Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 (NaCHK2)‐ and<scp>N</scp>a<scp>CHK</scp>3‐mediated perception modulate herbivory‐induced defense signaling and defenses in<i><scp>N</scp>icotiana attenuata</i>

Schäfer, M.; Meza-Canales, Iván David; Brütting, Christoph; Baldwin, Ian Thomas; Meldau, Stefan

doi:10.1111/nph.13404

Cited by 33 publications

(42 citation statements)

References 101 publications

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“…Interestingly, we reported increased levels of c Z(R) in ugt76c2 after KIN uptake ( Figure 7F ) and, reversely, lowered c Zs in ugt85a1-1 in whole plants ( Figure 5 ) as well as in detached leaves ( Figure 7F ). Increased levels of c Z(R)s were found in many plant species in response to both, abiotic and biotic stress (Schäfer et al, 2015), as well as after exogenous application of CK (Vyroubalová et al, 2009). This phenomenon can support the importance of UGT76C2 action and thus increased c Z(R)s accumulation when the action of the protein is impaired.…”

Section: Discussionmentioning

confidence: 99%

Cytokinin-Specific Glycosyltransferases Possess Different Roles in Cytokinin Homeostasis Maintenance

et al. 2016

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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.

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Section: Discussionmentioning

confidence: 99%

Cytokinin-Specific Glycosyltransferases Possess Different Roles in Cytokinin Homeostasis Maintenance

et al. 2016

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“…CKs are also known to regulate defense responses against pathogens (Choi et al ., ; Grosskinsky et al ., ; Argueso et al ., ) and herbivores (Smigocki et al ., , ; Dervinis et al ., ; Schäfer et al ., 2015a). Increasing CK levels amplify the accumulation of secondary metabolites in several plant species (Hino et al ., ; Grosskinsky et al ., ; Schäfer et al ., 2015a). However, these studies have not considered the action of CKs in the context of the OD theory and their influence on the developmental regulation of defense patterns.…”

Section: Introductionmentioning

confidence: 99%

“…One of the most abundant PAs, caffeoylputrescine (CP), whose biosynthesis is very nitrogen demanding (Ullmann‐Zeunert et al ., ), is highly inducible by herbivore attack and accumulates in developmental patterns consistent with the predictions of the OD theory with higher levels in younger leaves (Kaur et al ., ). CP accumulation in young, rosette‐stage plants is also regulated by CK levels and signaling (Schäfer et al ., 2015a). Here we use the accumulation of CP in leaves as a reliable marker to investigate mechanisms responsible for developmental patterns of herbivory‐inducible defenses.…”

Section: Introductionmentioning

confidence: 99%

Changes in cytokinins are sufficient to alter developmental patterns of defense metabolites in Nicotiana attenuata

et al. 2017

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SUMMARYPlant defense metabolites are well known to be regulated developmentally. The optimal defense (OD) theory posits that a t ssue's fitness values and probability of attack should determine defense metabolite allocations. Young leaves are expected to provide a larger fitness value to the plant, and therefore their defense allocations should be higher when compared with older leaves. The mechanisms that coordinate development with defense remain unknown and frequently confound tests of the OD theory predictions. Here we demonstrate that cytokinins (CKs) modulate ontogeny-dependent defenses in Nicotiana attenuata. We found that leaf CK levels highly correlate with inducible defense expressions with high levels in young and low levels in older leaves. We genetically manipulated the developmental patterns of two different CK classes by using senescenceand chemically inducible expression of CK biosynthesis genes. Genetically modifying the levels of different CKs in leaves was sufficient to alter ontogenic patterns of defense metabolites. We conclude that the developmental regulation of growth hormones that include CKs plays central roles in connecting development with defense and therefore in establishing optimal patterns of defense allocation in plants.

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“…Recent evidence also suggests that hormones that have traditionally been classified as growth regulators participate in induced defense responses. Cytokinins for instance modulate woundinduced local and systemic defense responses (Schäfer et al, 2015), and gibberellins are involved in regulating the plant's investment into growth and defense (Li et al, 2015;Hou et al, 2010;Yang et al, 2012).…”

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confidence: 99%

Auxin Is Rapidly Induced by Herbivore Attack and Regulates a Subset of Systemic, Jasmonate-Dependent Defenses

et al. 2016

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Plant responses to herbivore attack are regulated by phytohormonal networks. To date, the role of the auxin indole-3-acetic acid (IAA) in this context is not well understood. We quantified and manipulated the spatiotemporal patterns of IAA accumulation in herbivore-attacked Nicotiana attenuata plants to unravel its role in the regulation of plant secondary metabolism. We found that IAA is strongly, rapidly, and specifically induced by herbivore attack. IAA is elicited by herbivore oral secretions and fatty acid conjugate elicitors and is accompanied by a rapid transcriptional increase of auxin biosynthetic YUCCA-like genes. IAA accumulation starts 30 to 60 s after local induction and peaks within 5 min after induction, thereby preceding the jasmonate (JA) burst. IAA accumulation does not require JA signaling and spreads rapidly from the wound site to systemic tissues. Complementation and transport inhibition experiments reveal that IAA is required for the herbivore-specific, JA-dependent accumulation of anthocyanins and phenolamides in the stems. In contrast, IAA does not affect the accumulation of nicotine or 7-hydroxygeranyllinalool diterpene glycosides in the same tissue. Taken together, our results uncover IAA as a rapid and specific signal that regulates a subset of systemic, JA-dependent secondary metabolites in herbivore-attacked plants.

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Cytokinin concentrations and CHASE‐DOMAIN CONTAINING HIS KINASE 2 (NaCHK2)‐ andNaCHK3‐mediated perception modulate herbivory‐induced defense signaling and defenses inNicotiana attenuata

Cited by 33 publications

References 101 publications

Cytokinin-Specific Glycosyltransferases Possess Different Roles in Cytokinin Homeostasis Maintenance

Cytokinin-Specific Glycosyltransferases Possess Different Roles in Cytokinin Homeostasis Maintenance

Changes in cytokinins are sufficient to alter developmental patterns of defense metabolites in Nicotiana attenuata

Auxin Is Rapidly Induced by Herbivore Attack and Regulates a Subset of Systemic, Jasmonate-Dependent Defenses

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