Stomatal guard cell responses to kinetin and natriuretic peptides are cGMP-dependent

Pharmawati, Made; Billington, Timothy; Gehring, Chris

doi:10.1007/s000180050149

Cited by 82 publications

(65 citation statements)

References 19 publications

(29 reference statements)

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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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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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“…We are currently in the process of elucidating the biological role of AtGC1 with particular emphasis on cGMP dependent promotion of stomatal opening (12,13) and responses to plant hormones such as kinetin and immunoreactant plant natriuretic peptides (13)(14)(15).…”

Section: Discussionmentioning

confidence: 99%

“…Cell-permeable cGMP and cAMP analogs elicit elevation of cytosolic Ca 2ϩ in tobacco protoplasts and cause a physiological swelling response in plant protoplasts (11). Opening of the stomatal pore, which results from a swelling of the two neighboring guard cells, has been observed in response to cell-permeable cGMP analogs and is suppressed by guanylyl cyclase inhibitors (12). Like protoplast swelling, stomatal aperture regulation is likely to be tuned by Ca 2ϩ and cGMP cross-talk (13).…”

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confidence: 99%

Identification of a Novel Protein with Guanylyl Cyclase Activity in Arabidopsis thaliana

Ludidi

Gehring

2003

Journal of Biological Chemistry

165

147

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Guanylyl cyclases (GCs) catalyze the formation of the second messenger guanosine 3,5-cyclic monophosphate (cGMP) from guanosine 5-triphosphate (GTP). While many cGMP-mediated processes in plants have been reported, no plant molecule with GC activity has been identified. When the Arabidopsis thaliana genome is queried with GC sequences from cyanobacteria, lower and higher eukaryotes no unassigned proteins with significant similarity are found. However, a motif search of the A. thaliana genome based on conserved and functionally assigned amino acids in the catalytic center of annotated GCs returns one candidate that also contains the adjacent glycine-rich domain typical for GCs. In this molecule, termed AtGC1, the catalytic domain is in the N-terminal part. AtGC1 contains the arginine or lysine that participates in hydrogen bonding with guanine and the cysteine that confers substrate specificity for GTP. When AtGC1 is expressed in Escherichia coli, cell extracts yield >2.5 times more cGMP than control extracts and this increase is not nitric oxide dependent. Furthermore, purified recombinant AtGC1 has Mg 2؉ -dependent GC activity in vitro and >3 times less adenylyl cyclase activity when assayed with ATP as substrate in the absence of GTP. Catalytic activity in vitro proves that AtGC1 can function either as a monomer or homo-oligomer. AtGC1 is thus not only the first functional plant GC but also, due to its unusual domain organization, a member of a new class of GCs.

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“…A role for cGMP in kinetin-and natriuretic peptide-induced stomatal opening has been described in T. albiflora (Pharmawati et al, 1998). In C. communis and Arabidopsis, cGMP mediated auxin-induced stomatal opening (Cousson and Vavasseur, 1998;Cousson, 2003).…”

Section: -Nitro-cgmp Is a Novel Signaling Molecule In Plantsmentioning

confidence: 99%

“…By contrast, it did induce stomatal opening in Commelina communis, Tradescantia albiflora, fava bean (Vicia faba), and Arabidopsis (Cousson and Vavasseur, 1998;Pharmawati et al, 1998Pharmawati et al, , 2001Cousson, 2003). Thus, the issue of whether the NO/ cGMP cascade operates in guard cell signaling is still controversial.…”

Section: Introductionmentioning

confidence: 99%

Nitrated Cyclic GMP Modulates Guard Cell Signaling inArabidopsis

et al. 2013

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Nitric oxide (NO) is a ubiquitous signaling molecule involved in diverse physiological processes, including plant senescence and stomatal closure. The NO and cyclic GMP (cGMP) cascade is the main NO signaling pathway in animals, but whether this pathway operates in plant cells, and the mechanisms of its action, remain unclear. Here, we assessed the possibility that the nitrated cGMP derivative 8-nitro-cGMP functions in guard cell signaling. Mass spectrometry and immunocytochemical analyses showed that abscisic acid and NO induced the synthesis of 8-nitro-cGMP in guard cells in the presence of reactive oxygen species. 8-Nitro-cGMP triggered stomatal closure, but 8-bromoguanosine 39,59-cyclic monophosphate (8-bromocGMP), a membrane-permeating analog of cGMP, did not. However, in the dark, 8-bromo-cGMP induced stomatal opening but 8-nitro-cGMP did not. Thus, cGMP and its nitrated derivative play different roles in the signaling pathways that lead to stomatal opening and closure. Moreover, inhibitor and genetic studies showed that calcium, cyclic adenosine-59-diphosphate-ribose, and SLOW ANION CHANNEL1 act downstream of 8-nitro-cGMP. This study therefore demonstrates that 8-nitro-cGMP acts as a guard cell signaling molecule and that a NO/8-nitro-cGMP signaling cascade operates in guard cells.

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Stomatal guard cell responses to kinetin and natriuretic peptides are cGMP-dependent

Cited by 82 publications

References 19 publications

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

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

Identification of a Novel Protein with Guanylyl Cyclase Activity in Arabidopsis thaliana

Nitrated Cyclic GMP Modulates Guard Cell Signaling inArabidopsis

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Stomatal guard cell responses to kinetin and natriuretic peptides are cGMP-dependent

Cited by 82 publications

References 19 publications

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

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

Identification of a Novel Protein with Guanylyl Cyclase Activity in Arabidopsis thaliana

Nitrated Cyclic GMP Modulates Guard Cell Signaling inArabidopsis

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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

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