NtDRP is necessary for accurate zygotic division orientation and differentiation of basal cell lineage toward suspensor formation

New Phytologist

Volumn 212, Issue 3, 2016, Pages 598-612

  Zhao, Jing ^a   Xin, Haiping ^a,b   Cao, Lingyan ^c   Huang, Xiaorong ^a   Shi, Ce ^a   Zhao, Peng ^a   Fu, Ying ^c   Sun, Meng Xiang ^a  

^a WUHAN UNIVERSITY   (China)

^b Wuhan Institute of Botany Chinese Academy of Sciences   (China)

^c CHINA AGRICULTURAL UNIVERSITY   (China)

Author keywords

asymmetric cell division; cell fate; dynamin; embryo; microtubule; Nicotiana tabacum; Polyembryony; zygote

Indexed keywords

CELLS AND CELL COMPONENTS; DIFFERENTIATION; EMBRYO; MOLECULAR ANALYSIS; TOBACCO;

NICOTIANA TABACUM;

DYNAMIN; PLANT PROTEIN;

BODY PATTERNING; CELL DIFFERENTIATION; CELL DIVISION; CELL FRACTIONATION; CELL LINEAGE; CELL POLARITY; CYTOLOGY; DOWN REGULATION; EMBRYOLOGY; FERTILIZATION; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MICROTUBULE; PLANT SEED; PROTEIN TRANSPORT; RNA INTERFERENCE; SPINDLE APPARATUS; TOBACCO; ZYGOTE;

BODY PATTERNING; CELL DIFFERENTIATION; CELL DIVISION; CELL LINEAGE; CELL POLARITY; DOWN-REGULATION; DYNAMINS; FERTILIZATION; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE EXPRESSION REGULATION, PLANT; MICROTUBULES; PLANT PROTEINS; PROTEIN TRANSPORT; RNA INTERFERENCE; SEEDS; SPINDLE APPARATUS; SUBCELLULAR FRACTIONS; TOBACCO; ZYGOTE;

EID: 84978254432     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.14060     Document Type: Article

References (55)

1. Abe T, Hashimoto T. 2005. Altered microtubule dynamics by expression of modified alpha-tubulin protein causes right-handed helical growth in transgenic Arabidopsis plants. Plant Journal 43: 191–204.
2. Abrash EB, Bergmann DC. 2009. Asymmetric cell divisions: a view from plant development. Developmental Cell 16: 783–796.
3. Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W. 2009. Paternal control of embryonic patterning in Arabidopsis thaliana. Science 323: 1485–1488.
4. Bibikova TN, Blancaflor EB, Gilroy S. 1999. Microtubules regulate tip growth and orientation in root hairs of Arabidopsis thaliana. Plant Journal 17: 657–665.
5. Castoldi M, Popov AV. 2003. Purification of brain tubulin through two cycles of polymerization-depolymerization in a high-molarity buffer. Protein Expression and Purification 32: 83–88.
6. Chen Z, Gallie DR. 2012. Induction of monozygotic twinning by ascorbic acid in tobacco. PLoS ONE 7: e39147.
7. Dixit R, Cyr R. 2004. Encounters between dynamic cortical microtubules promote ordering of the cortical array through angle-dependent modifications of microtubule behavior. Plant Cell 16: 3274–3284.
8. Espiritu EB, Krueger LE, Ye A, Rose LS. 2012. CLASPs function redundantly to regulate astral microtubules in the C. elegans embryo. Developmental Biology 368: 242–254.
9. Fujimoto M, Arimura S, Ueda T, Takanashi H, Hayashi Y, Nakano A, Tsutsumi N. 2010. Arabidopsis dynamin-related proteins DRP2B and DRP1A participate together in clathrin-coated vesicle formation during endocytosis. Proceedings of the National Academy of Sciences, USA 107: 6094–6099.
10. Geldner N. 2009. Cell polarity in plants: a PARspective on PINs. Current Opinion in Plant Biology 12: 42–48.
11. Hamao K, Morita M, Hosoya H. 2009. New function of the proline rich domain in dynamin-2 to negatively regulate its interaction with microtubules in mammalian cells. Experimental Cell Research 315: 1336–1345.
12. He YC, He YQ, Qu LH, Sun MX, Yang HY. 2007. Tobacco zygotic embryogenesis in vitro: the original cell wall of the zygote is essential for maintenance of cell polarity, the apical-basal axis and typical suspensor formation. Plant Journal 49: 515–527.
13. Heymann JAW, Hinshaw JE. 2009. Dynamins at a glance. Journal of Cell Science 122: 3427–3431.
14. Hong Z, Bednarek SY, Blumwald E, Hwang I, Jurgens G, Menzel D, Osteryoung KW, Raikhel NV, Shinozaki K, Tsutsumi N et al. 2003. A unified nomenclature for Arabidopsis dynamin-related large GTPases based on homology and possible functions. Plant Molecular Biology 53: 261–265.
15. Jeong S, Palmer TM, Lukowitz W. 2011. The RWP-RK factor GROUNDED promotes embryonic polarity by facilitating YODA MAP kinase signaling. Current Biology 21: 1268–1276.
16. Jin JB, Kim YA, Kim SJ, Lee SH, Kim DH, Cheong GW, Hwang I. 2001. A new dynamin-like protein, ADL6, is involved in trafficking from the trans-Golgi network to the central vacuole in Arabidopsis. Plant Cell 13: 1511–1525.
17. Kang BH, Busse JS, Bednarek SY. 2003. Members of the Arabidopsis dynamin-like gene family, ADL1, are essential for plant cytokinesis and polarized cell growth. Plant Cell 15(4): 899–913.
18. Kang BH, Busse JS, Dickey C, Rancour DM, Bednarek SY. 2001. The Arabidopsis cell plate-associated dynamin-like protein, ADL1Ap, is required for multiple stages of plant growth and development. Plant Physiology 126: 47–68.
19. Kay Schneitz MH, Pruitt Robert E. 1995. Wild-type ovule development in Arabidopsis thaliana: a light microscope study of cleared whole-mount tissue. Plant Journal 7: 731–749.
20. Konopka CA, Bednarek SY. 2008. Comparison of the dynamics and functional redundancy of the Arabidopsis dynamin-related isoforms DRP1A and DRP1C during plant development. Plant Physiology 147: 1590–1602.
21. Korolev AV, Buschmann H, Doonan JH, Lloyd CW. 2007. AtMAP70-5, a divergent member of the MAP70 family of microtubule-associated proteins, is required for anisotropic cell growth in Arabidopsis. Journal of Cell Science 120(Pt 13): 2241–2247.
22. Lukowitz W, Roeder A, Parmenter D, Somerville C. 2004. A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116: 109–119.
23. Mao T, Jin L, Li H, Liu B, Yuan M. 2005. Two microtubule-associated proteins of the Arabidopsis MAP65 family function differently on microtubules. Plant Physiology 138: 654–662.
24. Mano S, Nakamori C, Kondo M, Hayashi M, Nishimura M. 2004. An Arabidopsis dynamin-related protein, DRP3A, controls both peroxisomal and mitochondrial division. Plant Journal 38: 487–498.
25. Mayer U, Büttner G, Jürgens G. 1993. Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 117: 149–162.
26. Menke FL, Scheres B. 2009. Plant asymmetric cell division, vive la difference!. Cell 137: 1189–1192.
27. Menon M, Schafer DA. 2013. Dynamin: expanding its scope to the cytoskeleton. International Review of Cell and Molecular Biology 302: 187–219.
28. Miyagishima SY, Kuwayama H, urushihara H Nakanishi H. 2008. Evolutionary linkage between eukaryotic cytokinesis and chloroplast division by dynamin proteins. Proceedings of the National Academy of Sciences, USA 105: 15202-15207.
29. Nakajima K, Furutani I, Tachimoto H, Matsubara H, Hashimoto T. 2004. SPIRAL1 encodes a plant-specific microtubule-localized protein required for directional control of rapidly expanding Arabidopsis cells. Plant Cell 16: 1178–1190.
30. Natesh S, Rau MA. 1984. The embryo. In: Johri BM, ed. Embryology of angiosperms. New York, NY, USA: Springer-Verlag, 567–610.
31. Ning J, Peng XB, Qu LH, Xin HP, Yan TT, Sun MX. 2006. Differential gene expression in egg cells and zygotes suggests that the transcriptome is restructed before the first zygotic division in tobacco. FEBS Letters 580: 1747–1752.
32. Perrin RM, Wang Y, Yuen CY, Will J, Masson PH. 2007. WVD2 is a novel microtubule-associated protein in Arabidopsis thaliana. Plant Journal 49: 961–971.
33. Petricka JJ, Van Norman JM, Benfey PN. 2009. Symmetry breaking in plants: molecular mechanisms regulating asymmetric cell divisions in Arabidopsis. Cold Spring Harbor Perspectives in Biology 1: a000497.
34. Sedbrook JC. 2004. MAPs in plant cells: delineating microtubule growth dynamics and organization. Current Opinion in Plant Biology 7: 632–640.
35. Shoji T, Narita NN, Hayashi K, Asada J, Hamada T, Sonobe S, Nakajima K, Hashimoto T. 2004. Plant-specific microtubule-associated protein SPIRAL2 is required for anisotropic growth in Arabidopsis. Plant Physiology 136: 3933–3944.
36. Shpetner HS, Vallee RB. 1989. Identification of dynamin, a novel mechanochemical enzyme that mediates interactions between microtubules. Cell 59: 421–432.
37. Sierro N, Battey JND, Ouadi S, Bovet L, Goepfert S, Bakaher N, Peitsch MC, Ivanov NV. 2013. Reference genomes and transcriptomes of Nicotiana sylvestris and Nicotiana tomentosiformis. Genome Biology 14: 1–17.
38. Su S, Liu Z, Chen C, Zhang Y, Wang X, Zhu L, Miao L, Wang XC, Yuan M. 2010. Cucumber mosaic virus movement protein severs actin filaments to increase the plasmodesmal size exclusion limit in tobacco. Plant Cell 22: 1373–1387.
39. Tamura K, Dudley J, Nei M, Kumar S. 2007. MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Molecular Biology and Evolution 24: 1596–1599.
40. Taylor NG. 2011. A role for Arabidopsis dynamin related proteins DRP2A/B in endocytosis; DRP2 function is essential for plant growth. Plant Molecular Biology 76: 117–129.
41. Thitamadee S, Tuchihara K, Hashimoto T. 2002. Microtubule basis for left-handed helical growth in Arabidopsis. Nature 417: 193–196.
42. Torres-Ruiz RA, Jurgens G. 1994. Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development 120: 2967–2978.
43. Truernit E, Bauby H, Dubreucq B, Grandjean O, Runions J, Barthelemy J, Palauqui JC. 2008. High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of Phloem development and structure in Arabidopsis. Plant Cell 20: 1494–1503.
44. Twell D, Park SK, Hawkins TJ, Schubert D, Schmidt R, Smertenko A, Hussey PJ. 2002. MOR1/GEM1 has an essential role in the plant-specific cytokinetic phragmoplast. Nature Cell Biology 4: 711–714.
45. Ueda M, Zhang Z, Laux T. 2011. Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Developmental Cell 20: 264–270.
46. Waki T, Hiki T, Watanabe R, Hashimoto T, Nakajima K. 2011. The Arabidopsis RWP-RK protein RKD4 triggers gene expression and pattern formation in early embryogenesis. Current Biology 21: 1277–1281.
47. Walker KL, Muller S, Moss D, Ehrhardt DW, Smith LG. 2007. Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Current Biology 17: 1827–1836.
48. Wang X, Zhu L, Liu B, Wang C, Jin L, Zhao Q, Yuan M. 2007. Arabidopsis MICROTUBULE-ASSOCIATED PROTEIN18 functions in directional cell growth by destabilizing cortical microtubules. Plant Cell 19: 877–889.
49. Wasteneys GO, Ambrose JC. 2009. Spatial organization of plant cortical microtubules: close encounters of the 2D kind. Trends in Cell Biology 19: 62–71.
50. Webb MC, Gunning BES. 1991. The microtubular cytoskeleton during development of the zygote, proembryo and free-nuclear endosperm in Arabidopsis thaliana (L.) Heynh. Planta 184: 187–195.
51. Webber JM. 1940. Polyembryony. Botanical Review 6: 575–598.
52. Weterings K, Apuya NR, Bi Y, Fischer RL, Harada JJ, Goldberg RB. 2001. Regional localization of suspensor mRNAs during early embryo development. Plant Cell 13: 2409–2425.
53. Xu XM, Zhao Q, Rodrigo-Peiris T, Brkljacic J, He CS, Muller S, Meier I. 2008. RanGAP1 is a continuous marker of the Arabidopsis cell division plane. Proceedings of the National Academy of Sciences, USA 105: 18637–18642.
54. Yoo SY, Bomblies K, Yoo SK, Yang JW, Choi MS, Lee JS, Weigel D, Ahn JH. 2005. The 35S promoter used in a selectable marker gene of a plant transformation vector affects the expression of the transgene. Planta 221: 523–530.
55. Zhao J, Xin H, Qu L, Ning J, Peng X, Yan T, Ma L, Li S, Sun M. 2011. Dynamic changes of transcript profiles after fertilization are associated with de novo transcription and maternal elimination in tobacco zygote, and mark the onset of the maternal-to-zygotic transition. Plant Journal 65: 131–145.