Cytokinins modulate auxin-induced organogenesis in plants via regulation of the auxin efflux
Jazyk angličtina Země Spojené státy americké Médium print-electronic
Typ dokumentu časopisecké články, práce podpořená grantem
PubMed
19211794
PubMed Central
PMC2640219
DOI
10.1073/pnas.0811539106
PII: 0811539106
Knihovny.cz E-zdroje
- MeSH
- Arabidopsis účinky léků růst a vývoj metabolismus MeSH
- biologický transport MeSH
- cytokininy farmakologie MeSH
- kořeny rostlin účinky léků růst a vývoj metabolismus MeSH
- kyseliny indoloctové metabolismus MeSH
- signální transdukce MeSH
- Publikační typ
- časopisecké články MeSH
- práce podpořená grantem MeSH
- Názvy látek
- cytokininy MeSH
- kyseliny indoloctové MeSH
Postembryonic de novo organogenesis represents an important competence evolved in plants that allows their physiological and developmental adaptation to changing environmental conditions. The phytohormones auxin and cytokinin (CK) are important regulators of the developmental fate of pluripotent plant cells. However, the molecular nature of their interaction(s) in control of plant organogenesis is largely unknown. Here, we show that CK modulates auxin-induced organogenesis (AIO) via regulation of the efflux-dependent intercellular auxin distribution. We used the hypocotyl explants-based in vitro system to study the mechanism underlying de novo organogenesis. We show that auxin, but not CK, is capable of triggering organogenesis in hypocotyl explants. The AIO is accompanied by endogenous CK production and tissue-specific activation of CK signaling. CK affects differential auxin distribution, and the CK-mediated modulation of organogenesis is simulated by inhibition of polar auxin transport. CK reduces auxin efflux from cultured tobacco cells and regulates expression of auxin efflux carriers from the PIN family in hypocotyl explants. Moreover, endogenous CK levels influence PIN transcription and are necessary to maintain intercellular auxin distribution in planta. Based on these findings, we propose a model in which auxin acts as a trigger of the organogenic processes, whose output is modulated by the endogenously produced CKs. We propose that an important mechanism of this CK action is its effect on auxin distribution via regulation of expression of auxin efflux carriers.
Zobrazit více v PubMed
Gierer A, et al. Regeneration of hydra from reaggregated cells. Nat New Biol. 1972;239:98–101. PubMed
Endo T, Bryant SV, Gardiner DM. A stepwise model system for limb regeneration. Dev Biol. 2004;270:135–145. PubMed
Skoog F, Miller CO. Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol. 1957;54:118–130. PubMed
Vieten A, Sauer M, Brewer PB, Friml J. Molecular and cellular aspects of auxin-transport-mediated development. Trends Plant Sci. 2007;12:160–168. PubMed
Tanaka H, Dhonukshe P, Brewer PB, Friml J. Spatiotemporal asymmetric auxin distribution: A means to coordinate plant development. Cell Mol Life Sci. 2006;63:2738–2754. PubMed PMC
Friml J, et al. Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature. 2003;426:147–153. PubMed
Friml J, et al. AtPIN4 mediates sink-driven auxin gradients and root patterning in Arabidopsis. Cell. 2002;108:661–673. PubMed
Blilou I, et al. The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature. 2005;433:39–44. PubMed
Friml J, Wisniewska J, Benkova E, Mendgen K, Palme K. Lateral relocation of auxin efflux regulator PIN3 mediates tropism in Arabidopsis. Nature. 2002;415:806–809. PubMed
Luschnig C, Gaxiola RA, Grisafi P, Fink GR. EIR1, a root-specific protein involved in auxin transport, is required for gravitropism in Arabidopsis thaliana. Genes Dev. 1998;12:2175–2187. PubMed PMC
Marchant A, et al. AUX1 regulates root gravitropism in Arabidopsis by facilitating auxin uptake within root apical tissues. EMBO J. 1999;18:2066–2073. PubMed PMC
Heisler MG, et al. Patterns of auxin transport and gene expression during primordium development revealed by live imaging of the Arabidopsis inflorescence meristem. Curr Biol. 2005;15:1899–1911. PubMed
Benkova E, et al. Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell. 2003;115:591–602. PubMed
Reinhardt D, et al. Regulation of phyllotaxis by polar auxin transport. Nature. 2003;426:255–260. PubMed
Dubrovsky JG, et al. Auxin acts as a local morphogenetic trigger to specify lateral root founder cells. Proc Natl Acad Sci USA. 2008;105:8790–8794. PubMed PMC
Kurakawa T, et al. Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature. 2007;445:652–655. PubMed
Scheres B, et al. Mutations affecting the radial organization of the Arabidopsis root display specific defects throughout the embryonic axis. Development. 1995;121(1):53–62.
Mahonen AP, et al. Cytokinin signaling and its inhibitor AHP6 regulate cell fate during vascular development. Science. 2006;311:94–98. PubMed
Werner T, et al. Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell. 2003;15:2532–2550. PubMed PMC
Laplaze L, et al. Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell. 2007;19:3889–3900. PubMed PMC
Dello Ioio R, et al. Cytokinins determine Arabidopsis root-meristem size by controlling cell differentiation. Curr Biol. 2007;17:678–682. PubMed
Kuderova A, et al. Effects of conditional IPT-dependent cytokinin overproduction on root architecture of Arabidopsis seedlings. Plant Cell Physiol. 2008;49:570–582. PubMed
Riefler M, Novak O, Strnad M, Schmulling T. Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell. 2006;18:40–54. PubMed PMC
Tran LS, et al. Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc Natl Acad Sci USA. 2007;104:20623–20628. PubMed PMC
Kim HJ, et al. Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc Natl Acad Sci USA. 2006;103:814–819. PubMed PMC
To JP, Kieber JJ. Cytokinin signaling: Two-components and more. Trends Plant Sci. 2008;13:85–92. PubMed
Kubo M, Kakimoto T. The cytokinin-hypersensitive genes of Arabidopsis negatively regulate the cytokinin-signaling pathway for cell division and chloroplast development. Plant J. 2000;23:385–394. PubMed
D'Agostino IB, Deruere J, Kieber JJ. Characterization of the response of the Arabidopsis response regulator gene family to cytokinin. Plant Physiol. 2000;124:1706–1717. PubMed PMC
Higuchi M, et al. In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci USA. 2004;101:8821–8826. PubMed PMC
Nishimura C, et al. Histidine kinase homologs that act as cytokinin receptors possess overlapping functions in the regulation of shoot and root growth in Arabidopsis. Plant Cell. 2004;16:1365–1377. PubMed PMC
Popelkova H, et al. Kinetic and chemical analyses of the cytokinin dehydrogenase-catalysed reaction: Correlations with the crystal structure. Biochem J. 2006;398:113–124. PubMed PMC
Werner T, Kollmer I, Bartrina I, Holst K, Schmulling T. New insights into the biology of cytokinin degradation. Plant Biology. 2006;8:371–381. PubMed
Delbarre A, Muller P, Imhoff V, Guern J. Comparison of mechanisms controlling uptake and accumulation of 2,4-dichlorophenoxy acetic acid, naphthalene-1-acetic acid, and indole-3-acetic acid in suspension-cultured tobacco cells. Planta. 1996;198:532–541. PubMed
Petrasek J, et al. PIN proteins perform a rate-limiting function in cellular auxin efflux. Science. 2006;312:914–918. PubMed
Ulmasov T, Murfett J, Hagen G, Guilfoyle TJ. Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell. 1997;9:1963–1971. PubMed PMC
Sabatini S, et al. An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell. 1999;99:463–472. PubMed
Katekar GF, Geissler AE. Auxin transport inhibitors: IV. Evidence of a common mode of action for a proposed class of auxin transport inhibitors: The phytotropins. Plant Physiol. 1980;66:1190–1195. PubMed PMC
Petrasek J, et al. Do phytotropins inhibit auxin efflux by impairing vesicle traffic? Plant Physiol. 2003;131:254–263. PubMed PMC
Chae HS, Faure F, Kieber JJ. The eto1, eto2, and eto3 mutations and cytokinin treatment increase ethylene biosynthesis in Arabidopsis by increasing the stability of ACS protein. Plant Cell. 2003;15:545–559. PubMed PMC
Ruzicka K, et al. Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell. 2007;19:2197–2212. PubMed PMC
Swarup R, et al. Ethylene upregulates auxin biosynthesis in Arabidopsis seedlings to enhance inhibition of root cell elongation. Plant Cell. 2007;19:2186–2196. PubMed PMC
Yang SF, Hoffman NE. Ethylene biosynthesis and its regulation in higher-plants. Annu Rev Plant Physiol Plant Mol Biol. 1984;35:155–189.
Hardtke CS. Transcriptional auxin-brassinosteroid crosstalk: Who's talking? BioEssays. 2007;29:1115–1123. PubMed
Gordon SP, et al. Pattern formation during de novo assembly of the Arabidopsis shoot meristem. Development. 2007;134:3539–3548. PubMed
Muller B, Sheen J. Cytokinin and auxin interaction in root stem-cell specification during early embryogenesis. Nature. 2008;453:1094–1097. PubMed PMC
Cytokinins - regulators of de novo shoot organogenesis
What Has Been Seen Cannot Be Unseen-Detecting Auxin In Vivo
Cytokinin-Auxin Crosstalk in the Gynoecial Primordium Ensures Correct Domain Patterning
Plants under Stress: Involvement of Auxin and Cytokinin
Cytokinin response factors regulate PIN-FORMED auxin transporters
Auxin influx inhibitors 1-NOA, 2-NOA, and CHPAA interfere with membrane dynamics in tobacco cells