Ligand-binding properties and subcellular localization of maize cytokinin receptors

Lomin, Sergey N.; Yonekura‐Sakakibara, Keiko; Romanov, Georgy A.; Sakakibara, Hitoshi

doi:10.1093/jxb/err220

Cited by 138 publications

(152 citation statements)

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“…In addition, ER localization of the cytokinin receptor ZmHK1 of Zea mays has also been demonstrated very recently (Lomin et al, 2011). This highlights the important role of this cellular compartment in cytokinin signaling and, more generally, the necessity of considering the subcellular topology of hormone metabolism and signaling as a relevant factor and additional layer of regulation in hormone biology.…”

Section: A Modified Model For Cytokinin Signalingmentioning

confidence: 85%

The Cytokinin Receptors of Arabidopsis Are Located Mainly to the Endoplasmic Reticulum

et al. 2011

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The plant hormone cytokinin is perceived by membrane-located sensor histidine kinases. Arabidopsis (Arabidopsis thaliana) possesses three cytokinin receptors: ARABIDOPSIS HISTIDINE KINASE2 (AHK2), AHK3, and CYTOKININ RESPONSE1/ AHK4. The current model predicts perception of the cytokinin signal at the plasma membrane. However, cytokinin-binding studies with membrane fractions separated by two-phase partitioning showed that in the wild type, as well as in mutants retaining only single cytokinin receptors, the major part of specific cytokinin binding was associated with endomembranes. Leaf epidermal cells of tobacco (Nicotiana benthamiana) expressing receptor-green fluorescent protein fusion proteins and bimolecular fluorescence complementation analysis showed strong fluorescence of the endoplasmic reticulum (ER) network for all three receptors. Furthermore, separation of the microsomal fraction of Arabidopsis plants expressing Myc-tagged AHK2 and AHK3 receptors by sucrose gradient centrifugation followed by immunoblotting displayed the Mg 2+ -dependent density shift typical of ER membrane proteins. Cytokinin-binding assays, fluorescent fusion proteins, and biochemical fractionation all showed that the large majority of cytokinin receptors are localized to the ER, suggesting a central role of this compartment in cytokinin signaling. A modified model for cytokinin signaling is proposed.

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Section: A Modified Model For Cytokinin Signalingmentioning

confidence: 85%

The Cytokinin Receptors of Arabidopsis Are Located Mainly to the Endoplasmic Reticulum

et al. 2011

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“…Three very recent studies reported the localisation of the Arabidopsis and maize CK receptors in the ER (Fig. 4; Wulfetange et al 2011;Lomin et al 2011;Caesar et al 2011). Although the general concept of CK signalling assumed that CK receptors are located in the plasma membrane (Kim et al 2006) and sense the extracellular hormone (Inoue et al 2001;Ueguchi et al 2001a), data on the pH dependence of CK binding by AHK3 and CRE1/AHK4 support the function of the receptors inside the plant cell (Romanov et al 2006).…”

Section: Ck Perception and Signal Transductionmentioning

confidence: 97%

“…Model of CK signalling and cellular distribution of biosynthetic CKs (AtITPs, in green rectangles) and degradation CKs (AtCKXs, in red rectangles) enzymes in Arabidopsis thaliana. CK signalling involves AHK receptors (AHK2, AHK3 and CRE1/AHK4) localised in the plasma membrane (Kim et al 2006) and the endoplasmatic reticulum (ER; Lomin et al 2011;Wulfetange et al 2011;Caesar et al 2011). CKI1 is involved in CK signalling but does not perceive CKs (Hejátko et al 2009;Yamada et al 2001).…”

Section: Ck Metabolismmentioning

confidence: 99%

“…Expression of CRE1/AHK4, AHK3 and AHK2-CHASE-TM (AHK2-CHASE including the two adjacent transmembrane domains) in Escherichia coli DrcsC and cps::lacZ mutant strains producing b-galactosidase in reaction to CK , and direct receptor binding assays (Romanov et al 2005) were used for molecular and biochemical characterisation of the receptors Yamada et al 2001;Spíchal et al 2004;Romanov et al 2006). It has been shown that the receptors bind isoprenoid and aromatic CKs, and also thidiazuron (a derivative of phenylurea), in a highly specific manner with K d in the nanomolar range Romanov et al 2005;Romanov et al 2006;Lomin et al 2011;Stolz et al 2011). Individual receptors of Arabidopsis thaliana are most sensitive to the bases of the isoprenoid-type CKs and thidiazuron, but differ in their recognition of CK metabolites.…”

Section: Ck Perception and Signal Transductionmentioning

confidence: 99%

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Cytokinins - recent news and views of evolutionally old molecules

Spíchal¹

2012

Functional Plant Biol.

159

169

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Cytokinins (CKs) are evolutionally old and highly conserved low-mass molecules that have been identified in almost all known organisms. In plants, they evolved into an important group of plant hormones controlling many physiological and developmental processes throughout the whole lifespan of the plant. CKs and their functions are, however, not unique to plants. In this review, the strategies and mechanisms of plants – and phylogenetically distinct plant-interacting organisms such as bacteria, fungi, nematodes and insects employing CKs or regulation of CK status in plants – are described and put into their evolutionary context. The major breakthroughs made in the last decade in the fields of CK biosynthesis, degradation and signalling are also summarised.

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“…3 At the cellular level, cytokinins are recognized by CHASE-domain-containing histidine kinases located in the plasma membrane 4 and/or the endoplasmic reticulum (ER). [5][6][7] Upon cytokinin binding, type-B response regulators in the nucleus are activated via His-Asp multi-step phospho-relays similar to those observed in bacterial twocomponent systems (TCS). In Arabidopsis, 11 type-B response regulators (ARRs) have been identified and act as transcription factors with redundant function that participate in various developmental processes mediated by cytokinins.…”

Section: 2mentioning

confidence: 86%

Attenuation of cytokinin signaling via proteolysis of a Type-B response regulator

Kim

Hwang²

2012

Plant Signaling & Behavior

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Type-B response regulators (ARRs) are a group of transcription factors that are activated by cytokinin-initiated phosphorelays and regulate the expression of cytokinin-responsive genes. Recently, we reported that proteolysis of ARR2 in Arabidopsis is facilitated by cytokinins, resulting in attenuation of the signaling output of two-component circuitry. Interestingly, despite similarities in the primary structures and conserved receiver domains, the proteolytic properties of ARR2 are distinct from those of the other type-B ARRs. Using a gain-of-function mutant (ARR2 K90G ) resistant to protein degradation, we clearly demonstrated that increased levels of ARR2 affected cytokinin-mediated processes such as primary root growth, callus induction, hypocotyl elongation and leaf senescence. At the molecular level, expression of type-A ARRs was increased in transgenics expressing ARR2 K90G , resulting in enhanced cytokinin sensitivity. Here, we describe these findings and how they may be incorporated into the currently accepted model for the regulation of cytokinin signaling. In addition, we describe the proteomic approaches used to identify proteins that interact with ARR2. The putative roles of ARR2 proteolysis are also addressed with regard to other developmental processes. In conclusion, cytokinin-facilitated degradation of ARR2 must be appreciated as a post-translational event important for regulating cytokinin signaling intensity.Cytokinins are a group of phytohormones that mediate various developmental processes (e.g., seed germination, vasculature development, meristem maintenance, apical dominance and leaf senescence) and (a)biotic stress adaptation processes in plants. 1,2 The physiological effects of cytokinin responses are largely modulated by cytokinin levels and the activation of target signaling pathways.3 At the cellular level, cytokinins are recognized by CHASE-domain-containing histidine kinases located in the plasma membrane 4 and/or the endoplasmic reticulum (ER). [5][6][7] Upon cytokinin binding, type-B response regulators in the nucleus are activated via His-Asp multi-step phospho-relays similar to those observed in bacterial twocomponent systems (TCS). In Arabidopsis, 11 type-B response regulators (ARRs) have been identified and act as transcription factors with redundant function that participate in various developmental processes mediated by cytokinins. 8The output intensities of TCS signaling are primarily regulated by post-transcriptional and post-translational modifications of TCS components.3 For example, in Arabidopsis, the expression levels of AHKs (histidine kinase proteins), AHPs (histidine phosphotransfer proteins) and ARRs fluctuate in response to changing environmental conditions.3 At the protein level, sequential phosphorylations initiated by cytokinin receptors are essential for propagating cytokinin signals. However, the duration and intensity of these phosphorylation-propagated signals must be properly mediated by negative regulatory mechanisms. AHK4, a histidine kinase receptor...

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Ligand-binding properties and subcellular localization of maize cytokinin receptors

Cited by 138 publications

References 53 publications

The Cytokinin Receptors of Arabidopsis Are Located Mainly to the Endoplasmic Reticulum

The Cytokinin Receptors of Arabidopsis Are Located Mainly to the Endoplasmic Reticulum

Cytokinins - recent news and views of evolutionally old molecules

Attenuation of cytokinin signaling via proteolysis of a Type-B response regulator

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