Involvement of YODA and mitogen activated protein kinase 6 in Arabidopsis post-embryogenic root development through auxin up-regulation and cell division plane orientation

New Phytologist

Volumn 203, Issue 4, 2014, Pages 1175-1193

  Smékalová, Veronika ^a   Luptovčiak, Ivan ^a   Komis, George ^a   Šamajová, Olga ^a   Ovečka, Miroslav ^a   Doskočilová, Anna ^a   Takáč, Tomáš ^a   Vadovič, Pavol ^a   Novák, Ondřej ^b   Pechan, Tibor ^c   Ziemann, Anja ^d   Košútová, Petra ^a   Šamaj, Jozef ^a  

^a PALACKÝ UNIVERSITY   (Czech Republic)

^b INSTITUTE OF EXPERIMENTAL BOTANY   (Czech Republic)

^c MISSISSIPPI STATE UNIVERSITY   (United States)

^d UNIVERSITY OF BONN   (Germany)

Author keywords

Arabidopsis; Cell division plane; MAP65 1; MAPKKK; Microtubules; MPK6; Root; YODA

Indexed keywords

ARABIDOPSIS; ARABIDOPSIS THALIANA;

ALPHA-(2,4-DIMETHYLPHENYLETHYL-2-OXO)INDOLE-3-ACETIC ACID; ARABIDOPSIS PROTEIN; INDOLEACETIC ACID DERIVATIVE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE; MPK6 PROTEIN, ARABIDOPSIS; PROTEIN BINDING; YODA PROTEIN, ARABIDOPSIS;

ANATOMY AND HISTOLOGY; ARABIDOPSIS; CELL DIVISION; CYTOKINESIS; CYTOLOGY; DRUG EFFECTS; EMBRYOLOGY; ENZYMOLOGY; FLUORESCENT ANTIBODY TECHNIQUE; GENETICS; INTERPHASE; MERISTEM; METABOLISM; MICROTUBULE; MITOSIS; MUTATION; PHENOTYPE; PHOSPHORYLATION; PLANT EPIDERMIS; PLANT ROOT; PROTEIN TRANSPORT; PROTEOMICS; UPREGULATION;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; CELL DIVISION; CYTOKINESIS; FLUORESCENT ANTIBODY TECHNIQUE; INDOLEACETIC ACIDS; INTERPHASE; MAP KINASE KINASE KINASES; MERISTEM; MICROTUBULES; MITOGEN-ACTIVATED PROTEIN KINASES; MITOSIS; MUTATION; PHENOTYPE; PHOSPHORYLATION; PLANT EPIDERMIS; PLANT ROOTS; PROTEIN BINDING; PROTEIN TRANSPORT; PROTEOMICS; UP-REGULATION;

EID: 84905121389     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12880     Document Type: Article

References (73)

1. Bartel B, Fink GR. 1994. Differential regulation of an auxin-producing nitrilase gene family in Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 91: 6649-6653.
2. 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.
3. Beck M, Komis G, Müller J, Menzel D, Šamaj J. 2010. Arabidopsis homologs of nucleus- and phragmoplast-localized kinase 2 and 3 and mitogen-activated protein kinase 4 are essential for microtubule organization. Plant Cell 22: 755-771.
4. Beck M, Komis G, Ziemann A, Menzel D, Šamaj J. 2011. Mitogen-activated protein kinase 4 is involved in the regulation of mitotic and cytokinetic microtubule transitions in Arabidopsis thaliana. New Phytologist 189: 1069-1083.
5. Benková E, Bielach A. 2010. Lateral root organogenesis - from cell to organ. Current Opinion Plant Biology 13: 677-683.
6. Bergmann DC, Lukowitz W, Somerville CR. 2004. Stomatal development and pattern controlled by a MAPKK kinase. Science 304: 1494-1497.
7. Binarová P, Dolezel J, Draber P, Heberle-Bors E, Strnad M, Bögre L. 1998. Treatment of Vicia faba root tip cells with specific inhibitors to cyclin-dependent kinases leads to abnormal spindle formation. Plant Journal 16: 697-707.
8. Bögre L, Calderini O, Binarova P, Mattauch M, Till S, Kiegerl S, Jonak C, Pollaschek C, Barker P, Huskisson NS et al. 1999. A MAP kinase is activated late in plant mitosis and becomes localized to the plane of cell division. Plant Cell 11: 101-113.
9. Breuninger H, Lenhard M. 2010. Control of tissue and organ growth in plants. Current Topics in Developmental Biology 91: 185-220.
10. Buschmann H, Chan J, Sanchez-Pulido L, Andrade-Navarro MA, Doonan JH, Lloyd CW. 2006. Microtubule-associated AIR9 recognizes the cortical division site at preprophase and cell-plate insertion. Current Biology 16: 1938-1943.
11. Buschmann H, Hauptmann M, Niessing D, Lloyd CW, Schäffner AR. 2009. Helical growth of the Arabidopsis mutant tortifolia2 does not depend on cell division patterns but involves handed twisting of isolated cells. Plant Cell 21: 2090-2106.
12. Bush SM, Krysan PJ. 2007. Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo development. Journal of Experimental Botany 58: 2181-2191.
13. Calderini O, Bögre L, Vicente O, Binarova P, Heberle-Bors E, Wilson C. 1998. A cell cycle regulated MAP kinase with a possible role in cytokinesis in tobacco cells. Journal of Cell Science 111: 3091-3100.
14. Colcombet J, Hirt H. 2008. Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. Biochemical Journal 413: 217-226.
15. van Damme D. 2009. Division plane determination during plant somatic cytokinesis. Current Opinion in Plant Biology 12: 745-751.
16. De Smet I. 2012. Lateral root initiation: one step at a time. New Phytologist 193: 867-873.
17. De Smet I, Beeckman T. 2011. Asymmetric cell division in land plants and algae: the driving force for differentiation. Nature Reviews Molecular Cell Biology 12: 177-188.
18. Dhonukshe P, Mathur J, Hülskamp M, Gadella TW Jr. 2005. Microtubule plus-ends reveal essential links between intracellular polarization and localized modulation of endocytosis during division-plane establishment in plant cells. BMC Biology 3: 11.
19. Doskočilová A, Kohoutová L, Volc J, Kourová H, Benada O, Chumová J, Plíhal O, Petrovská B, Halada P, Bögre L et al. 2013. NITRILASE1 regulates the exit from proliferation, genome stability and plant development. New Phytologist 198: 685-698.
20. Dubrovsky J, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benkova E. 2008. Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proceedings of the National Academy of Sciences, USA 105: 8790-8794.
21. Fujita S, Pytela J, Hotta T, Kato T, Hamada T, Akamatsu R, Ishida Y, Kutsuna N, Hasezawa S, Nomura Y et al. 2013. An atypical tubulin kinase mediates stress-induced microtubule depolymerization in Arabidopsis. Current Biology 23: 1969-1978.
22. Furutani I, Watanabe Y, Prieto R, Masukawa M, Suzuki K, Naoi K, Thitamadee S, Shikanai T, Hashimoto T. 2000. The SPIRAL genes are required for directional control of cell elongation in Arabidopsis thaliana. Development 127: 4443-4453.
23. Goh T, Vo U, Farcot E, Bennett MJ, Bishopp A. 2014. Systems biology approaches to understand the role of auxin in root growth and development. Physiologia Plantarum 151: 73-78.
24. TIR1 auxin receptor complex. ACS Chemical Biology 7: 590-598.
25. Hayashi K, Tan X, Zheng N, Hatate T, Kimura Y, Kepinski S, Nozaki H. 2008. Small-molecule agonists and antagonists of F-box protein-substrate interactions in auxin perception and signaling. Proceedings of the National Academy of Sciences, USA 105: 5632-5637.
26. Higaki T, Kutsuna N, Sano T, Hasezawa S. 2008. Quantitative analysis of changes in actin microfilament contribution to cell plate development in plant cytokinesis. BMC Plant Biology 8: 80.
27. Hoehenwarter W, Thomas M, Nukarinen E, Egelhofer V, Röhrig H, Weckwerth W, Conrath U, Beckers GJ. 2013. Identification of novel in vivo MAP kinase substrates in Arabidopsis thaliana through use of tandem metal oxide affinity chromatography. Molecular & Cell Proteomics 12: 369-380.
28. Hofhuis H, Laskowski M, Du Y, Prasad K, Grigg S, Pinon V, Scheres B. 2013. Phyllotaxis and rhizotaxis in Arabidopsis are modified by three PLETHORA transcription factors. Current Biology 23: 956-962.
29. Ishida T, Kaneko Y, Iwano M, Hashimoto T. 2007. Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana. Proceedings of the National Academy of Sciences, USA 104: 8544-8549.
30. Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, Muller J, Doerks T, Julien P, Roth A, Simonovic M et al. 2009. STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Research 37: D412-D416.
31. Karahara I, Suda J, Tahara H, Yokota E, Shimmen T, Misaki K, Yonemura S, Staehelin LA, Mineyuki Y. 2009. The preprophase band is a localized center of clathrin-mediated endocytosis in late prophase cells of the onion cotyledon epidermis. Plant Journal 57: 819-831.
32. Kim TW, Michniewicz M, Bergmann DC, Wang ZY. 2012. Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature 482: 419-422.
33. Kirik A, Ehrhardt DW, Kirik V. 2012. TONNEAU2/FASS regulates the geometry of microtubule nucleation and cortical array organization in interphase Arabidopsis cells. Plant Cell 24: 1158-1170.
34. Komis G, Illés P, Beck M, Šamaj J. 2011. Microtubules and mitogen-activated protein kinase signalling. Current Opinion in Plant Biology 14: 650-657.
35. Kong Z, Hotta T, Lee YR, Horio T, Liu B. 2010. The γ-tubulin complex protein GCP4 is required for organizing functional microtubule arrays in Arabidopsis thaliana. Plant Cell 22: 191-204.
36. Kosetsu K, Matsunaga S, Nakagami H, Colcombet J, Sasabe M, Soyano T, Takahashi Y, Hirt H, Machida Y. 2010. The MAP kinase MPK4 is required for cytokinesis in Arabidopsis thaliana. Plant Cell 22: 3778-3790.
37. Kutz A, Müller A, Hennig P, Kaiser WM, Piotrowski M, Weiler EW. 2002. A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant Journal 30: 95-106.
38. Lampard GR, Lukowitz W, Ellis BE, Bergmann DC. 2009. Novel and expanded roles for MAPK signaling in Arabidopsis stomatal cell fate revealed by cell type-specific manipulations. Plant Cell 21: 3506-3517.
39. Lau OS, Bergmann DC. 2012. Stomatal development: a plant's perspective on cell polarity, cell fate transitions and intercellular communication. Development 139: 3683-3692.
40. Lloyd C, Chan J. 2008. The parallel lives of microtubules and cellulose microfibrils. Current Opinion in Plant Biology 11: 641-646.
41. Lucas JR, Shaw SL. 2012. MAP65-1 and MAP65-2 promote cell proliferation and axial growth in Arabidopsis roots. Plant Journal 71: 454-463.
42. Lukowitz W, Roeder A, Parmenter D, Somerville C. 2004. A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 116: 109-119.
43. Mao G, Chan J, Calder G, Doonan JH, Lloyd CW. 2005. Modulated targeting of GFP-AtMAP65-1 to central spindle microtubules during division. Plant Journal 43: 469-478.
44. Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H et al. 2011. The main auxin biosynthesis pathway in Arabidopsis. Proceedings of the National Academy of Sciences, USA 108: 18512-18517.
45. Müller J, Beck M, Mettbach U, Komis G, Hause G, Menzel D, Šamaj J. 2010. Arabidopsis MPK6 is involved in cell division plane control during early root development, and localizes to the pre-prophase band, phragmoplast, trans-Golgi network and plasma membrane. Plant Journal 61: 234-248.
46. Müller S, Han S, Smith LG. 2006. Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Current Biology 16: 888-894.
47. Müller S, Smertenko A, Wagner V, Heinrich M, Hussey PJ, Hauser MT. 2004. The plant microtubule-associated protein AtMAP65-3/PLE is essential for cytokinetic phragmoplast function. Current Biology 14: 412-417.
48. Müller S, Wright AJ, Smith LG. 2009. Division plane control in plants: new players in the band. Trends in Cell Biology 19: 180-188.
49. Murata T, Sano T, Sasabe M, Nonaka S, Higashiyama T, Hasezawa S, Machida Y, Hasebe M. 2013. Mechanism of microtubule array expansion in the cytokinetic phragmoplast. Nature Communications 4: 1967.
50. Nadeau JA. 2009. Stomatal development: new signals and fate determinants. Current Opinion in Plant Biology 12: 29-35.
51. Novák O, Hényková E, Sairanen I, Kowalczyk M, Pospíšil T, Ljung K. 2012. Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant Journal 72: 523-536.
52. Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D et al. 2005. Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17: 444-463.
53. Ovečka M, Takáč T, Komis G, Vadovič P, Bekešová S, Doskočilová A, Smékalová V, Luptovčiak I, Šamajová O, Schweighofer A et al. 2014. Salt-induced subcellular kinase relocation and seeding susceptibility caused by overexpression of Medicago SIMKK in Arabidopsis. Journal of Experimental Botany 65: 2335-2350.
54. Panteris E. 2008. Cortical actin filaments at the division site of mitotic plant cells: a reconsideration of the 'actin-depleted zone'. New Phytologist 179: 334-341.
55. Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M, Snyder M, Dinesh-Kumar SP. 2009. MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes & Development 23: 80-92.
56. Qian P, Hou S, Guo G. 2009. Molecular mechanisms controlling pavement cell shape in Arabidopsis leaves. Plant Cell Reports 28: 1147-1157.
57. Rasmussen CG, Humphries JA, Smith LG. 2011a. Determination of symmetric and asymmetric division planes in plant cells. Annual Review of Plant Biology 62: 387-409.
58. Rasmussen CG, Sun B, Smith LG. 2011b. Tangled localization at the cortical division site of plant cells occurs by several mechanisms. Journal of Cell Science 124: 270-279.
59. Rasmussen MW, Roux M, Petersen M, Mundy J. 2012. MAP kinase cascades in Arabidopsis innate immunity. Frontiers in Plant Sciences 3: 169.
60. Šamajová O, Komis G, Šamaj J. 2013. Emerging topics in the cell biology of mitogen-activated protein kinases. Trends in Plant Science 18: 40-48.
61. Sasabe M, Kosetsu K, Hidaka M, Murase A, Machida Y. 2011. Arabidopsis thaliana MAP65-1 and MAP65-2 function redundantly with MAP65-3/PLEIADE in cytokinesis downstream of MPK4. Plant Signaling and Behavior 6: 743-747.
62. Sasabe M, Machida Y. 2012. Regulation of organization and function of microtubules by the mitogen-activated protein kinase cascade during plant cytokinesis. Cytoskeleton (Hoboken) 69: 913-918.
63. Sasabe M, Soyano T, Takahashi Y, Sonobe S, Igarashi H, Itoh TJ, Hidaka M, Machida Y. 2006. Phosphorylation of NtMAP65-1 by a MAP kinase down-regulates its activity of microtubule bundling and stimulates progression of cytokinesis of tobacco cells. Genes & Development 20: 1004-1014.
64. Sedbrook JC, Ehrhardt DW, Fisher SE, Scheible WR, Somerville CR. 2004. The Arabidopsis SKU6/SPIRAL1 gene encodes a plus end-localized microtubule-interacting protein involved in directional cell expansion. Plant Cell 16: 1506-1520.
65. Smertenko AP, Chang HY, Sonobe S, Fenyk SI, Weingartner M, Bögre L, Hussey PJ. 2006. Control of the AtMAP65-1 interaction with microtubules through the cell cycle. Journal of Cell Science 119: 3227-3237.
66. Szymanski DB, Cosgrove DJ. 2009. Dynamic coordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Current Opinion in Plant Biology 19: R800-R811.
67. Ten Hove CA, Heidstra R. 2008. Who begets whom? Plant cell fate determination by asymmetric cell division. Current Opinion in Plant Biology 11: 34-41.
68. Tian C, Muto H, Higuchi K, Matamura T, Tatematsu K, Koshiba T, Yamamoto KT. 2004. Disruption and overexpression of auxin response factor 8 gene of Arabidopsis affect hypocotyl elongation and root growth habit, indicating its possible involvement in auxin homeostasis in light condition. Plant Journal 40: 333-343.
69. Tominaga-Wada R, Ishida T, Wada T. 2011. New insights into the mechanism of development of Arabidopsis root hairs and trichomes. International Review of Cell and Molecular Biology 286: 67-106.
70. Walia A, Lee JS, Wasteneys G, Ellis B. 2009. Arabidopsis mitogen-activated protein kinase MPK18 mediates cortical microtubule functions in plant cells. Plant Journal 59: 565-575.
71. Walker KL, Müller S, Moss D, Ehrhardt DW, Smith LG. 2007. Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Current Biology 17: 1827-1836.
72. Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S. 2007. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 19: 63-73.
73. Xu XM, Zhao Q, Rodrigo-Peiris T, Brkljacic J, He CS, Müller 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.