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• W2057100981 abstract "Recent studies have revealed important new details of how cytokinin-dependent mechanisms control plant growth. Intriguingly, cytokinins are involved in both maintaining meristems and promoting differentiation. Recent studies have revealed important new details of how cytokinin-dependent mechanisms control plant growth. Intriguingly, cytokinins are involved in both maintaining meristems and promoting differentiation. Cytokinins were discovered 50 years ago as small adenine-derived molecules essential for plant growth and cell division [1Skoog F. Miller C.O. Chemical regulation of growth and organ formation in plant tissue cultures in vitro.Symp. Soc. Exp. Biol. 1957; 11: 118-131PubMed Google Scholar]. The last decade saw the discovery of genes required for the synthesis, degradation and perception of cytokinins, and for their immediate downstream transcriptional effectors [2Kakimoto T. Perception and signal transduction of cytokinins.Annu. Rev. Plant Biol. 2003; 54: 605-628Crossref PubMed Scopus (266) Google Scholar, 3Sakakibara H. Cytokinins: activity, biosynthesis, and translocation.Annu. Rev. Plant Biol. 2006; 57: 431-449Crossref PubMed Scopus (835) Google Scholar]. Despite these advances, how cytokinins cause changes to plant growth behavior is still poorly understood. Four new studies [4Tirichine L. Sandal N. Madsen L.H. Radutoiu S. Albrektsen A.S. Sato S. Asamizu E. Tabata S. Stougaard J. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis.Science. 2007; 315: 104-107Crossref PubMed Scopus (368) Google Scholar, 5Murray J.D. Karas B.J. Sato S. Tabata S. Amyot L. Szczyglowski K. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis.Science. 2007; 315: 101-104Crossref PubMed Scopus (357) Google Scholar, 6Kurakawa 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: 652-655Crossref PubMed Scopus (558) Google Scholar, 7Dello Ioio R. Linhares F.S. Scacchi E. Casamitjana-Martinez E. Heidstra R. Constantino P. Sabatini S. Cytokinins determine Arabidopsis root meristem size by controlling cell differentiation.Curr. Biol. 2007; 17: 678-682Abstract Full Text Full Text PDF PubMed Scopus (521) Google Scholar] have revealed exciting new mechanistic details of how cytokinins are required for meristem maintenance, symbiotic nodule formation and for differentiation at the apical end of the root meristem. The committing step of cytokinin synthesis is catalyzed by iso-pentenyl transferases, optionally followed by a cytochrome P450-dependent hydroxylation reaction, after which the sugar-phosphate moiety is cleaved off to yield the active cytokinin [3Sakakibara H. Cytokinins: activity, biosynthesis, and translocation.Annu. Rev. Plant Biol. 2006; 57: 431-449Crossref PubMed Scopus (835) Google Scholar]. Cytokinins are perceived by transmembrane histidine kinase receptors (AHKs) and the ensuing phosphorelay is then transmitted to the nucleus via AHP proteins to regulate the activity of genes encoding response regulators (ARRs) [2Kakimoto T. Perception and signal transduction of cytokinins.Annu. Rev. Plant Biol. 2003; 54: 605-628Crossref PubMed Scopus (266) Google Scholar]. ARRs come in two flavors: the B-type, which transcriptionally regulate many genes, including the A-type, which interfere with AHP function to dampen the level of responsivity to cytokinin. Thus, the proximal cytokinin effector network is constructed with a negative feedback loop to control the magnitude of subsequent responses [2Kakimoto T. Perception and signal transduction of cytokinins.Annu. Rev. Plant Biol. 2003; 54: 605-628Crossref PubMed Scopus (266) Google Scholar], and this provides an elegant mechanism for other inputs to control cellular responses to cytokinin [8Leibfried A. To J.P. Busch W. Stehling S. Kehle A. Demar M. Kieber J.J. Lohmann J.U. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators.Nature. 2005; 438: 1172-1175Crossref PubMed Scopus (575) Google Scholar]. Shoot apical meristem activity requires high cytokinin levels, and at least two components of the meristem gene regulatory network responsible for maintenance of stem cells and their indeterminate progeny are known: KNOX transcription factors, which are expressed in undifferentiated cells of the meristem, activate the expression of at least two genes for iso-pentenyl transferases, while WUSCHEL (WUS), which is required to maintain the stem cell niche of the shoot apical meristem, negatively regulates the expression of some genes for A-type ARRs [8Leibfried A. To J.P. Busch W. Stehling S. Kehle A. Demar M. Kieber J.J. Lohmann J.U. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators.Nature. 2005; 438: 1172-1175Crossref PubMed Scopus (575) Google Scholar, 9Jasinski S. Piazza P. Craft J. Hay A. Woolley L. Rieu I. Phillips A. Hedden P. Tsiantis M. KNOX action in Arabidopsis Is mediated by coordinate regulation of cytokinin and gibberellin activities.Curr. Biol. 2005; 15: 1560-1565Abstract Full Text Full Text PDF PubMed Scopus (472) Google Scholar]. The inactivation of multiple genes for A-type ARRs causes a relatively subtle phenotype [10To J.P. Haberer G. Ferreira F.J. Deruere J. Mason M.G. Schaller G.E. Alonso J.M. Ecker J.R. Kieber J.J. Type-A Arabidopsis response regulators are partially redundant negative regulators of cytokinin signaling.Plant Cell. 2004; 16: 658-671Crossref PubMed Scopus (475) Google Scholar], but expression of a constitutively active ARR has a strong meristem phenotype [8Leibfried A. To J.P. Busch W. Stehling S. Kehle A. Demar M. Kieber J.J. Lohmann J.U. WUSCHEL controls meristem function by direct regulation of cytokinin-inducible response regulators.Nature. 2005; 438: 1172-1175Crossref PubMed Scopus (575) Google Scholar]; the biological functions of individual B-type ARRs are not yet well known. A further mystery is how exactly the cellular machinery controlling growth is engaged by the cytokinin signaling network, but it has been shown that gratuitous cyclin D3 expression in Arabidopsis mediates some of the effects of cytokinin on proliferation [11Riou-Khamlichi C. Huntley R. Jacqmard A. Murray J.A. Cytokinin activation of Arabidopsis cell division through a D-type cyclin.Science. 1999; 283: 1541-1544Crossref PubMed Scopus (605) Google Scholar]. Kurakawa et al. [6Kurakawa 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: 652-655Crossref PubMed Scopus (558) Google Scholar] have now discovered an essential novel component of the cytokinin biosynthetic machinery. They identified the LONELY GUY (LOG) locus, which is required for meristem maintenance in rice. In recessive log mutants, the meristem prematurely terminates. LOG is the founding member of a small gene family found in both rice and Arabidopsis and encodes an enzyme which directly converts biologically inactive cytokinin nucleotides to active cytokinins. It was previously thought that this conversion was carried out in a two-step reaction, but the necessary enzymes had not previously been identified (Figure 1). LOG is expressed specifically in the stem cells of the shoot apical meristem and their immediate progeny, and together with the earlier observation that KNOX genes activate expression of genes for iso-pentenyl transferases, this suggests that these cells autonomously produce cytokinins. This would be advantageous on at least three counts. It would provide a positive reinforcement of the functional identity of shoot apical meristem cells by generating a high cytokinin environment. Moreover, it could provide a mechanism for directly coupling meristem activity to environmental cues that promote growth. For example, shoot apical meristem activity is promoted by abundant mineral nitrogen, nitrate for example, and nitrate promotes expression of genes encoding iso-pentenyl transferases [12Miyawaki K. Matsumoto-Kitano M. Kakimoto T. Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate.Plant J. 2004; 37: 128-138Crossref PubMed Scopus (441) Google Scholar]. Lastly, cytokinin production by meristem cells might highlight a salient feature of meristem gene regulatory networks: because plant cells are not mobile, such paracrine signaling may be essential to coordinate growth and proliferation in adjacent cells and to maintain a homeostatically stable cellular state. Cytokinin is not only essential for meristem maintenance, but also involved in establishing new meristems: for example, transgenic plants overexpressing genes for cytokinin oxidases, which are involved in cytokinin degradation, have increased lateral root formation [13Lohar D.P. Schaff J.E. Laskey J.G. Kieber J.J. Bilyeu K.D. Bird D.M. Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses.Plant J. 2004; 38: 203-214Crossref PubMed Scopus (237) Google Scholar, 14Werner T. Motyka V. Strnad M. Schmulling T. Regulation of plant growth by cytokinin.Proc. Natl. Acad. Sci. USA. 2001; 98: 10487-10492Crossref PubMed Scopus (697) Google Scholar]. The nodules that form as a consequence of a symbiotic interaction between nitrogen-fixing bacteria, such as Rhizobium spp., and susceptible plants, such as Lotus, recapitulate many aspects of lateral root formation (for example, stimulation of proliferation and outgrowth from internal tissues of the root; Figure 2). However, nodulation responds in the opposite manner to cytokinins: cytokinin treatments stimulate nodulation and transgenic plants with reduced cytokinin levels, as a result of overexpression of genes for cytokinin oxidases, produce significantly fewer nodules [13Lohar D.P. Schaff J.E. Laskey J.G. Kieber J.J. Bilyeu K.D. Bird D.M. Cytokinins play opposite roles in lateral root formation, and nematode and Rhizobial symbioses.Plant J. 2004; 38: 203-214Crossref PubMed Scopus (237) Google Scholar]. Two groups [4Tirichine L. Sandal N. Madsen L.H. Radutoiu S. Albrektsen A.S. Sato S. Asamizu E. Tabata S. Stougaard J. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis.Science. 2007; 315: 104-107Crossref PubMed Scopus (368) Google Scholar, 5Murray J.D. Karas B.J. Sato S. Tabata S. Amyot L. Szczyglowski K. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis.Science. 2007; 315: 101-104Crossref PubMed Scopus (357) Google Scholar] now report that AHK cytokinin receptors are crucial for the growth of nodules: Tirichine et al. [4Tirichine L. Sandal N. Madsen L.H. Radutoiu S. Albrektsen A.S. Sato S. Asamizu E. Tabata S. Stougaard J. A gain-of-function mutation in a cytokinin receptor triggers spontaneous root nodule organogenesis.Science. 2007; 315: 104-107Crossref PubMed Scopus (368) Google Scholar] identified a gain-of-function allele, spontaneous nodule formation 2 (snf2), of a Lotus japonicus gene for a histidine kinase (Lhk1) while Murray et al. [5Murray J.D. Karas B.J. Sato S. Tabata S. Amyot L. Szczyglowski K. A cytokinin perception mutant colonized by Rhizobium in the absence of nodule organogenesis.Science. 2007; 315: 101-104Crossref PubMed Scopus (357) Google Scholar] identified a loss-of-function allele, HYPERINFECTED 1 (HIT1), of the same Lhk1 gene. In the snf2 mutant, spontaneous root nodule formation is triggered, even in the absence of Mesorhizobium infection; while in the HIT1 mutant, nodules cannot be established, leading to a hyper-infected phenotype of roots with supernumerary infection threads. Stimulation of nodule initiation was shown to be genetically downstream of nod factor recognition, the earliest detectable event following the plant–microbe interaction at the root epidermis. It will be intriguing to dissect the downstream cytokinin-responsive effector network involved in nodulation in detail, as this could provide crucial information for engineering nodulation in crop plants not naturally capable of symbiotic nitrogen fixation. Arabidopsis plants overexpressing genes for cytokinin oxidases have larger root meristems and, because of the larger population of proliferating cells, more rapidly growing roots, indicating that cytokinins also regulate root growth [14Werner T. Motyka V. Strnad M. Schmulling T. Regulation of plant growth by cytokinin.Proc. Natl. Acad. Sci. USA. 2001; 98: 10487-10492Crossref PubMed Scopus (697) Google Scholar, 15Werner T. Motyka V. Laucou V. Smets R. Van Onckelen H. Schmulling T. 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: 2532-2550Crossref PubMed Scopus (982) Google Scholar]. Dello Ioio et al. [7Dello Ioio R. Linhares F.S. Scacchi E. Casamitjana-Martinez E. Heidstra R. Constantino P. Sabatini S. Cytokinins determine Arabidopsis root meristem size by controlling cell differentiation.Curr. Biol. 2007; 17: 678-682Abstract Full Text Full Text PDF PubMed Scopus (521) Google Scholar] have now dissected this role of cytokinins in greater detail. They first showed that cytokinin specifically affects cells exiting the meristem (the transition zone), but does not alter the rate of proliferation in the zone of meristem with high levels of cell division (Figure 2). As a corollary, in iso-pentenyl transferase triple mutants, which are severely compromised in cytokinin accumulation, root growth and meristem size is strongly enhanced. By spatially selective expression of a cytokinin oxidase gene in different domains of the root meristem, the authors then showed that cytokinin levels specifically in the transition zone control meristem size, while reduced cytokinin in the meristem has no effect on size. At the tissue level, it suffices to alter cytokinin levels in the vasculature of the transition zone to affect meristem size, while changes in other tissues had no effect. Dello Ioio et al. [7Dello Ioio R. Linhares F.S. Scacchi E. Casamitjana-Martinez E. Heidstra R. Constantino P. Sabatini S. Cytokinins determine Arabidopsis root meristem size by controlling cell differentiation.Curr. Biol. 2007; 17: 678-682Abstract Full Text Full Text PDF PubMed Scopus (521) Google Scholar] then analyzed whether root growth rate is controlled by any single cytokinin receptor. They found that the AHK3 cytokinin receptor specifically mediates this effect of cytokinin, while AHK2 and AHK4 had no significant effect on root growth. They also found evidence for a specific role of B-type ARRs in controlling root growth downstream of AHK3: ARR12 mediates the increase in meristem size early in seedling development, while ARR1 acts later to restrict meristem growth. This makes ARR1 a prime candidate for being the mediator of metabolic and environmental cues that affect root growth. These exciting papers highlight the significance and multiple roles of cytokinins in coordinating growth behavior in plants and underscore the potential for manipulating cellular responses to cytokinin to alter plant growth and improve crop productivity. Cynics and old hands in plant biology will chuckle and say that this just confirms what they had been saying for decades: counteracting gradients of auxin and cytokinins control root meristem activity. But the big difference is that we now know which genes are responsible for the effects, permitting the identification of their targets for regulation. Undoubtedly, the current gaps in understanding how ARRs and other transcription factors [16Rashotte A.M. Mason M.G. Hutchison C.E. Ferreira F.J. Schaller G.E. Kieber J.J. A subset of Arabidopsis AP2 transcription factors mediates cytokinin responses in concert with a two-component pathway.Proc. Natl. Acad. Sci. USA. 2006; 103: 11081-11085Crossref PubMed Scopus (259) Google Scholar] mechanistically control changes to growth behavior in response to cytokinins will soon be closed." @default.
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• W2057100981 title "Plant Meristems: Cytokinins — The Alpha and Omega of the Meristem" @default.
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