Hyperosmotic Stress Induces the Rapid Phosphorylation of a Soybean Phosphatidylinositol Transfer Protein Homolog through Activation of the Protein Kinases SPK1 and SPK2

Monks, Dave E.; Aghoram, Karthik; Courtney, Polly D.; DeWald, Daryll B.; Dewey, Ralph E.

doi:10.2307/3871374

Cited by 17 publications

(25 citation statements)

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“…1C). This difference between cells and plant tissues was also reported for the phosphorylation of the phosphatidylinositol transfer protein SSH1 induced by the hyperosmotic condition in tobacco (32). The activation occurred for a weaker stress strength in cells in comparison to leaf tissue and the authors explained this result by the difficulty to apply a uniform osmotic stress to all cells when using intact tissue.…”

Section: Figsupporting

confidence: 63%

“…Coherently, these two kinases are shown here to be activated by hyperosmotic and saline stresses. In soybean, Monks et al (32) described the activation of only two of four SnRK2 (SPK1 and SPK2) in yeast exposed to high hyperosmolarity. In the meantime, Kobayashi et al (39) described the salt activation of the 10 rice SnRK2 by transient expression assays.…”

Section: Figmentioning

confidence: 99%

“…A tobacco homolog of the Arabidopsis ASK1/ SnRK2-4 was shown to be activated by hyperosmotic stress in cell suspension (4), whereas dehydration activated SnRK2-E/ SnRK2-6 (30). In soybean, SPK3 and SPK4 were transcriptionally induced by drought and saline stress (31), whereas only SPK1 and SPK2 were activated by salt stress in yeast (32).…”

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Identification of Nine Sucrose Nonfermenting 1-related Protein Kinases 2 Activated by Hyperosmotic and Saline Stresses in Arabidopsis thaliana

Boudsocq

Barbier‐Brygoo

Laurière

2004

Journal of Biological Chemistry

408

403

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Several calcium-independent protein kinases were activated by hyperosmotic and saline stresses in Arabidopsis cell suspension. Similar activation profiles were also observed in seedlings exposed to hyperosmotic stress. One of them was identified to AtMPK6 (Droillard, M. J., Boudsocq, M., Barbier-Brygoo, H., and Lauriè re, C. (2002) FEBS Lett. 527, 43-50) but the others remained to be identified. They were assumed to belong to the SNF1 (sucrose nonfermenting 1)-related protein kinase 2 (SnRK2) family, which constitutes a plant-specific kinase group. The 10 Arabidopsis SnRK2 were expressed both in cells and seedlings, making the whole SnRK2 family a suitable candidate. Using a family-specific antibody raised against the 10 SnRK2, we demonstrated that these non-MAPK protein kinases activated by hyperosmolarity in cell suspension were SnRK2 proteins. Then, the molecular identification of the involved SnRK2 was investigated by transient expression assays. Nine of the 10 SnRK2 were activated by hyperosmolarity induced by mannitol, as well as NaCl, indicating an important role of the SnRK2 family in osmotic signaling. In contrast, none of the SnRK2 were activated by cold treatment, whereas abscisic acid only activated five of the nine SnRK2. The probable involvement of the different Arabidopsis SnRK2 in several abiotic transduction pathways is discussed.Environmental stresses such as drought, cold, and salinity impose osmotic stress on plants, leading to imbalance in ionic homeostasis, oxidative damages, and growth inhibition. Understanding how plants respond to these stresses is critical to improve plant resistance. Reversible protein phosphorylation is one of the major mechanisms for mediating intracellular responses, including responses to osmotic changes. Indeed, several protein kinases have been shown to be activated by hyperosmotic stresses in different plant species. Because of the well known osmosensing pathway in yeast involving a mitogenactivated protein kinase (MAPK), 1 much interest was focused on the MAPK family in plants. In Arabidopsis, AtMPK6 and AtMPK4 were shown to be activated by hyperosmolarity, salt, cold, or drought (1, 2), whereas the tobacco SIPK was activated by hyperosmotic or salt stresses (3-5). In alfalfa, SAMK was reported to be activated by cold and drought but not NaCl (6), whereas SIMK was activated by sorbitol, KCl, and NaCl (7).In mammals, MAPK cascades are composed of MAPK, MAPKK, and MAPKKK, each component being activated by phosphorylation by the upstream kinase. The involvement of MAPKK and MAPKKK in plant osmotic response was suggested by molecular and biochemical studies. The Arabidopsis MAPKKK AtMEKK1 was transcriptionally induced by salt stress and the protein was able to complement a yeast mutant affected in osmotic signaling (8). Moreover, Mizoguchi et al. Other kinase families have been shown to play a role in osmotic signaling. Among them, SOS2 (salt overly sensitive 2), which belongs to the sucrose nonfermenting 1-related protein kinase 3 (SnRK3) family, was transcription...

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Section: Figsupporting

confidence: 63%

Section: Figmentioning

confidence: 99%

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Identification of Nine Sucrose Nonfermenting 1-related Protein Kinases 2 Activated by Hyperosmotic and Saline Stresses in Arabidopsis thaliana

Boudsocq

Barbier‐Brygoo

Laurière

2004

Journal of Biological Chemistry

408

403

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“…The SnRK2 family, of which SRK2C is a member, is a relatively small, plant-specific gene family, i.e., 10 members within the Arabidopsis or rice genomes, all of which are activated by osmotic stress in rice (22). The osmotic-stress-activated SnRK2s have also been identified in tobacco (13) or soybean (38). Therefore, the signal transduction system of osmotic-stress-activated SnRK2s may be highly conserved among higher plants.…”

Section: Discussionmentioning

confidence: 99%

SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana

Umezawa

Yoshida

Maruyama

et al. 2004

Proc. Natl. Acad. Sci. U.S.A.

323

225

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Protein phosphorylation͞dephosphorylation are major signaling events induced by osmotic stress in higher plants. Here, we showed that a SNF1-related protein kinase 2 (SnRK2), SRK2C, is an osmoticstress-activated protein kinase in Arabidopsis thaliana that can significantly impact drought tolerance of Arabidopsis plants. Knockout mutants of SRK2C exhibited drought hypersensitivity in their roots, suggesting that SRK2C is a positive regulator of drought tolerance in Arabidopsis roots. Additionally, transgenic plants with CaMV35S promoter::SRK2C-GFP displayed higher overall drought tolerance than control plants. Whereas stomatal regulation in 35S::SRK2C-GFP plants was not altered, microarray analysis revealed that their drought tolerance coincided with up-regulation of many stress-responsive genes, for example, RD29A, COR15A, and DREB1A͞CBF3. From these results, we concluded that SRK2C is capable of mediating signals initiated during drought stress, resulting in appropriate gene expression. Our present study reveals new insights around signal output from osmotic-stress-activated SnRK2 protein kinase as well as supporting feasibility of manipulating SnRK2 toward improving plant osmotic-stress tolerance.

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“…Expression of genes encoding the SPK-3 and SPK-4 kinases from soybean, both members of the SnRK2 subfamily, is induced by dehydration and high salinity (23). Two other soybean protein kinases, SPK-1 and SPK-2 from the same group, are able to phosphorylate Ssh1p (soybean unusual phosphatidylinositol transfer-like protein), upon exposure of plant tissues to hyperosmotic stress (24).…”

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confidence: 99%

Nicotiana tabacum Osmotic Stress-activated Kinase Is Regulated by Phosphorylation on Ser-154 and Ser-158 in the Kinase Activation Loop

Burza

Pekala

Sikora

et al. 2006

Journal of Biological Chemistry

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NtOSAK (Nicotiana tabacum osmotic stress-activated protein kinase), a member of the SnRK2 subfamily, is activated rapidly in response to hyperosmotic stress. Our previous results as well as data presented by others indicate that phosphorylation is involved in activation of SnRK2 kinases. Here, we have mapped the regulatory phosphorylation sites of NtOSAK by mass spectrometry with collision-induced peptide fragmentation. We show that active NtOSAK, isolated from NaCl-treated tobacco BY-2 cells, is phosphorylated on Ser-154 and Ser-158 in the kinase activation loop. Prediction of the NtOSAK three-dimensional structure indicates that phosphorylation of Ser-154 and Ser-158 triggers changes in enzyme conformation resulting in its activation. The involvement of Ser-154 and Ser-158 phosphorylation in regulation of NtOSAK activity was confirmed by site-directed mutagenesis of NtOSAK expressed in bacteria and in maize protoplasts. Our data reveal that phosphorylation of Ser-158 is essential for NtOSAK activation, whereas phosphorylation of Ser-154 most probably facilitates Ser-158 phosphorylation. The time course of NtOSAK phosphorylation on Ser-154 and Ser-158 in BY-2 cells subjected to osmotic stress correlates with NtOSAK activity, indicating that NtOSAK is regulated by reversible phosphorylation of these residues in vivo. Importantly, Ser-154 and Ser-158 are conserved in all SnRK2 subfamily members, suggesting that phosphorylation at these sites may be a general mechanism for SnRK2 activation.Plants growing in natural conditions are challenged by various environmental stresses (e.g. drought, extreme temperatures, and high salinity), all of which cause osmotic stress in cells. To survive, plants induce various defense mechanisms. Perception of environmental stimuli and proper signal transduction are crucial for plant acclimatization and development. Protein kinases and phosphoprotein phosphatases play a pivotal role in these processes. Therefore, the activity of these enzymes has to be regulated very strictly inside the cell. Besides the enzymes belonging to the MAPK cascades and several other protein kinases conserved in all eukaryotic organisms ranging from yeast to human, plant genomes encode also plant-specific protein kinases, involved in the responses to harsh environmental conditions. Representative of such enzymes are some of the SNF1-related protein kinases (SnRKs). Plant SnRKs are classified into three subfamilies: SnRK1, SnRK2, and SnRK3 (for reviews, see Refs. 4 -6). Enzymes belonging to the SnRK1 group structurally and functionally resemble the yeast and animal SNF1/AMPK kinases, which play a role in protecting cells against nutritional and environmental stresses (for reviews, see Refs. 4,7,and 8). The SnRK2 and SnRK3 subfamilies are specific to plants (for reviews, see Refs. 4 and 5). Amassing data suggest that these enzymes participate in environmental stress signaling. Members of the SnRK3 subfamily, especially those that interact with calcineurin B-like proteins, are relatively well characterized. The...

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Hyperosmotic Stress Induces the Rapid Phosphorylation of a Soybean Phosphatidylinositol Transfer Protein Homolog through Activation of the Protein Kinases SPK1 and SPK2

Cited by 17 publications

References 0 publications

Identification of Nine Sucrose Nonfermenting 1-related Protein Kinases 2 Activated by Hyperosmotic and Saline Stresses in Arabidopsis thaliana

Identification of Nine Sucrose Nonfermenting 1-related Protein Kinases 2 Activated by Hyperosmotic and Saline Stresses in Arabidopsis thaliana

SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana

Nicotiana tabacum Osmotic Stress-activated Kinase Is Regulated by Phosphorylation on Ser-154 and Ser-158 in the Kinase Activation Loop

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