Cyclic GMP modulates stomatal opening induced by natriuretic peptides and immunoreactive analogues

Pharmawati, Made; Maryani, Maria M; Nikolakopoulos, Theo; Gehring, Chris; Irving, Helen Ruth

doi:10.1016/s0981-9428(01)01252-9

Cited by 62 publications

(67 citation statements)

References 30 publications

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“…4). The increases in cGMP are of similar orders of magnitude to those reported previously in response to extracellular signals such as gibberellic acid (40) or plant natriuretic peptide (31,41,55), where they have proven sufficient and critical for a downstream response. Furthermore, the increases in cGMP occur in a time frame that is consistent with activating the GC catalytic function of the PSKR1 receptor.…”

Section: Discussionsupporting

confidence: 77%

“…However, our results indicate that PSK stimulates production of cGMP, and this is possibly a component of the delayed adaptive response to PSK-␣, which could involve the activation of cGMP-dependent transcriptome. Several previous studies have implicated cGMP and calcium cross-talk in plant cell expansion (38,(55)(56)(57)(58), and further work is required to investigate such an interaction at PSKR1. This article cites 58 references, 21 of which can be accessed free at…”

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confidence: 99%

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The Phytosulfokine (PSK) Receptor Is Capable of Guanylate Cyclase Activity and Enabling Cyclic GMP-dependent Signaling in Plants

Kwezi

Ruzvidzo

Wheeler

et al. 2011

Journal of Biological Chemistry

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125

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Phytosulfokines (PSKs) are sulfated pentapeptides that stimulate plant growth and differentiation mediated by the PSK receptor (PSKR1), which is a leucine-rich repeat receptor-like kinase. We identified a putative guanylate cyclase (GC) catalytic center in PSKR1 that is embedded within the kinase domain and hypothesized that the GC works in conjunction with the kinase in downstream PSK signaling. We expressed the recombinant complete kinase (cytoplasmic) domain of AtPSKR1 and show that it has serine/threonine kinase activity using the Ser/Thr peptide 1 as a substrate with an approximate K m of 7.5 M and V max of 1800 nmol min ؊1 mg ؊1 of protein. This same recombinant protein also has GC activity in vitro that is dependent on the presence of either Mg 2؉ or Mn 2؉ . Overexpression of the full-length AtPSKR1 receptor in Arabidopsis leaf protoplasts raised the endogenous basal cGMP levels over 20-fold, indicating that the receptor has GC activity in vivo. In addition, PSK-␣ itself, but not the non-sulfated backbone, induces rapid increases in cGMP levels in protoplasts. Together these results indicate that the PSKR1 contains dual GC and kinase catalytic activities that operate in vivo and that this receptor constitutes a novel class of enzymes with overlapping catalytic domains.

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Section: Discussionsupporting

confidence: 77%

mentioning

confidence: 99%

The Phytosulfokine (PSK) Receptor Is Capable of Guanylate Cyclase Activity and Enabling Cyclic GMP-dependent Signaling in Plants

Kwezi

Ruzvidzo

Wheeler

et al. 2011

Journal of Biological Chemistry

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125

123

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“…In this study, we provide evidence that PSK promotes cell expansion via cGMP as a second messenger that activates the cation channel CNGC17 as its target. cGMP was previously shown to promote swelling of tobacco protoplasts (Volotovski et al, 1998) and stoma opening in Tradescantia albiflora, while inhibition of GC caused stoma closure, supporting a role for GC activity in guard cell expansion (Pharmawati et al, 1998(Pharmawati et al, , 2001). We further show that the PSK receptor PSKR1 interacts with the PM-localized ATPase isoforms AHA1 and AHA2, which in turn physically interact with CNGC17, thus providing indirect linkage between PSKR1 and the cGMP target CNGC17.…”

Section: Discussionmentioning

confidence: 83%

Phytosulfokine Regulates Growth in Arabidopsis through a Response Module at the Plasma Membrane That Includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H⁺-ATPase, and BAK1

et al. 2015

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Phytosulfokine (PSK) is perceived by the leucine-rich repeat receptor kinase PSKR1 and promotes growth in Arabidopsis thaliana. PSKR1 is coexpressed with the CYCLIC NUCLEOTIDE-GATED CHANNEL gene CNGC17. PSK promotes protoplast expansion in the wild type but not in cngc17. Protoplast expansion is likewise promoted by cGMP in a CNGC17-dependent manner. Furthermore, PSKR1-deficient protoplasts do not expand in response to PSK but are still responsive to cGMP, suggesting that cGMP acts downstream of PSKR1. Mutating the guanylate cyclase center of PSKR1 impairs seedling growth, supporting a role for PSKR1 signaling via cGMP in planta. While PSKR1 does not interact directly with CNGC17, it interacts with the plasma membrane-localized H + -ATPases AHA1 and AHA2 and with the BRI-associated receptor kinase 1 (BAK1). CNGC17 likewise interacts with AHA1, AHA2, and BAK1, suggesting that PSKR1, BAK1, CNGC17, and AHA assemble in a functional complex. Roots of deetiolated bak1-3 and bak1-4 seedlings were unresponsive to PSK, and bak1-3 and bak1-4 protoplasts expanded less in response to PSK but were fully responsive to cGMP, indicating that BAK1 acts in the PSK signal pathway upstream of cGMP. We hypothesize that CNGC17 and AHAs form a functional cation-translocating unit that is activated by PSKR1/BAK1 and possibly other BAK1/RLK complexes.

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“…[2][3][4][5] Here we shall mainly focus on GCs and cGMP. The latter is critically implicated in responses to both abiotic and biotic stress responses, 6-8 the gating of channels, 9,10 plant hormone signal transduction, 11,12 nitric oxide (NO)-dependent signaling [13][14][15][16] as well as the regulation of transcription. 17 While there are currently only two experimentally confirmed GCs in higher plants, 18,19 this number has been predicted to significantly increase based on the presence of putative GC catalytic centers in many Arabidopsis thaliana proteins 20 and the number (>100) of annotated nucleotide cyclases in Chlamydomonas reinhardtii.…”

Section: Guanylyl Cyclases and Cgmp In Higher Plantsmentioning

confidence: 99%

Deciphering cGMP signatures and cGMP-dependent pathways in plant defence

Meier

Madeo

Ederli

et al. 2009

Plant Signaling & Behavior

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Guanylyl Cyclases and cGMP in Higher PlantsIt is emerging that cyclic nucleotides and hence the cyclic nucleotide generating enzymes such as adenylyl and guanylyl cyclases (GCs) 1 have key roles in many and diverse biological processes. 2-5 Here we shall mainly focus on GCs and cGMP. The latter is critically implicated in responses to both abiotic and biotic stress responses, 6-8 the gating of channels, 9,10 plant hormone signal transduction, 11,12 nitric oxide (NO)-dependent signaling 13-16 as well as the regulation of transcription. 17 While there are currently only two experimentally confirmed GCs in higher plants, 18,19 this number has been predicted to significantly increase based on the presence of putative GC catalytic centers in many Arabidopsis thaliana proteins 20 and the number (>100) of annotated nucleotide cyclases in Chlamydomonas reinhardtii. 4,20 We hypothesize that many more processes that are also critically dependent on the second messenger cGMP remain to be discovered and that catalytic domains capable of generating cGMP from GTP are part of a growing family of highly diverse multi-domain enzymes. Cyclic GMP in Plant Stress ResponsesIt has been previously been demonstrated that cGMP levels in Arabidopsis thaliana seedlings increase very rapidly (onset: ≤5 seconds), time dependently and, importantly, to different degrees in response to salt and osmotic stress, and that salt stress activates two distinct cGMP signalling pathways. 7 The osmotic pathway is independent of the second messenger [Ca 2+ ] c while the ionic response pathway, triggered by high NaCl, is [Ca 2+ ] c -dependent. These findings are an indication that cGMP plays a complex role in stress responses that cannot be accounted for by simple "on/ off " mechanisms. Contrary to the rapid changes in response to osmoticum dependent and ionic stress, responses to NO 6 and gravitropic stimulus appear to be much slower 21 and to the best of our knowledge, to-date there is no indication to suggest a link between the causing stimulus and the amplitude of resulting cGMP increases in biotic interactions between pathogens and their plant hosts.We have measured cGMP accumulation in Arabidopsis thaliana leaves following inoculation with virulent (DC3000) and avirulent

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Cyclic GMP modulates stomatal opening induced by natriuretic peptides and immunoreactive analogues

Cited by 62 publications

References 30 publications

The Phytosulfokine (PSK) Receptor Is Capable of Guanylate Cyclase Activity and Enabling Cyclic GMP-dependent Signaling in Plants

The Phytosulfokine (PSK) Receptor Is Capable of Guanylate Cyclase Activity and Enabling Cyclic GMP-dependent Signaling in Plants

Phytosulfokine Regulates Growth in Arabidopsis through a Response Module at the Plasma Membrane That Includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H⁺-ATPase, and BAK1

Deciphering cGMP signatures and cGMP-dependent pathways in plant defence

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Cyclic GMP modulates stomatal opening induced by natriuretic peptides and immunoreactive analogues

Cited by 62 publications

References 30 publications

The Phytosulfokine (PSK) Receptor Is Capable of Guanylate Cyclase Activity and Enabling Cyclic GMP-dependent Signaling in Plants

The Phytosulfokine (PSK) Receptor Is Capable of Guanylate Cyclase Activity and Enabling Cyclic GMP-dependent Signaling in Plants

Phytosulfokine Regulates Growth in Arabidopsis through a Response Module at the Plasma Membrane That Includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H+-ATPase, and BAK1

Deciphering cGMP signatures and cGMP-dependent pathways in plant defence

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Phytosulfokine Regulates Growth in Arabidopsis through a Response Module at the Plasma Membrane That Includes CYCLIC NUCLEOTIDE-GATED CHANNEL17, H⁺-ATPase, and BAK1