Pollen wall development in flowering plants: Tansley review

New Phytologist

Volumn 174, Issue 3, 2007, Pages 483-498

  Blackmore, Stephen ^a   Wortley, Alexandra H ^a   Skvarla, John J ^b   Rowley, John R ^c  

^a ROYAL BOTANIC GARDEN EDINBURGH   (United Kingdom)

^b UNIVERSITY OF OKLAHOMA   (United States)

^c STOCKHOLM UNIVERSITY   (Sweden)

Author keywords

Compositae; Exine; Exine stratification; Exine substructure; Microsporogenesis; Pollen development; Primexine; Self assembly

Indexed keywords

ANGIOSPERM; COMPLEXITY; GENETICS; MORPHOLOGY; ONTOGENY; PALYNOLOGY; POLLEN; ULTRASTRUCTURE;

ANGIOSPERM; CELL WALL; CYTOLOGY; GENETICS; GROWTH, DEVELOPMENT AND AGING; MEIOSIS; PHYSIOLOGY; POLLEN; REVIEW; ULTRASTRUCTURE;

ANGIOSPERMS; CELL WALL; MEIOSIS; POLLEN;

ASTERACEAE; MAGNOLIOPHYTA;

EID: 34247396174     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/j.1469-8137.2007.02060.x     Document Type: Review

References (125)

1. Ahlers F, Bubert H, Steuernagel S, Wiermann R. 2000. The nature of oxygen in sporopollenin from the pollen of Typha angustifolia L. Zeitschrift für Naturforschung C 55: 129-136.
2. APG II. 2003. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Botanical Journal of the Linnean Society 141: 399-436.
3. 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 Molecular Biology 53: 107-116.
4. Ariizumi T, Hatakeyama K, Hinata K, Sato S, Kato T, Tabata S, Toriyama K. 2005. The HKM gene, which is identical to the MS1 gene of Arabidopsis thaliana, is essential for primexine formation and exine pattern formation. Sexual Plant Reproduction 18: 1-7.
5. Barnes SH, Blackmore S. 1986. Some functional features during pollen development. In: Blackmore S, Ferguson IK, eds. Pollen and spores: form and function. London, UK: Academic Press, 71-80.
6. Barnes SH, Blackmore S. 1987. Preliminary observations on the formation of the male germ unit in Catananche caerulea L. (Compositae: Lactuceae). Protoplasma 138: 187-189.
7. Barnes SH, Blackmore S. 1988. Pollen ontogeny in Catananche caerulea L. (Compositae: Lactuceae) II. Free microspore stage to the formation of the male germ unit. Annals of Botany 62: 615-623.
8. Becker JD, Boavida LC, Carneiro J, Haury M, Feijo JA. 2003. Transcriptional profiling of Arabidopsis tissues reveals the unique characteristics of the pollen transcriptome. Plant Physiology 133: 713-725.
9. Blackmore S. 1984. Compositae-Lactuceae. Review of Palaeobotany and Palynology 42: 45-85.
10. Blackmore S. 1986. Lophate pollen in the Compositae: its identification and taxonomic significance. Canadian Journal of Botany 64: 3101-3112.
11. Blackmore S. 1990. Sporoderm homologies and morphogenesis in land plants, with a discussion of Echinops sphaerocephala (Compositae). Plant Systematics and Evolution 5: 1-12.
12. Blackmore S. 2007. Pollen and spores: microscopic keys to understanding the earth's biodiversity. Plant Systematics and Evolution 263: 3-12.
13. Blackmore S, Barnes SH. 1985. Cosmos pollen ontogeny: a scanning electron microscope study. Protoplasma 126: 91-99.
14. Blackmore S, Barnes SH. 1987. Pollen wall morphogenesis in Tragopogon porrifolius (Compositae: Lactuceae) and its taxonomic significance. Review of Palaeobotany and Palynology 52: 233-246.
15. Blackmore S, Barnes SH. 1988. Pollen ontogeny in Catananche caerulea L. (Compositae: Lactuceae) I. Premeiotic phase to establishment of tetrads. Annals of Botany 62: 605-614.
16. Blackmore S, Barnes SH. 1995. Garside's rule and the microspore tetrads of Grevillea rosmarinifolia A. Cunningham and Dryandra polycephala Bentham (Proteaceae). Review of Palaeobotany and Palynology 85: 111-121.
17. Blackmore S, Claugher D. 1987. Observations on the substructural organisation of the exine in Fagus sylvatica L. (Fagaceae) and Scorzonera hispanica L. (Compositae: Lactuceae). Review of Palaeobotany and Palynology 53: 175-184.
18. Blackmore S, Crane PR. 1988. Systematic implications of pollen and spore ontogeny. In: Humphries CJ, ed. Ontogeny and systematics. New York, NY, USA: Columbia University Press, 83-115.
19. Blackmore S, Crane PR. 1998. The evolution of apertures in the spores and pollen grains of embryophytes. In: Owens SJ, Rudall PJ, eds. Reproductive biology. London, UK: Royal Botanic Gardens, Kew, 159-182.
20. Boavida LC, Becker JD, Feijo JA. 2005. The making of gametes in higher plants. International Journal of Developmental Biology 49: 595-614.
21. Brown RC, Lemmon BE. 1991. Pollen development in orchids. 1. Cytoskeletal control of division plane in irregular patterns of meiotic cytokinesis. Protoplasma 163: 9-18.
22. Brown RC, Lemmon BE. 1992a. Cytoplasmic domain: a model for spatial control of cytokinesis in reproductive cells of plants. EMSA Bulletin 22: 48-53.
23. Brown RC, Lemmon BE. 1992b. Control of division plane in normal and griseofulvin-treated microsporocytes of Magnolia. Journal of Cell Science 103: 1031-1038.
24. Bubert H, Lambert J, Steuernagel S, Ahlers F, Wiermann R. 2002. Continuous decomposition of sporopollenin from pollen of Typha angustifolia L. by acidic methanolysis. Zeitschrift für Naturforschung C 57: 1035-1041.
25. Chaloner WG. 1976. The evolution of adaptive features in fossil exines. In: Ferguson IK, Muller J, eds. Evolutionary significance of the exine. London, UK: Academic Press, 1-14.
26. Dickinson HG. 1970a. The fine structure of a peritapetal membrane investing the microsporangium of Pinus banksiana. New Phytologist 69: 1065-1068.
27. Dickinson HG. 1970b. Ultrastructural aspects of primexine formation in the microspore tetrad of Lilium longiflorum. Cytobiologie 1: 437-449.
28. Dickinson HG. 1976. Common factors in exine deposition. In: Ferguson IK, Muller J, eds. The evolutionary significance of the exine. London, UK: Academic Press, 67-89.
29. Dickinson HG, Heslop-Harrison J. 1968. A common mode of deposition of the sporopollenin of sexine and nexine. Nature 213: 976-977.
30. Dickinson HG, Heslop-Harrison J. 1976. Ribosomes, membranes and organelles during meiosis in Angiosperms. Philosophical Transactions of the Royal Society of London, Series B 277: 327-342.
31. Dickinson HG, Potter U. 1976. The development of patterning in the alveolar sexine of Cosmos bipinnatus. New Phytologist 76: 543-550.
32. Dickinson HG, Sheldon JM. 1986. The generation of patterning at the plasma membrane of the young microspores of Lilium. In: Blackmore S, Ferguson IK, eds. Pollen and spores: form and function. London, UK: Academic Press, 1-17.
33. Dominguez E, Mercado JA, Quesada MA, Heredia A. 1999. Pollen sporopollenin: degradation and structural elucidation. Sexual Plant Reproduction 12: 171-178.
34. Dong XY, Hong ZL, Sivaramakrishnan M, Mahfouz M, Verma DPS. 2005. Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant Journal 42: 315-328.
35. Dover GA. 1972. The organisation and polarity of pollen mother cells of Triticum aestivum. Journal of Cell Science 11: 699-711.
36. Dumas C, Knox RB, Gaude T. 1985. The spatial association of the sperm cell and vegetative nucleus in the pollen grain of Brassica. Protoplasma 124: 168-174.
37. Edlund AF, Swanson R, Preuss D. 2004. Pollen and stigma structure and function: the role of diversity in pollination. Plant Cell 16: S84-S97.
38. Enns LC, Kanaoka MM, Torii KU, Comai L, Okada K, Cleland RE. 2005. Two callose synthases, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility. Plant Molecular Biology 58: 333-349.
39. Farr CH. 1916. Cytokinesis of the pollen-mother-cells of certain dicotyledons. Memoirs of the New York Botanical Garden 6: 253-317.
40. Fitzgerald MA, Knox RB. 1995. Initiation of primexine in freeze-substituted microspores of Brassica campestris. Sexual Plant Reproduction 8: 99-104.
41. Francis KE, Lam SY, Copenhaver GP. 2006. Separation of Arabidopsis pollen tetrads is regulated by QUARTET1, a pectin methylesterase gene. Plant Physiology 142: 1004-1013.
42. Funk V, Bayer RJ, Keeley S, Chan R, Watson L, Gemeinholzer B, Schilling E, Panero JL, Baldwin BG, Garcia-Jacas N, Susanna A, Jansen RK. 2005. Everywhere but Antarctica: using a supertree to understand the diversity and distribution of the Compositae. Biologiske Skrifter 55: 343-374.
43. Furness CA, Rudall PJ, Sampson FB. 2002. Evolution of microsporogenesis in Angiosperms. International Journal of Plant Science 163: 235-260.
44. Gabarayeva N, Hemsley AR. 2006. The role of self-assembly in the development of pollen wall structure. Review of Palaeobotany and Palynology 138: 121-139.
45. Gates RR. 1920. A preliminary account of the meiotic phenomena in the mother cells and tapetum of lettuce (Lactuca sativa). Proceedings of the Royal Society of London, Series B 91: 216-223.
46. Gates RR, Rees EM. 1921. A cytological study of pollen development in Lactuca. Annals of Botany 35: 365-398.
47. Goldberg RB, Beals TP, Sanders PM. 1993. Anther development: basic principles and practical applications. Plant Cell 5: 1217-1229.
48. Golubovskaya IN. 1979. Genetic control of meiosis. International Review of Cytology 58: 247-290.
49. Goodwin H, Echlin P, Chapman B. 1967. The development of the pollen grain wall in Ipomoea purpurea (L.) Roth. Review of Palaeobotany and Palynology 3: 181-195.
50. Hemsley AR, Gabarayeva N. 2007. Exine development: the importance of looking through a colloid chemistry 'window'. Plant Systematics and Evolution 263: 25-49.
51. Hemsley AR, Barrie PJ, Chaloner WG, Scott AC. 1993. The composition of sporopollenin and its use in living and fossil plant systematics. Granasupplement 1: 2-11.
52. Hemsley AR, Griffiths PC, Matthias R, Moore SEM. 2003. A model for the role of surfactants in the assembly of exine structure. Grana 42: 38-42.
53. Heslop-Harrison J. 1963. An ultrastructural study of pollen wall ontogeny in Silene pendula. Grana Palynologica 4: 7-24.
54. Heslop-Harrison J. 1964. Cell walls, cell membranes and protoplasmic connections during meiosis and pollen development. In: Linskens HF, ed. Pollen physiology and fertilization. Amsterdam, the Netherlands: North Holland, 39-47.
55. Heslop-Harrison J. 1966. Cytoplasmic continuities during spore formation in flowering plants. Endeavour 25: 65-72.
56. Heslop-Harrison J. 1968. The pollen grain wall. Science 161: 230-237.
57. Heslop-Harrison J. 1969a. An acetolysis resistant membrane investing tapetum and sporogenous tissue in the anthers of certain Compositae. Canadian Journal of Botany 47: 541-542.
58. Heslop-Harrison J. 1969b. The origin of surface features of the pollen wall of Tagetes patula as observed by scanning electron microscopy. Cytobios 2: 177-186.
59. Heslop-Harrison J. 1971. Wall pattern formation in angiosperm microsporogenesis. Symposium of the Society for Experimental Biology 25: 277-300.
60. Heslop-Harrison J. 1972. Pattern in plant cell walls: morphogenesis in miniature. Proceedings of the Royal Institution of Great Britain 45: 335-351.
61. Heslop-Harrison J. 1974. The physiology of the pollen grain surface. Proceedings of the Royal Society of London, Series B 190: 275-299.
62. Heslop-Harrison J. 1976. The adaptive significance of the exine. In: Ferguson IK, Muller J, eds. The Evolutionary Significance of the Exine. London, UK: Academic Press, 27-37.
63. Heslop-Harrison J, Mackenzie A. 1967. Auto-radiography of (214C)-thymidine derivatives during meiosis and microsporogenesis in Lilium anthers. Journal of Cell Science 2: 387-400.
64. Honys D, Twell D. 2003. Comparative analysis of the Arabidopsis pollen transcriptome. Plant Physiology 132: 640-652.
65. Honys D, Twell D. 2004. Transcriptome analysis of haploid male gametophyte development in Arabidopsis. Genome Biology 5: R85.
66. Howden R, Park SK, Moore JM, Orem J, Grossniklaus U, Twell D. 1998. Selection of T-DNA-tagged male and female gametophytic mutants by segregation distortion in Arabidopsis. Genetics 149: 621-631.
67. Ingber DE. 1993. Cellular tensegrity: defining new rules of biological design that govern the cytoskeleton. Journal of Cell Science 104: 613-627.
68. Ito T, Shinozaki K. 2002. The male sterility1 gene of Arabidopsis, encoding a nuclear protein with a PHD-finger motif, is expressed in tapetal cells and is required for pollen maturation. Plant Cell Physiology 45: 1285-1292.
69. Izhar S, Frankel R. 1970. Mechanism of male sterility in Petunia: the relationship between Ph, callase activity in anthers and the breakdown of the microsporogenesis. Theoretical and Applied Genetics 41: 104-108.
70. Jack T. 2001. Relearning our ABCs: new twists on an old model. Trends in Plant Science 6: 310-316.
71. Kudlicka K, Brown RM. 1997. Cellulose and callose biosynthesis in higher plants. Plant Physiology 115: 643-656.
72. Lalane E, Twell D. 2002. Genetic control of male germ unit organization in Arabidopsis. Plant Physiology 129: 865-875.
73. de Leeuw JW, Versteegh GJM, van Bergen PF. 2006. Biomacromolecules of algae and plants and their fossil analogues. Plant Ecology 182: 209-233.
74. Longly B, Waterkeyn L. 1979. Etude de la cytocinese. III. Les cloissonments simultanées et successifs des microsporocytes. La Cellule 73: 65-80.
75. Ma H. 2005. Molecular genetic analyses of microsporogenesis and microgametogenesis in flowering plants. Annual Review of Plant Biology 56: 393-434.
76. Magnard JL, Yang M, Chen Y-CS, Leary M, McCormick S. 2001. The Arabidopsis gene tardy asynchronous meiosis is required for the normal pace and synchrony of cell division during male meiosis. Plant Physiology 127: 1157-1166.
77. McCormick S. 1993. Male gametophyte development. Plant Cell 5: 1265-1275.
78. McCormick S. 2004. Control of male gametophyte development. Plant Cell 16: S142-S153.
79. McKenzie A, Heslop-Harrison J, Dickinson HG. 1967. Elimination of ribosomes during meiotic prophase. Nature 215: 997-999.
80. Meuter-Gerhards A, Schwerdtfeger C, Steuernagel S, Wilmemeier S, Wiermann R. 1995. Studies on sporopollenin structure during pollen development. Zeitschrift für Naturforschung C 50: 487-492.
81. Meuter-Gerhards A, Rigert S, Wiermann R. 1999. Studies on sporopollenin biosynthesis in Cucurbita maxima (DUCH.) - II. The involvement of aliphatic metabolism. Journal of Plant Physiology 154: 431-436.
82. Owen HA, Makaroff CA. 1995. Ultrastructure of microsporogenesis and microgametogenesis in Arabidopsis thaliana (L.) Haynh. ecotype Wassilewskija (Brassicaceae). Protoplasma 185: 7-21.
83. Pacini E. 1997. Tapetum Character states: analytical keys for tapetum types and activities. Canadian Journal of Botany 75: 1448-1459.
84. Paxson-Sowders DM, Owen HA, Makaroff CA. 1997. A comparative ultrastructural analysis of exine pattern development in wild-type Arabidopsis and a mutant defective in pattern formation. Protoplasma 198: 53-65.
85. Paxson-Sowders DM, Dodrill CJ, Owen HA, Makaroff CA. 2001. DEX1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis. Plant Physiology 127: 1739-1749.
86. Piffanelli P, Ross JHE, Murphy DJ. 1998. Biogenesis and function of the lipidic structures of pollen grains. Sexual Plant Reproduction 11: 65-80.
87. Pina C, Pinto F, Feijó JA, Becker JD. 2005. Gene family analysis of the Arabidopsis pollen transcriptome reveals biological implications for cell growth, division control and gene expression regulation. Plant Physiology 138: 744-756.
88. Preuss D, Lemieux B, Yen G, Davis RW. 1993. A conditional sterile mutation eliminates surface components from Arabidopsis pollen and disrupts cell signaling during fertilization. Genes and Development 7: 974-985.
89. Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A. 2007. Glossary of pollen and spore terminology. Review of Palaeobotany and Palynology 143: 1-81.
90. Rhee SY, Osborne E, Poindexter PD, Somerville CR. 2003. Microspore separation in the quartet 3 mutants of Arabidopsis is impaired by a defect in a developmentally regulated polygalacturonase required for pollen mother cell wall degradation. Plant Physiology 133: 1170-1180.
91. Rowley JR. 1975. The germinal aperture in pollen. Taxon 24: 17-25.
92. Rowley JR, Dahl AO. 1977. Pollen development in Artemisa vulgaris with special reference to glycoclayx material (1). Pollen et Spores 14: 169-284.
93. Rowley JR, Dunbar A. 1990. Outward extension of spinules in exine of Centrolepis aristata (Centrolepidaceae). Botanica Acta B103: 323-434.
94. Rowley JR, Skvarla JJ. 1975. The glycoclayx and initiation of exine spinules on microspores of Canna. American Journal of Botany 62: 479-485.
95. Rowley JR, Southworth D. 1967. Deposition of sporopollenin on lamellae of unit dimensions. Nature 213: 703-704.
96. Rowley JR, Dahl AO, Rowley JS. 1981a. Substructure in exines of Artemisia vulgaris (Asteraceae). Review of Palaeobotany and Palynology 35: 1-38.
97. Rowley JR, Dahl AO, Sengupta S, Rowley JS. 1981b. A model of exine substructure based on dissection of pollen and spore exines. Palynology 5: 107-152.
98. Rowley JR, Claugher D, Skvarla JJ. 1999. Structure of the exine in Artemisia vulgaris (Asteraceae), a review. Taiwania 44: 1-21.
99. Scott RJ. 1994. Pollen exine - the sporopollenin enigma and the physics of pattern. In: Scott RJ, Stead MA, eds. Society for Experimental Biology Seminar Series 55: molecular and cellular aspects of plant reproduction. Cambridge, UK: Cambridge University Press, 49-81.
100. Scott RJ, Spielman M, Dickinson HG. 2004. Stamen structure and function. Plant Cell 16: S46-S60.
101. Sheldon JM, Dickinson HG. 1983. Determination of patterning in the pollen wall in Lilium henryi. Journal of Cell Science 63: 191-208.
102. Sheldon JM, Dickinson HG. 1986. The relationship between the microtubular cytoskeleton and formation of the pollen wall in Lilium henryi. Planta 168: 11-23.
103. Skvarla JJ, Larson DA. 1966. Fine structure studies of Zea mays pollen. I. Cell membranes and exine ontogeny. American Journal of Botany 53: 1112-1125.
104. Skvarla JJ, Turner BL, Patel VC, Tomb AS. 1977. Pollen morphology in the Compositae and in morphologically related families. In: Heywood VH, Harborne JB, Turner BL, eds. The biology and chemistry of the compositae, Vol. 1. London, UK: Academic Press, 141-248.
105. Southworth D. 1985a. Pollen exine substructure. I. Lilium longiflorum. American Journal of Botany 72: 1274-1283.
106. Southworth D. 1985b. Pollen exine substructure. II. Fagus sylvatica. Grana 24: 161-166.
107. Southworth D. 1986. Substructural organisation of pollen exines. In: Blackmore S, Ferguson IK, eds. Pollen and spores: form and function. London, UK: Academic Press, 61-69.
108. Southworth D, Jernstedt JA. 1995. Pollen exine development precedes microtubule rearrangement in Vigna unguiculata (Fabaceae): a model for pollen wall patterning. Protoplasma 187: 79-87.
109. Spielman M, Preuss D, Li FL, Browne WE, Scott RJ, Dickinson HG. 1997. TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development 124: 2645-2657.
110. Stix E. 1960. Pollenmorphologische Untersuchungen an Compositen. Grana 2: 41-104.
111. Takahashi M. 1986. Pattern determination of the exine in Caesalpinia japonica (Leguminosae: Caesalpinioideae). American Journal of Botany 76: 1615-1626.
112. Takahashi M. 1989. Development of the echinate pollen wall in Farfugium japonicum (Compositae: Senecioneae). Botanical Magazine, Tokyo 102: 219-234.
113. Takahashi M. 1991. Exine pattern formation by plasma membrane in Bougainvillea spectabilis Willd. (Nyctaginaceae). American Journal of Botany 78: 1063-1069.
114. Takahashi M, Kouchi J. 1988. Ontogenetic development of spinous exine in Hibiscus syriacus (Malvaceae). American Journal of Botany 75: 1549-1558.
115. Thompson DA. 1917. On growth and form. Cambridge, UK: Cambridge University Press.
116. Turing A. 1952. The chemical basis of morphogenesis. Philosophical Transactions of the Royal Society of London, Series B 237: 37-72.
117. Twell D, Howden R. 1998. Mechanisms of asymmetric division and cell fate determination in developing pollen. Berlin, Germany: INRA-Springer-Verlag.
118. Waterkeyn L. 1962. Les parois microsporocytaires de nature callosique chez Helleborus et Tradescantia. Cellule 62: 225-255.
119. Waterkeyn L, Bienfait A. 1970. On a possible function of the callosic special cell wall in Ipomoea purpurea (L.) Roth. Grana 10: 13-20.
120. Wilson ZA, Yang CY. 2004. Plant gametogenesis: conservation and contrasts in development. Reproduction 128: 483-492.
121. Wilson ZA, Morroll AM, Dawson J, Swarup R, Tighe PJ. 2001. The Arabidopsis MALE STERILITY1 (MS1) gene is a transcriptional regulator of male gametogenesis, with homology to the PHD-finger family of transcription factors. Plant Journal 28: 27-39.
122. Wodehouse RP. 1935. Pollen grains: their structure, identification and significance in science and medicine. New York, NY, USA: McGraw-Hill Co., Inc.
123. Worall D, Hird DL, Hodge R, Paul W, Draper J, Scott R. 1992. Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco. Plant Cell 4: 759-771.
124. Yamamoto Y, Nishimura M, Hara-Nishimura I, Noguchi T. 2003. Behaviour of vacuoles during microspore and pollen development in Arabidopsis thaliana. Plant and Cell Physiology 44: 1192-1201.
125. Yang C-Y, Spielman M, Coles JP, Li Y, Ghelani S, Bourdon V, Brown RC, Lemmon BE, Scott RJ, Dickinson HG. 2003. TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant Journal 34: 229-240.