bHLH heterodimer complex variations regulate cell proliferation activity in the meristems of Arabidopsis thaliana

. 2022 Nov 18 ; 25 (11) : 105364. [epub] 20221014

Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid36339262
Odkazy

PubMed 36339262
PubMed Central PMC9626673
DOI 10.1016/j.isci.2022.105364
PII: S2589-0042(22)01636-4
Knihovny.cz E-zdroje

Root, shoot, and lateral meristems are the main regions of cell proliferation in plants. It has been proposed that meristems might have evolved dedicated transcriptional networks to balance cell proliferation. Here, we show that basic helix-loop-helix (bHLH) transcription factor heterodimers formed by members of the TARGET OF MONOPTEROS5 (TMO5) and LONESOME HIGHWAY (LHW) subclades are general regulators of cell proliferation in all meristems. Yet, genetics and expression analyses suggest specific functions of these transcription factors in distinct meristems, possibly due to their expression domains determining heterodimer complex variations within meristems, and to a certain extent to the absence of some of them in a given meristem. Target gene specificity analysis for heterodimer complexes focusing on the LONELY GUY gene targets further suggests differences in transcriptional responses through heterodimer diversification that could allow a common bHLH heterodimer complex module to contribute to cell proliferation control in multiple meristems.

Zobrazit více v PubMed

Ben-Targem M., Ripper D., Bayer M., Ragni L. Auxin and gibberellin signaling cross-talk promotes hypocotyl xylem expansion and cambium homeostasis. J. Exp. Bot. 2021;72:3647–3660. PubMed

Berckmans B., Kirschner G., Gerlitz N., Stadler R., Simon R. CLE40 signaling regulates root stem cell fate. Plant Physiol. 2020;182:1776–1792. PubMed PMC

Bernhardt C., Lee M.M., Gonzalez A., Zhang F., Lloyd A., Schiefelbein J. The bHLH genes GLABRA3 (GL3) and ENHANCER OF GLABRA3(EGL3) specify epidermal cell fate in the Arabidopsis root. Development. 2003;130:6431–6439. PubMed

Beyer H.M., Gonschorek P., Samodelov S.L., Meier M., Weber W., Zurbriggen M.D. AQUA cloning: a versatile and simple enzyme-free cloning approach. PLoS One. 2015;10:e0137652. PubMed PMC

Brunoud G., Galvan-Ampudia C.S., Vernoux T. In: Plant Stem Cells. Naseem M., Dandekar T., editors. Springer US; 2020. Methods to visualize auxin and cytokinin signaling activity in the shoot apical meristem; pp. 79–89. (Methods in Molecular Biology). PubMed

Clark S.E., Running M.P., Meyerowitz E.M. CLAVATA1, a regulator of meristem and flower development in Arabidopsis. Development. 1993;119:397–418. PubMed

Clark S.E., Running M.P., Meyerowitz E.M. CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development. 1995;121:2057–2067.

De Rybel B., Adibi M., Breda A.S., Wendrich J.R., Smit M.E., Novák O., Yamaguchi N., Yoshida S., Van Isterdael G., Palovaara J., et al. Integration of growth and patterning during vascular tissue formation in Arabidopsis. Science. 2014;345:1255215. PubMed

De Rybel B., Möller B., Yoshida S., Grabowicz I., Barbier de Reuille P., Boeren S., Smith R.S., Borst J.W., Weijers D. A bHLH complex controls embryonic vascular tissue establishment and indeterminate growth in Arabidopsis. Dev. Cell. 2013;24:426–437. PubMed

De Smet I., Chaerle P., Vanneste S., De Rycke R., Inzé D., Beeckman T. An easy and versatile embedding method for transverse sections. J. Microsc. 2004;213:76–80. PubMed

Etchells J.P., Provost C.M., Mishra L., Turner S.R. WOX4 and WOX14 act downstream of the PXY receptor kinase to regulate plant vascular proliferation independently of any role in vascular organisation. Development. 2013;140:2224–2234. PubMed PMC

Etchells J.P., Turner S.R. Orientation of vascular cell divisions in Arabidopsis. Plant Signal. Behav. 2010;5:730–732. PubMed PMC

Fernandez R., Das P., Mirabet V., Moscardi E., Traas J., Verdeil J.-L., Malandain G., Godin C. Imaging plant growth in 4D: robust tissue reconstruction and lineaging at cell resolution. Nat. Methods. 2010;7:547–553. PubMed

Fisher K., Turner S. PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr. Biol. 2007;17:1061–1066. PubMed

Gaillochet C., Daum G., Lohmann J.U. O Cell, Where Art Thou? The mechanisms of shoot meristem patterning. Curr. Opin. Plant Biol. 2015;23:91–97. PubMed

Grove C.A., De Masi F., Barrasa M.I., Newburger D.E., Alkema M.J., Bulyk M.L., Walhout A.J.M. A multiparameter network reveals extensive divergence between C. elegans bHLH transcription factors. Cell. 2009;138:314–327. PubMed PMC

Hao Y., Zong X., Ren P., Qian Y., Fu A. Basic helix-loop-helix (bHLH) transcription factors regulate a wide range of functions in Arabidopsis. Int. J. Mol. Sci. 2021;22:7152. PubMed PMC

Karimi M., Depicker A., Hilson P. Recombinational cloning with plant Gateway vectors. Plant Physiol. 2007;145:1144–1154. PubMed PMC

Kurakawa T., Ueda N., Maekawa M., Kobayashi K., Kojima M., Nagato Y., Sakakibara H., Kyozuka J. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature. 2007;445:652–655. PubMed

Kurihara D., Mizuta Y., Sato Y., Higashiyama T. ClearSee: a rapid optical clearing reagent for whole-plant fluorescence imaging. Development. 2015;142:4168–4179. PubMed PMC

Kuroha T., Tokunaga H., Kojima M., Ueda N., Ishida T., Nagawa S., Fukuda H., Sugimoto K., Sakakibara H. Functional analyses of LONELY GUY cytokinin-activating enzymes reveal the importance of the direct activation pathway in Arabidopsis. Plant Cell. 2009;21:3152–3169. PubMed PMC

Laux T., Mayer K.F., Berger J., Jürgens G. The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development. 1996;122:87–96. PubMed

Massari M.E., Murre C. Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol. Cell Biol. 2000;20:429–440. PubMed PMC

Miyashima S., Roszak P., Sevilem I., Toyokura K., Blob B., Heo J.O., Mellor N., Help-Rinta-Rahko H., Otero S., Smet W., et al. Mobile PEAR transcription factors integrate positional cues to prime cambial growth. Nature. 2019;565:490–494. PubMed

Motte H., Vanneste S., Beeckman T. Molecular and environmental regulation of root development. Annu. Rev. Plant Biol. 2019;70:465–488. PubMed

Müller K., Siegel D., Rodriguez Jahnke F., Gerrer K., Wend S., Decker E.L., Reski R., Weber W., Zurbriggen M.D. A red light-controlled synthetic gene expression switch for plant systems. Mol. Biosyst. 2014;10:1679–1688. PubMed

Murashige T., Skoog F. A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol. Plantarum. 1962;15:473–497.

Ochoa-Fernandez R., Abel N.B., Wieland F.G., Schlegel J., Koch L.A., Miller J.B., Engesser R., Giuriani G., Brandl S.M., Timmer J., et al. Optogenetic control of gene expression in plants in the presence of ambient white light. Nat. Methods. 2020;17:717–725. PubMed

Ochoa-Fernandez R., Samodelov S.L., Brandl S.M., Wehinger E., Müller K., Weber W., Zurbriggen M.D. Optogenetics in plants: red/far-red light control of gene expression. Methods Mol. Biol. 2016;1408:125–139. PubMed

Ohashi-Ito K., Bergmann D.C. Regulation of the Arabidopsis root vascular initial population by LONESOME HIGHWAY. Development. 2007;134:2959–2968. PubMed PMC

Ohashi-Ito K., Matsukawa M., Fukuda H. An atypical bHLH transcription factor regulates early xylem development downstream of auxin. Plant Cell Physiol. 2013;54:398–405. PubMed

Ohashi-Ito K., Oguchi M., Kojima M., Sakakibara H., Fukuda H. Auxin-associated initiation of vascular cell differentiation by LONESOME HIGHWAY. Development. 2013;140:765–769. PubMed

Ohashi-Ito K., Saegusa M., Iwamoto K., Oda Y., Katayama H., Kojima M., Sakakibara H., Fukuda H. A bHLH complex activates vascular cell division via cytokinin action in root apical meristem. Curr. Biol. 2014;24:2053–2058. PubMed

Qian Y., Zhang T., Yu Y., Gou L., Yang J., Xu J., Pi E. Regulatory mechanisms of bHLH transcription factors in plant adaptive responses to various abiotic stresses. Front. Plant Sci. 2021;12:677611. PubMed PMC

Ragni L., Greb T. Secondary growth as a determinant of plant shape and form. Semin. Cell Dev. Biol. 2018;79:58–67. PubMed

Samodelov S.L., Beyer H.M., Guo X., Augustin M., Jia K.-P., Baz L., Ebenhöh O., Beyer P., Weber W., Al-Babili S., Zurbriggen M.D. StrigoQuant: a genetically encoded biosensor for quantifying strigolactone activity and specificity. Sci. Adv. 2016;2:e1601266. PubMed PMC

Sarrion-Perdigones A., Vazquez-Vilar M., Palací J., Castelijns B., Forment J., Ziarsolo P., Blanca J., Granell A., Orzaez D. GoldenBraid 2.0: a comprehensive DNA assembly framework for plant synthetic biology. Plant Physiol. 2013;162:1618–1631. PubMed PMC

Schlereth A., Möller B., Liu W., Kientz M., Flipse J., Rademacher E.H., Schmid M., Jürgens G., Weijers D. MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature. 2010;464:913–916. PubMed

Serra O., Mähönen A.P., Hetherington A.J., Ragni L. The making of plant armor: the periderm. Annu. Rev. Plant Biol. 2022;73:405–432. annurev-arplant-102720-031405. PubMed

Shimotohno A., Scheres B. Topology of regulatory networks that guide plant meristem activity: similarities and differences. Curr. Opin. Plant Biol. 2019;51:74–80. PubMed

Smet W., Sevilem I., de Luis Balaguer M.A., Wybouw B., Mor E., Miyashima S., Blob B., Roszak P., Jacobs T.B., Boekschoten M., et al. DOF2.1 controls cytokinin-dependent vascular cell proliferation downstream of TMO5/LHW. Curr. Biol. 2019;29:520–529.e6. PubMed PMC

Stahl Y., Grabowski S., Bleckmann A., Kühnemuth R., Weidtkamp-Peters S., Pinto K.G., Kirschner G.K., Schmid J.B., Wink R.H., Hülsewede A., et al. Moderation of Arabidopsis root stemness by CLAVATA1 and ARABIDOPSIS CRINKLY4 receptor kinase complexes. Curr. Biol. 2013;23:362–371. PubMed

Suer S., Agusti J., Sanchez P., Schwarz M., Greb T. WOX4 imparts auxin responsiveness to cambium cells in Arabidopsis. Plant Cell. 2011;23:3247–3259. PubMed PMC

Theisel H., Rossl C., Zayer R., Seidel H.-P. 12th Pacific Conference on Computer Graphics and Applications, 2004. PG 2004. Proceedings. (IEEE: Seoul, Korea) 2004. Normal based estimation of the curvature tensor for triangular meshes; pp. 288–297.

Trigg S.A., Garza R.M., MacWilliams A., Nery J.R., Bartlett A., Castanon R., Goubil A., Feeney J., O'Malley R., Huang S.S.C., et al. CrY2H-seq: a massively multiplexed assay for deep-coverage interactome mapping. Nat. Methods. 2017;14:819–825. PubMed PMC

Truernit E., Haseloff J. A simple way to identify non-viable cells within living plant tissue using confocal microscopy. Plant Methods. 2008;4:15. PubMed PMC

Ursache R., Andersen T.G., Marhavý P., Geldner N. A protocol for combining fluorescent proteins with histological stains for diverse cell wall components. Plant J. 2018;93:399–412. PubMed

Vera-Sirera F., De Rybel B., Úrbez C., Kouklas E., Pesquera M., Álvarez-Mahecha J.C., Minguet E.G., Tuominen H., Carbonell J., Borst J.W., et al. A bHLH-based feedback loop restricts vascular cell proliferation in plants. Dev. Cell. 2015;35:432–443. PubMed

Wang B., Smith S.M., Li J. Genetic regulation of shoot architecture. Annu. Rev. Plant Biol. 2018;69:437–468. PubMed

Weijers D., Franke-van Dijk M., Vencken R.J., Quint A., Hooykaas P., Offringa R. An Arabidopsis Minute-like phenotype caused by a semi-dominant mutation in a RIBOSOMAL PROTEIN S5 gene. Development. 2001;128:4289–4299. PubMed

Yang B., Minne M., Brunoni F., Plačková L., Petřík I., Sun Y., Nolf J., Smet W., Verstaen K., Wendrich J.R., et al. Non-cell autonomous and spatiotemporal signalling from a tissue organizer orchestrates root vascular development. Native Plants. 2021;7:1485–1494. PubMed PMC

Zhang F., Gonzalez A., Zhao M., Payne C.T., Lloyd A. A network of redundant bHLH proteins functions in all TTG1-dependent pathways of Arabidopsis. Development. 2003;130:4859–4869. PubMed

Zhao M., Morohashi K., Hatlestad G., Grotewold E., Lloyd A. The TTG1-bHLH-MYB complex controls trichome cell fate and patterning through direct targeting of regulatory loci. Development. 2008;135:1991–1999. PubMed

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Cytokinins - regulators of de novo shoot organogenesis

. 2023 ; 14 () : 1239133. [epub] 20230818

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace