Induction of embryogenesis in brassica napus microspores produces a callosic subintinal layer and abnormal cell walls with altered levels of callose and cellulose

Frontiers in Plant Science

Volumn 6, Issue NOVEMBER, 2015, Pages 1-17

  Parra Vega, Verónica ^a   Corral Martínez, Patricia ^a   Rivas Sendra, Alba ^a   Seguí Simarro, Jose M ^a  

^a UNIVERSITAT POLITÈCNICA DE VALÈNCIA   (Spain)

Author keywords

Androgenesis; Benzyl alcohol; Caffeine; Cell wall carbohydrates; Doubled haploids; Microspore embryogenesis; Rapeseed

Indexed keywords

EID: 84948736545     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2015.01018     Document Type: Article

References (91)

1. Abdollahi, M. R., Ghazanfari, P., Corral-Martínez, P., Moieni, A., and Seguí- Simarro, J. M. (2012). Enhancing secondary embryogenesis in Brassica napus by selecting hypocotyl-derived embryos and using plant-derived smoke extract in culture medium. Plant Cell Tissue Organ Cult. 110, 307-315. doi: 10.1007/s11240-012-0152-7
2. Abramova, L. I., Avalkina, N. A., Golubeva, E. A., Pyzhenkova, Z. S., and Golubovskaya, I. N. (2003). Synthesis and deposition of callose in anthers and ovules of meiotic mutants of maize (Zea mays). Russ. J. Plant Physiol. 50, 324-329. doi: 10.1023/a:1023866019102
3. Albersheim, P., Darvill, A., Roberts, K., Sederoff, R., and Staehelin, A. (2011). Plant Cell Walls. New York, NY: Garland Science.
4. Anderson, C. T., Carroll, A., Akhmetova, L., and Somerville, C. (2010). Real-time imaging of cellulose reorientation during cell wall expansion in Arabidopsis roots. Plant Physiol. 152, 787-796. doi: 10.1104/pp.109.150128
5. Austin, J. R., Seguí-Simarro, J. M., and Staehelin, L. A. (2005). Quantitative analysis of changes in spatial distribution and plus-end geometry of microtubules involved in plant-cell cytokinesis. J. Cell Sci. 118, 3895-3903. doi: 10.1242/jcs.02512
6. Barany, I., Fadon, B., Risueno, M. C., and Testillano, P. S. (2010). Cell wall components and pectin esterification levels as markers of proliferation and differentiation events during pollen development and pollen embryogenesis in Capsicum annuum L. J. Exp. Bot. 61, 1159-1175. doi: 10.1093/jxb/erp392
7. Beeckman, T., Przemeck, G. K. H., Stamatiou, G., Lau, R., Terryn, N., De Rycke, R., et al. (2002). Genetic complexity of cellulose synthase a gene function in Arabidopsis embryogenesis. Plant Physiol. 130, 1883-1893. doi: 10.1104/pp.102.010603
8. Borderies, G., Le Bechec, M., Rossignol, M., Lafitte, C., Le Deunff, E., Beckert, M., et al. (2004). Characterization of proteins secreted during maize microspore culture: arabinogalactan proteins (AGPs) stimulate embryo development. Eur. J. Cell Biol. 83, 205-212. doi: 10.1078/0171-9335-00378
9. Brown, R. C., and Lemmon, B. E. (1991). Pollen development in orchids. 3. A novel generative pole microtubule system predicts unequal pollen mitosis. J. Cell Sci. 99, 273-281.
10. Brown, R. C., and Lemmon, B. E. (2009). "Callose in cell division," in Chemistry, Biochemistry, and Biology of (1-3)-b-Glucans and Related Polysaccharides, eds A. Bacic, G. B. Fincher, and B. A. Stone (Amsterdam: Elsevier Science), 425-438.
11. Carpita, N. C., and McCann, M. C. (2000). "Chapter 2: the cell wall," in Biochemistry and Molecular Biology of Plants, eds B. B. Buchanan, W. Gruissem, and R. L. Jones (Rockville, MD: American Society of Plant Physiologists).
12. Chen, X.-Y., and Kim, J.-Y. (2009). Callose synthesis in higher plants. Plant Signal. Behav. 4, 1-4.
13. Corral-Martínez, P., Nuez, F., and Seguí-Simarro, J. M. (2011). Genetic, quantitative and microscopic evidence for fusion of haploid nuclei and growth of somatic calli in cultured ms1035 tomato anthers. Euphytica 178, 215-228. doi: 10.1007/s10681-010-0303-z
14. Corral-Martínez, P., Parra-Vega, V., and Seguí-Simarro, J. M. (2013). Novel features of Brassica napus embryogenic microspores revealed by high pressure freezing and freeze substitution: evidence for massive autophagy and excretion-based cytoplasmic cleaning. J. Exp. Bot. 64, 3061-3075. doi: 10.1093/jxb/ert151
15. Custers, J. (2003). "Microspore culture in rapeseed (Brassica napus L.)," in Doubled Haploid Production in Crop Plants, eds M. Maluszynski, K. J. Kasha, B. P. Forster, and I. Szarejko (Dordrecht: Kluwer Academic Publishers), 185-193.
16. Custers, J. B. M., Cordewener, J. H. G., Nöllen, Y., Dons, J. J., and Van Lookeren-Campagne, M. M. (1994). Temperature controls both gametophytic and sporophytic development in microspore cultures of Brassica napus. Plant Cell Rep. 13, 267-271. doi: 10.1007/BF00233317
17. De Storme, N., De Schrijver, J., Van Criekinge, W., Wewer, V., Dörmann, P., and Geelen, D. (2013). GLUCAN SYNTHASE-LIKE8 and STEROL METHYLTRANSFERASE2 are required for ploidy consistency of the sexual reproduction system in Arabidopsis. Plant Cell 25, 387-403. doi: 10.1105/tpc.112.106278
18. Dong, X., Hong, Z., Sivaramakrishnan, M., Mahfouz, M., and Verma, D. P. S. (2005). Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis. Plant J. 42, 315-328. doi: 10.1111/j.1365-313X.2005.02379.x
19. Drakakaki, G. (2015). Polysaccharide deposition during cytokinesis: challenges and future perspectives. Plant Sci. 236, 177-184. doi: 10.1016/j.plantsci.2015.03.018
20. Dubas, E., Custers, J., Kieft, H., Wedzony, M., and Van Lammeren, A. A. (2013). Characterization of polarity development through 2- and 3-D imaging during the initial phase of microspore embryogenesis in Brassica napus L. Protoplasma 251, 103-113. doi: 10.1007/s00709-013-0530-y
21. Dubois, T., Guedira, M., Dubois, J., and Vasseur, J. (1991). Direct somatic embryogenesis in leaves of Cichorium: a histological and SEM study of early stages. Protoplasma 162, 120-127. doi: 10.1007/BF02562555
22. El-Tantawy, A.-A., Solís, M.-T., Costa, M. L., Coimbra, S., Risueño, M.-C., and Testillano, P. S. (2013). Arabinogalactan protein profiles and distribution patterns during microspore embryogenesis and pollen development in Brassica napus. Plant Reprod. 26, 231-243. doi: 10.1007/s00497-013-0217-8
23. Evans, N. A., Hoyne, P. A., and Stone, B. A. (1984). Characteristics and specificity of the interaction of a fluorochrome from aniline blue (Sirofluor) with polysaccharides. Carbohydr. Polym. 4, 215-230. doi: 10.1016/0144-8617(84)90012-2
24. Ferguson, C, Teeri, T. T, Siika-Aho, M, Read, S. M., and Bacic, A. (1998). Location of cellulose and callose in pollen tubes and grains of Nicotiana tabacum. Planta 206, 452-460. doi: 10.1007/s004250050421
25. Forster, B. P., Heberle-Bors, E., Kasha, K. J., and Touraev, A. (2007). The resurgence of haploids in higher plants. Trends Plant Sci. 12, 368-375. doi: 10.1016/j.tplants.2007.06.007
26. Fortes, A. M., Testillano, P. S., Risueno, M. D., and Pais, M. S. (2002). Studies on callose and cutin during the expression of competence and determination for organogenic nodule formation from internodes of Humulus lupulus var. Nugget. Physiol. Plant. 116, 113-120. doi: 10.1034/j.1399-3054.2002.1160114.x
27. Gilkey, J. C., and Staehelin, L. A. (1986). Advances in ultrarapid freezing for the preservation of cellular ultrastructure. J. Electron Microsc. Tech. 3, 177-210. doi: 10.1002/jemt.1060030206
28. Gong, M., Van Der Luit, A. H., Knight, M. R., and Trewavas, A. J. (1998). Heat-shock-induced changes in intracellular Ca2+ level in tobacco seedlings in relation to thermotolerance. Plant Physiol. 116, 429-437. doi: 10.1104/pp.116.1.429
29. González-Melendi, P., Ramírez, C., Testillano, P. S., Kumlehn, J., and Risueño, M. C. (2005). Three dimensional confocal and electron microscopy imaging define the dynamics and mechanisms of diploidisation at early stages of barley microspore-derived embryogenesis. Planta 222, 47-57. doi: 10.1007/s00425-005-1515-7
30. González-Melendi, P., Testillano, P. S., Ahmadian, P., Fadón, B., Vicente, O., and Risueño, M. C. (1995). In situ characterization of the late vacuolate microspore as a convenient stage to induce embryogenesis in Capsicum. Protoplasma 187, 60-71. doi: 10.1007/BF01280233
31. Gorska-Brylass, A. (1967). Transitory callose envelope surrounding the generative cell in pollen grains. Acta Soc. Bot. Pol. 36, 419-422. doi: 10.5586/asbp.1967.038
32. Hayashi, T., Read, S. M., Bussell, J., Thelen, M., Lin, F. C., Brown, R. M., et al. (1987). UDP-glucose: (1-- > 3)-beta-glucan synthases from mung bean and cotton: differential effects of Ca and Mg on enzyme properties and on macromolecular structure of the glucan product. Plant Physiol. 83, 1054-1062. doi: 10.1104/pp.83.4.1054
33. Heslop-Harrison, J. (1968). Synchronous pollen mitosis and the formation of the generative cell in massulate orchids. J. Cell Sci. 3, 457-466.
34. Heslop-Harrison, J. (1979). Aspects of the structure, cytochemistry and germination of the pollen of rye (Secale cereale L.). Ann. Bot. 44(Suppl. 1), 1-47.
35. Heslop-Harrison, J., and Mackenzie, A. (1967). Autoradiography of soluble [2-I4C] thymidine derivatives during meiosis and microsporogenesis in Lilium anthers. J. Cell Sci. 2, 387-400.
36. Horvath, I., Glatz, A., Nakamoto, H., Mishkind, M. L., Munnik, T., Saidi, Y., et al. (2012). Heat shock response in photosynthetic organisms: membrane and lipid connections. Prog. Lipid Res. 51, 208-220. doi: 10.1016/j.plipres.2012.02.002
37. Hughes, J. E., and Gunning, B. E. S. (1980). Glutaraldehyde-induced deposition of callose. Can. J. Bot. 58, 250-258. doi: 10.1139/b80-025
38. Kakimoto, T., and Shibaoka, H. (1992). Synthesis of polysaccharides in phragmoplasts isolated from tobacco BY-2 cells. Plant Cell Physiol. 33, 353-361.
39. Kasha, K. J., Hu, T. C., Oro, R., Simion, E., and Shim, Y. S. (2001). Nuclear fusion leads to chromosome doubling during mannitol pretreatment of barley (Hordeum vulgare L.) microspores. J. Exp. Bot. 52, 1227-1238. doi: 10.1093/jexbot/52.359.1227
40. Levy, A., Erlanger, M., Rosenthal, M., and Epel, B. L. (2007). A plasmodesmata- associated beta-1,3-glucanase in Arabidopsis. Plant J. 49, 669-682. doi: 10.1111/j.1365-313X.2006.02986.x
41. Lichter, R. (1982). Induction of haploid plants from isolated pollen of Brassica napus. Z. Pflanzenphysiol. 105, 427-434. doi: 10.1016/S0044-328X(82)80040-8
42. Maheswaran, G., and Williams, E. G. (1985). Origin and development of somatic embryoids formed directly on immature embryos of Trifolium repens in vitro. Ann. Bot. 56, 619-630.
43. Malik, M. R., Wang, F., Dirpaul, J. M., Zhou, N., Polowick, P. L., Ferrie, A. M. R., et al. (2007). Transcript profiling and identification of molecular markers for early microspore embryogenesis in Brassica napus. Plant Physiol. 144, 134-154. doi: 10.1104/pp.106.092932
44. Maraschin, S. D., Vennik, M., Lamers, G. E. M., Spaink, H. P., and Wang, M. (2005). Time-lapse tracking of barley androgenesis reveals position-determined cell death within pro-embryos. Planta 220, 531-540. doi: 10.1007/s00425-004-1371-x
45. Mayer, U., Herzog, U., Berger, F., Inze, D., and Jürgens, G. (1999). Mutations in the pilz group genes disrupt the microtubule cytoskeleton and uncouple cell cycle progression from cell division in Arabidopsis embryo and endosperm. Eur. J. Cell Biol. 78, 100-108. doi: 10.1016/S0171-9335(99)80011-9
46. Meikle, P. J., Bonig, I., Hoogenraad, N. J., Clarke, A. E., and Stone, B. A. (1991). The location of (1→3)-b-glucans in the walls of pollen tubes of Nicotiana alata using a (1→3)-b-glucan-specific monoclonal antibody. Planta 185, 1-8. doi: 10.1007/BF00194507
47. Muller, S., Fuchs, E., Ovecka, M., Wysocka-Diller, J., Benfey, P. N., and Hauser, M. T. (2002). Two new loci, PLEIADE and HYADE, implicate organ-specific regulation of cytokinesis in Arabidopsis. Plant Physiol. 130, 312-324. doi: 10.1104/pp.004416
48. Nickle, T. C., and Meinke, D. W. (1998). A cytokinesis-defective mutant of Arabidopsis (cyt1) characterized by embryonic lethality, incomplete cell walls, and excessive callose accumulation. Plant J. 15, 321-332. doi: 10.1046/j.1365-313X.1998.00212.x
49. Otegui, M. S., and Staehelin, L. A. (2000). Cytokinesis in flowering plants: more than one way to divide a cell. Curr. Opin. Plant Biol. 3, 493-502. doi: 10.1016/S1369-5266(00)00119-9
50. Park, S. K., and Twell, D. (2001). Novel patterns of ectopic cell plate growth and lipid body distribution in the Arabidopsis gemini pollen1 mutant. Plant Physiol. 126, 899-909. doi: 10.1104/pp.126.2.899
51. Pauls, K. P., Chan, J., Woronuk, G., Schulze, D., and Brazolot, J. (2006). When microspores decide to become embryos - cellular and molecular changes. Can. J. Bot. 84, 668-678.
52. Pedroso, M. C., and Pais, M. S. (1992). A scanning electron-microscopy and X-ray-microanalysis study during induction of morphogenesis in Camellia japonica L. Plant Sci. 87, 99-108. doi: 10.1016/0168-9452(92)90197-t
53. Pickett-Heaps, J. D., and Northcote, D. H. (1966). Organization of microtubules and endoplasmic reticulum during mitosis and cytokinesis in wheat meristems. J. Cell Sci. 1, 109-120.
54. Rashid, A., Siddiqui, A. W., and Reinert, J. (1982). Subcellular aspects of origin and structure of pollen embryos of Nicotiana. Protoplasma 113, 202-208. doi: 10.1007/bf01280908
55. Saidi, Y., Finka, A., Muriset, M., Bromberg, Z., Weiss, Y. G., Maathuis, F. J. M., et al. (2009). The heat shock response in moss plants is regulated by specific calcium-permeable channels in the plasma membrane. Plant Cell 21, 2829-2843. doi: 10.1105/tpc.108.065318
56. Samuels, A. L., Giddings, T. H. Jr., and Staehelin, L. A. (1995). Cytokinesis in tobacco BY-2 and root tip cells: a new model of cell plate formation in higher plants. J. Cell Biol. 130, 1345-1357. doi: 10.1083/jcb.130.6.1345
57. Samuels, A. L., and Staehelin, L. A. (1996). Caffeine inhibits cell plate formation by disrupting membrane reorganization just after the vesicle fusion step. Protoplasma 195, 144-155. doi: 10.1007/BF01279193
58. Sangwan, V., Foulds, I., Singh, J., and Dhindsa, R. S. (2001). Cold-activation of Brassica napus BN115 promoter is mediated by structural changes in membranes and cytoskeleton, and requires Ca2+ influx. Plant J. 27, 1-12. doi: 10.1046/j.1365-313x.2001.01052.x
59. Sato, S., Katoh, N., Iwai, S., and Hagimori, M. (2005). Frequency of spontaneous polyploidization of embryos regenerated from cultured anthers or microspores of Brassica rapa var. pekinensis L. and B. oleracea var. capitata L. Breed. Sci. 55, 99-102. doi: 10.1270/jsbbs.55.99
60. Schulze, D., and Pauls, K. P. (2002). Flow cytometric analysis of cellulose tracks development of embryogenic Brassica cells in microspore cultures. New Phytol. 154, 249-254. doi: 10.1046/j.1469-8137.2002.00350.x
61. Seguí-Simarro, J. M., Austin, J. R., White, E. A., and Staehelin, L. A. (2004).Electron tomographic analysis of somatic cell plate formation in meristematic cells of Arabidopsis preserved by high-pressure freezing. Plant Cell 16, 836-856. doi: 10.1105/tpc.017749
62. Seguí-Simarro, J. M., Bárány, I., Suárez, R., Fadón, B., Testillano, P. S., and Risueño, M. C. (2006). Nuclear bodies domain changes with microspore reprogramming to embryogenesis. Eur. J. Histochem. 50, 35-44.
63. Seguí-Simarro, J. M., and Nuez, F. (2007). Embryogenesis induction, callogenesis, and plant regeneration by in vitro culture of tomato isolated microspores and whole anthers. J. Exp. Bot. 58, 1119-1132. doi: 10.1093/jxb/erl271
64. Seguí-Simarro, J. M., and Nuez, F. (2008a). How microspores transform into haploid embryos: changes associated with embryogenesis induction and microspore-derived embryogenesis. Physiol. Plant. 134, 1-12. doi: 10.1111/j.1399-3054.2008.01113.x
65. Seguí-Simarro, J. M., and Nuez, F. (2008b). Pathways to doubled haploidy: chromosome doubling during androgenesis. Cytogenet. Genome Res. 120, 358-369. doi: 10.1159/000121085
66. Seguí-Simarro, J. M., Otegui, M. S., Austin, J. R., and Staehelin, L. A. (2008). "Plant cytokinesis - insights gained from electron tomography studies," in Cell Division Control in Plants, eds D. P. S. Verma and Z. Hong (Berlin: Springer), 251-287.
67. Seguí-Simarro, J. M., Testillano, P. S., and Risueño, M. C. (2003). Hsp70 and Hsp90 change their expression and subcellular localization after microspore embryogenesis induction in Brassica napus L. cv Topas. J. Struct. Biol. 142, 379-391. doi: 10.1016/S1047-8477(03)00067-4
68. Shariatpanahi, M. E., Bal, U., Heberle-Bors, E., and Touraev, A. (2006). Stresses applied for the re-programming of plant microspores towards in vitro embryogenesis. Physiol. Plant. 127, 519-534. doi: 10.1111/j.1399-3054.2006.00675.x
69. Shi, X., Sun, X., Zhang, Z., Feng, D., Zhang, Q., Han, L., et al. (2014). GLUCAN SYNTHASE-LIKE 5 (GSL5) plays an essential role in male fertility by regulating callose metabolism during microsporogenesis in rice. Plant Cell Physiol. 56, 497-509. doi: 10.1093/pcp/pcu193
70. Simmonds, D. H., and Keller, W. A. (1999). Significance of preprophase bands of microtubules in the induction of microspore embryogenesis of Brassica napus. Planta 208, 383-391. doi: 10.1007/s004250050573
71. Sitte, P. (1953). Untersuchungen zur submikroskopischen morphologie der pollen und sporoenmembranen. Microskopie 8, 290-299.
72. Solis, M.-T., Pintos, B., Prado, M.-J., Bueno, M.-A., Raska, I., Risueno, M.- C., et al. (2008). Early markers of in vitro microspore reprogramming to embryogenesis in olive (Olea europaea L.). Plant Sci. 174, 597-605. doi: 10.1016/j.plantsci.2008.03.014
73. Stone, B. A., and Clarke, A. E. (1992). "Chemistry and physiology of higher plant 1,3-β-glucans (callose)," in Chemistry and Biology of (1-3)-β-Glucans, eds B. A. Stone and A. E. Clarke (Bundoora, VIC: La Trobe University Press), 365-429.
74. Strompen, G., El Kasmi, F., Richter, S., Lukowitz, W., Assaad, F. F., Jürgens, G., et al. (2002). The Arabidopsis HINKEL gene encodes a kinesin-related protein involved in cytokinesis and is expressed in a cell cycle-dependent manner. Curr. Biol. 12, 153-158. doi: 10.1016/S0960-9822(01)00655-8
75. Sunderland, N., and Dunwell, J. M. (1974). "Anther and pollen culture," in Plant Tissue and Cell Culture, ed. H. E. Street (Oxford: Blackwell Scientific Publications), 223-265.
76. Suzuki, T., Fujikura, K., Higashiyama, T., and Takata, K. (1997). DNA staining for fluorescence and laser confocal microscopy. J. Histochem. Cytochem. 45, 49-53. doi: 10.1177/002215549704500107
77. Telmer, C. A., Newcomb, W., and Simmonds, D. H. (1993). Microspore development in Brassica napus and the effect of high temperature on division in vivo and in vitro. Protoplasma 172, 154-165. doi: 10.1007/BF01379373
78. Telmer, C. A., Newcomb, W., and Simmonds, D. H. (1995). Cellular changes during heat shock induction and embryo development of cultured microspores of Brassica napus cv. Topas. Protoplasma 185, 106-112. doi: 10.1007/BF01272758
79. Testillano, P. S., Georgiev, S., Mogensen, H. L., Coronado, M. J., Dumas, C., Risueno, M. C., et al. (2004). Spontaneous chromosome doubling results from nuclear fusion during in vitro maize induced microspore embryogenesis. Chromosoma 112, 342-349. doi: 10.1007/s00412-004-0279-3
80. Thomas, J., Ingerfeld, M., Nair, H., Chauhan, S. S., and Collings, D. A. (2013). Pontamine fast scarlet 4B: a new fluorescent dye for visualising cell wall organisation in radiata pine tracheids. Wood Sci. Technol. 47, 59-75. doi: 10.1007/s00226-012-0483-x
81. Van Lammeren, A. A. M., Keijzer, C. J., Willemse, M. T., and Kieft, H. (1985). Structure and function of the microtubular cytoskeleton during pollen development in Gasteria verrucosa (Mill) H. Duval. Planta 165, 1-11. doi: 10.1007/BF00392205
82. Vaughn, K. C., Hoffman, J. C., Hahn, M. G., and Staehelin, L. A. (1996). The herbicide dichlobenil disrupts cell plate formation: immunogold characterization. Protoplasma 194, 117-132. doi: 10.1007/bf01882020
83. Verma, D. P. S. (2001). Cytokinesis and building of the cell plate in plants. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 751-784. doi: 10.1146/annurev.arplant.52.1.751
84. Verma, D. P. S., and Hong, Z. (2001). Plant callose synthase complexes. Plant Mol. Biol. 47, 693-701. doi: 10.1023/A:1013679111111
85. Worden, N., Park, E., and Drakakaki, G. (2012). Trans-Golgi network: an intersection of trafficking cell wall components. J. Integr. Plant Biol. 54, 875-886. doi: 10.1111/j.1744-7909.2012.01179.x
86. Xie, B., Deng, Y., Kanaoka, M. M., Okada, K., and Hong, Z. (2012). Expression of Arabidopsis callose synthase 5 results in callose accumulation and cell wall permeability alteration. Plant Sci. 183, 1-8. doi: 10.1016/j.plantsci.2011.10.015
87. You, X. L., Yi, J. S., and Choi, Y. E. (2006). Cellular change and callose accumulation in zygotic embryos of Eleutherococcus senticosus caused by plasmolyzing pretreatment result in high frequency of single-cell-derived somatic embryogenesis. Protoplasma 227, 105-112. doi: 10.1007/s00709-006- 0149-3
88. Zaki, M. A., and Dickinson, H. G. (1990). Structural changes during the first divisions of embryos resulting from anther and free microspore culture in Brassica napus. Protoplasma 156, 149-162. doi: 10.1007/BF01560653
89. Zaki, M. A. M., and Dickinson, H. G. (1991). Microspore-derived embryos in Brassica: the significance of division symmetry in pollen mitosis I to embryogenic development. Sex. Plant Reprod. 4, 48-55. doi: 10.1007/BF00194572
90. Zhang, C., Guinel, F. C., and Moffatt, B. A. (2002). A comparative ultrastructural study of pollen development in Arabidopsis thaliana ecotype Columbia and male-sterile mutant apt1-3. Protoplasma 219, 59-71. doi: 10.1007/s007090200006
91. Zuo, J. R., Niu, Q. W., Nishizawa, N., Wu, Y., Kost, B., and Chua, N. H. (2000). KORRIGAN, an Arabidopsis endo-1,4-beta-glucanase, localizes to the cell plate by polarized targeting and is essential for cytokinesis. Plant Cell 12, 1137-1152. doi: 10.2307/3871261