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

. 2014 Sep ; 203 (4) : 1175-1193. [epub] 20140613

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid24923680

Grantová podpora
P20 GM103476 NIGMS NIH HHS - United States

The role of YODA MITOGEN ACTIVATED PROTEIN KINASE KINASE KINASE 4 (MAPKKK4) upstream of MITOGEN ACTIVATED PROTEIN KINASE 6 (MPK6) was studied during post-embryonic root development of Arabidopsis thaliana. Loss- and gain-of-function mutants of YODA (yda1 and ΔNyda1) were characterized in terms of root patterning, endogenous auxin content and global proteomes. We surveyed morphological and cellular phenotypes of yda1 and ΔNyda1 mutants suggesting possible involvement of auxin. Endogenous indole-3-acetic acid (IAA) levels were up-regulated in both mutants. Proteomic analysis revealed up-regulation of auxin biosynthetic enzymes tryptophan synthase and nitrilases in these mutants. The expression, abundance and phosphorylation of MPK3, MPK6 and MICROTUBULE ASSOCIATED PROTEIN 65-1 (MAP65-1) were characterized by quantitative polymerase chain reaction (PCR) and western blot analyses and interactions between MAP65-1, microtubules and MPK6 were resolved by quantitative co-localization studies and co-immunoprecipitations. yda1 and ΔNyda1 mutants showed disoriented cell divisions in primary and lateral roots, abortive cytokinesis, and differential subcellular localization of MPK6 and MAP65-1. They also showed deregulated expression of TANGLED1 (TAN1), PHRAGMOPLAST ORIENTING KINESIN 1 (POK1), and GAMMA TUBULIN COMPLEX PROTEIN 4 (GCP4). The findings that MPK6 localized to preprophase bands (PPBs) and phragmoplasts while the mpk6-4 mutant transformed with MPK6AEF (alanine (A)-glutamic acid (E)-phenylanine (F)) showed a root phenotype similar to that of yda1 demonstrated that MPK6 is an important player downstream of YODA. These data indicate that YODA and MPK6 are involved in post-embryonic root development through an auxin-dependent mechanism regulating cell division and mitotic microtubule (PPB and phragmoplast) organization.

Zobrazit více v PubMed

Bartel B, Fink GR. Differential regulation of an auxin-producing nitrilase gene family. Arabidopsis thaliana Proceedings of the National Academy of Sciences, USA. 1994;91:6649–6653. PubMed PMC

Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W. Paternal control of embryonic patterning in Arabidopsis thaliana. Science. 2009;323:1485–1488. PubMed

Beck M, Komis G, Müller J, Menzel D, Šamaj J. Arabidopsis homologs of nucleus-and phragmoplast-localized kinase 2 and 3 and mitogen-activated protein kinase 4 are essential for microtubule organization. Plant Cell. 2010;22:755–771. PubMed PMC

Beck M, Komis G, Ziemann A, Menzel D, Šamaj J. Mitogen-activated protein kinase 4 is involved in the regulation of mitotic and cytokinetic microtubule transitions in Arabidopsis thaliana. New Phytologist. 2011;189:1069–1083. PubMed

Benková E, Bielach A. Lateral root organogenesis – from cell to organ. Current Opinion Plant Biology. 2010;13:677–683. PubMed

Bergmann DC, Lukowitz W, Somerville CR. Stomatal development and pattern controlled by a MAPKK kinase. Science. 2004;304:1494–1497. PubMed

Binarová P, Dolezel J, Draber P, Heberle-Bors E, Strnad M, Bögre L. Treatment of Vicia faba root tip cells with specific inhibitors to cyclin-dependent kinases leads to abnormal spindle formation. Plant Journal. 1998;16:697–707. PubMed

Bögre L, Calderini O, Binarova P, Mattauch M, Till S, Kiegerl S, Jonak C, Pollaschek C, Barker P, Huskisson NS, et al. A MAP kinase is activated late in plant mitosis and becomes localized to the plane of cell division. Plant Cell. 1999;11:101–113. PubMed PMC

Breuninger H, Lenhard M. Control of tissue and organ growth in plants. Current Topics in Developmental Biology. 2010;91:185–220. PubMed

Buschmann H, Chan J, Sanchez-Pulido L, Andrade-Navarro MA, Doonan JH, Lloyd CW. Microtubule-associated AIR9 recognizes the cortical division site at preprophase and cell-plate insertion. Current Biology. 2006;16:1938–1943. PubMed

Buschmann H, Hauptmann M, Niessing D, Lloyd CW, Schäffner AR. Helical growth of the Arabidopsis mutant tortifolia2 does not depend on cell division patterns but involves handed twisting of isolated cells. Plant Cell. 2009;21:2090–2106. PubMed PMC

Bush SM, Krysan PJ. Mutational evidence that the Arabidopsis MAP kinase MPK6 is involved in anther, inflorescence, and embryo development. Journal of Experimental Botany. 2007;58:2181–2191. PubMed

Calderini O, Bögre L, Vicente O, Binarova P, Heberle-Bors E, Wilson C. A cell cycle regulated MAP kinase with a possible role in cytokinesis in tobacco cells. Journal of Cell Science. 1998;111:3091–3100. PubMed

Colcombet J, Hirt H. Arabidopsis MAPKs: a complex signalling network involved in multiple biological processes. BiochemicalJournal. 2008;413:217–226. PubMed

van Damme D. Division plane determination during plant somatic cytokinesis. Current Opinion in Plant Biology. 2009;12:745–751. PubMed

De Smet I. Lateral root initiation: one step at a time. New Phytologist. 2012;193:867–873. PubMed

De Smet I, Beeckman T. Asymmetric cell division in land plants and algae: the driving force for differentiation. Nature Reviews Molecular Cell Biology. 2011;12:177–188. PubMed

Dhonukshe P, Mathur J, Hülskamp M, Gadella TW., Jr Microtubule plus-ends reveal essential links between intracellular polarization and localized modulation of endocytosis during division-plane establishment in plant cells. BMC Biology. 2005;3:11. PubMed PMC

Doskočilová A, Kohoutová L, Volc J, Kourová H, Benada O, Chumová J, Plihal O, Petrovská B, Halada P, Bögre L, et al. NITRILASE1 regulates the exit from proliferation, genome stability and plant development. New Phytologist. 2013;198:685–698. PubMed

Dubrovsky J, Sauer M, Napsucialy-Mendivil S, Ivanchenko MG, Friml J, Shishkova S, Celenza J, Benkova E. Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proceedings of the National Academy of Sciences, USA. 2008;105:8790–8794. PubMed PMC

Fujita S, Pytela J, Hotta T, Kato T, Hamada T, Akamatsu R, Ishida Y, Kutsuna N, Hasezawa S, Nomura Y, et al. An atypical tubulin kinase mediates stress-induced microtubule depolymerization in Arabidopsis. Current Biology. 2013;23:1969–1978. PubMed

Furutani I, Watanabe Y, Prieto R, Masukawa M, Suzuki K, Naoi K, Thitamadee S, Shikanai T, Hashimoto T. The SPIRAL genes are required for directional control of cell elongation in Arabidopsis thaliana. Development. 2000;127:4443–4453. PubMed

Goh T, Voβ U, Farcot E, Bennett MJ, Bishopp A. Systems biology approaches to understand the role of auxin in root growth and development. Physiologia Plantarum. 2014;151:73–78. PubMed

Hayashi K, Nave J, Zheng N, Hirose M, Kuboki A, Shimada Y, Kepinski S, Nozaki H. Rational design of an auxin antagonist of the SCFTIR1 auxin receptor complex. ACS Chemical Biology. 2012;7:590–598. PubMed

Hayashi K, Tan X, Zheng N, Hatate T, Kimura Y, Kepinski S, Nozaki H. Small-molecule agonists and antagonists of F-box protein-substrate interactions in auxin perception and signaling. Proceedings of the National Academy of Sciences, USA. 2008;105:5632–5637. PubMed PMC

Higaki T, Kutsuna N, Sano T, Hasezawa S. Quantitative analysis of changes in actin microfilament contribution to cell plate development in plant cytokinesis. BMC Plant Biology. 2008;8:80. PubMed PMC

Hoehenwarter W, Thomas M, Nukarinen E, Egelhofer V, Röhrig H, Weckwerth W, Conrath U, Beckers GJ. Identification of novel in vivo MAP kinase substrates in Arabidopsis thaliana through use of tandem metal oxide affinity chromatography. Molecular & Cell Proteomics. 2013;12:369–380. PubMed PMC

Hofhuis H, Laskowski M, Du Y, Prasad K, Grigg S, Pinon V, Scheres B. Phyllotaxis and rhizotaxis in Arabidopsis are modified by three PLETHORA transcription factors. Current Biology. 2013;23:956–962. PubMed

Ishida T, Kaneko Y, Iwano M, Hashimoto T. Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana. Proceeding of the National Academy of Sciences, USA. 2007;104:8544–8549. PubMed PMC

Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, Muller J, Doerks T, Julien P, Roth A, Simonovic M, et al. STRING 8-a global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Research. 2009;37:D412–D416. PubMed PMC

Karahara I, Suda J, Tahara H, Yokota E, Shimmen T, Misaki K, Yonemura S, Staehelin LA, Mineyuki Y. The preprophase band is a localized center of clathrin-mediated endocytosis in late prophase cells of the onion cotyledon epidermis. Plant Journal. 2009;57:819–831. PubMed

Kim TW, Michniewicz M, Bergmann DC, Wang ZY. Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway. Nature. 2012;482:419–422. PubMed PMC

Kirik A, Ehrhardt DW, Kirik V. TONNEAU2/FASS regulates the geometry of microtubule nucleation and cortical array organization in interphase Arabidopsis cells. Plant Cell. 2012;24:1158–1170. PubMed PMC

Komis G, Illés P, Beck M, Šamaj J. Microtubules and mitogen-activated protein kinase signalling. Current Opinion in Plant Biology. 2011;14:650–657. PubMed

Kong Z, Hotta T, Lee YR, Horio T, Liu B. The γ-tubulin complex protein GCP4 is required for organizing functional microtubule arrays in Arabidopsis thaliana. Plant Cell. 2010;22:191–204. PubMed PMC

Kosetsu K, Matsunaga S, Nakagami H, Colcombet J, Sasabe M, Soyano T, Takahashi Y, Hirt H, Machida Y. The MAP kinase MPK4 is required for cytokinesis in Arabidopsis thaliana. Plant Cell. 2010;22:3778–3790. PubMed PMC

Kutz A, Müller A, Hennig P, Kaiser WM, Piotrowski M, Weiler EW. A role for nitrilase 3 in the regulation of root morphology in sulphur-starving Arabidopsis thaliana. Plant Journal. 2002;30:95–106. PubMed

Lampard GR, Lukowitz W, Ellis BE, Bergmann DC. Novel and expanded roles for MAPK signaling in Arabidopsis stomatal cell fate revealed by cell type-specific manipulations. Plant Cell. 2009;21:3506–3517. PubMed PMC

Lau OS, Bergmann DC. Stomatal development: a plant’s perspective on cell polarity, cell fate transitions and intercellular communication. Development. 2012;139:3683–3692. PubMed PMC

Lloyd C, Chan J. The parallel lives of microtubules and cellulose microfibrils. Current Opinion in Plant Biology. 2008;11:641–646. PubMed

Lucas JR, Shaw SL. MAP65-1 and MAP65-2 promote cell proliferation and axial growth in Arabidopsis roots. Plant Journal. 2012;71:454–463. PubMed

Lukowitz W, Roeder A, Parmenter D, Somerville C. A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell. 2004;116:109–119. PubMed

Mao G, Chan J, Calder G, Doonan JH, Lloyd CW. Modulated targeting of GFP-AtMAP65-1 to central spindle microtubules during division. Plant Journal. 2005;43:469–478. PubMed

Mashiguchi K, Tanaka K, Sakai T, Sugawara S, Kawaide H, Natsume M, Hanada A, Yaeno T, Shirasu K, Yao H, et al. The main auxin biosynthesis pathway in Arabidopsis. Proceedings of the National Academy of Sciences, USA. 2011;108:18512–18517. PubMed PMC

Muller J, Beck M, Mettbach U, Komis G, Hause G, Menzel D, Šamaj J. 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. 2010;61:234–248. PubMed

Müller S, Han S, Smith LG. Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Current Biology. 2006;16:888–894. PubMed

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. Current Biology. 2004;14:412–417. PubMed PMC

Müller S, Wright AJ, Smith LG. Division plane control in plants: new players in the band. Trends in Cell Biology. 2009;19:180–188. PubMed

Murata T, Sano T, Sasabe M, Nonaka S, Higashiyama T, Hasezawa S, Machida Y, Hasebe M. Mechanism of microtubule array expansion in the cytokinetic phragmoplast. Nature Communications. 2013;4:1967. PubMed PMC

Nadeau JA. Stomatal development: new signals and fate determinants. Current Opinion in Plant Biology. 2009;12:29–35. PubMed PMC

Novák O, Hényková E, Sairanen I, Kowalczyk M, Pospíšil T, Ljung K. Tissue-specific profiling of the Arabidopsis thaliana auxin metabolome. Plant Journal. 2012;72:523–536. PubMed

Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, et al. Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell. 2005;17:444–463. PubMed PMC

Ovečka M, Takáč T, Komis G, Vadovič P, Bekešová S, Doskočilová A, Smékalova V, Luptovčiak I, Šamajová O, Schweighofer A, et al. Salt-induced subcellular kinase relocation and seeding susceptibility caused by overexpression of Medicago SIMKK in Arabidopsis. Journal of Experimental Botany. 2014;65:2335–2350. PubMed PMC

Panteris E. Cortical actin filaments at the division site of mitotic plant cells: a reconsideration of the ‘actin-depleted zone’. New Phytologist. 2008;179:334–341. PubMed

Popescu SC, Popescu GV, Bachan S, Zhang Z, Gerstein M, Snyder M, Dinesh-Kumar SP. MAPK target networks in Arabidopsis thaliana revealed using functional protein microarrays. Genes & Development. 2009;23:80–92. PubMed PMC

Qian P, Hou S, Guo G. Molecular mechanisms controlling pavement cell shape in Arabidopsis leaves. Plant Cell Reports. 2009;28:1147–1157. PubMed

Rasmussen CG, Humphries JA, Smith LG. Determination of symmetric and asymmetric division planes in plant cells. Annual Review of Plant Biology. 2011a;62:387–409. PubMed

Rasmussen CG, Sun B, Smith LG. Tangled localization at the cortical division site of plant cells occurs by several mechanisms. Journal of Cell Science. 2011b;124:270–279. PubMed

Rasmussen MW, Roux M, Petersen M, Mundy J. MAP kinase cascades in Arabidopsis innate immunity. Frontiers in Plant Sciences. 2012;3:169. PubMed PMC

Šamajová O, Komis G, Šamaj J. Emerging topics in the cell biology of mitogen-activated protein kinases. Trends in Plant Science. 2013;18:40–48. PubMed

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 Signaling and Behavior. 2011;6:743–747. PubMed PMC

Sasabe M, Machida Y. Regulation of organization and function of microtubules by the mitogen-activated protein kinase cascade during plant cytokinesis. Cytoskeleton (Hoboken) 2012;69:913–918. PubMed

Sasabe M, Soyano T, Takahashi Y, Sonobe S, Igarashi H, Itoh TJ, Hidaka M, Machida Y. 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. 2006;20:1004–1014. PubMed PMC

Sedbrook JC, Ehrhardt DW, Fisher SE, Scheible WR, Somerville CR. The Arabidopsis SKU6/SPIRAL1 gene encodes a plus end-localized microtubule-interacting protein involved in directional cell expansion. Plant Cell. 2004;16:1506–1520. PubMed PMC

Smertenko AP, Chang HY, Sonobe S, Fenyk SI, Weingartner M, Bögre L, Hussey PJ. Control of the AtMAP65-1 interaction with microtubules through the cell cycle. Journal of Cell Science. 2006;119:3227–3237. PubMed

Szymanski DB, Cosgrove DJ. Dynamic coordination of cytoskeletal and cell wall systems during plant cell morphogenesis. Current Opinion in Plant Biology. 2009;19:R800–R811. PubMed

Ten Hove CA, Heidstra R. Who begets whom? Plant cell fate determination by asymmetric cell division. Current Opinion in Plant Biology. 2008;11:34–41. PubMed

Tian C, Muto H, Higuchi K, Matamura T, Tatematsu K, Koshiba T, Yamamoto KT. 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. 2004;40:333–343. PubMed

Tominaga-Wada R, Ishida T, Wada T. New insights into the mechanism of development of Arabidopsis root hairs and trichomes. International Review of Cell and Molecular Biology. 2011;286:67–106. PubMed

Walia A, Lee JS, Wasteneys G, Ellis B. Arabidopsis mitogen-activated protein kinase MPK18 mediates cortical microtubule functions in plant cells. Plant Journal. 2009;59:565–575. PubMed

Walker KL, Müller S, Moss D, Ehrhardt DW, Smith LG. Arabidopsis TANGLED identifies the division plane throughout mitosis and cytokinesis. Current Biology. 2007;17:1827–1836. PubMed PMC

Wang H, Ngwenyama N, Liu Y, Walker JC, Zhang S. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell. 2007;19:63–73. PubMed PMC

Xu XM, Zhao Q, Rodrigo-Peiris T, Brkljacic J, He CS, Müller S, Meier I. RanGAP1 is a continuous marker of the Arabidopsis cell division plane. Proceedings of the National Academy of Sciences, USA. 2008;105:18637–18642. PubMed PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

ROOT HAIR DEFECTIVE 2 vesicular delivery to the apical plasma membrane domain during Arabidopsis root hair development

. 2022 Mar 04 ; 188 (3) : 1563-1585.

CRISPR/Cas9-Induced Loss-of-Function Mutation in the Barley Mitogen-Activated Protein Kinase 6 Gene Causes Abnormal Embryo Development Leading to Severely Reduced Grain Germination and Seedling Shootless Phenotype

. 2021 ; 12 () : 670302. [epub] 20210730

HEAT SHOCK PROTEIN 90 proteins and YODA regulate main body axis formation during early embryogenesis

. 2021 Jul 06 ; 186 (3) : 1526-1544.

TALEN-Based HvMPK3 Knock-Out Attenuates Proteome and Root Hair Phenotypic Responses to flg22 in Barley

. 2021 ; 12 () : 666229. [epub] 20210429

Spatiotemporal Pattern of Ectopic Cell Divisions Contribute to Mis-Shaped Phenotype of Primary and Lateral Roots of katanin1 Mutant

. 2020 ; 11 () : 734. [epub] 20200609

Phosphorylation of Plant Microtubule-Associated Proteins During Cell Division

. 2019 ; 10 () : 238. [epub] 20190311

Multicolour three dimensional structured illumination microscopy of immunolabeled plant microtubules and associated proteins

. 2019 ; 15 () : 22. [epub] 20190309

Advances in Imaging Plant Cell Dynamics

. 2018 Jan ; 176 (1) : 80-93. [epub] 20171122

Feedback Microtubule Control and Microtubule-Actin Cross-talk in Arabidopsis Revealed by Integrative Proteomic and Cell Biology Analysis of KATANIN 1 Mutants

. 2017 Sep ; 16 (9) : 1591-1609. [epub] 20170713

Comparative proteomic study of Arabidopsis mutants mpk4 and mpk6

. 2016 Jun 21 ; 6 () : 28306. [epub] 20160621

Preparation of plants for developmental and cellular imaging by light-sheet microscopy

. 2015 Aug ; 10 (8) : 1234-47. [epub] 20150723

Monitoring protein phosphorylation by acrylamide pendant Phos-Tag™ in various plants

. 2015 ; 6 () : 336. [epub] 20150513

Advantages and limitations of shot-gun proteomic analyses on Arabidopsis plants with altered MAPK signaling

. 2015 ; 6 () : 107. [epub] 20150225

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...