Cytokinin signaling: from the ER or from the PM? That is the question!

Romanov, Georgy A.; Lomin, Sergey N.; Schmülling, Thomas

doi:10.1111/nph.14991

Cited by 89 publications

(95 citation statements)

References 113 publications

(204 reference statements)

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“… Cytokinins are mobile multifunctional plant hormones with roles in development and stress resilience 1,2 . Although cytokinin receptors are substantially localised to the endoplasmic reticulum 3–5 , the cellular sites of cytokinin perception continue to be debated 1,6,7 . Several cytokinin types display bioactivity 8,9 and recently a cell-specific cytokinin gradient was reported in roots 10 .…”

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confidence: 99%

Cell-surface receptors enable perception of extracellular cytokinins

Antoniadi

Novák

Gelová

et al. 2019

Preprint

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phone 30 +46 90 786 8355 karin.ljung@slu.se 31 32Cytokinins are mobile multifunctional plant hormones with roles in development and 33 stress resilience 1,2 . Although cytokinin receptors are substantially localised to the 34 endoplasmic reticulum [3][4][5] , the cellular sites of cytokinin perception continue to be 35 debated 1,6,7 . Several cytokinin types display bioactivity 8,9 and recently a cell-specific 36 cytokinin gradient was reported in roots 10 . Yet, the importance of spatially heterogeneous 37 cytokinin distribution and the specific cytokinin(s) that account for the different responses 38 remain unclear. Here we show that cytokinin perception by plasma membrane receptors is 39 an effective path for cytokinin response in root cells. Readout from a Two Component 40 Signalling cytokinin-specific reporter (TCSn::GFP; 11 ) is closely matched to intracellular 41 cytokinin content, yet a proportion of bioactive cytokinins are detected in the extracellular 42 fluid. Using cytokinins covalently linked to beads that could not pass the plasma 43 membrane, we demonstrate that strong TCSn activation still occurs and that this response 44 is greatly diminished in cytokinin receptor mutants. Although intracellular receptors play 45 significant roles, we argue for a revision of concepts of cytokinin perception to include the 46 spatial dimensions. In particular, selective ligand-receptor affinities, cellular localisation 47 and tissue distribution of bioactive cytokinins, their receptors, transporters and 48 inactivation enzymes appear all to be components of the signalling regulatory 49 mechanisms. 50 Cytokinins are key hormones regulating cell division and differentiation, root and shoot 51 architecture, senescence and responses to environmental stresses 1 . The active forms are 52 the cytokinin free bases, which comprise a range of N 6 -modified adenine molecules 8,9 , 53 especially trans-zeatin (tZ) and isopentenyl adenine (iP). Homeostatic regulation of active 54 cytokinin pools occurs at the level of biosynthesis, and also through metabolic deactivation 55 by glucosylation, phosphoribosylation or irreversible degradation by cytokinin 56 dehydrogenase (CKX) 9,12 . Cytokinin signalling commences with perception of bioactive 57 molecules by hybrid histidine kinases (HKs) 1,13,14 . Several reports show GFP-fused 58 Arabidopsis HKs (AHKs) mainly localised to the endoplasmic reticulum (ER) membrane 3-5 , 59 yet the originally proposed extracellular site of cytokinin perception at plasma membrane 60 receptors 13,15,16 has never been discounted. Notably, several classes of cytokinin 61 3 transporters facilitate movement of cytokinins in and out of the cell 7 . Cytokinins binding to 62 receptors trigger a phosphorelay cascade, resulting in activation of B-type ARABIDOPSIS 63 RESPONSE REGULATORS (ARR-B) transcription factors 17 . The cytokinin-responsive synthetic 64 promoter fusion TCSn::GFP reflects global ARR-B transcriptional activity 11 and has facilitated 65 in vivo monitoring of cytokinin responses, leading t...

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confidence: 99%

Cell-surface receptors enable perception of extracellular cytokinins

Antoniadi

Novák

Gelová

et al. 2019

Preprint

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“…Different roles for root-derived t Z and t ZR have been reported by Osugi et al (2017). It might be that the ability of certain tissues to convert inactive t ZR to active t Z, as discussed in Romanov et al (2018), might have an impact on the plant’s response to photoperiod stress.…”

Section: Discussionmentioning

confidence: 95%

Root-derived trans-zeatin cytokinin protects Arabidopsis plants against photoperiod stress

Frank

Cortleven

Schmülling

2020

Preprint

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Running title: Protective role of root-borne cytokinin 1 2 Root-derived trans-zeatin cytokinin protects Arabidopsis plants against photoperiod 3 stress 4 5 ABSTRACT 27 Recently, a novel type of abiotic stress caused by a prolongation of the light period -coined 28 photoperiod stress -has been described in Arabidopsis. During the night after the 29 prolongation of the light period, stress and cell death marker genes are induced. The next day, 30 strongly stressed plants display a reduced photosynthetic efficiency and leaf cells eventually 31 enter programmed cell death. The phytohormone cytokinin (CK) acts as a negative regulator of 32 this photoperiod stress syndrome. In this study, we show that Arabidopsis wild-type plants 33 increase the CK concentration in response to photoperiod stress. Analysis of cytokinin 34 synthesis and transport mutants revealed that root-derived trans-zeatin (tZ)-type CKs protect 35 against photoperiod stress. The CK signaling proteins ARABIDOPSIS HISTIDINE 36 PHOSPHOTRANSFER PROTEIN 2 (AHP2), AHP3 and AHP5 and transcription factors 37 ARABIDOPSIS RESPONSE REGULATOR 2 (ARR2), ARR10 and ARR12 are required for the 38 protective activity of CK. Analysis of higher order B-type arr mutants suggested that a complex 39 regulatory circuit exists in which the loss of ARR10 or ARR12 can rescue the arr2 phenotype. 40 Together the results revealed the role of root-derived CK acting in the shoot through the two-41 component signaling system to protect from the negative consequences of strong photoperiod 42 stress. 43 44 45

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“…As both poly Q and poly HQ domains are prominent in the RGO protein (Fig. 1A) and as the RGO protein is localized to the ER., we speculate that RGO may interact with CK signaling components as CK signaling components reside in the ER (Caesar et al, 2011; Lomin et al, 2011; Wulfetange et al, 2011; Lomin et al, 2018; Romanov et al, 2018) as well as mediating CK homeostasis by CKXs which takes place in the ER (Schmülling et al, 2003; Werner et al, 2003). Mechanistic aspect of RGO at protein level is under investigation.…”

Section: Discussionmentioning

confidence: 99%

“…The current knowledge of CK signalling involves a multistep signal transduction system that begins with the perception of CK by the Arabidopsis Histidine Kinases ( AHK2 , AHK3 , CRE1 / AHK4 ) in the endoplasmic reticulum (ER) phosphate transfer via the Arabidopsis Histidine Phosphotransfer proteins (AHPs). The information is transmitted to the nucleus where the transcription factors such as the type-B Arabidopsis Response Regulators (ARRs) affect gene expression (Kieber and Schaller, 2014; Romanov et al, 2018).…”

Section: Introductionmentioning

confidence: 99%

The Arabidopsis gene RGO mediates cytokinin responses and increases seed yield

Murmu

Allard

Chabot

et al. 2020

Preprint

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17One-sentence summary: RGO, a novel gene from Arabidopsis, is essential for plant development, 18 mediates CK signaling and increases seed yield in Arabidopsis and rapeseed when overexpressed. Abstract 1 A novel gene, At1g77960, from Arabidopsis thaliana was characterized. At1g77960 transcripts 2 accumulate to very high levels in plants ectopically overexpressing the Golden2-like1 (GLK1) 3 transcription factor and is designated as a Response to GLK1 Overexpression (RGO) gene. RGO 4 encodes a protein with domains of tandem QH and QN repeats. Transcripts and promoter GUS 5 reporter analyses indicated that RGO is expressed in roots, leaves, stems, floral and siliques tissues 6 but not in seeds. Expression of the RGO:YFP fusion protein demonstrated that RGO is localized 7 to the endoplasmic reticulum. MicroRNA mediated silencing of RGO resulted in severe reductions 8 in vegetative and root growth, delayed flowering and reduced seed yield and viability, suggesting 9 that RGO is essential for plant development. Conversely, ectopic overexpression of RGO resulted 10 in enhanced vegetative growth including increased axillary bud formation and a 20% higher seed 11 yield. Stable overexpression of RGO in Brassica napus also produced a similar increase in seed 12 yield. Cytokinin (CK) response assays including root growth, green calli formation from excised 13 hypocotyls and chlorophyll retention during dark-induced senescence suggest that one role of RGO 14 is to mediate CK responses in plant development. These results suggest that RGO could be a target 15 gene for increasing crop seed yields. 16 Keywords 17 Arabidopsis thaliana, At1g77960, GLK1 overexpression, cytokinin response, seed yield 18 19 [Type text] [Type text] 4 1A direct link between GLKs and CK signalling however, is lacking. There is evidence to suggest 2 that type B ARRs coordinate the expression of HY5 (elongated hypocotyl 5), which is required by 3 GLK2 for maximal (although not essential) greening in roots (Kobayashi et al., 2012).

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Cytokinin signaling: from the ER or from the PM? That is the question!

Cited by 89 publications

References 113 publications

Cell-surface receptors enable perception of extracellular cytokinins

Cell-surface receptors enable perception of extracellular cytokinins

Root-derived trans-zeatin cytokinin protects Arabidopsis plants against photoperiod stress

The Arabidopsis gene RGO mediates cytokinin responses and increases seed yield

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