Extra- and intracellular distribution of cytokinins in the leaves of monocots and dicots

Jiskrová, Eva; Novák, Ondřej; Pospíšilová, Hana; Holubová, Katarína; Karády, Michal; Galuszka, Petr; Robert, Stéphanie; Frébort, Ivo

doi:10.1016/j.nbt.2015.12.010

Cited by 32 publications

(45 citation statements)

References 46 publications

Supporting

Mentioning

Contrasting

Unclassified

Order By: Relevance

“…Since glycosylation makes molecules more hydrophilic and better accessible to membrane-bound transporters (Lim and Bowles, 2004), we further hypothesize a transport mechanism of CK-glucosides out of the cytosol with specificity to t ZOG. In fact, glucosides can enter other more hydrophilic compartments such vacuoles, which was proved for CK-glucosides except t ZOG (Jiskrová et al, 2016). Apart from the CK non-specific transport mediated by PUP and ENT transporters across plasma membrane (Gillissen et al, 2000; Bürkle et al, 2003; Hirose et al, 2005, 2007; Sun et al, 2005), not much is known about the CK transport mechanism in general; thus, we emphasize importance of elucidation of CK inter-compartmental transport to overall understanding of CK signalization.…”

Section: Discussionmentioning

confidence: 76%

“…Besides the cited works, only little is known about localization of the CK glucosides on the subcellular level. Although CK O -glucosides were observed to be present within vacuoles of Chenopodium rubrum (Fusseder and Ziegler, 1988; Mok et al, 1992), our recent work shows predominant localization of both types of CK glucosides in extracellular space (Jiskrová et al, 2016). …”

Section: Introductionmentioning

confidence: 65%

“…As discussed in an outstanding review by Lim and Bowels, glycosylation and deglycosylation can regulate levels of metabolites in pathways through controlling their exit and re-entry from cytosol into their reaction environments (Lim and Bowles, 2004). Based on our newly gained knowledge of CK glucosylation taking place in cytosol, along with the current finding of CK forms compartmentation in Arabidopsis (Jiskrová et al, 2016), we present a new hypothesis of CK metabolism compartmentation on subcellular level schematically illustrated in Figure 10 . We employed former schemes of exquisite reviews (Kasahara et al, 2004; Frébort et al, 2011; Ha et al, 2012; Spíchal, 2012; Zalabák et al, 2013) and supplemented them with all currently known information on CK metabolism compartmentation.…”

Section: Discussionmentioning

confidence: 99%

“…Interestingly, this is the only CKX isoform with a rather constitutive expression pattern (Mik et al, 2011; Motte et al, 2013). Further, when taking into account kinetic parameters of CKX and UGT enzymes in general (Bilyeu et al, 2001; Hou et al, 2004), we propose that CK glucosylation within the cytosol might serve as an immediate fine-tuning mechanism of inner CK homeostasis that subsequently contributes to overall CK metabolism status once the formed CK-glucosides are accumulated in extracellular space (Jiskrová et al, 2016). Since glycosylation makes molecules more hydrophilic and better accessible to membrane-bound transporters (Lim and Bowles, 2004), we further hypothesize a transport mechanism of CK-glucosides out of the cytosol with specificity to t ZOG.…”

Section: Discussionmentioning

confidence: 99%

“…Glycosylation alters chemical properties of the inactivated molecules enabling their inter-compartment re-localization driven by newly gained increased hydrophilicity (Bowles et al, 2005). This raises a question whether inactive CK glucosides are destined to retargeting to cellular compartments or whether they serve as long-distance transport forms, which is more likely, since high levels of glucosides were found in xylem sap of cucumber (Kato et al, 2002) or extracellular space of Arabidopsis and barley leaves (Jiskrová et al, 2016). This hypothesis was further supported by Kato et al (2002) whose research documented shoot greening mediated by CK glucosides uptake by roots.…”

Section: Introductionmentioning

confidence: 99%

See 4 more Smart Citations

Cytokinin-Specific Glycosyltransferases Possess Different Roles in Cytokinin Homeostasis Maintenance

et al. 2016

Self Cite

View full text Add to dashboard Cite

Plant hormones cytokinins (CKs) are one of the major mediators of physiological responses throughout plant life span. Therefore, a proper homeostasis is maintained by regulation of their active levels. Besides degradation, CKs are deactivated by uridine diphosphate glycosyltransferases (UGTs). Physiologically, CKs active levels decline in senescing organs, providing a signal to nutrients that a shift to reproductive tissues has begun. In this work, we show CK glucosides distribution in Arabidopsis leaves during major developmental transition phases. Besides continuous accumulation of N-glucosides we detected sharp maximum of the glucosides in senescence. This is caused prevalently by N7-glucosides followed by N9-glucosides and specifically also by trans-zeatin-O-glucoside (tZOG). Interestingly, we observed a similar trend in response to exogenously applied CK. In Arabidopsis, only three UGTs deactivate CKs in vivo: UGT76C1, UGT76C2 and UGT85A1. We thereby show that UGT85A1 is specifically expressed in senescent leaves whereas UGT76C2 is activated rapidly in response to exogenously applied CK. To shed more light on the UGTs physiological roles, we performed a comparative study on UGTs loss-of-function mutants, characterizing a true ugt85a1-1 loss-of-function mutant for the first time. Although no altered phenotype was detected under standard condition we observed reduced chlorophyll degradation with increased anthocyanin accumulation in our experiment on detached leaves accompanied by senescence and stress related genes modulated expression. Among the mutants, ugt76c2 possessed extremely diminished CK N-glucosides levels whereas ugt76c1 showed some specificity toward cis-zeatin (cZ). Besides tZOG, a broader range of CK glucosides was decreased in ugt85a1-1. Performing CK metabolism gene expression profiling, we revealed that activation of CK degradation pathway serves as a general regulatory mechanism of disturbed CK homeostasis followed by decreased CK signaling in all UGT mutants. In contrast, a specific regulation of CKX7, CKX1 and CKX2 was observed for each individual UGT mutant isoform after exogenous CK uptake. Employing an in silico prediction we proposed cytosolic localization of UGT76C1 and UGT76C2, that we further confirmed by GFP tagging of UGT76C2. Integrating all the results, we therefore hypothesize that UGTs possess different physiological roles in Arabidopsis and serve as a fine-tuning mechanism of active CK levels in cytosol.

show abstract

Section: Discussionmentioning

confidence: 76%

Section: Introductionmentioning

confidence: 65%

Section: Discussionmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Cytokinin-Specific Glycosyltransferases Possess Different Roles in Cytokinin Homeostasis Maintenance

et al. 2016

Self Cite

View full text Add to dashboard Cite

show abstract

Cytokinin isopentenyladenine and its glucoside isopentenyladenine‐9G delay leaf senescence through activation of cytokinin‐associated genes

Hallmark

Rashotte

2020

Plant Direct

View full text Add to dashboard Cite

Cytokinins (CKs) are well‐known as a class of phytohormones capable of delaying senescence in detached leaves. However, CKs are often treated as a monolithic group of compounds even though dozens of CK species are present in plants with varied degrees of reported biological activity. One specific type of CK, isopentenyladenine base (iP), has been demonstrated as having roles in delaying leaf senescence, inhibition of root growth, and promoting shoot regeneration. However, its N‐glucosides isopentenyladenine‐7‐ and ‐9‐glucoside (iP7G, iP9G) have remained understudied and thought of as inactive cytokinins for several decades, despite their relatively high concentrations in plants such as the model species Arabidopsis thaliana . Here we show that iP and one of its glucosides, iP9G, are capable of delaying senescence in leaves, though the glucosides having little to no activity in other bioassays. Additionally, we performed the first transcriptomic study of iP‐delayed cotyledon senescence which shows that iP is capable of upregulating photosynthetic genes and downregulating catabolic genes in detached cotyledons. Transcriptomic analysis also shows iP9G has limited effects on gene expression, but that the few affected genes are CK‐related and are similar to those seen from iP effects during senescence as seen for the type‐A response regulator ARR6. These findings suggest that iP9G functions as an active CK during senescence.

show abstract

Cytokinins, the Cinderella of plant growth regulators

2019

View full text Add to dashboard Cite

Extra- and intracellular distribution of cytokinins in the leaves of monocots and dicots

Cited by 32 publications

References 46 publications

Cytokinin-Specific Glycosyltransferases Possess Different Roles in Cytokinin Homeostasis Maintenance

Cytokinin-Specific Glycosyltransferases Possess Different Roles in Cytokinin Homeostasis Maintenance

Cytokinin isopentenyladenine and its glucoside isopentenyladenine‐9G delay leaf senescence through activation of cytokinin‐associated genes

Cytokinins, the Cinderella of plant growth regulators

Contact Info

Product

Resources

About