An Atypical Tubulin Kinase Mediates Stress-Induced Microtubule Depolymerization in Arabidopsis

Fujita, Satoshi; Pytela, Jaromir; Hotta, Takashi; Kato, Tadahiro; Hamada, Takahiro; Akamatsu, Rie; Ishida, Yasumasa; Kutsuna, Natsumaro; Hasezawa, Seiichiro; Nomura, Yuko; Nakagami, Hirofumi; Hashimoto, Takashi

doi:10.1016/j.cub.2013.08.006

Cited by 114 publications

(152 citation statements)

References 38 publications

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“…Null alleles of PHS1 are phenotypically indistinguishable from the wild type under standard growth conditions (Pytela et al 2010), but do not induce MT depolymerization upon hyperosmotic stress (Fujita et al 2013). In addition to the MPK phosphatase domain, PHS1 contains an atypical kinase domain that phosphorylates Thr349 of a-tubulin (Fujita et al 2013). This threonine residue is well conserved among eukaryotic a-tubulins and is located at the longitudinal interdimer interface of the tubulin heterodimer.…”

Section: Signaling Pathwaysmentioning

confidence: 99%

“…An Arabidopsis phs1-1d allele was isolated as a gain-of-function mutant that displayed partial destabilization of cortical MTs and possessed a missense mutation in the putative kinase-interacting motif of a MPK phosphatase . Null alleles of PHS1 are phenotypically indistinguishable from the wild type under standard growth conditions (Pytela et al 2010), but do not induce MT depolymerization upon hyperosmotic stress (Fujita et al 2013). In addition to the MPK phosphatase domain, PHS1 contains an atypical kinase domain that phosphorylates Thr349 of a-tubulin (Fujita et al 2013).…”

Section: Signaling Pathwaysmentioning

confidence: 99%

“…Threonine 349 of a-tubulin in Arabidopsis plants is transiently phosphorylated upon acute hyperosmotic stress and then gradually de-phosphorylated (Ban et al, 2013;Fujita et al, 2013). This threonine residue is located at the longitudinal interdimer interface, and its phosphorylation effectively inhibits MT polymerization in vitro and induces rapid MT depolymerization in vivo (Fujita et al, 2013).…”

Section: Small Molecules That Interact With Mtsmentioning

confidence: 99%

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Microtubules in Plants

Hashimoto

2015

The Arabidopsis Book

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Microtubules (MTs) are highly conserved polar polymers that are key elements of the eukaryotic cytoskeleton and are essential for various cell functions. αβ-tubulin, a heterodimer containing one structural GTP and one hydrolysable and exchangeable GTP, is the building block of MTs and is formed by the sequential action of several molecular chaperones. GTP hydrolysis in the MT lattice is mechanistically coupled with MT growth, thus giving MTs a metastable and dynamic nature. MTs adopt several distinct higher-order organizations that function in cell division and cell morphogenesis. Small molecular weight compounds that bind tubulin are used as herbicides and as research tools to investigate MT functions in plant cells. The de novo formation of MTs in cells requires conserved γ-tubulin-containing complexes and targeting/activating regulatory proteins that contribute to the geometry of MT arrays. Various MT regulators and tubulin modifications control the dynamics and organization of MTs throughout the cell cycle and in response to developmental and environmental cues. Signaling pathways that converge on the regulation of versatile MT functions are being characterized.

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Section: Signaling Pathwaysmentioning

confidence: 99%

Section: Signaling Pathwaysmentioning

confidence: 99%

Section: Small Molecules That Interact With Mtsmentioning

confidence: 99%

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Microtubules in Plants

Hashimoto

2015

The Arabidopsis Book

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“…Recently, TUA phosphorylation at this residue was shown to influence overall microtubule stability (Fujita et al, 2013). This previous work showed that TUA phosphorylation occurred under osmotic stress conditions and resulted in a polymerizationincompetent protein isoform that contributed to microtubule destabilization and depolymerization (Ban et al, 2013;Fujita et al, 2013).…”

Section: Tubulin Phosphorylationmentioning

confidence: 99%

Phosphoproteomic Analyses Reveal Early Signaling Events in the Osmotic Stress Response

2014

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Elucidating how plants sense and respond to water loss is important for identifying genetic and chemical interventions that may help sustain crop yields in water-limiting environments. Currently, the molecular mechanisms involved in the initial perception and response to dehydration are not well understood. Modern mass spectrometric methods for quantifying changes in the phosphoproteome provide an opportunity to identify key phosphorylation events involved in this process. Here, we have used both untargeted and targeted isotope-assisted mass spectrometric methods of phosphopeptide quantitation to characterize proteins in Arabidopsis (Arabidopsis thaliana) whose degree of phosphorylation is rapidly altered by hyperosmotic treatment. Thus, protein phosphorylation events responsive to 5 min of 0.3 M mannitol treatment were first identified using 15 N metabolic labeling and untargeted mass spectrometry with a high-resolution ion-trap instrument. The results from these discovery experiments were then validated using targeted Selected Reaction Monitoring mass spectrometry with a triple quadrupole. Targeted Selected Reaction Monitoring experiments were conducted with plants treated under nine different environmental perturbations to determine whether the phosphorylation changes were specific for osmosignaling or involved cross talk with other signaling pathways. The results indicate that regulatory proteins such as members of the mitogen-activated protein kinase family are specifically phosphorylated in response to osmotic stress. Proteins involved in 59 messenger RNA decapping and phosphatidylinositol 3,5-bisphosphate synthesis were also identified as targets of dehydration-induced phosphoregulation. The results of these experiments demonstrate the utility of targeted phosphoproteomic analysis in understanding protein regulation networks and provide new insight into cellular processes involved in the osmotic stress response.

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“…19 NaCl/osmotic stress induces transient depolymerization and repolymerization of microtubules, which is essential for stress acclimation 20,21 and triggered by tubulin kinase PHS1. 22 Because CSCs associate with cortical microtubules via the CSI1/POM2 protein, 23,24 and microtubules are required for both, guiding CSCs at the PM as well as their secretion and internalization, 19,25 stress-induced microtubule depolymerization likely results in transient disruption of CSC and KOR1 organization. Perhaps, re-establishing microtubule-association of CSCs and KOR1 are essential steps for recovery from the salt shock and resuming growth under persisting salt stress.…”

mentioning

confidence: 99%

Arabidopsis thalianaKORRIGAN1 protein: N-glycan modification, localization, and function in cellulose biosynthesis and osmotic stress responses

Schaewen

Rips

Jeong

et al. 2015

Plant Signaling & Behavior

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Plant cellulose biosynthesis is a complex process involving cellulose-synthase complexes (CSCs) and various auxiliary factors essential for proper orientation and crystallinity of cellulose microfibrils in the apoplast. Among them is KORRIGAN1 (KOR1), a type-II membrane protein with multiple N-glycans within its C-terminal cellulase domain. N-glycosylation of the cellulase domain was important for KOR1 targeting to and retention within the trans-Golgi network (TGN), and prevented accumulation of KOR1 at tonoplasts. The degree of successful TGN localization of KOR1 agreed well with in vivo-complementation efficacy of the rsw2-1 mutant, suggesting non-catalytic functions in the TGN. A dynamic interaction network involving microtubules, CSCs, KOR1, and currently unidentified glycoprotein component(s) likely determines stress-triggered re-organization of cellulose biosynthesis and resumption of cell-wall growth under stress.

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An Atypical Tubulin Kinase Mediates Stress-Induced Microtubule Depolymerization in Arabidopsis

Cited by 114 publications

References 38 publications

Microtubules in Plants

Microtubules in Plants

Phosphoproteomic Analyses Reveal Early Signaling Events in the Osmotic Stress Response

Arabidopsis thalianaKORRIGAN1 protein: N-glycan modification, localization, and function in cellulose biosynthesis and osmotic stress responses

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