Cytokinesis in plant male meiosis

Plant Signaling and Behavior

Volumn 8, Issue 3, 2013, Pages

  De Storme, Nico ^a   Geelen, Danny ^a  

^a GHENT UNIVERSITY   (Belgium)

Author keywords

Callose; Cytokinesis; Phragmoplast; Plant meiosis; RMA

Indexed keywords

CALLOSE; GLUCAN;

ARTICLE; CELL NUCLEUS; CELL WALL; COLD; CYTOKINESIS; CYTOLOGY; CYTOPLASM; CYTOSKELETON; GENETICS; HAPLOIDY; MEIOSIS; METABOLISM; PHRAGMOPLAST; PHYSIOLOGICAL STRESS; PLANT; PLANT MEIOSIS; POLLEN; RMA;

CALLOSE; CYTOKINESIS; PHRAGMOPLAST; PLANT MEIOSIS; RMA;

CELL NUCLEUS; CELL WALL; COLD TEMPERATURE; CYTOKINESIS; CYTOPLASM; CYTOSKELETON; GLUCANS; HAPLOIDY; MEIOSIS; PLANTS; POLLEN; STRESS, PHYSIOLOGICAL;

EID: 84874690051     PISSN: 15592316     EISSN: 15592324     Source Type: Journal    
DOI: 10.4161/psb.23394     Document Type: Article

References (101)

1. Söllner R;, Glässer G, Wanner G, Somerville CR, Jürgens G, Assaad FF. Cytokinesis-defective mutants of Arabidopsis. Plant Physiol 2002; 129:678-90. PMID:12068111; http://dx.doi.org/10.1104/pp.004184.
2. Castrillon DH, Wasserman SA. Diaphanous is required for cytokinesis in Drosophila and shares domains of similarity with the products of the limb deformity gene. Development 1994; 120:3367-77. PMID:7821209.
3. Wu JQ, Bähler J, Pringle JR. Roles of a fimbrin and an alpha-actinin-like protein in fission yeast cell polarization and cytokinesis. Mol Biol Cell 2001; 12:1061-77. PMID:11294907.
4. Oliferenko S, Chew TG, Balasubramanian MK.Positioning cytokinesis. Genes Dev 2009; 23:660-74. PMID:19299557; http://dx.doi.org/10.1101/gad.1772009.
5. Dhonukshe P, Samaj J, Baluska F, Friml J. A unifying new model of cytokinesis for the dividing plant and animal cells. Bioessays 2007; 29:371-81. PMID:17373659; http://dx.doi.org/10.1002/bies.20559.
6. Green RA, Paluch E, Oegema K. Cytokinesis in animal cells. Annu Rev Cell Dev Biol 2012; 28:29-58. PMID:22804577; http://dx.doi.org/10.1146/annurevcellbio-101011-155718.
7. Balasubramanian MK, Bi E, Glotzer M. Comparative analysis of cytokinesis in budding yeast, fission yeast and animal cells. Curr Biol 2004; 14:R806-18. PMID:15380095; http://dx.doi.org/10.1016/j.cub.2004.09.022.
8. Wu JQ, Kuhn JR, Kovar DR, Pollard TD. Spatial and temporal pathway for assembly and constriction of the contractile ring in fission yeast cytokinesis. Dev Cell 2003; 5:723-34. PMID:14602073; http://dx.doi.org/10.1016/S1534-5807(03)00324-1.
9. Bringmann H, Hyman AA. A cytokinesis furrow is positioned by two consecutive signals. Nature 2005; 436:731-4. PMID:16079852; http://dx.doi.org/10.1038/nature03823.
10. Bi E. Cytokinesis in budding yeast: the relationship between actomyosin ring function and septum formation. Cell Struct Funct 2001; 26:529-37. PMID:11942606; http://dx.doi.org/10.1247/csf.26.529.
11. Müller S, Wright AJ, Smith LG. Division plane control in plants: new players in the band. Trends Cell Biol 2009; 19:180-8. PMID:19285867; http://dx.doi.org/10.1016/j.tcb.2009.02.002.
12. Eggert US, Mitchison TJ, Field CM. Animal cytokinesis: from parts list to mechanisms. Annu Rev Biochem 2006; 75:543-66. PMID:16756502; http://dx.doi.org/10.1146/annurev.biochem.74.082803.133425.
13. Granger CL, Cyr RJ. Microtubule reorganization in tobacco BY-2 cells stably expressing GFP-MBD. Planta 2000; 210:502-9. PMID:10750909; http://dx.doi.org/10.1007/s004250050037.
14. Assaad FF. Plant cytokinesis. Exploring the links. Plant Physiol 2001; 126:509-16. PMID:11402182; http://dx.doi.org/10.1104/pp.126.2.509.
15. Seguí-Simarro JM, Austin JR 2, White EA, Staehelin LA. Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 2004; 16:836-56. PMID:15020749; http://dx.doi.org/10.1105/tpc.017749.
16. Brown RC, Lemmon BE. The cytoskeleton and spatial control of cytokinesis in the plant life cycle. Protoplasma 2001; 215:35-49. PMID:11732063; http://dx.doi.org/10.1007/BF01280302.
17. Van Damme D, Inzé D, Russinova E. Vesicle trafficking during somatic cytokinesis. Plant Physiol 2008; 147:1544-52. PMID:18678745; http://dx.doi.org/10.1104/pp.108.120303.
18. Jürgens G. Cytokinesis in higher plants. Annu Rev Plant Biol 2005; 56:281-99. PMID:15862097; http://dx.doi.org/10.1146/annurev.arplant.55.031903.141636.
19. Verma DPS. Cytokinesis and building of the cell plate in plants. Annu Rev Plant Physiol Plant Mol Biol 2001; 52:751-84. PMID:11337415; http://dx.doi.org/10.1146/annurev.arplant.52.1.751.
20. Baluška F, Menzel D, Barlow PW. Cytokinesis in plant and animal cells: endosomes 'shut the door'. Dev Biol 2006; 294:1-10. PMID:16580662; http://dx.doi.org/10.1016/j.ydbio.2006.02.047.
21. Samuels AL, Giddings TH Jr., Staehelin LA. Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J Cell Biol 1995; 130:1345-57. PMID:7559757; http://dx.doi.org/10.1083/jcb.130.6.1345.
22. Baluska F, Liners F, Hlavacka A, Schlicht M, Van Cutsem P, McCurdy DW, et al. Cell wall pectins and xyloglucans are internalized into dividing root cells and accumulate within cell plates during cytokinesis. Protoplasma 2005; 225:141-55. PMID:16228896; http://dx.doi.org/10.1007/s00709-005-0095-5.
23. Nadot S, Furness CA, Sannier J, Penet L, Triki-Teurtroy S, Albert B, et al. Phylogenetic comparative analysis of microsporogenesis in angiosperms with a focus on monocots. Am J Bot 2008; 95:1426-36. PMID:21628150; http://dx.doi.org/10.3732/ajb.0800110.
24. Nunes ELP, Bona C, Moço MC, Coan AI. Release of developmental constraints on tetrad shape is confirmed in inaperturate pollen of Potamogeton. Ann Bot 2009; 104:1011-5. PMID:19567417; http://dx.doi.org/10.1093/aob/mcp160.
25. Penet L, Nadot S, Ressayre A, Forchioni A, Dreyer L, Gouyon PH. Multiple developmental pathways leading to a single morph: monosulcate pollen (examples from the Asparagales). Ann Bot 2005; 95:331-43. PMID:15567807; http://dx.doi.org/10.1093/aob/mci030.
26. Zhang YN, et al. Microtubule organization during successive microsporogenesis in Allium cepa and simultaneous cytokinesis in Nicotiana tabacum. Biol Plant 2011; 55:752-6; http://dx.doi.org/10.1007/s10535-011-0181-9.
27. Bhatt AM, Canales C, Dickinson HG. Plant meiosis: the means to 1N. Trends Plant Sci 2001; 6:114-21. PMID:11239610; http://dx.doi.org/10.1016/S1360-1385(00)01861-6.
28. Rudall PJ, et al. Microsporogenesis and pollen sulcus type in Asparagales (Lilianae). Canadian Journal of Botany-Revue Canadienne De Botanique 1997; 75:408-30; http://dx.doi.org/10.1139/b97-044.
29. Furness CA, Rudall PJ. Microsporogenesis in monocotyledons. Ann Bot (Lond) 1999; 84:475-99; http://dx.doi.org/10.1006/anbo.1999.0942.
30. Owen HA, Makaroff CA. Ultrastructure of Microsporogenesis and Microgametogenesis in Arabidopsis-Thaliana (L) Heynh Ecotype Wassilewskija (Brassicaceae). Protoplasma 1995; 185:7-21; http://dx.doi.org/10.1007/BF01272749.
31. Ressayre A, Dreyer L, Triki-Teurtroy S, Forchioni A, Nadot S. Post-meiotic cytokinesis and pollen aperture pattern ontogeny: comparison of development in four species differing in aperture pattern. Am J Bot 2005; 92:576-83. PMID:21652436; http://dx.doi.org/10.3732/ajb.92.4.576.
32. Shamina NV, Gordeeva EI, Kovaleva NM, Seriukova EG, Dorogova NV. Formation and function of phragmoplast during successive cytokinesis stages in higher plant meiosis. Cell Biol Int 2007; 31:626-35. PMID:17291791; http://dx.doi.org/10.1016/j.cellbi.2006.12.001.
33. Brown RC. (1991) The cytokinetic apparatus in meiosis: control of division plane in the absence of a preprophase band of microtubules. In The cytoskeletal basis of plant growth and form (Lloyd, C.W., ed), pp. 269-273, Academic Press.
34. Shamina NV, Dorogova N, Trunova S. Radial spindle and the phenotype of the maize meiotic mutant, dv. Cell Biol Int 2000; 24:729-36. PMID:11023651; http://dx.doi.org/10.1006/cbir.2000.0533.
35. Otegui M, Staehelin LA. Cytokinesis in flowering plants: more than one way to divide a cell. Curr Opin Plant Biol 2000; 3:493-502. PMID:11074381; http://dx.doi.org/10.1016/S1369-5266(00)00119-9.
36. Staiger CJ, Cande WZ. Microfilament Distribution in Maize Meiotic Mutants Correlates with Microtubule Organization. Plant Cell 1991; 3:637-44. PMID:12324607.
37. Traas JA, et al. The Organization of the Cytoskeleton during Meiosis in Eggplant (Solanum-Melongena (L)) - Microtubules and F-Actin Are Both Necessary for Coordinated Meiotic Division. J Cell Sci 1989; 92:541-50.
38. Otegui MS, Staehelin LA. Electron tomographic analysis of post-meiotic cytokinesis during pollen development in Arabidopsis thaliana. Planta 2004; 218:501-15. PMID:14610676; http://dx.doi.org/10.1007/s00425-003-1125-1.
39. Heese M, Mayer U, Jürgens G. Cytokinesis in flowering plants: cellular process and developmental integration. Curr Opin Plant Biol 1998; 1:486-91. PMID:10066634; http://dx.doi.org/10.1016/S1369-5266(98)80040-X.
40. Wick SM. Spatial aspects of cytokinesis in plant cells. Curr Opin Cell Biol 1991; 3:253-60. PMID:1883618; http://dx.doi.org/10.1016/0955-0674(91)90149-S.
41. Brown RC, Lemmon BE. Nuclear cytoplasmic domains, microtubules and organelles in microsporocytes of the slipper orchid Cypripedium californicum A Gray dividing by simultaneous cytokinesis. Sex Plant Reprod 1996; 9:145-52; http://dx.doi.org/10.1007/BF02221394.
42. Brown RC, Lemmon BE. Microtubules Associated with Simultaneous Cytokinesis of Coenocytic Microsporocytes. Am J Bot 1988; 75:1848-56; http://dx.doi.org/10.2307/2444739.
43. Yang CY, Spielman M, Coles JP, Li Y, Ghelani S, Bourdon V, et al. TETRASPORE encodes a kinesin required for male meiotic cytokinesis in Arabidopsis. Plant J 2003; 34:229-40. PMID:12694597; http://dx.doi.org/10.1046/j.1365-313X.2003.01713.x.
44. Shimamura M, Brown RC, Lemmon BE, Akashi T, Mizuno K, Nishihara N, et al. Gamma-tubulin in basal land plants: characterization, localization, and implication in the evolution of acentriolar microtubule organizing centers. Plant Cell 2004; 16:45-59. PMID:14660802; http://dx.doi.org/10.1105/tpc.016501.
45. Brown RC, Lemmon BE. Minispindles and Cytoplasmic Domains in Microsporogenesis of Orchids. Protoplasma 1989; 148:26-32; http://dx.doi.org/10.1007/BF01403988.
46. Brown RC, Lemmon BE. Control of Division Plane in Normal and Griseofulvin-Treated Microsporocytes of Magnolia. J Cell Sci 1992; 103:1031-8.
47. Peirson BN, Bowling SE, Makaroff CA. A defect in synapsis causes male sterility in a T-DNA-tagged Arabidopsis thaliana mutant. Plant J 1997; 11:659-69. PMID:9161029; http://dx.doi.org/10.1046/j.1365-313X.1997.11040659.x.
48. Brown RC, Lemmon BE. Nguyen H, Olsen OA. Development of endosperm in Arabidopsis thaliana. Sex Plant Reprod 1999; 12:32-42; http://dx.doi.org/10.1007/s004970050169.
49. Otegui M, Staehelin LA. Syncytial-type cell plates: a novel kind of cell plate involved in endosperm cellularization of Arabidopsis. Plant Cell 2000; 12:933-47. PMID:10852938.
50. Russell SD. The Egg Cell: Development and Role in Fertilization and Early Embryogenesis. Plant Cell 1993; 5:1349-59. PMID:12271034.
51. Chen XY, Liu L, Lee E, Han X, Rim Y, Chu H, et al. The Arabidopsis callose synthase gene GSL8 is required for cytokinesis and cell patterning. Plant Physiol 2009; 150:105-13. PMID:19286936; http://dx.doi.org/10.1104/pp.108.133918.
52. Teng NJ, et al. Microsporogenesis and pollen development in Leymus chinensis with emphasis on dynamic changes in callose deposition. Flora 2005; 200:256-63; http://dx.doi.org/10.1016/j.flora.2004.12.001.
53. Abramova LI, Avalkina NA, Golubeva EA, Pyzhenkova ZS, Golubovskaya IN. Synthesis and deposition of callose in anthers and ovules of meiotic mutants of maize (Zea mays). Russ J Plant Physiol 2003; 50:324-9; http://dx.doi.org/10.1023/A:1023866019102.
54. Kuran N. Callose Localization in the Walls of Megasporocytes and Megaspores in the Course of Development of Monospore Embryo Sacs. Acta Societatis Botanicorum Poloniae 1972; 41:520-34.
55. Dong XY, Hong Z, Sivaramakrishnan M, Mahfouz M, Verma DP. Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J 2005; 42:315-28. PMID:15842618; http://dx.doi.org/10.1111/j.1365-313X.2005.02379.x.
56. Worrall D, Hird DL, Hodge R, Paul W, Draper J, Scott R. Premature dissolution of the microsporocyte callose wall causes male sterility in transgenic tobacco. Plant Cell 1992; 4:759-71. PMID:1392594.
57. Enns LC, Kanaoka MM, Torii KU, Comai L, Okada K, Cleland RE. Two callose synthases, GSL1 and GSL5, play an essential and redundant role in plant and pollen development and in fertility. Plant Mol Biol 2005; 58:333-49. PMID:16021399; http://dx.doi.org/10.1007/s11103-005-4526-7.
58. Chen RZ, Zhao X, Shao Z, Wei Z, Wang Y, Zhu L, et al. Rice UDP-glucose pyrophosphorylase1 is essential for pollen callose deposition and its cosuppression results in a new type of thermosensitive genic male sterility. Plant Cell 2007; 19:847-61. PMID:17400897; http://dx.doi.org/10.1105/tpc.106.044123.
59. Ressayre A, Raquin C, Mignot A, Godelle B, Gouyon PH. Correlated variation in microtubule distribution, callose deposition during male post-meiotic cytokinesis, and pollen aperture number across Nicotiana species (Solanaceae). Am J Bot 2002; 89:393-400. PMID:21665634; http://dx.doi.org/10.3732/ajb.89.3.393.
60. Albert B, Nadot S, Dreyer L, Ressayre A. The influence of tetrad shape and intersporal callose wall formation on pollen aperture pattern ontogeny in two eudicot species. Ann Bot 2010; 106:557-64. PMID:20685726; http://dx.doi.org/10.1093/aob/mcq152.
61. Albert B, Ressayre A, Nadot S. Correlation between pollen aperture pattern and callose deposition in late tetrad stage in three species producing atypical pollen grains. Am J Bot 2011; 98:189-96. PMID:21613108; http://dx.doi.org/10.3732/ajb.1000195.
62. Zuo JR, Niu QW, Nishizawa N, Wu Y, Kost B, Chua NH. KORRIGAN, an Arabidopsis endo-1,4-betaglucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell 2000; 12:1137-52. PMID:10899980.
63. Lukowitz W, Mayer U, Jürgens G. Cytokinesis in the Arabidopsis embryo involves the syntaxin-related KNOLLE gene product. Cell 1996; 84:61-71. PMID:8548827; http://dx.doi.org/10.1016/S0092-8674(00)80993-9.
64. Lauber MH, Waizenegger I, Steinmann T, Schwarz H, Mayer U, Hwang I, et al. The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J Cell Biol 1997; 139:1485-93. PMID:9396754; http://dx.doi.org/10.1083/jcb.139.6.1485.
65. Hulskamp M, Parekh NS, Grini P, Schneitz K, Zimmermann I, Lolle SJ, et al. The STUD gene is required for male-specific cytokinesis after telophase II of meiosis in Arabidopsis thaliana. Dev Biol 1997; 187:114-24. PMID:9224679; http://dx.doi.org/10.1006/dbio.1997.8554.
66. Spielman M, Preuss D, Li FL, Browne WE, Scott RJ, Dickinson HG. TETRASPORE is required for male meiotic cytokinesis in Arabidopsis thaliana. Development 1997; 124:2645-57. PMID:9217006.
67. Soyano T, Nishihama R, Morikiyo K, Ishikawa M, Machida Y. NQK1/NtMEK1 is a MAPKK that acts in the NPK1 MAPKKK-mediated MAPK cascade and is required for plant cytokinesis. Genes Dev 2003; 17:1055-67. PMID:12704083; http://dx.doi.org/10.1101/gad.1071103.
68. Kosetsu K, Matsunaga S, Nakagami H, Colcombet J, Sasabe M, Soyano T, et al. The MAP kinase MPK4 is required for cytokinesis in Arabidopsis thaliana. Plant Cell 2010; 22:3778-90. PMID:21098735; http://dx.doi.org/10.1105/tpc.110.077164.
69. Kim AJ, Endow SA. A kinesin family tree. J Cell Sci 2000; 113:3681-2. PMID:11034894.
70. Strompen G, El Kasmi F, Richter S, Lukowitz W, Assaad FF, Jürgens G, et al. The Arabidopsis HINKEL gene encodes a kinesin-related protein involved in cytokinesis and is expressed in a cell cycle-dependent manner. Curr Biol 2002; 12:153-8. PMID:11818068; http://dx.doi.org/10.1016/S0960-9822(01)00655-8.
71. Nishihama R, Soyano T, Ishikawa M, Araki S, Tanaka H, Asada T, et al. Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex. Cell 2002; 109:87-99. PMID:11955449; http://dx.doi.org/10.1016/S0092-8674(02)00691-8.
72. Takahashi Y, Soyano T, Kosetsu K, Sasabe M, Machida Y. HINKEL kinesin, ANP MAPKKKs and MKK6/ANQ MAPKK, which phosphorylates and activates MPK4 MAPK, constitute a pathway that is required for cytokinesis in Arabidopsis thaliana. Plant Cell Physiol 2010; 51:1766-76. PMID:20802223; http://dx.doi.org/10.1093/pcp/pcq135.
73. Petersen M, Brodersen P, Naested H, Andreasson E, Lindhart U, Johansen B, et al. Arabidopsis map kinase 4 negatively regulates systemic acquired resistance. Cell 2000; 103:1111-20. PMID:11163186; http://dx.doi.org/10.1016/S0092-8674(00)00213-0.
74. Zeng QN, Chen JG, Ellis BE. AtMPK4 is required for male-specific meiotic cytokinesis in Arabidopsis. Plant J 2011; 67:895-906. PMID:21575092; http://dx.doi.org/10.1111/j.1365-313X.2011.04642.x.
75. Krysan PJ, Jester PJ, Gottwald JR, Sussman MR. An Arabidopsis mitogen-activated protein kinase kinase kinase gene family encodes essential positive regulators of cytokinesis. Plant Cell 2002; 14:110-920. PMID:12034900; http://dx.doi.org/10.1105/tpc.001164.
76. Sasabe M, Kosetsu K, Hidaka M, Murase A, Machida Y. Arabidopsis thaliana MAP65-1 and MAP65-2 function redundantly with MAP65-3/PLEIADE in cytokinesis downstream of MPK4. Plant Signal Behav 2011; 6:743-7. PMID:21455028; http://dx.doi.org/10.4161/psb.6.5.15146.
77. Sasabe M, Soyano T, Takahashi Y, Sonobe S, Igarashi H, Itoh TJ, et al. Phosphorylation of NtMAP651 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells. Genes Dev 2006; 20:1004-14. PMID:16598040; http://dx.doi.org/10.1101/gad.1408106.
78. Mao TL, Jin L, Li H, Liu B, Yuan M. Two microtubule-associated proteins of the Arabidopsis MAP65 family function differently on microtubules. Plant Physiol 2005; 138:654-62. PMID:15908607; http://dx.doi.org/10.1104/pp.104.052456.
79. Smertenko AP, Chang HY, Wagner V, Kaloriti D, Fenyk S, Sonobe S, et al. The Arabidopsis microtubule-associated protein AtMAP65-1: molecular analysis of its microtubule bundling activity. Plant Cell 2004; 16:2035-47. PMID:15273298; http://dx.doi.org/10.1105/tpc.104.023937.
80. Van Damme D, Van Poucke K, Boutant E, Ritzenthaler C, Inzé D, Geelen D. In vivo dynamics and differential microtubule-binding activities of MAP65 proteins. Plant Physiol 2004; 136:3956-67. PMID:15557096; http://dx.doi.org/10.1104/pp.104.051623.
81. Gaillard J, Neumann E, Van Damme D, Stoppin-Mellet V, Ebel C, Barbier E, et al. Two microtubuleassociated proteins of Arabidopsis MAP65s promote antiparallel microtubule bundling. Mol Biol Cell 2008; 19:4534-44. PMID:18667529; http://dx.doi.org/10.1091/mbc.E08-04-0341.
82. Li H, Mao T, Zhang Z, Yuan M. The AtMAP65- 1 cross-bridge between microtubules is formed by one dimer. Plant Cell Physiol 2007; 48:866-74. PMID:17504815; http://dx.doi.org/10.1093/pcp/pcm059.
83. Ho CMK, Hotta T, Guo F, Roberson RW, Lee YR, Liu B. Interaction of antiparallel microtubules in the phragmoplast is mediated by the microtubuleassociated protein MAP65-3 in Arabidopsis. Plant Cell 2011; 23:2909-23. PMID:21873565; http://dx.doi.org/10.1105/tpc.110.078204.
84. Ho CMK, Lee YR, Kiyama LD, Dinesh-Kumar SP, Liu B. Arabidopsis microtubule-associated protein MAP65-3 cross-links antiparallel microtubules toward their plus ends in the phragmoplast via its distinct C-terminal microtubule binding domain. Plant Cell 2012; 24:2071-85. PMID:22570443; http://dx.doi.org/10.1105/tpc.111.092569.
85. Mao GJ, Chan J, Calder G, Doonan JH, Lloyd CW. Modulated targeting of GFP-AtMAP65-1 to central spindle microtubules during division. Plant J 2005; 43:469-78. PMID:16098102; http://dx.doi.org/10.1111/j.1365-313X.2005.02464.x.
86. Müller S, Smertenko A, Wagner V, Heinrich M, Hussey PJ, Hauser MT. The plant microtubule-associated protein AtMAP65-3/PLE is essential for cytokinetic phragmoplast function. Curr Biol 2004; 14:412-7. PMID:15028217; http://dx.doi.org/10.1016/j.cub.2004.02.032.
87. Liu Z, Makaroff CA. Arabidopsis separase AESP is essential for embryo development and the release of cohesin during meiosis. Plant Cell 2006; 18:1213-25. PMID:16582011; http://dx.doi.org/10.1105/tpc.105.036913.
88. Yang XH, Boateng KA, Strittmatter L, Burgess R, Makaroff CA. Arabidopsis separase functions beyond the removal of sister chromatid cohesion during meiosis. Plant Physiol 2009; 151:323-33. PMID:19592426; http://dx.doi.org/10.1104/pp.109.140699.
89. Yang XH, Boateng KA, Yuan L, Wu S, Baskin TI, Makaroff CA. The radially swollen 4 separase mutation of Arabidopsis thaliana blocks chromosome disjunction and disrupts the radial microtubule system in meiocytes. PLoS ONE 2011; 6:e19459. PMID:21559383; http://dx.doi.org/10.1371/journal.pone.0019459.
90. Yang M, Ma H. Male meiotic spindle lengths in normal and mutant arabidopsis cells. Plant Physiol 2001; 126:622-30. PMID:11402192; http://dx.doi.org/10.1104/pp.126.2.622.
91. Staiger CJ, Cande WZ. Microtubule distribution in dv, a maize meiotic mutant defective in the prophase to metaphase transition. Dev Biol 1990; 138:231-42. PMID:2407578; http://dx.doi.org/10.1016/0012-1606(90)90193-M.
92. Verma DPS, Hong ZL. Plant callose synthase complexes. Plant Mol Biol 2001; 47:693-701. PMID:11785931; http://dx.doi.org/10.1023/A:1013679111111.
93. Hong ZL, Delauney AJ, Verma DP. A cell plate-specific callose synthase and its interaction with phragmoplastin. Plant Cell 2001; 13:755-68. PMID:11283334
94. Andrawis A, Solomon M, Delmer DP. Cotton fiber annexins: a potential role in the regulation of callose synthase. Plant J 1993; 3:763-72. PMID:8401609; http://dx.doi.org/10.1111/j.1365-313X.1993.00763.x.
95. Amor Y, Haigler CH, Johnson S, Wainscott M, Delmer DP. A membrane-associated form of sucrose synthase and its potential role in synthesis of cellulose and callose in plants. Proc Natl Acad Sci USA 1995; 92:9353-7. PMID:7568131; http://dx.doi.org/10.1073/pnas.92.20.9353.
96. Jacobs AK, Lipka V, Burton RA, Panstruga R, Strizhov N, Schulze-Lefert P, et al. An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 2003; 15:2503-13. PMID:14555698; http://dx.doi.org/10.1105/tpc.016097.
97. Ostergaard L, Petersen M, Mattsson O, Mundy J. An Arabidopsis callose synthase. Plant Mol Biol 2002; 49:559-66. PMID:12081364; http://dx.doi.org/10.1023/A:1015558231400.
98. Tang ZH, Zhang L, Yang D, Zhao C, Zheng Y. Cold stress contributes to aberrant cytokinesis during male meiosis I in a wheat thermosensitive genic male sterile line. Plant Cell Environ 2011; 34:389-405. PMID:21062315; http://dx.doi.org/10.1111/j.1365-3040.2010.02250.x.
99. Xu C, Liu Z, Zhang L, Zhao C, Yuan S, Zhang F.organization of actin cytoskeleton during meiosis I in a wheat thermo-sensitive genic male sterile line. Protoplasma 2012. PMID:22350736; http://dx.doi.org/10.1007/s00709-012-0386-6.
100. De Storme N, Copenhaver GP, Geelen D. Production of diploid male gametes in Arabidopsis by cold-induced destabilization of postmeiotic radial microtubule arrays. Plant Physiol 2012; 160:1808-26. PMID:23096158; http://dx.doi.org/10.1104/pp.112.208611.
101. Mason AS, Nelson MN, Yan G, Cowling WA. Production of viable male unreduced gametes in Brassica interspecific hybrids is genotype specific and stimulated by cold temperatures. BMC Plant Biol 2011; 11:103. PMID:21663695; http://dx.doi.org/10.1186/1471-2229-11-103.