bHLH heterodimer complex variations regulate cell proliferation activity in the meristems of Arabidopsis thaliana
Status PubMed-not-MEDLINE Jazyk angličtina Země Spojené státy americké Médium electronic-ecollection
Typ dokumentu časopisecké články
PubMed
36339262
PubMed Central
PMC9626673
DOI
10.1016/j.isci.2022.105364
PII: S2589-0042(22)01636-4
Knihovny.cz E-zdroje
- Klíčová slova
- Biological sciences, Molecular plant pathology, Natural sciences, Plant biology,
- Publikační typ
- časopisecké články MeSH
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
Cytokinins - regulators of de novo shoot organogenesis