Exine Export in Pollen

Part of the Signaling and Communication in Plants book series (SIGCOMM, volume 22)


Pollen as a sperm cell carrier is mainly protected by outer pollen wall (called exine) from physical and biological stresses. The major composition of exine is the highly resistant biopolymer sporopollenin, which mainly consists of hydrophobic lipids, phenylpropanoids, and aromatic compounds. The biosynthesis of these constituents has been shown to be catalyzed by enzymes preferentially expressed in the sporophytic tapetal layer, a nutritive tissue supporting pollen development. How the synthesized sporopollenin precursors are exported from tapetal cells onto the surface of microspore for pollen exine formation remains largely unknown. Here, we review the structure of tapetal cella and pollen exine in the model monocot rice (Oryza sativa) and the model dicot Arabidopsis thaliana. In addition, we highlight the update understanding on the role of ATP-binding cassette (ABC), lipid transfer protein (LTP), and multidrug and toxic efflux (MATE) transporters in trafficking of sporopollenin precursors across tapetal cells for exine development in rice and Arabidopsis. We also discuss the future research focus on the transport of sporopollenin precursors for exine synthesis.



We thank Dr. Jianxin Shi for comments and reading on this chapter. This work was supported by funds from National Natural Science Foundation of China Grants 31230051, 30971739, 31270222 and 31110103915; China Innovative Research Team, Ministry of Education; 111 Project (B14016).


  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 12:615–623PubMedCrossRefGoogle Scholar
  2. Ahlers F, Thom I, Lambert J, Kuckuk R, Wiermann R (1999) 1H NMR analysis of sporopollenin from Typha Angustifolia. Phytochemistry 50:1095–1098CrossRefGoogle Scholar
  3. Ariizumi T, Toriyama K (2011) Genetic regulation of sporopollenin synthesis and pollen exine development. Annu Rev Plant Biol 62:437–460PubMedCrossRefGoogle Scholar
  4. 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 21:1453–1472PubMedCentralPubMedCrossRefGoogle Scholar
  5. Blackmore S, Wortley AH, Skvarla JJ, Rowley JR (2007) Pollen wall development in flowering plants. New Phytologist 174:483–498PubMedCrossRefGoogle Scholar
  6. Chen W, Yu X-H, Zhang K, Shi J, De Oliveira S, Schreiber L, Shanklin J, Zhang D (2011) Male Sterile2 encodes a plastid-localized fatty acyl carrier protein reductase required for pollen exine development in Arabidopsis. Plant Physiol 157:842–853PubMedCentralPubMedCrossRefGoogle Scholar
  7. 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 65:181–193PubMedCrossRefGoogle Scholar
  8. Dobritsa AA, Shrestha J, Morant M, Pinot F, Matsuno M, Swanson R, Møller BL, Preuss D (2009) CYP704B1 is a long-chain fatty acid ω-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis. Plant Physiol 151:574–589PubMedCentralPubMedCrossRefGoogle Scholar
  9. Dobritsa AA, Lei Z, Nishikawa S-I, 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 Physiology 153:937–955PubMedCentralPubMedCrossRefGoogle Scholar
  10. 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 53:74–88PubMedCrossRefGoogle Scholar
  11. Furness CA, Rudall PJ (2001) The tapetum in basal angiosperms: early diversity. Int J Plant Sci 162:375–392CrossRefGoogle Scholar
  12. Grienenberger E, Kim SS, Lallemand B, Geoffroy P, Heintz D, de Azevedo Souza C, Heitz T, Douglas CJ, Legrand M (2010) Analysis of TETRAKETIDE α-PYRONE REDUCTASE function in Arabidopsis thaliana reveals a previously unknown, but conserved, biochemical pathway in sporopollenin monomer biosynthesis. Plant Cell 22:4067–4083PubMedCentralPubMedCrossRefGoogle Scholar
  13. Hsieh K, Huang AH (2007) Tapetosomes in Brassica tapetum accumulate endoplasmic reticulum–derived flavonoids and alkanes for delivery to the pollen surface. Plant Cell 19:582–596PubMedCentralPubMedCrossRefGoogle Scholar
  14. Huang MD, Chen TL, Huang AH (2013) Abundant type III lipid transfer proteins in Arabidopsis tapetum are secreted to the locule and become a constituent of the pollen exine. Plant Physiol 163:1218–1229PubMedCentralPubMedCrossRefGoogle Scholar
  15. Huysmans S, El-Ghazaly G, Smets E (1998) Orbicules in angiosperms: morphology, function, distribution, and relation with tapetum types. Bot Rev 64:240–272CrossRefGoogle Scholar
  16. Jung K-H, Han M-J, Lee Y-S, Kim Y-W, Hwang I, Kim M-J, Kim Y-K, Nahm BH, An G (2005) Rice Undeveloped Tapetum1 is a major regulator of early tapetum development. Plant Cell 17:2705–2722PubMedCentralPubMedCrossRefGoogle Scholar
  17. Jung K-H, Han M-J, Lee D-Y, Lee Y-S, Schreiber L, Franke R, Faust A, Yephremov A, Saedler H, Kim Y-W, 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 18:3015–3032PubMedCentralPubMedCrossRefGoogle Scholar
  18. Kader J-C (1996) Lipid-transfer proteins in plants. Annu Rev Plant Biol 47:627–654CrossRefGoogle Scholar
  19. Kang J, Park J, Choi H, Burla B, Kretzschmar T, Lee Y, Martinoia E (2011) Plant ABC transporters. The Arabidopsis book/American Society of Plant Biologists 9Google Scholar
  20. Kim SS, Grienenberger E, Lallemand B, Colpitts CC, Kim SY, de Azevedo Souza C, Geoffroy P, Heintz D, Krahn D, Kaiser M (2010) LAP6/POLYKETIDE SYNTHASE A and LAP5/POLYKETIDE SYNTHASE B encode hydroxyalkyl α-pyrone synthases required for pollen development and sporopollenin biosynthesis in Arabidopsis thaliana. Plant Cell 22:4045–4066PubMedCentralPubMedCrossRefGoogle Scholar
  21. Kitamura S, Shikazono N, Tanaka A (2004) TRANSPARENT TESTA 19 is involved in the accumulation of both anthocyanins and proanthocyanidins in Arabidopsis. The Plant Journal 37:104–114PubMedCrossRefGoogle Scholar
  22. Kunst L, Samuels A (2003) Biosynthesis and secretion of plant cuticular wax. Progres Lipid Res 42:51–80CrossRefGoogle Scholar
  23. 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 107:2361–2366PubMedCentralPubMedCrossRefGoogle Scholar
  24. Li H, Zhang D (2010) Biosynthesis of anther cuticle and pollen exine in rice. Plant Signal Behav 5:1121–1123PubMedCentralPubMedCrossRefGoogle Scholar
  25. Li N, Zhang D-S, Liu H-S, Yin C-S, Li X-X, Liang W-Q, Yuan Z, Xu B, Chu H-W, Wang J, Wen T-Q, Huang H, Luo D, Ma H, Zhang D-B (2006) The rice Tapetum Degeneration Retardation gene is required for tapetum degradation and anther development. Plant Cell 18:2999–3014PubMedCentralPubMedCrossRefGoogle Scholar
  26. Li H, Pinot F, Sauveplane V, Werck-Reichhart D, Diehl P, Schreiber L, Franke R, Zhang P, Chen L, Gao Y (2010) 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 22:173–190PubMedCentralPubMedCrossRefGoogle Scholar
  27. Li H, Yuan Z, Vizcay-Barrena G, Yang C, Liang W, Zong J, Wilson ZA, Zhang D (2011) PERSISTENT TAPETAL CELL1 encodes a PHD-finger protein that is required for tapetal cell death and pollen development in rice. Plant Physiol 156:615–630PubMedCentralPubMedCrossRefGoogle Scholar
  28. Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD, Baud S, Bird D, DeBono A, Durrett TP (2010) Acyl-lipid metabolism. The Arabidopsis Book/American Society of Plant Biologists 8Google Scholar
  29. Ma H (2005) Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annu Rev Plant Biol 56:393–434PubMedCrossRefGoogle Scholar
  30. Marinova K, Pourcel L, Weder B, Schwarz M, Barron D, Routaboul J-M, Debeaujon I, Klein M (2007) The Arabidopsis MATE transporter TT12 acts as a vacuolar flavonoid/H+-antiporter active in proanthocyanidin-accumulating cells of the seed coat. Plant Cell 19:2023–2038PubMedCentralPubMedCrossRefGoogle Scholar
  31. Morant M, Jørgensen K, Schaller H, Pinot F, Møller 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 19:1473–1487PubMedCentralPubMedCrossRefGoogle Scholar
  32. Ohlrogge JB, Kuhn DN, Stumpf P (1979) Subcellular localization of acyl carrier protein in leaf protoplasts of Spinacia oleracea. Proc Natl Acad Sci 76:1194–1198PubMedCentralPubMedCrossRefGoogle Scholar
  33. Piffanelli P, Ross JH, Murphy D (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex Plant Reprod 11:65–80CrossRefGoogle Scholar
  34. Qin P, Tu B, Wang Y, Deng L, Quilichini TD, Li T, Wang H, Ma B, Li S (2013) ABCG15 encodes an ABC transporter protein, and is essential for post-meiotic anther and pollen exine development in rice. Plant Cell Physiol 54:138–154PubMedCrossRefGoogle Scholar
  35. 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 154:678–690PubMedCentralPubMedCrossRefGoogle Scholar
  36. Scott R (1994) Pollen exine-the sporopollenin enigma and the physics of pattern. In: Seminar series-society for experimental biology, Vol 55. (Cambridge University Press), pp 49–49Google Scholar
  37. Shi J, Tan H, Yu X-H, Liu Y, Liang W, Ranathunge K, Franke RB, Schreiber L, Wang Y, Kai G, Shanklin J, Ma H, Zhang D-B (2011) Defective Pollen Wall is required for anther and microspore development in rice and encodes a fatty acyl carrier protein reductase. Plant Cell 23:2225–2246PubMedCentralPubMedCrossRefGoogle Scholar
  38. Sorensen AM, Kröber S, Unte US, Huijser P, Dekker K, Saedler H (2003) The Arabidopsis ABORTED MICROSPORES (AMS) gene encodes a MYC class transcription factor. Plant J 33:413–423PubMedCrossRefGoogle Scholar
  39. 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 21:507–525CrossRefGoogle Scholar
  40. Spector AA, Soboroff JM (1972) Studies on the cellular mechanism of free fatty acid uptake using an analog, hexadecanol. J Lipid Res 13:790–796PubMedGoogle Scholar
  41. Sun Y, Li H, Huang J-R (2012) Arabidopsis TT19 functions as a carrier to transport anthocyanin from the cytosol to tonoplasts. Mol Plant 5:387–400PubMedCrossRefGoogle Scholar
  42. Tang LK, Chu H, Yip WK, Yeung EC, Lo C (2009) An anther‐specific Dihydroflavonol 4‐Reductase‐Like gene (DRL1) is essential for male fertility in Arabidopsis. New Phytologist 181:576–587PubMedCrossRefGoogle Scholar
  43. Ting JT, Wu SS, Ratnayake C, Huang AH (1998) Constituents of the tapetosomes and elaioplasts in Brassica campestristapetum and their degradation and retention during microsporogenesis. Plant J 16:541–551PubMedCrossRefGoogle Scholar
  44. 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 100:14487–14492PubMedCentralPubMedCrossRefGoogle Scholar
  45. Wilson ZA, Zhang D-B (2009) From Arabidopsis to rice: pathways in pollen development. J Exp Bot 60:1479–1492PubMedCrossRefGoogle Scholar
  46. Xu J, Yang C, Yuan Z, Zhang D, Gondwe MY, Ding Z, Liang W, Zhang D, Wilson ZA (2010) The ABORTED MICROSPORES regulatory network is required for postmeiotic male reproductive development in Arabidopsis thaliana. Plant Cell 22:91–107PubMedCentralPubMedCrossRefGoogle Scholar
  47. Yang C, Vizcay-Barrena G, Conner K, Wilson ZA (2007) MALE STERILITY1 is required for tapetal development and pollen wall biosynthesis. Plant Cell 19:3530–3548PubMedCentralPubMedCrossRefGoogle Scholar
  48. Yeats TH, Rose JK (2008) The biochemistry and biology of extracellular plant lipid‐transfer proteins (LTPs). Protein Sci 17:191–198PubMedCentralPubMedCrossRefGoogle Scholar
  49. Zhang D, Wilson ZA (2009) Stamen specification and anther development in rice. Chn Sci Bull 54:2342–2353CrossRefGoogle Scholar
  50. Zhang D, Liang W, Yin C, Zong J, Gu F, Zhang D (2010) OsC6, encoding a lipid transfer protein, is required for postmeiotic anther development in rice. Plant Physiol 154:149–162PubMedCentralPubMedCrossRefGoogle Scholar
  51. Zhang D, Luo X, Zhu L (2011) Cytological analysis and genetic control of rice anther development. J Genet Genom 38:379–390CrossRefGoogle Scholar
  52. Zhao J, Dixon RA (2009) MATE transporters facilitate vacuolar uptake of epicatechin 3′-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. Plant Cell 21:2323–2340PubMedCentralPubMedCrossRefGoogle Scholar
  53. Zhu L, Shi J, Zhao G, Zhang D, Liang W (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 56:59–68CrossRefGoogle Scholar
  54. 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 126:5431–5440PubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2014

Authors and Affiliations

  1. 1.School of Life Sciences and BiotechnologyShanghai Jiao Tong UniversityShanghaiChina
  2. 2.Department of Botany and Plant SciencesUniversity of CaliforniaRiversideUSA

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