Skip to main content
Log in

The Role of Physical Processes in Pollen Wall Morphogenesis: Hypothesis and Experimental Confirmation

  • REVIEWS
  • Published:
Russian Journal of Developmental Biology Aims and scope Submit manuscript

Abstract

The review is devoted to the analysis and generalization of modern knowledge about the mechanisms underlying the ontogeny of the male gametophyte envelope. New and earlier data on exine development аre discussed, and recurrent phases in the development of exine of phylogenetically distant plant species are emphasized. Though exine formation has been shown to be dependent on plenty of genes, the reiteration of exine patterns in different plant species (e.g. columellate, granular, “white-lined” lamellae) suggests that these patterns are based on some non-biological principles of space-filling operations. However, mechanisms involved remained obscure until it became clear that the sequence of structures observed during exine development coincided with the sequence of self-assembling micellar mesophases. It was discovered later that another physical-chemical process—phase separation—participated in exine formation. To confirm that exine-like patterns are capable of generating in vitro by simple physical processes, and their formation does not require regulation at the genome level, some our and other authors’ in vitro experiments were undertaken; the data obtained are discussed. Several series of our new experiments on modeling exine development with mixtures of surface-active substances resulted in some patterns simulating the main types of natural exine. Transmission electron microscopy analysis of the samples has shown that patterns simulating the full range of exine types were obtained by joint action of phase separation and micellar self-assembly. The reconsideration and analysis of our and other authors’ morphogenetic and modeling data revealed that molecular-genetic mechanisms and physical forces work in tandem, with considerable input of physical processes.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1.
Fig. 2.
Fig. 3.
Fig. 4.
Fig. 5.
Fig. 6.
Fig. 7.
Fig. 8.
Fig. 9.
Fig. 10.

REFERENCES

  1. Ariizumi, T., Hatakeyama, K., Hinata, K., Sato, S., Kato, T., Tabata, S., and Toriyama, K., The HKM gene, which is identical to the MS1 gene of Arabidopsis thaliana, is essential for primexine formation and exine pattern formation, Sex Plant Reprod., 2005, vol. 18, pp. 1–7. https://doi.org/10.1007/s00497-005-0242-3

    Article  CAS  Google Scholar 

  2. Ariizumi, T. and Toriyama, K., Genetic regulation on sporopollenin synthesis and pollen exine development, Ann. Rev. Plant. Biol., 2011, vol. 62, pp. 1–24. https://doi.org/10.1146/annurev-arplant-042809-112312

    Article  CAS  Google Scholar 

  3. Ariizumi, T., Hatakeyama, K., Hinata, K., 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., 2004, vol. 39, pp. 170–181. https://doi.org/10.1111/j.1365-313X.2004.02118.x

    Article  CAS  PubMed  Google Scholar 

  4. Ball, P., Designing the Molecular World, Princeton: Princeton Univ. Press, 1994, pp. 216–255.

    Book  Google Scholar 

  5. Benítez, M., An interdisciplinary view on dynamic models for plant genetics and morphogenesis: Scope, examples and emerging research avenues, Front. Plant Sci., 2013, vol. 4, p. 7. https://doi.org/10.3389/fpls.2013.00007

    Article  PubMed  Google Scholar 

  6. Blackmoore, S. and Skvarla, J.J., John Rowley (1926–2010), palynologist extraordinaire, Grana, 2012, vol. 51, no. 2, pp. 77–83. https://doi.org/10.1080/00173134.2012.661454

    Article  Google Scholar 

  7. Blackmore, S., Wortley, A.H., Skvarla, J.J., Gabarayeva, N.I., and Rowley, J.R., Developmental origins of structural diversity in pollen walls of Compositae, Plant Systematics and Evolution, 2010, vol. 284, pp. 17–32. https://doi.org/10.1007/s00606-009-0232-2

    Article  Google Scholar 

  8. Blackmore, S., Wortley, A.H., Skvarla, J.J., and Rowley, J.R., Pollen wall development in flowering plants, New Phytol., 2007, vol. 174, pp. 483–498. https://doi.org/10.1111/j.1469-8137.2007.02060

    Article  CAS  PubMed  Google Scholar 

  9. Bray, D., Model for membrane movements in the neural growth cone, Nature, 1973, vol. 244, pp. 93–96. https://doi.org/10.1038/244093a0

    Article  CAS  PubMed  Google Scholar 

  10. Chaikovsky, J.V., Autopoiesis, Moscow: Soc. Sci. Ed. KMK, 2018.

  11. Coen, E.S. and Meyerowitz, E.M., The war of the whorls: Genetic interactions controlling flower development, Nature, 1991, vol. 353, pp. 31–37. https://doi.org/10.1038/353031a0

    Article  CAS  PubMed  Google Scholar 

  12. Curantz, C. and Manceau, M., Trends and variation in vertebrate patterns as outcomes of self-organization, Curr. Opin. Genet. Dev., 2021, vol. 1 (69), pp. 147–153.

    Article  Google Scholar 

  13. Dickinson, H.G. and Sheldon, J.M., The generation of patterning at the plasma membrane of the young microspore of Lilium, in Pollen and Spores: Form and Function, Blackmore, S. and Ferguson, I.K., Eds., London: Academic Press, 1986, pp. 1–18.

    Google Scholar 

  14. Dobritsa, A.A. and Coerper, D., The novel plant protein INAPERTURATE POLLEN1 marks distinct cellular domains and controls formation of apertures in the Arabidopsis pollen exine, Plant Cell, 2012, vol. 24, pp. 4452–4464. https://doi.org/10.1105/tpc.112.101220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Dobritsa, A.A., Geanconteri, A., Shrestha, J., Carlson, A., Kooyers, N., Coerper, D., Urbanczyk-Wochniak, E., Bench, B.J., Sumner, L.W., Swanson, R., and Preuss, D., A Large-scale genetic screen in Arabidopsis to identify genes involved in pollen exine production, Plant Physiol. (Lancaster), 2011, vol. 157, pp. 947–970. https://doi.org/10.1104/pp.111.179523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Dong, X.Y., Hong, Z.L., Sivaramakrichnan, M., Mahfouz, M., and Verma, M.P.S., Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis, Plant J., 2005, vol. 42, pp. 315–328. https://doi.org/10.1111/j.1365-313X.2005.02379.x

    Article  CAS  PubMed  Google Scholar 

  17. Fridrichsberg, D.A., Colloidal Chemistry, St. Petersburg: Khimiya, 1995.

    Google Scholar 

  18. Gabarayeva, N.I., Hypothetical ways of exine structure determination, Bot. Zh., 1990, vol. 75, pp. 1353–1362.

    Google Scholar 

  19. Gabarayeva, N.I., Hypothetical ways of exine pattern determination, Grana, 1993, vol. 33, pp. 54–59. https://doi.org/10.1080/00173139309428980

    Article  Google Scholar 

  20. Gabarayeva, N.I. and El-Ghazaly, G., Sporoderm development in Nymphaea mexicana (Nymphaeaceae), Plant Syst. Evol., 1997, vol. 204, pp. 1–19. https:// www.jstor.org/stable/23642922.

    Article  Google Scholar 

  21. Gabarayeva, N.I. and Grigorjeva, V.V., Exine development in Stangeria eriopus (Stangeriaceae): ultrastructure and substructure, sporopollenin accumulation, the equivocal character of the aperture, and stereology of microspore organelles, Rev. Palaeobot. Palynol., 2002, vol. 122, pp. 185–218. https://doi.org/10.1016/S0034-6667(02)00183-5

    Article  Google Scholar 

  22. Gabarayeva, N.I. and Grigorjeva, V.V., Exine development in Encephalartos altensteinii (Cycadaceae): ultrastructure, substructure and the modes of sporopollenin accumulation, Rev. Palaeobot. Palynol., 2004, vol. 132, pp. 175–193. https://doi.org/10.1016/j.revpalbo.2004.05.005

    Article  Google Scholar 

  23. Gabarayeva, N.I. and Grigorjeva, V.V., Sporoderm ontogeny in Chamaedorea microspadix (Arecaceae). Self-assembly as the underlying cause of development, Grana, 2010, vol. 49, pp. 91–114.

    Article  Google Scholar 

  24. Gabarayeva, N.I. and Grigorjeva, V.V., Sporoderm development in Swida alba (Cornaceae), interpreted as a self-assembling colloidal system, Grana, 2011, vol. 50, pp. 81–101.

    Article  Google Scholar 

  25. Gabarayeva, N. and Grigorjeva, V., Sporoderm development and substructure in Magnolia sieboldii and other Magnoliaceae: An interpretation, Grana, 2012, vol. 51, pp. 119–147.

    Article  Google Scholar 

  26. Gabarayeva, N. and Grigorjeva, V., Sporoderm and tapetum development in Eupomatia laurina (Eupomatiaceae). An interpretation, Protoplasma, 2014b, vol. 251, pp. 1321–1345. https://doi.org/10.1007/s00709-014-0631-2

    Article  PubMed  Google Scholar 

  27. Gabarayeva, N. and Grigorjeva, V., Simulation of exine patterns by self-assembly, Plant Syst. Evol., 2016, vol. 302, pp. 1135–1156. https://doi.org/10.1007/s00606-016-1322-6

    Article  Google Scholar 

  28. Gabarayeva, N.I. and Grigorjeva, V.V., An integral insight into pollen wall development: Involvement of physical processes in exine ontogeny in Calycanthus floridus L., with an experimental approach, Plant J., 2021, vol. 105, pp. 736–753. https://doi.org/10.1111/tpj.15070

    Article  CAS  PubMed  Google Scholar 

  29. Gabarayeva, N.I. and Hemsley, A.R., Merging concepts: The role of self-assembly in the development of pollen wall structure, Rev. Palaeobot. Palynol., 2006, vol. 138, pp. 121–139. https://doi.org/10.1016/j.revpalbo.2005.12.001

    Article  Google Scholar 

  30. Gabarayeva, N.I., Grigorjeva, V.V., Rowley, J.R., and Hemsley, A.R., Sporoderm development in Trevesia burckii (Araliaceae). I. Tetrad period: Further evidence for the participation of self-assembly processes, Rev. Paleobot. Palynol., 2009, vol. 156, nos. 1–2, pp. 211–232. https://doi.org/10.1016/j.revpalbo.2008.12.001

    Article  Google Scholar 

  31. Gabarayeva, N.I., Grigorjeva, V.V., and Rowley, J.R., A new look at sporoderm ontogeny in Persea americana. Micelles and the hidden side of development, Ann. Bot., 2010, vol. 105, pp. 939–955. https://doi.org/10.1093/aob/mcq075

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Gabarayeva, N.I., Grigorjeva, V.V., and Rowley, J.R., Sporoderm development in Acer tataricum (Aceraceae). An interpretation, Protoplasma, 2010a, vol. 247, pp. 65–81. https://doi.org/10.1007/s00709-010-0141-9

    Article  PubMed  Google Scholar 

  33. Gabarayeva, N.I., Grigorjeva, V.V., and Polevova, S.V., Exine and tapetum development in Symphytum officinale (Boraginaceae). Exine substructure and its interpretation, Plant Sys. Evol., 2011, vol. 296, pp. 101–120.

    Article  Google Scholar 

  34. Gabarayeva, N.I., Grigorjeva, V.V., and Kosenko, Y.V., Primexine development in Passiflora racemosa Brot. Overlooked aspects of development, Plant Syst. Evol., 2013, vol. 299, pp. 1013–1035.

    Article  CAS  Google Scholar 

  35. Gabarayeva, N., Grigorjeva, V., Polevova, S., and Hemsley, A.R., Pollen wall and tapetum development in Plantago major L. (Plantaginaceae): Assisting self-assembly, Grana, 2016, vol. 56, no. 2, pp. 81–111. https://doi.org/10.1080/00173134.2016.1159729

    Article  Google Scholar 

  36. Gabarayeva, N.I., Polevova, S.V., Grigorjeva, V.V., and Blackmore, S., Assembling the thickest plant cell wall: Exine development in Echinops (Asteraceae, Cynareae), Planta, 2018, vol. 248, pp. 323–346. https://doi.org/10.1007/s00425-018-2902-1

    Article  CAS  PubMed  Google Scholar 

  37. Gabarayeva, N.I., Grigorjeva, V.V., and Shavarda, A.L., Mimicking pollen and spore walls: self-assembly in action, Ann. Bot., 2019, vol. 123, pp. 1205–1218. https://doi.org/10.1093/aob/mcz027

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Gabarayeva, N.I., Grigorjeva, V.V., and Lavrentovich, M.O., Artificial pollen walls simulated by the tandem processes of phase separation and self-assembly in vitro, New Phytol., 2020. https://doi.org/10.1111/nph.16318

  39. Gabarayeva, N.I., Polevova, S.V., Grigorjeva, V.V., and Hiscock, S.J., Underlying mechanisms of development: pollen wall ontogeny in Chloranthus japonicus and a reconsideration of pollen ontogeny in early-diverging lineages of angiosperms, Bot. J. Linn. Soc., 2021, vol. 20, pp. 1–21.

    Google Scholar 

  40. Gerasimova-Navashina, E.N., Physico-chemical nature of primexine formation of angiosperm pollen grains, in Embryology of Angiosperms, Kovarski, A., Ed., Kishinev: Ştiinţǎ, 1973, pp. 57–70.

  41. Gingell, D., Membrane permeability change by aggregation of mobile glycoprotein units, J. Theor. Biol., 1973, vol. 38, pp. 677–679.

    Article  CAS  PubMed  Google Scholar 

  42. Grienenberger, E., Kim, S.S., Lallemand, B., Geoffroy, P., Heintz, D., Souza, C. de A., Heitz, T., Douglas, C.J., and Legrand, M., Analysis of TETRAKETIDE α-PYRONE REDUCTASE function in Arabidopsis thaliana reveals a previously unknown, but conserved, biochemical pathway in sporopollenin monomer biosynthesis, Plant Cell, 2010, vol. 22, pp. 4067–4083. https://doi.org/10.1105/tpc.110.080036

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Grigorjeva, V. and Gabarayeva, N., The development of sporoderm, tapetum and Ubisch bodies in Dianthus deltoides (Caryophyllaceae): Self-assembly in action, Rev. Palaeobot. Palynol., 2015, vol. 219, pp. 1–27. https://doi.org/10.1016/j.revpalbo.2015.03.005

    Article  Google Scholar 

  44. Grigorjeva, V.V. and Gabarayeva, N., Pollen wall ontogeny in Polemonium caeruleum (Polemoniaceae) and suggested underlying mechanisms of development, Protoplasma, 2018, vol. 255, pp. 109–128. https://doi.org/10.1007/s00709-017-1121-0

    Article  PubMed  Google Scholar 

  45. Grigorjeva, V.V., Polevova, S.V., and Gabarayeva, N.I., Pollen wall development in Hydrangea bretschneiderii Dippel. (Hydrangeaceae): Advanced interpretation through physical input, with in vitro experimental verification, Protoplasma, 2021. https://doi.org/10.1007/s00709-020-01571-4

  46. Gubatz, S., Herminghaus, S., Meurer, B., Strack, D., and Wiermann, R., The location of hydroxycinnamic acid amides in the exine of Corylus pollen, Pollen and Spores, 1986, vol. 28, pp. 347–354.

    Google Scholar 

  47. Gunning, B.E.S. and Steer, M.W., Plant Cell Biology. An Ultrastructural Approach, Dublin: University College, 1986.

    Google Scholar 

  48. Hamley, I., Introduction to Soft Matter. Polymers, Colloids, Amphiphiles and Liquid Crystals, Chichester: John Wiley and Sons, 2000.

    Google Scholar 

  49. Hemsley, A.R., Nonlinear variation in simulated complex pattern development, J. Theor. Biol., 1998, vol. 192, pp. 73–79.

    Article  CAS  PubMed  Google Scholar 

  50. Hemsley, A.R., Collinson, M.E., and Brain, A.P.R., Colloidal crystal-like structure of sporopollenin in the megaspore walls of recent Selaginella and similar fossil spores, Bot. J. Linn. Soc., 1992, vol. 108, pp. 307–320.

    Article  Google Scholar 

  51. Hemsley, A.R., and Gabarayeva, N.I., Exine development: The importance of looking through a colloid chemistry “window,” Plant Syst. Evol., 2007, vol. 263, pp. 25–49.

    Article  Google Scholar 

  52. Hemsley, A.R., Lewis, J., and Griffiths, P.C., Soft and sticky development: Some underlying reasons for microarchitectural pattern convergence, Rev. Pal. Pal., 2004, vol. 130, pp. 105–119.

    Article  Google Scholar 

  53. Hemsley, A.R., Scott, A.C., Barrie, P.J., and Chaloner, W.G., Studies of fossil and modern spore wall biomacromolecules using 13C solid state NMR, Ann Bot., 1996, vol. 78, pp. 83–94.

    Article  Google Scholar 

  54. Herminghaus, S., Gubatz, S., Arendt, S., and Wiermann, R., The occurrence of phenols as degradation products of natural sporopollenin—a comparison with “synthetic sporopollenin,” Zeit für Nat., 1988, vol. 43, pp. 491–500.

    CAS  Google Scholar 

  55. Heslop-Harrison, J., Pattern in plant cell walls: morphogenesis in miniature, Proc. R. Inst. GB, 1972, vol. 45, pp. 335–351.

    Google Scholar 

  56. Hu, J., Wang, Z., Zhang, L., and Sun, M.X., The Arabidopsis Exine Formation Defect (EFD) gene is required for primexine patterning and is critical for pollen fertility, New Phytol., 2014, vol. 203, pp. 140–154. https://doi.org/10.1111/nph.12788

    Article  CAS  PubMed  Google Scholar 

  57. Ingber, D., Cellular tensegrity: Defining new rules of biological design that govern the cytoskeleton, J. Cell Sci., 1993, vol. 104, pp. 613–627. https://doi.org/10.1242/jcs.104.3.613

    Article  PubMed  Google Scholar 

  58. Ingber, D.E., Tensegrity I. Cell structure and hierarchical systems biology, J. Cell Sci., 2003a, vol. 116, pp. 1157–1173. https://doi.org/10.1242/jcs.00359

    Article  CAS  PubMed  Google Scholar 

  59. Ingber, D.E., Tensegrity II. How structural networks influence cellular information processing networks, J. Cell Sci., 2003b, vol. 116, pp. 1397–1408. https://doi.org/10.1242/jcs.00360

    Article  CAS  PubMed  Google Scholar 

  60. Ingber, D.E. and Jamieson, J.D., Cells as tensegrity structures: Architectural regulation of histodifferentiation by physical forces transduced over basement membrane, in Gene Expression during Normal and Malignant Differentiation, Andersson, L.C., Gahmberg, C.G., and Ekblom, P., Eds., Orlando, FL: Academic Press, 1985, pp. 13–32.

    Google Scholar 

  61. Jia, Q.S., Zhu, J., Xu, X.F., Lou, Y., Zhang, Z.L., Zhang, Z.P., and Yang, Z.N., Arabidopsis AT-hook protein TEK positively regulates the expression of arabinogalactan proteins for nexine formation, Mol. Plant, 2015, vol. 8, pp. 251–260. https://doi.org/10.1016/j.molp.2014.10.001

    Article  CAS  PubMed  Google Scholar 

  62. Kadzik R.S., Homa K.E., and Kovar, D.R., F-actin cytoskeleton network self-organization through competition and cooperation, Ann. Rev. Cell Devel. Biol., 2020, vol. 6, no. 36, pp. 35–60.

    Article  Google Scholar 

  63. Kanaoka, M.M., Shimizu, K.K., Xie, B., Urban, S., Freeman, M., Hong, Z., and Okada, K., KOMPEITO, an atypical Arabidopsis rhomboid-related gene, is required for callose accumulation and pollen wall development, Int. J. Mol. Sci., 2022, vol. 23, p. 5959. https://doi.org/10.3390/ijms23115959

    Article  CAS  PubMed  Google Scholar 

  64. Kauffman, S.A., The Origin of Order, Oxford: Oxford University Press, 1993.

    Book  Google Scholar 

  65. Kim, M.J., Kim, M., Kee, M.R., Park, S.K., and Kim, J., Lateral Organ Boundaries Domain (LDB) 10 interacts with SIDECAR POLLEN/LBD27 to control pollen development in Arabidopsis, Plant J., 2015, vol. 81, pp. 794–809. https://doi.org/10.1111/tpj.12767

    Article  CAS  PubMed  Google Scholar 

  66. Kurakin, A., Self-organization versus watchmaker: stochastic dynamics of cellular organization, Biol. Chem., 2005, vol. 386, pp. 247–254.

    Article  CAS  PubMed  Google Scholar 

  67. Lavrentovich, M.O., Horsley, E.M., Radja, A., Sweeney, A.M., and Kamien, R.D., First-order patterning transitions on a sphere as a route to cell morphology, Proc. Natl. Acad. Sci. USA, 2016, vol. 113, pp. 5189–5194. https://doi.org/10.1073/pnas.1600296113

    Article  CAS  PubMed  Google Scholar 

  68. Lecuit, T., “Developmental mechanics”: cellular patterns controlled by adhesion, cortical tension and cell division, HFSP J., 2008, vol. 2, pp. 72–78. https://doi.org/10.2976/1.2896332

    Article  PubMed  Google Scholar 

  69. Lecuit, T. and Lenne, P.F., Cell surface mechanics and the control of cell shape, tissue patterns and morphogenesis, Mol. Cell Biol., 2007, vol. 8, pp. 633–644.

    CAS  Google Scholar 

  70. Lehmann, O., Flüssige Kristalle, sowie Plastizität von Kristallen im Allgemeinen, molekulare Umlagerungen und Aggregatzustandsänderungen, Leipzig: Engelmann, 1904.

    Google Scholar 

  71. Leibler, S. and Andelman, D., Ordered and curved meso-structures in membranes and amphiphilic films, J. Phys. (Paris), 1987, vol. 48, pp. 2013–2018. https://doi.org/10.1051/jphys:0198700480110201300

    Article  CAS  Google Scholar 

  72. Li, F.S., Phyo, P., Jacobowitz, J., Hong, M., and Weng, J.K., The molecular structure of plant sporopollenin, Nat. Plants, 2019, vol. 5, pp. 41–46. https://doi.org/10.1038/s41477-018-0330-7

    Article  CAS  PubMed  Google Scholar 

  73. Li, J., Yu, M., Geng, L.L., and Zhao, J., The fasciclin-like arabinogalactan protein gene, FLA3, is involved in microspore development of Arabidopsis, Plant J., 2010, vol. 64, pp. 482–497. https://doi.org/10.1111/j.1365-313X.2010.04344.x

    Article  CAS  PubMed  Google Scholar 

  74. Li, W., Liu, Y., and Douglas, C., Role of glycosyltransferases in pollen wall primexine formation and exine patterning, Plant Physiol., 2017, vol. 173, pp. 167–182. https://doi.org/10.1104/pp.16.00471

    Article  CAS  PubMed  Google Scholar 

  75. Lintilhac, P.M., The problem of morphogenesis: unscripted biophysical control systems in plants, Protoplasma, 2014, vol. 251, pp. 25–36.

    Article  CAS  PubMed  Google Scholar 

  76. Liu, L. and Wang, T., Male gametophyte development in flowering plants: A story of quarantine and sacrifice, J. Plant Physiol., 2021, vols. 258–259, p. 153365. https://doi.org/10.1016/j.jplph.2021.153365

    Article  CAS  PubMed  Google Scholar 

  77. Lou, Y., Xu, X.F., Zhu, J., Gu, J.N., Blackmore, S., and Yang, Z.N., The tapetal AHL family protein TEK determines nexine formation in the pollen wall, Nat. Commun., 2014, vol. 5, p. 3855. https://doi.org/10.1038/ncomms4855

    Article  CAS  PubMed  Google Scholar 

  78. Mandelbrot, B.B., The Fractal Geometry of Nature, San Francisco: WH Freeman and Co., 1982.

    Google Scholar 

  79. Meyen, S.V., Basic features of gymnosperm systematics and phylogeny as evidenced by the fossil record, Bot. Rev., 1984, vol. 50, p. 1. https://doi.org/10.1007/BF02874305

    Article  Google Scholar 

  80. Mi, L., Mo, A., Yang, J., Liu, H., Ren, D., Chen, W., Long, H., Jiang, N., Zhang, T., and Lu, P., Arabdopsis novel microgametophyte defective mutant 1 is required for pollen viability via influencing intine development in Arabidopsis. Front. Plant Sci., 2022, vol. 13.

  81. Moore, S.E.M., Gabarayeva, N., and Hemsley, A.R., Morphological, developmental and ultrastructural comparison of Osmunda regalis L. spores with spore mimics, Rev. Paleobot. Palynol., 2009, vol. 156, pp. 177–184.

    Article  Google Scholar 

  82. Neto, A. and Salinas, S., The Physics of Lyotropic Liquid Crystals: Phase Transitions and Structural Properties, Oxford: Oxford Science Publications, 2005.

    Book  Google Scholar 

  83. Nishikawa, S., Zinkl, G.M., Swanson, R.J., Maruyama, D., and Preuss, D., Callose (β-1,3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth, BMC Plant Biol., 2005, vol. 5, pp. 22–30. https://doi.org/10.1186/1471-2229-5-22

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Padmanaban, S., Czerny, D.D., Levin, K.A., Leydon, A.R., Su, R.T., Maugel, T.K., Zou, Y., Chanroj, S., Cheung, A.Y., Johnson, M.A., and Sze, H., Transporters involved in pH and K+ homeostasis affect pollen wall formation, male fertility, and embryo development, J. Exp. Bot., 2017, vol. 68, pp. 3165–3178. https://doi.org/10.1093/jxb/erw483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Paxson-Sowders, D.M., Dodrill, C.H., Owen, H.A., and Makaroff, C.A., Dex1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis, Plant Physiol., 2001, vol. 127, pp. 1739–1749. https://doi.org/10.1104/pp.010517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Paxson-Sowders, D.M., Owen, H.A., and Makaroff, C.A., A comparative ultrastructural analysis of exine pattern development in wild-type Arabidopsis and a mutant defective in pattern formation, Protoplasma, 1997, vol. 198, pp. 53–65.

    Article  Google Scholar 

  87. Pettitt, J.M., Ultrastructure and cytochemistry of spore wall morphogenesis, in The Experimental Biology of Ferns, Dyer, A.F., Ed., London: Academic Press, 1979, pp. 211–252.

    Google Scholar 

  88. Pettitt, J.M. and Jermy, A.C., The surface coats on spores, Biol. J. Linn. Soc., 1974, vol. 6, pp. 245–257.

    Article  Google Scholar 

  89. Plourde, S.M., Amom, P., Tan, M., Dawes, A.T., and Dobritsa, A.A., Changes in morphogen kinetics and pollen grain size are potential mechanisms of aberrant pollen aperture patterning in previously observed and novel mutants of Arabidopsis thaliana, PLoS Comput. Biol., 2019, vol. 15, p. e1006800. https://doi.org/10.1371/journal.pcbi.1006800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Polevova, S.V., Grigorjeva, V.V., and Gabarayeva, N.I., Pollen wall and tapetal development in Cymbalaria muralis: The role of physical processes, evidenced by in vitro modeling, Protoplasma, 2019, vol. 260, pp. 281–298. https://doi.org/10.1007/s00709-022-01777-8

    Article  Google Scholar 

  91. Pozhidaev, A.E., Polymorphism of pollen in the genus Acer (Aceraceae). Isomorphism of deviant forms of Angiosperm pollen, Grana, 1993, vol. 32, pp. 79–85. https://doi.org/10.1080/00173139309429457

    Article  Google Scholar 

  92. Pozhidaev, A.E., Pollen morphology of the genus Aesculus (Hippocastanaceae). Patterns in the variety of morphological characteristics, Grana, 1995, vol. 34, pp. 10–20. https://doi.org/10.1080/00173139509429028

    Article  Google Scholar 

  93. Pozhidaev, A.E., Hypothetical way of pollen aperture patterning. 1. Formation of 3-colpate patterns and endoaperture geometry, Rev. Palaeobot. Palynol., 1998, vol. 104, pp. 67–83.

    Article  Google Scholar 

  94. Pozhidaev, A.E., Hypothetical way of pollen aperture patterning. 2. Formation of polycolpate patterns and pseudoaperture geometry, Rev. Palaeobot. Palynol., 2000, vol. 109, pp. 235–254.

    Article  CAS  PubMed  Google Scholar 

  95. Pozhidaev, A.E., Hypothetical way of pollen aperture patterning. 3. A family-based study of Krameriaceae, Rev. Palaeobot. Palynol., 2002, vol. 127, pp. 1–23.

    Google Scholar 

  96. Pozhidaev, A.E. and Petrova, N.V., Structure of variability of palynomorphological features within and beyond the genus Galeopsis L. Hjl. (Lamiaceae) in the context of divergent morphological evolution, Biol. Bull. Rev., 2023, vol. 13, pp. 63–80. https://doi.org/10.1134/S2079086423010061

    Article  Google Scholar 

  97. Quilichini, T.D., Grienenberger, E., and Douglas, C.J., The biosynthesis, composition and assembly of the outer pollen wall: A tough case to crack, Phytochemistry, 2015, vol. 113, pp. 170–182. https://doi.org/10.1016/j.phytochem.2014.05.002

    Article  CAS  PubMed  Google Scholar 

  98. Radja, A., Pollen wall patterns as a model for biological self-assembly, J. Exp. Zool. Part B: Mol. Dev. Evol., 2020, vol. 336, no. 8, pp. 629–641. https://doi.org/10.1002/jez.b.23005

    Article  Google Scholar 

  99. Radja, A., Horsley, E.M., Lavrentovich, M.O., and Sweeney, A.M., Pollen patterns form from modulated phases, Cell, 2019, vol. 176, pp. 856–868. https://doi.org/10.1016/j.cell.2019.01.014

    Article  CAS  PubMed  Google Scholar 

  100. Regier, J.C. and Hatzopoulos, A.K., Evolution in steps: The role of regulatory alterations in the diversification of the moth chorion morphogenetic pathway, in Self-Assembling Architecture, Varner, J.E., Ed., New York: Alan R. Liss, 1988, pp. 179–202.

    Google Scholar 

  101. Reinitzer, F., Zur Kenntnis des Cholesterins, Monatshefte, 1888, vol. 9, pp. 421–441.

    Article  Google Scholar 

  102. Rowley, J.R., Implications on the nature of sporopollenin based upon pollen development, in Sporopollenin, Brooks, J., Grant, P.R., Muir, M.D., van Gijzel, P., and Shaw, G., Eds., London: Academic Press, 1971, pp. 174–218.

    Google Scholar 

  103. Rowley, J.R., Formation of pollen exine bacules and microchannels on a glycocalyx, Grana, 1973, vol. 13, pp. 129–138.

    Article  Google Scholar 

  104. Rowley, J.R., Lipopolysaccharide embedded within the exine of pollen grains, in 33rd Ann. Proc. Electron Microscopy Soc. Am., Las Vegas, Bailey, G.W., Ed., 1975, pp. 572–573.

  105. Rowley, J.R. and Dahl, A.O., Pollen development in Artemisia vulgaris with special reference to glycocalyx material, Pollen Spores, 1977, vol. 19, pp. 169–284.

    Google Scholar 

  106. Schweisguth, F. and Corson, F., Self-organization in pattern formation, Dev. Cell, 2019, vol. 49, no. 5, pp. 659–677.

    Article  CAS  PubMed  Google Scholar 

  107. Scott, R.J., Pollen exine—the sporopollenin enigma and the physics of pattern, in Molecular and Cellular Aspects of Plant Reproduction, Society for Experimental Biology Seminar Series 55, Scott, R.J. and Stead, M.A., Eds., Cambridge Univ. Press, 1994, pp. 49–81.

  108. Shapiro, B.E., Tobin, C., Mjolsness, E., and Meyerowitz, E.M., Analysis of cell division patterns in the Arabidopisis shoot apical meristem, PNAS, 2015, vol. 112, pp. 4815–4820. https://doi.org/10.1073/pnas.1502588112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Sheldon, J.M. and Dickinson, H.G., Determination of patterning in the pollen wall of Lilium henryi, J. Cell Sci., 1983, vol. 63, pp. 191–208.

    Article  CAS  PubMed  Google Scholar 

  110. Shellard, A. and Mayor, R., Sculpting with stiffness: Rigidity as a regulator of morphogenesis, Biochemical Society Transactions, 2023, BST20220826.

  111. Shi, J., Cui, M., Yang, L., Lim, Y.J., and Zhang, D., Genetic and biochemical mechanisms of pollen wall development, Trends Plant Sci., 2015, vol. 20, pp. 741–753. https://doi.org/10.1016/j.tplants.2015.07.01

    Article  CAS  PubMed  Google Scholar 

  112. Sitte, P., Role of lipid self-assembly in subcellular morphogenesis, in Cytomorphogenesis in Plants, Kiermayer, O., Ed., Cell Biology Monographs 8, Wien: Springer, 1981, pp. 401–421. https://doi.org/10.1007/978-3-7091-8602-2_15

  113. Skriven, L.E., Equilibrium bicontinuous structures, in Micellization, Solubilization, and Microemulsions 1, 2, Mittal, K.L., Ed., New York: Plenum Press, 1977, pp. 548–567.

    Google Scholar 

  114. Stillman, N.R. and Mayor, R., Generative models of morphogenesis in developmental biology, Seminars in Cell and Developmental Biology, 2023, vol. 147, pp. 83–90.

    Article  CAS  PubMed  Google Scholar 

  115. Suzuki, T., Narciso, J., Zeng, W., van de Meene, A., Yasutomi, M., Takemura, S., Lampugnani, E., Doblin, M., Bacic, A., and Ishiguro, S., KNS4/UPEX1: A type II arabinogalactan β(1,3)-galactosyltransferase required for pollen exine development, Plant Physiol., 2017, vol. 173, pp. 183–205. https://doi.org/10.1104/pp.16.01385

    Article  CAS  PubMed  Google Scholar 

  116. Tan, W., Cheng, S., Li, Y., et al., Phase separation modulates the assembly and dynamics of a polarity related scaffold-signaling hub, Nat. Commun., 2022, vol. 13, p. 7181. https://doi.org/10.1038/s41467-022-35000-2

    Article  CAS  PubMed  Google Scholar 

  117. Taylor, M., Cooper, R.L., Schneider, E.L., and Osborn, J.M., Pollen structure and development in Nymphaeales: Insights into character evolution in an ancient angiosperm lineage, Am. J. Bot., 2015, vol. 102, pp. 1–18. https://doi.org/10.3732/ajb.1500249

    Article  Google Scholar 

  118. Taylor, M.L., Altrichter, K.M., and Aeilts, L.B., Pollen ontogeny in Ruppia (Alismatidae), Int. J. Plant Sci., 2018, vol. 179, pp. 217–230. https://doi.org/10.1086/696535

    Article  Google Scholar 

  119. Taylor, M.L., Hudson, P.J., Rigg, J.M., Strandquist, J.N., Green, J.S., Thiemann, T.C., and Osborn, J.M., Pollen ontogeny in Victoria (Nymphaeales), Int. J. Plant Sci., 2013, vol. 174, pp. 1259–1276. https://doi.org/10.1086/673246

    Article  Google Scholar 

  120. Thompson, D.A., On Growth and Form, Cambridge: Cambridge University Press, 1917.

    Book  Google Scholar 

  121. van Bergen, P.F., Blokker, P., Collinson, M.E., Sinninghe Damsté, J.S., and de Leeuw, J.W., Structural biomacromolecules in plants: What can be learnt from the fossil record?, in The Evolution of Plant Physiology, Hemsley, A.R. and Poole, I., Eds., Amsterdam: Academic Press, 2004, pp. 134–154. https://doi.org/10.1016/B978-012339552-8/50009-3

    Book  Google Scholar 

  122. Van Uffelen, G.A., The control of spore wall formation, in Pollen and Spores: Patterns of Diversification, Blackmore, S. and Barnes, S.H., Eds., Oxford: Clarendon Press, 1991, pp. 89–102.

    Google Scholar 

  123. Vignaud, T., Blanchoin, L., and Théry, M., Directed cytoskeleton self-organization, Trends in Cell Biology, 2012, vol. 22, no. 12, pp. 671–682.

    Article  CAS  PubMed  Google Scholar 

  124. Wallace, S., Fleming, A., Wellman, Ch.H., and Beerling, D.J., Evolutionary development of the plant spore and pollen wall, AoB Plants, 2011, vol. 2011, plr027. https://doi.org/10.1093/aobpla/plr027

    Article  PubMed  PubMed Central  Google Scholar 

  125. Wang, R. and Dobritsa, A., Exine and aperture patterns on the pollen surface: Their formation and roles in plant reproduction, Ann. Plant Rev., 2018, vol. 1, pp. 1–40. https://doi.org/10.1002/9781119312994.apr0625

    Article  Google Scholar 

  126. Wang, R. and Dobritsa, A., Loss of THIN EXINE2 disrupts multiple processes in the mechanism of pollen exine formation, Plant Physiol., 2021, vol. 187, pp. 133–157. https://doi.org/10.1093/plphys/kiab244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Wang, R., Owen, H.A., and Dobritsa, A.A., Dynamic changes in primexine during the tetrad stage of pollen development, Plant Physiol., 2021, kiab426. https://doi.org/10.1093/plphys/kiab426

  128. Weber, M., The formation of pollenkitt in Apium nodiflorum (Apiaceae), Ann. Bot., 1992, vol. 70, pp. 573–577. https://doi.org/10.1093/oxfordjournals.aob.a088519

    Article  Google Scholar 

  129. Wiermann, R., Ahlers, F., and Schmitz-Thom, I., Sporopollenin, in Biopolymers—Lignin, Humic Substances and Coal, Hofrichter, M. and Steinbüchel, A., Eds., Weinheim: Wiley-VCH, 2001, vol. 1, pp. 209–227.

    Google Scholar 

  130. Wiermann, R. and Gubatz, S., Pollen wall and sporopollenin, Int. Rev. Cytol., 1992, vol. 140, pp. 35–72.

    Article  CAS  Google Scholar 

  131. Wilmesmeier, S. and Wiermann, R., Influence of EPTC (S-ethyl-dipropyl-thiocarbamate) on the composition of surface waxes and sporopollenin structure in Zea mays, J. PlNT Physiol., 1995, vol. 146, pp. 22–28.

    Article  CAS  Google Scholar 

  132. Wilmesmeier, S. and Wiermann, R., Immunocytochemical localization of phenolic compounds in pollen walls using antibodies against p-coumaric acid coupled to bovine serum albumin, Protoplasma, 1997, vol. 197, pp. 148–159.

    Article  Google Scholar 

  133. Wodehouse, R.P., Pollen Grains: Their Structure, Identification and Significance in Science and Medicine, New York: McGraw-Hill, 1935.

    Google Scholar 

  134. Xiong, S.-X., Zeng, Q.-Y., Hou, J.-Q., Hou, L.-L., Zhu, J., Yang, M., Yang, Z.-N., and Lou, Y., The temporal regulation of TEK contributes to pollen wall exine patterning, PLoS Genet., 2020, vol. 16, no. 5, p. e1008807. https://doi.org/10.1371/journal.pgen.1008807

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  135. Xu, M., Yan, X., Wang, Y., Liu, Ch., Yang, Q., Tian, D., Bednarek, S.Y., Pan, J., and Wang, J., ADAPTOR PROTEIN-1 complex-mediated post-Golgi trafficking is critical for pollen wall development in Arabidopsis, New Phytol., 2022, vol. 235, pp. 472–487. https://doi.org/10.1111/nph.18170

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Zhang, Z.B., Zhu, J., Gao, J.F., Wang, C., Li, H., Li, H., Zhang, H.Q., Zhang, S., Wang, D.M., Wang, Q.X., Huang, H., Xia, H.J., and Yang, Z.N., Transcription factor AtMYB103 is required for anther development by regulating tapetum development, callose dissolution and exine formation in Arabidopsis, Plant J., 2007, vol. 52, pp. 528–538. https://doi.org/10.1111/j.1365-313X.2007.03254.x

    Article  CAS  PubMed  Google Scholar 

Download references

ACKNOWLEDGMENTS

I thank all my coauthors of the previously published papers, cited here: S. Blackmore, G. El-Ghazaly, V.V. Grigorjeva, A.R. Hemsley, Y. Kosenko, M.O. Lavrentovich, S.E.M. Moore, S. Polevova, J.R. Rowley and A.L. Shavarda. Special thanks are to S. Blackmore for many suggestions and English checking. I thank my anonymous reviewers for their undertaken labor on reading the manuscript and for important comments.

Funding

This work was supported by a grant to Nina Gabarayeva from the Russian Foundation for Basic Research no. 20-04-00174 and conducted using the equipment of the Core Facility “Cellular and Molecular Technologies in Plant Science” of the Komarov Botanical Institute (St. Petersburg).

Author information

Authors and Affiliations

Authors

Contributions

The author of this this paper has written this review, invented and did the modelling experiment, described in this paper, synthesized simulations and conducted ultrastructural study with TEM. The author summarized all the data and prepared the text for submission.

Corresponding author

Correspondence to N. I. Gabarayeva.

Ethics declarations

ETHICS APPROVAL AND CONSENT TO PARTICIPATE

In the course of this work people and animals were not the objects.

CONFLICT OF INTEREST

As author of this work, I declare that I have no conflicts of interest.

Additional information

Publisher’s Note.

Pleiades Publishing remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Gabarayeva, N.I. The Role of Physical Processes in Pollen Wall Morphogenesis: Hypothesis and Experimental Confirmation. Russ J Dev Biol 54, 255–275 (2023). https://doi.org/10.1134/S1062360423050053

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1062360423050053

Keywords:

Navigation