Sporogenesis in Bryophytes: Patterns and Diversity in Meiosis

Botanical Review

Volumn 79, Issue 2, 2013, Pages 178-280

  Brown, Roy C ^a   Lemmon, Betty E ^a  

^a UNIVERSITY OF LOUISIANA AT LAFAYETTE   (United States)

Author keywords

Cell division; Meiosis; Microtubules; Mitosis; MTOC; QMS; Quadripolarity

Indexed keywords

ALGAE; ANTHOCEROTOPHYTA; BACTERIA (MICROORGANISMS); BLASIA; BRYOPHYTA; BRYOPHYTES; EMBRYOPHYTA; JUNGERMANNIOPSIDA; MARCHANTIOPHYTA; MARCHANTIOPSIDA; SPERMATOPHYTA;

EID: 84878112940     PISSN: 00068101     EISSN: None     Source Type: Journal    
DOI: 10.1007/s12229-012-9115-2     Document Type: Article

References (124)

1. Becker, B. & B. Marin. 2009. Streptophyte algae and the origin of embryophytes. Annals of Botany 103: 999-1004.
2. Bednara, J. & B. Rodkiewicz. 1984. Distribution of plastids and mitochondria during sporogenesis in Equisetum hyemale. pp 17-20. In: M. T. M. Willemse & J. L. van Went (eds). Sexual reproduction in seed plants, ferns and mosses. Pudoc, Wageningen.
3. ---, L. Gielwanowska & B. Rodkiewicz. 1986. Regular arrangements of mitochondria and plastids during sporogenesis in Equisetum. Protoplasma 130: 145-152.
4. Binarová, P., V. Cenklová, J. Procházková, A. Doskocilová, J. Volc, M. Vrlik & L. Bögre. 2006. γ-Tubulin is essential for acentrosomal microtubule nucleation and coordination of late mitotic events in Arabidopsis. Plant Cell 18: 1199-1212.
5. Blackmore, S. & S. H. Barnes. 1987. Embryophyte spore walls: origin, development, and homologies. Cladistics 3: 185-195.
6. --- & R. B. Knox. 1990. Microspores Evolution and ontogeny. Academic, London.
7. ---, A. H. Wortley, J. J. Skvarla & J. R. Rowley. 2007. Pollen wall development in flowering plants. New Phytologist 174: 483-498.
8. Brown, R. C. & B. E. Lemmon. 1982a. Ultrastructure of meiosis in the moss Rhynchostegium serrulatum I. Prophasic microtubules and spindle dynamics. Protoplasma 110: 23-33.
9. --- & ---. 1982b. Ultrastructure of sporogenesis in the moss. Amblystegium riparium I. meiosis and cytokinesis. American Journal of Botany 69: 1096-1107.
10. --- & ---. 1983. Microtubule organization and morphogenesis in young spores of the moss Tetraphis pellucida Hedw. Protoplasma 116: 115-124.
11. --- & ---. 1986. Spore wall development in the liverwort, Haplomitrium hookeri. Canadian Journal of Botany 64: 1174-1182.
12. --- & ---. 1987a. Division polarity, development and configuration of microtubule arrays in bryophyte meiosis I: meiotic prophase to metaphase I. Protoplasma 137: 84-99.
13. --- & ---. 1987b. Division polarity, development and configuration of microtubule arrays in bryophyte meiosis II: anaphase I to the tetrad. Protoplasma 138: 1-10.
14. --- & ---. 1988a. Sporogenesis in bryophytes. Advances in Bryology 3: 159-223.
15. --- & ---. 1988b. Preprophasic microtubule systems and development of the mitotic spindle in hornworts (Bryophyta). Protoplasma 143: 11-21.
16. --- & ---. 1988c. Cytokinesis occurs at boundaries of domains delimited by nuclear-based microtubules in sporocytes of Conocephalum conicum (Bryophyta). Cell Motility and the Cytoskeleton 11: 139-146.
17. --- & ---. 1990. Polar organizers mark division axis prior to preprophase band formation in mitosis of the hepatic Reboulia hemisphaerica (Bryophyta). Protoplasma 156: 74-81.
18. --- & ---. 1991. The cytokinetic apparatus in meiosis: Control of division plane in the absence of a preprophase band of microtubules. pp 259-272. In: C. W. Lloyd (ed). The cytoskeletal basis of plant growth and form. Academic, New York.
19. --- & ---. 1992. Cytoplasmic domain: a model for spatial control of cytokinesis in reproductive cells of plants. Electron Microscopy Society of America Bulletin 22: 48-53.
20. --- & ---. 1993. Diversity of cell division in simple land plants holds clues to evolution of the mitotic and cytokinetic apparatus in higher plants. Memoirs of the Torrey Botanical Club 25: 45-62.
21. --- & ---. 1995. Methods in plant immunolight microscopy. Methods in Cell Biology 49: 85-107.
22. --- & ---. 1997. The quadripolar microtubule system in lower land plants. Journal of Plant Research 110: 93-106.
23. --- & ---. 2001. The cytoskeleton and the spatial control of cytokinesis in the plant life cycle. Protoplasma 215: 35-49.
24. --- & ---. 2004. γ-Tubulin, microtubule arrays, and quadripolarity during sporogenesis in the hepatic Aneura pinguis (L.) Dumort. (Metzgeriales). Journal of Plant Research 117: 371-376.
25. --- & ---. 2006. Polar organizers and girdling bands of microtubules are associated with γ-tubulin and act in establishment of meiotic quadripolarity in the hepatic Aneura pinguis (Bryophyta). Protoplasma 227: 77-85.
26. --- & ---. 2007. The pleiomorphic plant MTOC: an evolutionary perspective. Journal of Integrative Plant Biology 49: 1142-1153.
27. --- & ---. 2008. γ-Tubulin and microtubule organization during meiosis in the liverwort Ricciocarpus natans (Ricciaceae). American Journal of Botany 95: 664-671.
28. --- & ---. 2009. Pre-meiotic bands and novel meiotic spindle ontogeny in quadrilobed sporocytes of leafy liverworts (Jungermannidae, Bryophyta). Protoplasma 237: 41-49. doi: 10. 1007/s00709-009-0073-4.
29. --- & ---. 2011a. Spores before sporophytes: hypothesizing the origin of sporogenesis at the algal-plant transition. New Phytologist 190: 875-881. doi: 10. 1111/j. 1469-8137. 2011. 03709. x.
30. --- & ---. 2011b. Dividing without centrioles: innovative MTOCs organize mitotic spindles in bryophytes, the earliest extant lineages of land plants. AoB Plants 2011. doi: 10. 1093/aobpla/plr028.
31. ---, --- & Z. Carothers. 1982a. Spore wall development in Sphagnum lescurii. Canadian Journal of Botany 60: 2394-2409.
32. ---, --- & ---. 1982b. Spore wall ultrastructure of Sphagnum lescurii Sull. Review of Palaeobotany and Palynology 38: 99-107.
33. ---, --- & K. S. Renzaglia. 1986. Sporocytic control of spore wall pattern in liverworts. American Journal of Botany 73: 593-596.
34. ---, --- & T. Horio. 2004. γ-Tubulin localization changes from discrete polar organizers to anastral spindles and phragmoplasts in mitosis of Marchantia polymorpha L. Protoplasma 224: 187-193.
35. ---, --- & M. Shimamura. 2007. Transformations of the pleiomorphic plant MTOC during sporogenesis in the hepatic Marchantia polymorpha L. Journal of Integrative Plant Biology 49: 1244-1252.
36. ---, --- & ---. 2010. Diversity in meiotic spindle origin and determination of cytokinetic planes in sporogenesis of complex thalloid liverworts (Marchantiopsida). Journal of Plant Research 123: 589-605.
37. Browning, A. J. & B. E. S. Gunning. 1979a. Structure and function of transfer cells in the sporophyte haustorium of Funaria hygrometrica Hedw. II. Kinetics of labelled sugars and localization of absorbed products by freeze-substitution and autoradiography. Journal of Experimental Botany 30: 1247-1264.
38. --- & ---. 1979b. Structure and function of transfer cells in the sporophyte haustorium of Funaria hygrometrica Hedw. II. Translocation of assimilate into the attached sporophyte and along the seta of attached and excised sporophytes. Journal of Experimental Botany 30: 1265-1273.
39. Busby, C. H. & B. E. S. Gunning. 1988a. Establishment of plastid-based quadripolarity in spore mother cells of the moss Funaria hygrometrica. Journal of Cell Science 91: 117-126.
40. --- & ---. 1988b. Development of the quadripoIar meiotic cytoskeleton in spore mother cells of the moss Funaria hygrometrica. Journal of Cell Science 91: 127-137.
41. --- & ---. 1989. Development of the quadripolar meiotic apparatus in Funaria spore mother cells: analysis by means of anti-microtubule drug treatments. Journal of Cell Science 93: 267-277.
42. Carafa, A., J. G. Duckett & R. Ligrone. 2003. The placenta in Monoclea fosteri Hook. and Treubia lacunosa (Col.) Prosk.: insights into placental evolution in liverworts. Annals of Botany 92: 299-307.
43. ---, ---, J. P. Knox & R. Ligrone. 2005. Distribution of cell-wall xylans in bryophytes and tracheophytes: new insights into basal interrelationships of land plants. New Phytologist 168: 231-240.
44. Crandall-Stotler, B. 1980. Morphogenetic designs and a theory of bryophyte origins and divergence. BioScience 30: 580-585.
45. --- & R. E. Stotler. 2000. Morphology and classification of the Marchantiophyta. pp 21-70. In: A. J. Shaw & B. Goffinet (eds). Bryophyte biology. Cambridge University Press, Cambridge.
46. ---, --- & D. G. Long. 2009a. Morphology and classification of the Marchantiophyta. pp 1-54. In: B. Goffinet & A. J. Shaw (eds). Bryophyte biology, ed. 2nd. Cambridge University Press, Cambridge.
47. ---, --- & ---. 2009b. Phylogeny and classification of the Marchantiophyta. Edinburgh Journal of Botany 66: 155-198.
48. Crum, H. A. & L. E. Anderson. 1981. Mosses of eastern North America. 2 vols. Columbia University Press, New York.
49. Davis, B. M. 1899. The spore-mother-cell of Anthoceros. Botanical Gazette 27: 89-109.
50. Doonan, J. H. & J. G. Duckett. 1988. The bryophyte cytoskeleton. Advances in Bryology 3: 1-31.
51. ---, D. J. Cove, F. M. K. Cork & C. W. Lloyd. 1987. Pre-prophase band of microtubules absent from tip-growing moss filaments, arises in leafy shoots during transition to intercalary growth. Cell Motility and the Cytoskeleton 7: 138-153.
52. Duckett, J. G., S. Pressel, K. M. Y. P'Ng & K. S. Renzaglia. 2009. Exploding a myth: the capsule dehiscence mechanism and the function of pseudostomata in Sphagnum. New Phytologist 183: 1053-1063.
53. Edwards, D., J. G. Duckett & J. B. Richardson. 1995. Hepatic characters in the earliest land plants. Nature 374: 635-636.
54. Farmer, J. B. 1895. On spore-formation and nuclear division in the Hepaticae. Annals of Botany 9: 469-523.
55. --- 1904. On the interpretation of the quadripolar spindle in the Hepaticae. Botanical Gazette 37: 63-65.
56. Farr, C. H. 1916. Cytokinesis of the pollen-mother-cells of certain dicotyledons. Memoirs of the New York Botanical Garden 6: 253-316.
57. Finet, C., R. E. Timme, C. F. Delwiche & F. Marlétaz. 2010. Multigene phylogeny of the green lineage reveals the origin and diversification of land plants. Current Biology 20: 2217-2222.
58. Forrest, L. L., E. C. Davis, D. G. Long, B. Crandall-Stotler, A. Clark & M. L. Hollingsworth. 2006. Unraveling the evolutionary history of the liverworts (Marchantiophyta): multiple taxa, genomes and analyses. Bryologist 109: 303-334.
59. Frey, W. & M. Stech. 2005. A morpho-molecular classification of the liverworts (Hepaticophytina, Bryophyta). Nova Hedwigia 81: 55-78.
60. Furness, C. A. & P. J. Rudall. 1999. Microsporogenesis in monocotyledons. Annals of Botany 84: 475-499.
61. ---, --- & F. B. Sampson. 2002. Evolution of microsporogenesis in angiosperms. International Journal of Plant Science 163: 235-260.
62. Garbary, D. J. & K. S. Renzaglia. 1998. Bryophyte phylogeny and the evolution of land plants: evidence from development and ultrastructure. pp 45-63. In: J. W. Bates, N. W. Ashton, & J. G. Duckett (eds). Bryology for the twenty-first century. Maney and the British Bryological Society, Leeds.
63. Goffinet, B. & A. J. Shaw. 2009. Bryophyte biology, ed. 2nd. Cambridge, New York.
64. Graham, L. E. 1993. Origin of land plants. John Wiley, New York.
65. --- 1996. Green algae to land plants: an evolutionary transition. Journal of Plant Research 109: 241-251.
66. ---, M. E. Cook & J. S. Busse. 2000. The origin of plants: body plan changes contributing to a major evolutionary radiation. Proceedings of the National Academy of Sciences USA 97: 4535-4540.
67. Gray, J. 1993. Major Paleozoic land plant evolutionary bio-events. Palaeogeography, Palaeoclimatology, Palaeoecology 104: 153-169.
68. Gunning, B. E. S. 1982. The cytokinetic apparatus: its development and spatial regulation. pp 229-292. In: C. W. Lloyd (ed). The cytoskeleton in plant growth and development. Academic, London.
69. Hattori, S. & M. Mizutani. 1959. What is Takakia lepidozioides? Journal of the Hattori Botanical Laboratory 20: 285-303.
70. Hedderson, T. A., R. L. Chapman & W. L. Rootes. 1996. Phylogenetic relationships of bryophytes inferred from nuclear-encoded rRNA gene sequences. Plant Systematics and Evolution 200: 213-224.
71. ---, R. Chapman & C. J. Cox. 1998. Bryophytes and the origins and diversification of land plants: new evidence from molecules. pp 65-77. In: J. W. Bates, N. W. Ashton, & J. G. Duckett (eds). Bryology for the twenty-first century. Maney and the British Bryological Society, Leeds.
72. Heslop-Harrison, J. 1966. Cytoplasmic continuities during spore formation in flowering plants. Endeavour 25: 65-72.
73. --- 1972. Pattern in plant cell walls: morphogenesis in miniature. Proceedings of the Royal Institution of Great Britain 45: 335-351.
74. Horner, H. T., N. R. Lersten & C. C. Bowen. 1966. Spore development in the liverwort Riccardia pinguis. American Journal of Botany 53: 1048-1064.
75. Juel, H. O. 1897. Die kerntheilungen in den pollenmutterzellen von Hemerocallis fulva und die bei denselben auftretenden unregelmässigkeiten. Jahrbücher für wissenschaftliche Botanik 30: 205-226.
76. Kelley, C. B. & W. T. Doyle. 1975. Differentiation of intracapsular cells in the sporophyte of Sphaerocarpos donnellii. American Journal of Botany 62: 547-559.
77. Kenrick, P. & C. Crane. 1997. The origin and early evolution of plants on land. Nature 389: 33-39.
78. Ligrone, R. & R. Gambardella. 1988. The sporophyte-gametophyte junction in bryophytes. Advances in Bryology 3: 225-274.
79. Liu, B., J. Marc, H. C. Joshi & B. A. Palevitz. 1993. A γ-tubulin-related protein associated with the microtubule arrays of higher plants in a cell cycle-dependent manner. Journal of Cell Science 104: 1217-1228.
80. Mazia, D. 1961. Mitosis and the physiology of cell division. pp 77-412. In: J. Brachet & A. Mirsky (eds). The cell, vol. 3. Academic, New York.
81. Miller, N. G. (ed.). 1993. Biology of Sphagnum. Advances in Bryology 5: 1-338.
82. Mineyuki, Y. 1999. The preprophase band of microtubules: its function as a cytokinetic apparatus in higher plants. International Review of Cytology 187: 1-49.
83. --- 2007. Plant microtubule studies: past and present. Journal of Plant Research 120: 45-51.
84. Mishler, B. D. & S. P. Churchill. 1984. A cladistic approach to the phylogeny of the "bryophytes". Brittonia 36: 406-424.
85. Moore, A. C. 1905. Sporogenesis in Pallavacinia. Botanical Gazette 40: 81-96.
86. Neidhart, H. V. 1978. Ultrastructural aspects of sporogenesis in Riella affinis Howe and Underwood (Hepaticae). Journal of Bryology 10: 145-154.
87. Otegui, M. & L. A. Staehelin. 2000. Cytokinesis in flowering plants: more than one way to divide a cell. Current Opinions in Plant Biology 3: 493-502.
88. Ovenchkina, Y. & B. R. Oakley. 2001. γ-Tubulin in plant cells. Methods in Cell Biology 67: 195-212.
89. Pate, J. S. & B. E. S. Gunning. 1972. Transfer cells. Annual Review of Plant Physiology 23: 173-196.
90. Pickett-Heaps, J. D. 1969. The evolution of the mitotic apparatus: an attempt at comparative ultrastructural cytology in dividing plant cells. Cytobios 1: 257-280.
91. --- 1974. Cell division in Stichococcus. British Phycological Journal 9: 63-73.
92. Proskauer, J. 1954. On Sphaerocarpos stipitatus and the genus Sphaerocarpos. Journal of the Linnaean Society of London, Botany 55: 143-157.
93. Qiu, Y.-L., Y. Cho, J. C. Cox & J. D. Palmer. 1998. The gain of three mitochondrial introns identifies liverworts as the earliest land plants. Nature 394: 671-674.
94. Renzaglia, K. S., R. C. Brown, B. E. Lemmon, J. G. Duckett & R. Ligrone. 1994. Occurrence and phylogenetic significance of monoplastidic meiosis in liverworts. Canadian Journal of Botany 72: 65-72.
95. ---, K. D. McFarland & D. K. Smith. 1997. Anatomy and ultrastructure of the sporophyte of Takakia ceratophylla (Bryophyta). American Journal of Botany 84: 1337-1350.
96. ---, R. J. Duff, D. L. Nickrent & D. J. Garbary. 2000. Vegetative and reproductive innovations of early land plants: implications for a unified phylogeny. Philosophical Transactions of the Royal Society of London B Biological Sciences: 355: 769-793.
97. ---, S. Schuette, R. J. Duff, R. Ligrone, A. J. Shaw, B. D. Mishler & J. G. Duckett. 2007. Bryophyte phylogeny: Advancing the molecular and morphological frontiers. Bryologist 110: 179-213.
98. ---, J. C. Villarreal & R. J. Duff. 2009. New insights into morphology, anatomy, and systematics of hornworts. pp 139-171. In: B. Goffinet & A. J. Shaw (eds). Bryophyte biology, ed. 2nd. Cambridge University Press, New York.
99. Rodkiewicz, B., J. Bednara, A. Mostowska, E. Duda & H. Stobiecka. 1986. The change in disposition of plastids and mitochondria during microsporogenesis and sporogenesis in some higher plants. Acta Botanica Neerlandica 35: 209-215.
100. Rudall, P. J., M. V. Remizowa, A. S. Beer, E. Bradshaw, D. W. Stevenson, T. D. Macfarlane, R. E. Tuckett, S. R. Yadav & D. D. D. Sokoloff. 2008. Comparative ovule and megagametophyte development in Hydatellaceae and water lilies reveal a mosaic of features among the earliest angiosperms. Annals of Botany 101: 941-956.
101. Schepf, E. 1984. Pre- and postmitotic reorientation of microtubule arrays in young Sphagnum leaflets: transitional stages and initiation sites. Protoplasma 120: 100-112.
102. Schmit, A.-C. 2002. Acentrosomal microtubule nucleation in higher plants. International Review of Cytology 220: 257-289.
103. Schuster, R. M. 1984. Evolution, phylogeny and classification of the Hepaticae. pp 892-1070. In: R. M. Schuster (ed). New manual of bryology, Vol. 2. Hattori Botanical Laboratory, Nichinan.
104. --- 1992. The Hepaticae and Anthocerotae of North America east of the hundreth meridian, Vol. VI. Field Museum of Natural History, Chicago.
105. Shaw, J. & K. S. Renzaglia. 2004. Phylogeny and diversification of bryophytes. American Journal of Botany 91: 1557-1581.
106. Shimamura, M. & H. Deguchi. 2008. Sporophyte anatomy of Oedipodium griffithianum (Oedipodiaceae). pp 319-325. In: I. H. Mohamed, B. B. Baki, A. Nasrulhaq-Boyce, & P. K. Y. Lee (eds). Bryology in the new millennium. University of Malaysia Press, Kuala Lumpur.
107. ---, --- & Y. Mineyuki. 1998. Meiotic cytokinetic apparatus in the formation of the linear spore tetrads of Conocephalum japonicum (Bryophyta). Planta 206: 604-610.
108. ---, Y. Mineyuki & H. Deguchi. 2000. Monoplastidic meiosis in Dumortiera hirsuta (Bryophyta; Marchantiales). Journal of the Hattori Botanical Laboratory 88: 267-270.
109. ---, A. Kitamura, Y. Mineyuki & H. Deguchi. 2001. Occurrence of monoplastidic sporocytes and quadripolar microtubule systems in Marchantiales (Bryophyta; Marchantiidae). Hikobia 13: 551-562.
110. ---, H. Deguchi & Y. Mineyuki. 2003. A review of the occurrence of monoplastidic meiosis in liverworts. Journal of the Hattori Botanical Laboratory 94: 179-186.
111. ---, R. C. Brown, B. E. Lemmon, T. Akashi, K. Mizuno, N. Nishihara, K.-I. Tomizawa, K. Yoshimoto, H. Deguchi, H. Hosoya, T. Horio & Y. Mineyuki. 2004. γ-Tubulin in basal land plants: Characterization, localization and implication in the evolution of acentriolar microtubule organizing centers. Plant Cell 16: 45-59.
112. ---, T. Furuki & H. Deguchi. 2005. Sporophyte anatomy of Cavicularia densa (Blasiaceae). Bryologist 108: 420-426.
113. ---, M. Itouga & H. Tsubota. 2011. Evolution of apolar sporocytes in marchantialean liverworts: implications from molecular phylogeny. Journal of Plant Research. doi: 10. 1007/s10265-0425-y.
114. Smith, D. K. 1990. Sporophyte of Takakia discovered. Bryological Times 57(58): 1-4.
115. Taylor, W. A. & P. K. Strother. 2008. Ultrastructure of some Cambrian palynomorphs from the Bright Angel Shale, Arizona, USA. Review of Palaeobotany and Palynology 151: 41-50.
116. Tobe, H., Y. Kimoto & N. Prakash. 2007. Development and structure of the female gametophyte in Austrobaileya scandens (Austrobaileyaceae). Journal of Plant Research. 120: 431-436.
117. Turner, R. G. 1993. Peat and people: a review. Advances in Bryology 5: 315-328.
118. Villarreal, J. C., D. C. Cargill, A. Hagborg, L. Söderström & K. S. Renzaglia. 2010. A synthesis of hornwort diversity: Patterns, causes and future work. Phytotaxa 9: 150-166.
119. Von Konrat, M., J. Shaw & K. S. Renzaglia. 2010a. A special issue of Phytotaxa dedicated to Bryophytes: The closest living relatives of early land plants. Phytotaxa 9: 5-10.
120. ---, L. Söderström, M. A. M. Renner, A. Hagborg, L. Briscoe & J. J. Engel. 2010b. Early land plants today (ELPT): How many liverwort species are there? Phytotaxa 9: 22-40.
121. Wallace, S., A. Fleming, C. H. Wellman & D. J. Beerling. 2011. Evolutionary development of the plant spore and pollen wall. AoB Plants. doi: 10. 1093/aobpla/plr027.
122. Wasteneys, G. O. 2002. Microtubule organization in the green kingdom: chaos or self-order? Journal of Cell Science 115: 1345-1354.
123. Wiese, C. & Y. Zheng. 2006. Microtubule nucleation: γ-tubulin and beyond. Journal of Cell Science 119: 4143-4153.
124. Williams, J. H. & W. E. Friedman. 2004. The four-celled female gametophyte of Illicium (Illiciaceae; Austrobaileyales): implications for understanding the origin and early evolution of monocots, eumagnoliids, and eudicots. American Journal of Botany 91: 332-351.