrial fission in pollen growth. Plant Physiol. 180, 813–826 (2019).

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Li, Z. et al. Global dynamic transcriptome programming of rapeseed (Brassica napus L.) anther at different development stages. PLoS ONE 11, e0154039 (2016).

    PubMed  PubMed Central  Google Scholar 

  111. Hernández-Pinzón, I., Ross, J. H., Barnes, K. A., Damant, A. P. & Murphy, D. J. Composition and role of tapetal lipid bodies in the biogenesis of the pollen coat of Brassica napus. Planta 208, 588–598 (1999).

    PubMed  Google Scholar 

  112. Wu, S. S., Moreau, R. A., Whitaker, B. D. & Huang, A. H. Steryl esters in the elaioplasts of the tapetum in developing Brassica anthers and their recovery on the pollen surface. Lipids 34, 517–523 (1999).

    CAS  PubMed  Google Scholar 

  113. Kim, H. U., Wu, S. S., Ratnayake, C. & Huang, A. H. Brassica rapa has three genes that encode proteins associated with different neutral lipids in plastids of specific tissues. Plant Physiol. 126, 330–341 (2001).

    CAS  PubMed  PubMed Central  Google Scholar 

  114. Suzuki, T. et al. Development and disintegration of tapetum-specific lipid-accumulating organelles, elaioplasts and tapetosomes, in Arabidopsis thaliana and Brassica napus. Plant Sci. 207, 25–36 (2013).

    CAS  PubMed  Google Scholar 

  115. Ting, J. T., Wu, S. S., Ratnayake, C. & Huang, A. H. Constituents of the tapetosomes and elaioplasts in Brassica campestris tapetum and their degradation and retention during microsporogenesis. Plant J. 16, 541–551 (1998).

    CAS  PubMed  Google Scholar 

  116. Zheng, S. et al. A cytosolic pentatricopeptide repeat protein is essential for tapetal plastid development by regulating OsGLK1 transcript levels in rice. New Phytol. 234, 1678–1695 (2022).

    CAS  PubMed  Google Scholar 

  117. Mamun, E. A., Cantrill, L. C., Overall, R. L. & Sutton, B. G. Cellular organisation in meiotic and early post-meiotic rice anthers. Cell Biol. Int. 29, 903–913 (2005).

    CAS  PubMed  Google Scholar 

  118. Mamun, E. A., Alfred, S., Cantrill, L. C., Overall, R. L. & Sutton, B. G. Effects of chilling on male gametophyte development in rice. Cell Biol. Int. 30, 583–591 (2006).

    CAS  PubMed  Google Scholar 

  119. El-Ghazaly, G. & Jensen, W. A. Development of wheat (Triticum aestivum) pollen. ii. Histochemical differentiation of wall and Ubisch bodies during development. Am. J. Bot. 74, 1396–1418 (1987).

    Google Scholar 

  120. Huysmans, S. & Smets, E. G. Orbicules in angiosperms: morphology, function, distribution, and relation with tapetum types. Botanical Rev. 64, 240–272 (1998).

    Google Scholar 

  121. Sharma, A., Singh, M. B. & Bhalla, P. L. Cytochemistry of pollen development in Brachypodium distachyon. Plant Syst. Evol. 300, 1639–1648 (2014).

    CAS  Google Scholar 

  122. Pacini, E., Guarnieri, M. & Nepi, M. Pollen carbohydrates and water content during development, presentation, and dispersal: a short review. Protoplasma 228, 73–77 (2006).

    CAS  PubMed  Google Scholar 

  123. Morant, M. et al. 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 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  124. Dobritsa, A. A. et al. CYP704B1 is a long-chain fatty acid omega-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis. Plant Physiol. 151, 574–589 (2009).

    CAS  PubMed  PubMed Central  Google Scholar 

  125. Chen, W. et al. Male Sterile2 encodes a plastid-localized fatty acyl carrier protein reductase required for pollen exine development in Arabidopsis. Plant Physiol. 157, 842–853 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  126. Yang, X. et al. Rice CYP703A3, a cytochrome P450 hydroxylase, is essential for development of anther cuticle and pollen exine. J. Integr. Plant Biol. 56, 979–994 (2014).

    CAS  PubMed  Google Scholar 

  127. Li, H. et al. Cytochrome P450 family member CYP704B2 catalyzes the ω-hydroxylation of fatty acids and is required for anther cutin biosynthesis and pollen exine formation in rice. Plant Cell 22, 173–190 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  128. Shi, J. et al. 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 (2011).

    CAS  PubMed  PubMed Central  Google Scholar 

  129. Lu, J. Y. et al. MS1, a direct target of MS188, regulates the expression of key sporophytic pollen coat protein genes in Arabidopsis. J. Exp. Bot. 71, 4877–4889 (2020).

    CAS  PubMed  PubMed Central  Google Scholar 

  130. Feng, B. et al. Regulation of the Arabidopsis anther transcriptome by DYT1 for pollen development. Plant J. 72, 612–624 (2012).

    CAS  PubMed  Google Scholar 

  131. Zhu, J. et al. Defective in Tapetal development and function 1 is essential for anther development and tapetal function for microspore maturation in Arabidopsis. Plant J. 55, 266–277 (2008).

    CAS  PubMed  Google Scholar 

  132. Lou, Y. et al. Positive regulation of AMS by TDF1 and the formation of a TDF1-AMS complex are required for anther development in Arabidopsis thaliana. New Phytol. 217, 378–391 (2018).

    CAS  PubMed  Google Scholar 

  133. Gu, J. N. et al. DYT1 directly regulates the expression of TDF1 for tapetum development and pollen wall formation in Arabidopsis. Plant J. 80, 1005–1013 (2014).

    CAS  PubMed  Google Scholar 

  134. Xu, J. et al. The ABORTED MICROSPORES regulatory network is required for postmeiotic male reproductive development in Arabidopsis thaliana. Plant Cell 22, 91–107 (2010).

    CAS  PubMed  PubMed Central  Google Scholar 

  135. Xu, J. et al. ABORTED MICROSPORES acts as a master regulator of pollen wall formation in Arabidopsis. Plant Cell 26, 1544–1556 (2014).

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Ito, T. et al. Arabidopsis MALE STERILITY1 encodes a PHD-type transcription factor and regulates pollen and tapetum development. Plant Cell 19, 3549–3562 (2007).

    CAS  PubMed  PubMed Central  Google Scholar 

  137. Jung, K. H. et al. Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17, 2705–2722 (2005).

    CAS  PubMed  PubMed Central  Google Scholar 

  138. Cai, C. F. et al. The functional analysis of OsTDF1 reveals a conserved genetic pathway for tapetal development between rice and Arabidopsis. Sci. Bull. 60, 1073–1082 (2015).

    CAS  Google Scholar 

  139. Zhang, S., Fang, Z., Zhu, J., Gao, J. & Yang, Z. OsMYB103 is required for rice anther development by regulating tapetum development and exine formation. Chin. Sci. Bull. 55, 3288–3297 (2010).

    CAS  Google Scholar 

  140. Han, Y. et al. OsMS188 is a key regulator of tapetum development and sporopollenin synthesis in rice. Rice 14, 4 (2021).

    CAS  PubMed  PubMed Central  Google Scholar 

  141. Yang, Z. et al. OsMS1 functions as a transcriptional activator to regulate programmed tapetum development and pollen exine formation in rice. Plant Mol. Biol. 99, 175–191 (2019).

    CAS  PubMed  Google Scholar 

  142. Liu, X. et al. The ZmMYB84-ZmPKSB regulatory module controls male fertility through modulating anther cuticle-pollen exine trade-off in maize anthers. Plant Biotechnol. J. 20, 2342–2356 (2022).

    CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

We thank M. Sun, Z. Yang and C. Xu for the helpful comments and editing of the manuscript. This research was supported by the National Key Research and Development Program of China (no. 2022YFF1003500) and the National Natural Science Foundation of China (no. 32101769, 31530050, 3191001081).

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Y.Q., B.H. and X.Q. contributed to the writing and editing of the manuscript and the generation of the figures.

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Qiao, Y., Hou, B. & Qi, X. Biosynthesis and transport of pollen coat precursors in angiosperms. Nat. Plants 9, 864–876 (2023). https://doi.org/10.1038/s41477-023-01413-0

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