Ca2+-dependent phosphoregulation of the plasma membrane Ca2+-ATPase ACA8 modulates stimulus-induced calcium signatures

Costa, Alex; Luoni, Laura; Marrano, Claudia Adriana; Hashimoto, Kenji; Köster, Philipp; Giacometti, Sonia; Michelis, Maria Ida De; Kudla, Jörg; Bonza, Maria Cristina

doi:10.1093/jxb/erx162

Cited by 72 publications

(50 citation statements)

References 92 publications

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“…Increases in [Ca 2+ ] cyt were accompanied by cytosolic acidification as illustrated by the superimposed averaged traces from independent experiments normalized to the pre-stimulus level (R 0 ) ( Figure 1). Leaf wounding generated the characteristic Ca 2+ signature featuring two maxima as observed previously (Beneloujaephajri et al, 2013;Costa et al, 2017) ( Figure 1A, Supplemental Movie 1). The first maximum showed a sharp onset and decline with a high amplitude and…”

Section: Resultssupporting

confidence: 69%

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

et al. 2018

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Ca 2+ play a key role in cell signaling across organisms. The question of how a simple ion can mediate specific outcomes has spurred research into the role of Ca 2+ signatures and their encoding and decoding machinery. Such studies have frequently focused on Ca 2+ alone and our understanding of how Ca 2+ signaling is integrated with other responses is poor. Using in vivo imaging with different genetically encoded fluorescent sensors in Arabidopsis (Arabidopsis thaliana) cells, we show that Ca 2+ transients do not occur in isolation but are accompanied by pH changes in the cytosol. We estimate the degree of cytosolic acidification at up to 0.25 pH units in response to external ATP in seedling root tips. We validated this pH-Ca 2+ link for distinct stimuli. Our data suggest that the association with pH may be a general feature of Ca 2+ transients that depends on the transient characteristics and the intracellular compartment. These findings suggest a fundamental link between Ca 2+ and pH dynamics in plant cells, generalizing previous observations of their association in growing pollen tubes and root hairs. Ca 2+ signatures act in concert with pH signatures, possibly providing an additional layer of cellular signal transduction to tailor signal specificity.

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Section: Resultssupporting

confidence: 69%

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

et al. 2018

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“…Interestingly, CPK16 can phosphorylate S22 of ACA8 in vitro (Giacometti et al ., ), suggesting a role of CPK16 in the PTI and ETI signaling pathways. CBL‐INTERACTING PROTEIN KINASE‐9 (CIPK9) in a complex with the plasma membrane Ca 2+ sensor CALCINEURIN B‐LIKE PROTEIN‐1 (CBL1) phosphorylates ACA8, thereby regulating its activity (Costa et al ., ). However, the role of ACA8, as well as CPK16, CIPK9 and CBL1, during ETI remains to be elucidated.…”

Section: Resultsmentioning

confidence: 97%

“…nd, not detected. (Costa et al, 2017). However, the role of ACA8, as well as CPK16, CIPK9 and CBL1, during ETI remains to be elucidated.…”

Section: Overlap In Rps2-and Fls2-induced Phosphorylation Sitesmentioning

confidence: 99%

Quantitative phosphoproteomic analysis reveals common regulatory mechanisms between effector‐ and PAMP‐triggered immunity in plants

et al. 2018

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Summary Plant immunity consists of two arms: pathogen‐associated molecular pattern (PAMP)‐triggered immunity (PTI), induced by surface‐localized receptors, and effector‐triggered immunity (ETI), induced by intracellular receptors. Despite the little structural similarity, both receptor types activate similar responses with different dynamics. To better understand phosphorylation events during ETI, we employed a phosphoproteomic screen using an inducible expression system of the bacterial effector avrRpt2 in Arabidopsis thaliana, and identified 109 differentially phosphorylated residues of membrane‐associated proteins on activation of the intracellular RPS2 receptor. Interestingly, several RPS2‐regulated phosphosites overlap with sites that are regulated during PTI, suggesting that these phosphosites may be convergent points of both signaling arms. Moreover, some of these sites are residues of important defense components, including the NADPH oxidase RBOHD, ABC‐transporter PEN3, calcium‐ATPase ACA8, noncanonical Gα protein XLG2 and H+‐ATPases. In particular, we found that S343 and S347 of RBOHD are common phosphorylation targets during PTI and ETI. Our mutational analyses showed that these sites are required for the production of reactive oxygen species during both PTI and ETI, and immunity against avirulent bacteria and a virulent necrotrophic fungus. We provide, for the first time, large‐scale phosphoproteomic data of ETI, thereby suggesting crucial roles of common phosphosites in plant immunity.

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“…Both Ca 2+ influx and efflux systems contribute to the generation of [Ca 2+ ] cyt signatures (Edel & Kudla, ; Costa et al ., ). The expression of CAX1 , ACA4 and ACA8 in myb30 mutants and the OE lines was similar to that in wild‐type.…”

Section: Discussionmentioning

confidence: 97%

MYB30 transcription factor regulates oxidative and heat stress responses through ANNEXIN‐mediated cytosolic calcium signaling in Arabidopsis

2017

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Cytosolic calcium signaling is critical for regulating downstream responses in plants encountering unfavorable environmental conditions. In a genetic screen for Arabidopsis thaliana mutants defective in stress-induced cytosolic free Ca ([Ca ] ) elevations, we identified the R2R3-MYB transcription factor MYB30 as a regulator of [Ca ] in response to H O and heat stresses. Plants lacking MYB30 protein exhibited greater elevation of [Ca ] in response to oxidative and heat stimuli. Real-time reverse transcription-polymerase chain reaction (RT-PCR) results indicated that the expression of a number of ANNEXIN (ANN) genes, which encode Ca -regulated membrane-binding proteins modulating cytosolic calcium signatures, were upregulated in myb30 mutants. Further analysis showed that MYB30 bound to the promoters of ANN1 and ANN4 and repressed their expression. myb30 mutants were sensitive to methyl viologen (MV) and heat stresses. The H O - and heat-induced abnormal [Ca ] in myb30 was dependent on the function of ANN proteins. Moreover, the MV and heat sensitivity of myb30 was suppressed in mutants lacking ANN function or by application of LaCl , a calcium channel blocker. These results indicate that MYB30 regulates oxidative and heat stress responses through calcium signaling, which is at least partially mediated by ANN1 and ANN4.

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Ca2+-dependent phosphoregulation of the plasma membrane Ca2+-ATPase ACA8 modulates stimulus-induced calcium signatures

Abstract: The plasma membrane Ca2+-ATPase ACA8 is a novel target of Ca2+-dependent CIPK–CBL complexes which tunes the pump activity affecting a stimulus-induced cytosolic Ca2+ transient in planta.

Cited by 72 publications

References 92 publications

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

Quantitative phosphoproteomic analysis reveals common regulatory mechanisms between effector‐ and PAMP‐triggered immunity in plants

MYB30 transcription factor regulates oxidative and heat stress responses through ANNEXIN‐mediated cytosolic calcium signaling in Arabidopsis

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Ca2+-dependent phosphoregulation of the plasma membrane Ca2+-ATPase ACA8 modulates stimulus-induced calcium signatures

Abstract: The plasma membrane Ca2+-ATPase ACA8 is a novel target of Ca2+-dependent CIPK–CBL complexes which tunes the pump activity affecting a stimulus-induced cytosolic Ca2+ transient in planta.

Cited by 72 publications

References 92 publications

Cellular Ca2+ Signals Generate Defined pH Signatures in Plants

Cellular Ca2+ Signals Generate Defined pH Signatures in Plants

Quantitative phosphoproteomic analysis reveals common regulatory mechanisms between effector‐ and PAMP‐triggered immunity in plants

MYB30 transcription factor regulates oxidative and heat stress responses through ANNEXIN‐mediated cytosolic calcium signaling in Arabidopsis

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Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants

Cellular Ca²⁺ Signals Generate Defined pH Signatures in Plants