The Evolution of Cell Division: From Streptophyte Algae to Land Plants

Trends in Plant Science

Volumn 21, Issue 10, 2016, Pages 872-883

  Buschmann, Henrik ^a   Zachgo, Sabine ^a  

^a UNIVERSITY OF OSNABRÜCK   (Germany)

Author keywords

algae; centrosome; evolution; land plant; phragmoplast; preprophase band

Indexed keywords

CELL DIVISION; CENTROSOME; EVOLUTION; GENETICS; PHYLOGENY; PHYSIOLOGY; PLANT; PLANT PHYSIOLOGY; PROPHASE; STREPTOPHYTA;

BIOLOGICAL EVOLUTION; CELL DIVISION; CENTROSOME; PHYLOGENY; PLANT PHYSIOLOGICAL PHENOMENA; PLANTS; PROPHASE; STREPTOPHYTA;

EID: 84979784994     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2016.07.004     Document Type: Review

References (100)

1. 1 Oliferenko, S., et al. Positioning cytokinesis. Genes Dev. 23 (2009), 660–674.
2. 2 Van Damme, D., Division plane determination during plant somatic cytokinesis. Curr. Opin. Plant Biol. 12 (2009), 745–751.
3. 3 Pickett-Heaps, J.D., Green Algae: Structure, Reproduction and Evolution in Selected Genera. 1975, Sinauer.
4. 4 Dubois, F., et al. The petunia tra1 gene controls cell elongation and plant development, and mediates responses to cytokinins. Plant J. 10 (1996), 47–59.
5. 5 Torres-Ruiz, R.A., Jürgens, G., Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120 (1994), 2967–2978.
6. 6 Traas, J., et al. Normal differentiation patterns in plants lacking microtubular preprophase bands. Nature 375 (1995), 676–677.
7. 7 Cleary, A.L., Smith, L.G., The Tangled1 gene is required for spatial control of cytoskeletal arrays associated with cell division during maize leaf development. Plant Cell 10 (1998), 1875–1888.
8. 8 Müller, S., et al. Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr. Biol. 16 (2006), 888–894.
9. 9 Xu, X.M., et al. RanGAP1 is a continuous marker of the Arabidopsis cell division plane. Proc. Natl. Acad. Sci. U.S.A. 105 (2008), 18637–18642.
10. 10 Rasmussen, C.G., et al. Determination of symmetric and asymmetric division planes in plant cells. Annu. Rev. Plant Biol. 62 (2011), 387–409.
11. 11 Smertenko, A.P., et al. The origin of phragmoplast asymmetry. Curr. Biol. 21 (2011), 1924–1930.
12. 12 Lee, Y.R., Liu, B., The rise and fall of the phragmoplast microtubule array. Curr. Opin. Plant Biol. 16 (2013), 757–763.
13. 13 Boruc, J., Van Damme, D., Endomembrane trafficking overarching cell plate formation. Curr. Opin. Plant Biol. 28 (2015), 92–98.
14. 14 Austin, J.R. 2nd, et al. Quantitative analysis of changes in spatial distribution and plus-end geometry of microtubules involved in plant-cell cytokinesis. J. Cell Sci. 118 (2005), 3895–3903.
15. 15 Karahara, I., et al. The preprophase band is a localized center of clathrin-mediated endocytosis in late prophase cells of the onion cotyledon epidermis. Plant J. 57 (2009), 819–831.
16. 16 Zachariadis, M., et al. Organization of the endoplasmic reticulum in dividing cells of the gymnosperms Pinus brutia and Pinus nigra, and of the pterophyte Asplenium nidus. Cell Biol. Int. 27 (2003), 31–40.
17. 17 Burgess, J., Northcote, D.H., A function of preprophase band of microtubules in Phleum pratense. Planta, 75, 1967, 319.
18. 18 Cleary, A.L., F-actin redistributions at the division site in living Tradescantia stomatal complexes as revealed by microinjection of rhodamine–phalloidin. Protoplasma 185 (1995), 152–165.
19. 19 Pickett-Heaps, J.D., Northcote, D.H., Organization of microtubules and endoplasmatic reticulum during mitosis and cytokinesis in wheat meristems. J. Cell. Sci. 1 (1966), 109–120.
20. 20 Pickett-Heaps, J.D., Northcote, D.H., Cell division in the formation of the stomatal complex of young leaves of wheat. J. Cell Sci. 1 (1966), 121–128.
21. 21 Müller, S., Universal rules for division plane selection in plants. Protoplasma 249 (2012), 239–253.
22. 22 Van Damme, D., et al. Cortical division zone establishment in plant cells. Trends Plant Sci. 12 (2007), 458–464.
23. 23 Buschmann, H., et al. Microtubule-associated AIR9 recognizes the cortical division site at preprophase and cell-plate insertion. Curr. Biol. 16 (2006), 1938–1943.
24. 24 Buschmann, H., et al. Arabidopsis KCBP interacts with AIR9 but stays in the cortical division zone throughout mitosis via its MyTH4-FERM domain. J. Cell Sci. 128 (2015), 2033–2046.
25. 25 Lipka, E., et al. The phragmoplast-orienting kinesin-12 class proteins translate the positional information of the preprophase band to establish the cortical division zone in Arabidopsis thaliana. Plant Cell 26 (2014), 2617–2632.
26. 26 Wu, S.Z., Bezanilla, M., Myosin VIII associates with microtubule ends and together with actin plays a role in guiding plant cell division. eLife, 3, 2014, e03498.
27. 27 Walker, K.L., et al. Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Curr. Biol. 17 (2007), 1827–1836.
28. 28 Lokhorst, G.M., et al. The ultrastructure of mitosis and cytokinesis in the sarcinoid Chlorokybus atmophyticus (Chlorophyta, Charophyceae) revealed by rapid freeze fixation and freeze substitution. J. Phycol. 24 (1988), 237–248.
29. 29 Manton, I., Ettl, H., Observations on the fine structure of Mesostigma viride Lauterborn. J. Linn. Soc. 59 (1965), 175–184.
30. 30 Braun, M., Wasteneys, G.O., Reorganization of the actin and microtubule cytoskeleton throughout blue-light-induced differentiation of characean protonemata into multicellular thalli. Protoplasma 202 (1998), 38–53.
31. 31 Stewart, K.D., Mattox, K.R., Comparative cytology, evolution and classification of green-algae with some consideration of origin of other organisms with chlorophylls a and b. Bot. Rev. 41 (1975), 104–135.
32. 32 Leliaert, F., et al. Phylogeny and molecular evolution of the green algae. Crit. Rev. Plant Sci. 31 (2012), 1–46.
33. 33 Jürgens, G., Plant cytokinesis: fusion by fission. Trends Cell Biol. 15 (2005), 277–283.
34. 34 Pickett-Heaps, J.D., et al. The cytoplast concept in dividing plant cells: cytoplasmic domains and the evolution of spatially organized cell division. Am. J. Bot. 86 (1999), 153–172.
35. 35 Mollinari, C., et al. PRC1 is a microtubule binding and bundling protein essential to maintain the mitotic spindle midzone. J. Cell Biol. 157 (2002), 1175–1186.
36. 36 Lukowitz, W., et al. Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 84 (1996), 61–71.
37. 37 Smertenko, A., et al. A new class of microtubule-associated proteins in plants. Nat. Cell Biol. 2 (2000), 750–753.
38. 38 Hotta, T., et al. Characterization of the Arabidopsis augmin complex uncovers its critical function in the assembly of the acentrosomal spindle and phragmoplast microtubule arrays. Plant Cell 24 (2012), 1494–1509.
39. 39 Fowke, L.C., Pickett-Heaps, J.D., Cell division in Spirogyra. II. Cytokinesis. J. Phycol. 5 (1969), 273–281.
40. 40 Pickett-Heaps, J.D., Wetherbee, R., Spindle function in the green alga Mougeotia: absence of anaphase A correlates with postmitotic nuclear migration. Cell Motil. Cytoskeleton 7 (1987), 68–77.
41. 41 Gontcharov, A.A., Phylogeny and classification of Zygnematophyceae (Streptophyta): current state of affairs. Fottea 8 (2008), 87–104.
42. 42 Hall, J.D., et al. Phylogeny of the conjugating green algae based on chloroplast and mitochondrial nucleotide sequence data. J. Phycol. 44 (2008), 467–477.
43. 43 Brown, R.C., Lemmon, B.E., Polar organizers in monoplastidic mitosis of hepatics (Bryophyta). Cell Motil. Cytoskeleton 22 (1992), 72–77.
44. 44 Brown, R.C., Lemon, B.E., Microtubules associated with simultaneous cytokinesis of coenocytic microsporocytes. Am. J. Bot. 75 (1988), 1848–1856.
45. 45 Otegui, M.S., Staehelin, L.A., Electron tomographic analysis of post-meiotic cytokinesis during pollen development in Arabidopsis thaliana. Planta 218 (2004), 501–515.
46. 46 Schmit, A.C., Acentrosomal microtubule nucleation in higher plants. Int. Rev. Cytol. 220 (2002), 257–289.
47. 47 Katsaros, C.I., et al. Comparative immunofluorescence and ultrastructural analysis of microtubule organization in Uronema sp., Klebsormidium flaccidum, K. subtilissimum, Stichococcus bacillaris and S. chloranthus (Chlorophyta). Protist 162 (2011), 315–331.
48. 48 Brown, R.C., et al. Morphogenetic plastid migration and microtubule arrays in mitosis and cytokinesis in the green-alga Coleochaete Orbicularis. Am. J. Bot. 81 (1994), 127–133.
49. 49 Galway, M.E., Hardham, A.R., Immunofluorescent localization of microtubules throughout the cell-cycle in the green-alga Mougeotia (Zygnemataceae). Am. J. Bot. 78 (1991), 451–461.
50. 50 Fowke, L.C., Pickett-Heaps, J.D., Electron microscope study of vegetative cell division in two species of Marchantia. Can. J. Bot. 56 (1978), 467–475.
51. 51 Brown, R.C., Lemmon, B.E., Polar organizers mark division axis prior to preprophase band formation in mitosis of the hepatic Reboulia hemisphaerica (Bryophyta). Protoplasma 156 (1990), 74–81.
52. 52 Buschmann, H., et al. Microtubule dynamics of the centrosome-like polar organizers from the basal land plant Marchantia polymorpha. New Phytol. 209 (2016), 999–1013.
53. 53 Webb, M.C., Gunning, B.E.S., The microtubular cytoskeleton during development of the zygote, proembryo and free-nuclear endosperm in Arabidopsis thaliana (L) Heynh. Planta 184 (1991), 187–195.
54. 54 Webb, M.C., Gunning, B.E.S., Embryo sac development in Arabidopsis thaliana. II. The cytoskeleton during megagametogenesis. Sex. Plant Reprod. 7 (1994), 153–163.
55. 55 Gunning, B.E.S., et al. Pre-prophase bands of microtubules in all categories of formative and proliferative cell division in Azolla roots. Planta 143 (1978), 145–160.
56. 56 Brown, R.C., Lemmon, B.E., Monoplastidic cell-division in lower land plants. Am. J. Bot. 77 (1990), 559–571.
57. 57 Brown, R.C., Lemmon, B.E., Dividing without centrioles: innovative plant microtubule organizing centres organize mitotic spindles in bryophytes, the earliest extant lineages of land plants. AoB plants, 2011, 2011, plr028.
58. 58 Doonan, J.H., et al. Pre-prophase band of microtubules, Absent from tip-growing moss filaments, arises in leafy shoots during transition to intercalary growth. Cell Motil. Cytoskel. 7 (1987), 138–153.
59. 59 Sawidis, T., et al. Presence and absence of the preprophase band of microtubules in moss protonemata–a clue to understanding its function. Protoplasma 163 (1991), 156–161.
60. 60 Graham, L.E., et al. The origin of plants: body plan changes contributing to a major evolutionary radiation. Proc. Natl. Acad. Sci. U.S.A. 97 (2000), 4535–4540.
61. 61 Miki, T., et al. Endogenous localizome identifies 43 mitotic kinesins in a plant cell. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), E1053–E1061.
62. 62 Menand, B., et al. Both chloronemal and caulonemal cells expand by tip growth in the moss Physcomitrella patens. J. Exp. Bot. 58 (2007), 1843–1849.
63. 63 Vidali, L., Bezanilla, M., Physcomitrella patens: a model for tip cell growth and differentiation. Curr. Opin. Plant Biol. 15 (2012), 625–631.
64. 64 Graham, L.E., Kaneko, Y., Subcellular structures of relevance to the origin of land plants (embryophytes) from green-algae. Crit. Rev. Plant Sci. 10 (1991), 323–342.
65. 65 Doty, K.F., et al. Immunofluorescence localization of the tubulin cytoskeleton during cell division and cell growth in members of the Coleochaetales (Streptophyta). J. Phycol. 50 (2014), 624–639.
66. 66 Kiermayer, O., Distribution of microtubules in differentiating cells of Micrasterias denticulata Breb. Planta 83 (1968), 223–236.
67. 67 Kallio, P., The significance of nuclear quantity in the genus Micrasterias. Ann. bot. Soc. zool.-bot. fenn. ‘Vanamo’ 24 (1951), 1–22.
68. 68 Hogetsu, T., Oshima, Y., Immunofluorescence microscopy of microtubule arrangement in Closterium acerosum (Schrank) Ehrenberg. Planta 166 (1985), 169–175.
69. 69 Ochs, J., et al. The cortical cytoskeletal network and cell-wall dynamics in the unicellular charophycean green alga Penium margaritaceum. Ann. Bot. – London 114 (2014), 1237–1249.
70. 70 Domozych, D.S., et al. Disruption of the microtubule network alters cellulose deposition and causes major changes in pectin distribution in the cell wall of the green alga, Penium margaritaceum. J. Exp. Bot. 65 (2014), 465–479.
71. 71 Bakker, M.E., Lokhorst, G.M., Ultrastructure of mitosis and vytokinesis in Zygnema sp. (Zygnematales, Chlorophyta). Protoplasma 138 (1987), 105–118.
72. 72 Yoon, M., et al. Cytoskeletal changes during the nuclear and cell division in the freshwater alga Zygnema cruciatum. Algae 25 (2010), 197–204.
73. 73 Darwin, C., On the Origin of Species by Means of Natural Selection. 1859, John Murray.
74. 74 Wu, S.Z., et al. Myosin VIII regulates protonemal patterning and developmental timing in the moss Physcomitrella patens. Mol. Plant 4 (2011), 909–921.
75. 75 Hori, K., et al. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun., 5, 2014, 3978.
76. 76 Conant, G.C., Wolfe, K.H., Turning a hobby into a job: how duplicated genes find new functions. Nat. Rev. Genet. 9 (2008), 938–950.
77. 77 Hiwatashi, Y., et al. Kinesins have a dual function in organizing microtubules during both tip growth and cytokinesis in Physcomitrella patens. Plant Cell 26 (2014), 1256–1266.
78. 78 Jacob, F., Evolution and tinkering. Science 196 (1977), 1161–1166.
79. 79 Ohno, S., Evolution by Gene Duplication. 1970, Allen & Unwin and Springer-Verlag.
80. 80 Lee, Y.R., et al. Kinesin motors in plants: from subcellular dynamics to motility regulation. Curr. Opin. Plant Biol. 28 (2015), 120–126.
81. 81 O'Brien, T.P., The preprophase band of microtubules: does it block cleavage?. Cytobios 37 (1983), 101–105.
82. 82 Cook, M.E., Structure and asexual reproduction of the enigmatic charophycean green alga Entransia fimbriata (Klebsormidiales, Charophyceae). J. Phycol. 40 (2004), 424–431.
83. 83 Mikhailyuk, T., et al. Morphology and ultrastructure of Interfilum and Klebsormidium (Klebsormidiales, Streptophyta) with special reference to cell division and thallus formation. Eur. J. Phycol. 49 (2014), 395–412.
84. 84 Pickett-Heaps, J., Ultrastructure and differentiation in Chara sp. 2. Mitosis. Aust. J. Biol. Sci. 20 (1967), 883–894.
85. 85 Kotak, S., Gönczy, P., Mechanisms of spindle positioning: cortical force generators in the limelight. Curr. Opin. Cell Biol. 25 (2013), 741–748.
86. 86 McNally, F.J., Mechanisms of spindle positioning. J. Cell Biol. 200 (2013), 131–140.
87. 87 Siller, K.H., Doe, C.Q., Spindle orientation during asymmetric cell division. Nat. Cell Biol. 11 (2009), 365–374.
88. 88 Wickstead, B., Gull, K., Dyneins across eukaryotes: a comparative genomic analysis. Traffic 8 (2007), 1708–1721.
89. 89 Richardson, D.N., et al. Comprehensive comparative analysis of kinesins in photosynthetic eukaryotes. BMC Genomics, 7, 2006, 18.
90. 90 Jonsson, E., et al. Clustering of a kinesin-14 motor enables processive retrograde microtubule-based transport in plants. Nat. Plants, 1, 2015, 15087.
91. 91 Becker, B., Marin, B., Streptophyte algae and the origin of embryophytes. Ann. Bot. – London 103 (2009), 999–1004.
92. 92 Delwiche, C.F., Cooper, E.D., The evolutionary origin of a terrestrial flora. Curr. Biol. 25 (2015), R899–R910.
93. 93 Zhong, B.J., et al. Streptophyte algae and the origin of land plants revisited using heterogeneous models with three new algal chloroplast genomes. Mol. Biol. Evol. 31 (2014), 177–183.
94. 94 Civan, P., et al. Analyses of charophyte Chloroplast cenomes help characterize the ancestral chloroplast genome of land plants. Genome Biol. Evol. 6 (2014), 897–911.
95. 95 Ruhfel, B.R., et al. From algae to angiosperms–inferring the phylogeny of green plants (Viridiplantae) from 360 plastid genomes. BMC Evol. Biol., 14, 2014, 23.
96. 96 Wodniok, S., et al. Origin of land plants: do conjugating green algae hold the key?. BMC Evol. Biol., 11, 2011, 104.
97. 97 Timme, R.E., et al. Broad phylogenomic sampling and the sister lineage of land plants. PLoS ONE, 7, 2012, e29696.
98. 98 Zhong, B.J., et al. Origin of land plants using the multispecies coalescent model. Trends Plant Sci. 18 (2013), 492–495.
99. 99 Wickett, N.J., et al. Phylotranscriptomic analysis of the origin and early diversification of land plants. Proc. Natl. Acad. Sci. U.S.A. 111 (2014), E4859–E4868.
100. 100 Harholt, J., et al. Why plants were terrestrial from the beginning. Trends Plant Sci. 21 (2016), 96–101.