A calmodulin‐like protein regulates plasmodesmal closure during bacterial immune responses

Xu, Bo; Cheval, Cécilia; Laohavisit, Anuphon; Hocking, Bradleigh; Chiasson, David; Olsson, Tjelvar S. G.; Shirasu, Ken; Faulkner, Christine; Gilliham, Matthew

doi:10.1111/nph.14599

Cited by 97 publications

(81 citation statements)

References 38 publications

(62 reference statements)

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“…S1P in guard triggers alteration in nitric oxide (NO), cytoplasmic calcium and cytoplasmic pH (Ng et al, 2001; Puli et al, 2016). Reactive oxygen species and cytoplasmic calcium are well known trigger of callose accumulation, probably through posttranslational regulation of callose synthases (Xu et al, 2017; Wu et al, 2018). Thus, a reduction of S1P by DMS treatment or in sphk1 mutants may accompany a diminution of callose synthase activity by posttranslational modification.…”

Section: Discussionmentioning

confidence: 99%

Glucosylhydroxyceramides Modulate Secretion Machinery of a Subset of Plasmodesmata Proteins and a Change in the Callose Accumulation

Iswanto

Shon

et al. 2020

Preprint

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The plasma membranes encapsulated in the plasmodesmata (PDs) with symplasmic nano-channels contain abundant lipid rafts, which are enriched by sphingolipids and sterols. The attenuation of sterol compositions has demonstrated the role played by lipid raft integrity in the intercellular trafficking of glycosylphosphatidylinositol (GPI)-anchored PD proteins, particularly affecting in the callose enhancement. The presence of callose at PD is tightly attributed to the callose metabolic enzymes, callose synthases (CalSs) and β-1,3-glucanases (BGs) in regulating callose accumulation and callose degradation, respectively. Sphingolipids have been implicated in signaling and membrane protein trafficking, however the underlying processes linking sphingolipid compositions to the control of symplasmic apertures remain unknown. A wide variety of sphingolipids in plants prompts us to investigate which sphingolipid molecules are important in regulating symplasmic apertures. Here, we demonstrate that perturbations of sphingolipid metabolism by introducing several potential sphingolipid (SL) pathway inhibitors and genetically modifying SL contents from two independent SL pathway mutants are able to modulate callose deposition to control symplasmic connectivity. Our data from pharmacological and genetic approaches show that the alteration in glucosylhydroxyceramides (GlcHCers) particularly disturb the secretory machinery for GPI-anchored PdBG2 protein, resulting in an over accumulated callose. Moreover, our results reveal that SL-enriched lipid rafts link symplasmic channeling to PD callose homeostasis by controlling the targeting of GPI-anchored PdBG2. This study elevates our understanding of the molecular linkage underlying intracellular trafficking and precise targeting to specific destination of GPI-anchored PD proteins incorporated with GlcHCers contents.

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Section: Discussionmentioning

confidence: 99%

Glucosylhydroxyceramides Modulate Secretion Machinery of a Subset of Plasmodesmata Proteins and a Change in the Callose Accumulation

Iswanto

Shon

et al. 2020

Preprint

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“…A GUS histochemical assay was performed using the methods described previously 44 . 3-4 week-old transgenic pGAD2∷GUS plants were stained in buffer containing 50 mM Na phosphate pH = 7.0, 10 mM EDTA, 2 mM potassium ferrocyanide, 2 mM potassium ferricyanide, 0.1% (v/v) Triton X-100, 0.1% (w/v) X-Gluc (5-bromo-4-chloro-3-indolyl β- d -glucuronide) during a 1.5 h incubation at 37 °C in the dark.…”

Section: Methodsmentioning

confidence: 99%

GABA signalling in guard cells acts as a ‘stress memory’ to optimise plant water loss

Long

Feng

et al. 2019

Preprint

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25The non-protein amino acid γ-aminobutyric acid (GABA) has been proposed to be 26 an ancient messenger for cellular communication conserved across biological 27 kingdoms. GABA has well-defined signalling roles in animals; however, whilst 28 GABA accumulates in plants under stress it has not been determined if, how, where 29 and when GABA acts as an endogenous plant signalling molecule. Here, we 30 establish that endogenous GABA is a bona fide plant signal, acting via a 31 mechanism not found in animals. GABA antagonises stomatal movement in 32 response to opening and closing stimuli in multiple plant families including dicot 33 and monocot crops. Using Arabidopsis thaliana, we show guard cell GABA 34 production is necessary and sufficient to influence stomatal aperture, 35 transpirational water loss and drought tolerance via inhibition of stomatal guard cell 36 plasma membrane and tonoplast-localised anion transporters. This study proposes 37 a novel role for GABA -as a 'stress memory' -opening new avenues for improving 38 plant stress tolerance. 39 40The regulation of stomatal pore aperture is a key determinant of plant productivity 41 and drought tolerance, and profoundly impacts climate due to its influence on 42 global carbon and water cycling 1, 2, 3 . The stomatal pore is delineated by a guard 43 cell pair. Fine control of ion and water movement across guard cell membranes, 44 via transport proteins, determines cell volume and pore aperture following opening 45 and closing signals such as light and dark 2, 4, 5 (Fig. 1a, b). Due to their critical roles, 46and their ability to respond to and integrate multiple stimuli, guard cells have 47 105 GABA accumulation in guard cells contributes to the regulation of 106 transpiration and drought performance 107Stomatal control is explicitly linked with the regulation of plant water loss, which 108 impacts the survival of plants under drought 7 ; the wider the stomatal aperture, the 109 greater the water loss of plants, the poorer the survival of plants under a limited 110 water supply. As GABA has often been found to accumulate under stress 23 and 111 modulates the extent of opening and closure (Fig. 2), we examined the hypothesis 112 that endogenous GABA might increase in concentration under a water deficit and 113 act as a signal. In wildtype plants, a drought treatment was applied by withholding 114watering. This resulted in the gradual depletion of soil gravimetric water and a 115 reduction in leaf relative water content (RWC) ( Supplementary Fig. 4a, b). GABA 116 accumulation in drought stressed leaves increased by 35% compared to that of 117 well-watered leaves (water vs. drought at 7 d: 1.07 ± 0.08 vs. 1.44 ± 0.11 nmol mg -118 1 FW) ( Supplementary Fig. 4c). 119 120Arabidopsis T-DNA insertional mutants for the major leaf GABA synthesis gene, 121Glutamate Decarboxylase 2 (GAD2) (gad2-1 and gad2-2) had >75% less GABA 122 accumulation in leaves than in wildtype plants, whilst concentrations in roots were 123 unchanged ( Fig. 3a; Supplementary Fig. 4d-f). Further...

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“…For example, Loss of CML42 was associated with aberrant trichomes, whereas CML41 was reported to regulate plasmodesmal closure during plant immune responses. Moreover, CML24 and CML9 were found to be involved in abscisic acid (ABA) responses and ionic stress, whereas CML36 was reported to regulate the activity of the Ca 2+ ATPase ACA8 (Delk et al, 2005;Magnan et al, 2008;Dobney et al, 2009;Astegno et al, 2017;Xu et al, 2017).…”

Section: The Ca 2+ Decoding Toolkit In Plantsmentioning

confidence: 99%

Advances and current challenges in calcium signaling

et al. 2018

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Content Summary414I.Introduction415II.Ca2+ importer and exporter in plants415III.The Ca2+ decoding toolkit in plants415IV.Mechanisms of Ca2+ signal decoding417V.Immediate Ca2+ signaling in the regulation of ion transport418VI.Ca2+ signal integration into long‐term ABA responses419VIIIntegration of Ca2+ and hormone signaling through dynamic complex modulation of the CCaMK/CYCLOPS complex420VIIICa2+ signaling in mitochondria and chloroplasts422IXA view beyond recent advances in Ca2+ imaging423XModeling approaches in Ca2+ signaling424XIConclusions: Ca2+ signaling a still young blooming field of plant research424Acknowledgements425ORCID425References425 Summary Temporally and spatially defined changes in Ca2+ concentration in distinct compartments of cells represent a universal information code in plants. Recently, it has become evident that Ca2+ signals not only govern intracellular regulation but also appear to contribute to long distance or even organismic signal propagation and physiological response regulation. Ca2+ signals are shaped by an intimate interplay of channels and transporters, and during past years important contributing individual components have been identified and characterized. Ca2+ signals are translated by an elaborate toolkit of Ca2+‐binding proteins, many of which function as Ca2+ sensors, into defined downstream responses. Intriguing progress has been achieved in identifying specific modules that interconnect Ca2+ decoding proteins and protein kinases with downstream target effectors, and in characterizing molecular details of these processes. In this review, we reflect on recent major advances in our understanding of Ca2+ signaling and cover emerging concepts and existing open questions that should be informative also for scientists that are currently entering this field of ever‐increasing breath and impact.

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A calmodulin‐like protein regulates plasmodesmal closure during bacterial immune responses

Cited by 97 publications

References 38 publications

Glucosylhydroxyceramides Modulate Secretion Machinery of a Subset of Plasmodesmata Proteins and a Change in the Callose Accumulation

Glucosylhydroxyceramides Modulate Secretion Machinery of a Subset of Plasmodesmata Proteins and a Change in the Callose Accumulation

GABA signalling in guard cells acts as a ‘stress memory’ to optimise plant water loss

Advances and current challenges in calcium signaling

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