Plant membrane assays with cytokinin receptors underpin the unique role of free cytokinin bases as biologically active ligands

Lomin, Sergey N.; Krivosheev, Dmitry M.; Steklov, Mikhail; Arkhipov, Dmitry V.; Osolodkin, Dmitry I.; Schmülling, Thomas; Romanov, Georgy A.

doi:10.1093/jxb/eru522

Cited by 127 publications

(171 citation statements)

References 70 publications

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“…A significant stomatal closure was observed from 10 nM with an optimal effect at 1 mM. These concentrations are physiologically relevant as AHK3 has a high affinity for t-Z with a K d of 4.3 nM (Lomin et al, 2015). Moreover, we found that, within the CK receptors, only AHK3 participates in t-Zmediated stomatal responses.…”

Section: A Plant Growth-promoting Hormone Induces Stomatal Closurementioning

confidence: 54%

Cytokinin-Mediated Regulation of Reactive Oxygen Species Homeostasis Modulates Stomatal Immunity in Arabidopsis

et al. 2017

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Stomata play an important role in preinvasive defense responses by limiting pathogen entry into leaves. Although the stress hormones salicylic acid (SA) and abscisic acid (ABA) are known to regulate stomatal immunity, the role of growth promoting hormones is far from understood. Here, we show that in Arabidopsis thaliana, cytokinins (CKs) function in stomatal defense responses. The cytokinin receptor HISTIDINE KINASE3 (AHK3) and RESPONSE REGULATOR2 (ARR2) promote stomatal closure triggered by pathogen-associated molecular pattern (PAMP) and resistance to Pseudomonas syringae pv tomato bacteria. Importantly, the cytokinin trans-zeatin induces stomatal closure and accumulation of reactive oxygen species (ROS) in guard cells through AHK3 and ARR2 in an SA-dependent and ABA-independent manner. Using pharmacological and reverse genetics approaches, we found that CK-mediated stomatal responses involve the apoplastic peroxidases PRX4, PRX33, PRX34, and PRX71, but not the NADPH oxidases RBOHD and RBOHF. Moreover, ARR2 directly activates the expression of PRX33 and PRX34, which are required for SA-and PAMP-triggered ROS production. Thus, the CK signaling pathway regulates ROS homeostasis in guard cells, which leads to enhanced stomatal immunity and plant resistance to bacteria.

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Section: A Plant Growth-promoting Hormone Induces Stomatal Closurementioning

confidence: 54%

Cytokinin-Mediated Regulation of Reactive Oxygen Species Homeostasis Modulates Stomatal Immunity in Arabidopsis

et al. 2017

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“…The cytokinin molecule may be inactivated by the removal of the side chain by cytokinin oxidase/dehydrogenase (CKX), or metabolized to storage O-glucosides (which can be released to active forms by b-glucosidases) or 7-and 9-glucosides (which appear not to be reactivated). The free bases are considered the active forms perceived by cytokinin receptors (Lomin et al, 2015) and the ribosides the translocated forms. Cytokinins may also be formed by tRNA-IPTs.…”

Section: Introductionmentioning

confidence: 99%

Infection byRhodococcus fasciansmaintains cotyledons as a sink tissue for the pathogen

Dhandapani

Song

Novák

et al. 2016

Ann Bot

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Background and Aims Pisum sativum L. (pea) seed is a source of carbohydrate and protein for the developing plant. By studying pea seeds inoculated by the cytokinin-producing bacterium, Rhodococcus fascians, we sought to determine the impact of both an epiphytic (avirulent) strain and a pathogenic strain on source-sink activity within the cotyledons during and following germination.Methods Bacterial spread was monitored microscopically, and real-time reverse transcription-quantitative PCR was used to determine the expression of cytokinin biosynthesis, degradation and response regulator gene family members, along with expression of family members of SWEET, SUT, CWINV and AAP genes -gene families identified initially in pea by transcriptomic analysis. The endogenous cytokinin content was also determined.Key Results The cotyledons infected by the virulent strain remained intact and turned green, while multiple shoots were formed and root growth was reduced. The epiphytic strain had no such marked impact. Isopentenyl adenine was elevated in the cotyledons infected by the virulent strain. Strong expression of RfIPT, RfLOG and RfCKX was detected in the cotyledons infected by the virulent strain throughout the experiment, with elevated expression also observed for PsSWEET, PsSUT and PsINV gene family members. The epiphytic strain had some impact on the expression of these genes, especially at the later stages of reserve mobilization from the cotyledons.Conclusions The pathogenic strain retained the cotyledons as a sink tissue for the pathogen rather than the cotyledon converting completely to a source tissue for the germinating plant. We suggest that the interaction of cytokinins, CWINVs and SWEETs may lead to the loss of apical dominance and the appearance of multiple shoots.

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“…This suggests that LCO-induced accumulation of 414iP is more sensitive to negative regulation by ethylene, as compared to accumulation of tZ.415However, the mechanistic basis for this difference is currently unclear. Sensitivity to different 416 cytokinins differs between individual cytokinin receptors(Lomin et al, 2015; Stolz et al, 417 2011). The arabidopsis AtAHK4/AtCRE1 cytokinin receptor possesses similar sensitivity to 418 both iP and tZ(Lomin et al, 2015;Stolz et al, 2011).…”

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confidence: 99%

“…Sensitivity to different 416 cytokinins differs between individual cytokinin receptors(Lomin et al, 2015; Stolz et al, 417 2011). The arabidopsis AtAHK4/AtCRE1 cytokinin receptor possesses similar sensitivity to 418 both iP and tZ(Lomin et al, 2015;Stolz et al, 2011). AtAHK4/MtCRE1 represents that 419 closest ortholog of MtCRE1 and LjLHK1 and was shown to functionally complement the 420 nodulation defect of the Ljlhk1 mutant(Gonzalez-Rizzo et al, 2006;Held et al, 2014; Op den 421 Camp et al, 2011;Plet et al, 2011).…”

mentioning

confidence: 99%

Rhizobium Lipo-chitooligosaccharide Signaling Triggers Accumulation of Cytokinins in Medicago truncatula Roots

Zeijl¹,

Camp²,

et al. 2015

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Legume rhizobium symbiosis is initiated upon perception of bacterial secreted lipo-chitooligosaccharides (LCOs). Perception of these signals by the plant initiates a signaling cascade that leads to nodule formation. Several studies have implicated a function for cytokinin in this process. However, whether cytokinin accumulation and subsequent signaling are an integral part of rhizobium LCO signaling remains elusive. Here, we show that cytokinin signaling is required for the majority of transcriptional changes induced by rhizobium LCOs. In addition, we demonstrate that several cytokinins accumulate in the root susceptible zone 3 h after rhizobium LCO application, including the biologically most active cytokinins, trans-zeatin and isopentenyl adenine. These responses are dependent on calcium- and calmodulin-dependent protein kinase (CCaMK), a key protein in rhizobial LCO-induced signaling. Analysis of the ethylene-insensitive Mtein2/Mtsickle mutant showed that LCO-induced cytokinin accumulation is negatively regulated by ethylene. Together with transcriptional induction of ethylene biosynthesis genes, it suggests a feedback loop negatively regulating LCO signaling and subsequent cytokinin accumulation. We argue that cytokinin accumulation is a key step in the pathway leading to nodule organogenesis and that this is tightly controlled by feedback loops.

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Plant membrane assays with cytokinin receptors underpin the unique role of free cytokinin bases as biologically active ligands

Abstract: HighlightCytokinin receptors studied in a novel plant assay system recognize cytokinin ribosides poorly, unlike cytokinin bases. Molecular modelling explained this receptor feature. Some receptors were suggested to function as pH sensors.

Cited by 127 publications

References 70 publications

Cytokinin-Mediated Regulation of Reactive Oxygen Species Homeostasis Modulates Stomatal Immunity in Arabidopsis

Cytokinin-Mediated Regulation of Reactive Oxygen Species Homeostasis Modulates Stomatal Immunity in Arabidopsis

Infection byRhodococcus fasciansmaintains cotyledons as a sink tissue for the pathogen

Rhizobium Lipo-chitooligosaccharide Signaling Triggers Accumulation of Cytokinins in Medicago truncatula Roots

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