Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
REVIEW

cGMP signalling in plants: from enigma to main stream

Jean-Charles Isner A and Frans J. M. Maathuis B C
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences, Life Sciences Building, University of Bristol, Woodland Road, 24 Tyndall Avenue, Bristol BS8 1TQ, UK.

B Department of Biology, University of York, York YO10 5DD, UK.

C Corresponding author. Email: fjm3@york.ac.uk

This paper originates from a presentation at the Fourth International Symposium on Plant Signaling and Behavior, Komarov Botanical Institute RAS/Russian Science Foundation, Saint Petersburg, Russia, 1923 June 2016.

Functional Plant Biology 45(2) 93-101 https://doi.org/10.1071/FP16337
Submitted: 29 September 2016  Accepted: 25 November 2016   Published: 20 December 2016

Abstract

All living organisms communicate with their environment, and part of this dialogue is mediated by secondary messengers such as cyclic guanosine mono phosphate (cGMP). In plants, most of the specific components that allow production and breakdown of cGMP have now been identified apart from cGMP dependent phosphodiesterases, enzymes responsible for cGMP catabolism. Irrespectively, the role of cGMP in plant signal transductions is now firmly established with involvement of this nucleotide in development, stress response, ion homeostasis and hormone function. Within these areas, several consistent themes where cGMP may be particularly relevant are slowly emerging: these include regulation of cation fluxes, for example via cyclic nucleotide gated channels and in stomatal functioning. Many details of signalling pathways that incorporate cGMP remain to be unveiled. These include downstream targets other than a small number of ion channels, in particular cGMP dependent kinases. Improved genomics tools may help in this respect, especially since many proteins involved in cGMP signalling appear to have multiple and often overlapping functional domains which hampers identification on the basis of simple homology searches. Another open question regards the topographical distribution of cGMP signals are they cell limited? Does long distance cGMP signalling occur and if so, by what mechanisms? The advent of non-disruptive fluorescent reporters with high spatial and temporal resolution will provide a tool to accelerate progress in all these areas. Automation can facilitate large scale screens of mutants or the action of effectors that impact on cGMP signalling.

Additional keywords: cyclic guanosine mono phosphate, CNGC, guard cell, ion homeostasis, signalling, stress.


References

Ashton AR (2011) Guanylyl cyclase activity in plants? Proceedings of the National Academy of Sciences of the United States of America 108, E96
Guanylyl cyclase activity in plants?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtlKrs7k%3D&md5=2da4769ec571628b5f9db4d5aa0a7b1cCAS |

Bailey-Serres J, Mittler R (2006) The roles of reactive oxygen species in plant cells. Plant Physiology 141, 311
The roles of reactive oxygen species in plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xmt1aksLs%3D&md5=69aae80d862a1a65dcef9c1fcc008665CAS |

Beligni MV, Lamattina L (2000) Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants. Planta 210, 215–221.
Nitric oxide stimulates seed germination and de-etiolation, and inhibits hypocotyl elongation, three light-inducible responses in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXisVWqtg%3D%3D&md5=0da3a3917688b09fc3bc443b9afbc432CAS |

Bojar D, Martinez J, Santiago J, Rybin V, Bayliss R, Hothorn M (2014) Crystal structures of the phosphorylated BRI1 kinase domain and implications for brassinosteroid signal initiation. The Plant Journal 78, 31–43.
Crystal structures of the phosphorylated BRI1 kinase domain and implications for brassinosteroid signal initiation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXkvVGmt7k%3D&md5=5d2fb66cda3c03b6dd2632fecd6007feCAS |

Chou H, Zhu YF, Ma Y, Berkowitz GA (2016) The CLAVATA signaling pathway mediating stem cell fate in shoot meristems requires Ca2+ as a secondary cytosolic messenger. The Plant Journal 85, 494–506.
The CLAVATA signaling pathway mediating stem cell fate in shoot meristems requires Ca2+ as a secondary cytosolic messenger.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xitl2gsL0%3D&md5=a33ce148c29e501cbaf0ec8cb27b6ed6CAS |

Cousson A (2003) Pharmacological evidence for a positive influence of the cyclic GMP-independent transduction on the cyclic GMP-mediated Ca2+-dependent pathway within Arabidopsis stomatal opening in response to auxin. Plant Science 164, 759–767.
Pharmacological evidence for a positive influence of the cyclic GMP-independent transduction on the cyclic GMP-mediated Ca2+-dependent pathway within Arabidopsis stomatal opening in response to auxin.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXivFeqsLk%3D&md5=e1b4c2263bf93083c53e97fabdaffaa3CAS |

Cousson A (2010) Indolyl-3-butyric acid-induced Arabidopsis stomatal opening mediated by 3ʹ, 5ʹ-cyclic guanosine-monophosphate. Plant Physiology and Biochemistry 48, 977–986.
Indolyl-3-butyric acid-induced Arabidopsis stomatal opening mediated by 3ʹ, 5ʹ-cyclic guanosine-monophosphate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtlKmsr7L&md5=c938f0bc2528dc2581389bfd95e691c3CAS |

Demidchik V, Maathuis FJM (2007) Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytologist 175, 387–404.
Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXpvFSqs7w%3D&md5=28f18af110308042d50ac9b976eb612bCAS |

Desikan R, Cheung MK, Bright J, Henson D, Hancock JT, Neill SJ (2004) ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells. Journal of Experimental Botany 55, 205–212.
ABA, hydrogen peroxide and nitric oxide signalling in stomatal guard cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslaq&md5=441028a67382fce1342b1bbeb9814941CAS |

Dodd AN, Kudla J, Sanders D (2010) The language of calcium signaling. Annual Reviews of Plant Biology 61, 593–620.
The language of calcium signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnslSjsbs%3D&md5=b459ba19deeb3eb1b8084070ab179380CAS |

Donaldson L, Ludidi N, Knight MR, Gehring C, Denby K (2004) Salt and osmotic stress cause rapid increases in Arabidopsis thaliana cGMP levels. FEBS Letters 569, 317–320.
Salt and osmotic stress cause rapid increases in Arabidopsis thaliana cGMP levels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXlt1amu7g%3D&md5=a917d6dc3cbe223af44119b637614477CAS |

Dubovskaya LV, Bakakina YS, Kolesneva EV, Sodel DL, McAinsh MR, Hetherington AM, Volotovski ID (2011) cGMP-dependent ABA-induced stomatal closure in the ABA-insensitive Arabidopsis mutant abi1-1. New Phytologist 191, 57–69.
cGMP-dependent ABA-induced stomatal closure in the ABA-insensitive Arabidopsis mutant abi1-1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXptVyhsb0%3D&md5=dec5dcdfd1c68075e4975ed954152ec3CAS |

Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proceedings of the National Academy of Sciences of the United States of America 95, 10328–10333.
Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXlsFGgtrw%3D&md5=beff85c0c03299ffa5f90b7ee05287f3CAS |

Essah PA, Davenport R, Tester M (2003) Sodium influx and accumulation in Arabidopsis. Plant Physiology 133, 307–318.
Sodium influx and accumulation in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXntlaiur8%3D&md5=094631d6228bdf03a231e1b46bd833ecCAS |

Gaupels F, Furch ACU, Zimmermann MR, Chen FX, Kaever V, Buhtzt A, Kehr J, Sarioglu H, Koger KH, Durner J (2016) Systemic induction of NO-, redox-, and cGMP signaling in the pumpkin extrafascicular phloem upon local leaf wounding. Frontiers in Plant Science 7, 154
Systemic induction of NO-, redox-, and cGMP signaling in the pumpkin extrafascicular phloem upon local leaf wounding.Crossref | GoogleScholarGoogle Scholar |

Gilroy S, Suzuki N, Miller G, Choi WG, Toyota M, Devireddy AR, Mittler R (2014) A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling. Trends in Plant Science 19, 623–630.
A tidal wave of signals: calcium and ROS at the forefront of rapid systemic signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXht1Wjs7vO&md5=407f872a39b69a7b2fdb58c1269f95a6CAS |

Gomez-Cadenas A, Zentella R, Walker-Simmons MK, Ho TH (2001) Gibberellin/abscisic acid antagonism in barley aleurone cells: site of action of the protein kinase PKABA1 in relation to gibberellin signaling molecules. The Plant Cell 13, 667–679.
Gibberellin/abscisic acid antagonism in barley aleurone cells: site of action of the protein kinase PKABA1 in relation to gibberellin signaling molecules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXis1akt7w%3D&md5=2939c97a9498088eb8a6b2017c39c6d4CAS |

Honda K, Yamada N, Yoshida R, Ihara H, Sawa T, Akaike T, Iwai S (2015) 8-mercapto-cyclic GMP mediates hydrogen sulfide-induced stomatal closure in Arabidopsis. Plant & Cell Physiology 56, 1481–1489.
8-mercapto-cyclic GMP mediates hydrogen sulfide-induced stomatal closure in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28Xht12hs7jO&md5=f2b2b7749f6383aa02488cd7ca57d947CAS |

Hu X, Neill SJ, Tang Z, Cai W (2005) Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiology 137, 663–670.
Nitric oxide mediates gravitropic bending in soybean roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhs1Kqsbc%3D&md5=ca758b4d653cce95ef948772944cb765CAS |

Inoue T, Fukuo K, Nakahashi T, Hata S, Morimoto S, Ogihara T (1995) cGMP upregulates nitric oxide synthase expression in vascular smooth muscle cells. Hypertension 25, 711–714.
cGMP upregulates nitric oxide synthase expression in vascular smooth muscle cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2MXlvVemsbw%3D&md5=55e33610fb4c4d9af566bd6d58aae448CAS |

Ishioka N, Tanimoto S (1990) Involvement of cyclic AMP in adventitious bud initiation of Torenia stem segments. Plant & Cell Physiology 31, 91–97.

Isner JC, Maathuis FJM (2011) Measurement of cellular cGMP in plant cells and tissues using the endogenous fluorescent reporter FlincG. The Plant Journal 65, 329–334.
Measurement of cellular cGMP in plant cells and tissues using the endogenous fluorescent reporter FlincG.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsl2mt70%3D&md5=f992e867497384a14a5fdb28d7f372b1CAS |

Isner JC, Nuhse T, Maathuis FJM (2012) The cyclic nucleotide cGMP is involved in plant hormone signalling and alters phosphorylation of Arabidopsis thaliana root proteins. Journal of Experimental Botany 63, 3199–3205.
The cyclic nucleotide cGMP is involved in plant hormone signalling and alters phosphorylation of Arabidopsis thaliana root proteins.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xnt1elsr8%3D&md5=daca7cb7bf701a8e0aee626bec6ce070CAS |

Joudoi T, Shichiri Y, Kamizono N, Akaike T, Sawa T, Yoshitake J, Yamada N, Iwai S (2013) Nitrated cyclic GMP modulates guard cell signaling in Arabidopsis. The Plant Cell 25, 558–571.
Nitrated cyclic GMP modulates guard cell signaling in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlvVOisr4%3D&md5=c24f714705f900fe0dfce2d1b85fa93fCAS |

Kaplan B, Sherman T, Fromm H (2007) Cyclic nucleotide-gated channels in plants. FEBS Letters 581, 2237–2246.
Cyclic nucleotide-gated channels in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXls1aiurg%3D&md5=11d3c93068801f78cbc7d46612259365CAS |

Kwezi L, Ruzvidzo O, Wheeler JI, Govender K, Iacuone S, Thompson PE, Gehring C, Irving HR (2011) The phytosulfokine (psk) receptor is capable of guanylate cyclase activity and enabling cyclic GMP-dependent signaling in plants. Journal of Biological Chemistry 286, 22580–22588.
The phytosulfokine (psk) receptor is capable of guanylate cyclase activity and enabling cyclic GMP-dependent signaling in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXns1Kkt7s%3D&md5=2913cdf67fda483dc3992a658b7fc5ebCAS |

Ladwig F, Dahlke RI, Stuhrwohldt N, Hartmann J, Harter K, Sauter M (2015) Phytosulfokine regulates growth in Arabidopsis through a response module at the plasma membrane that includes CYCLIC NUCLEOTIDE- GATED CHANNEL17, H+-ATPase, and BAK1. The Plant Cell 27, 1718–1729.
Phytosulfokine regulates growth in Arabidopsis through a response module at the plasma membrane that includes CYCLIC NUCLEOTIDE- GATED CHANNEL17, H+-ATPase, and BAK1.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXht1SlsL7E&md5=04ee1f7542c4565baad716d21cce044aCAS |

Lanteri ML, Pagnussat GC, Lamattina L (2006) Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber. Journal of Experimental Botany 57, 1341–1351.
Calcium and calcium-dependent protein kinases are involved in nitric oxide- and auxin-induced adventitious root formation in cucumber.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtFSkt7w%3D&md5=f0c64374bc850a2c3f5486f6eb4c90d8CAS |

Li SW, Xue LG (2010) The interaction between H2O2 and NO, Ca2+, cGMP, and MAPKs during adventitious rooting in mung bean seedlings. Cellular & Developmental Biology. Plant 46, 142–148.
The interaction between H2O2 and NO, Ca2+, cGMP, and MAPKs during adventitious rooting in mung bean seedlings.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlvFWlurY%3D&md5=89f26f27bf55c3318343d799b8aa81faCAS |

Li JS, Jia HL, Wang J (2014) cGMP and ethylene are involved in maintaining ion homeostasis under salt stress in Arabidopsis roots. Plant Cell Reports 33, 447–459.
cGMP and ethylene are involved in maintaining ion homeostasis under salt stress in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar |

Ludidi N, Gehring C (2003) Identification of a novel protein with guanylyl cyclase activity in Arabidopsis thaliana. Journal of Biological Chemistry 278, 6490–6494.
Identification of a novel protein with guanylyl cyclase activity in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXht1ejsL0%3D&md5=b42c6224cc3d410114a97f21661b8046CAS |

Ma Y, Zhao YC, Walker RK, Berkowitz GA (2013) Molecular steps in the immune signaling pathway evoked by plant elicitor peptides: Ca2+-dependent protein kinases, nitric oxide, and reactive oxygen species are downstream from the early Ca2+ signal. Plant Physiology 163, 1459–1471.
Molecular steps in the immune signaling pathway evoked by plant elicitor peptides: Ca2+-dependent protein kinases, nitric oxide, and reactive oxygen species are downstream from the early Ca2+ signal.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsl2nurfP&md5=bd217cb197173812ac1e3f1aa8436f43CAS |

Maathuis FJM (2006) cGMP modulates gene transcription and cation transport in Arabidopsis roots. The Plant Journal 45, 700–711.
cGMP modulates gene transcription and cation transport in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjt1SjtrY%3D&md5=df0fb3f4c600da9aa053e862f0200cbfCAS |

Maathuis FJ, Sanders D (2001) Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides. Plant Physiology 127, 1617–1625.
Sodium uptake in Arabidopsis roots is regulated by cyclic nucleotides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XjtVWmsw%3D%3D&md5=059c32a7acaa4a015d3bae6c5b7213caCAS |

Marondedze C, Groen AJ, Thomas L, Lilley KS, Gehring C (2016) A quantitative phosphoproteome analysis of cGMP-dependent cellular responses in Arabidopsis thaliana. Molecular Plant 9, 621–623.
A quantitative phosphoproteome analysis of cGMP-dependent cellular responses in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsVKltb0%3D&md5=0626d24958470b663295a0ac62f7a4f5CAS |

Martinez-Atienza J, Van Ingelgem C, Roef L, Maathuis FJ (2007) Plant cyclic nucleotide signalling: facts and fiction. Plant Signaling & Behavior 2, 540–543.
Plant cyclic nucleotide signalling: facts and fiction.Crossref | GoogleScholarGoogle Scholar |

Meier S, Madeo L, Ederli L, Donaldson L, Pasqualini S, Gehring C (2009) Deciphering cGMP signatures and cGMP-dependent pathways in plant defence. Plant Signaling & Behavior 4, 307–309.
Deciphering cGMP signatures and cGMP-dependent pathways in plant defence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXpsVyqu70%3D&md5=abf1608f701382aec84a5604cf697d7eCAS |

Meier S, Ruzvidzo O, Morse M, Donaldson L, Kwezi L, Gehring C (2010) The Arabidopsis wall associated kinase-like 10 gene encodes a functional guanylyl cyclase and is co-expressed with pathogen defense related genes. Plos One 5,
The Arabidopsis wall associated kinase-like 10 gene encodes a functional guanylyl cyclase and is co-expressed with pathogen defense related genes.Crossref | GoogleScholarGoogle Scholar |

Munnik T, Testerink C (2009) Plant phospholipid signaling: ‘in a nutshell’. Journal of Lipid Research 50, S260–S265.
Plant phospholipid signaling: ‘in a nutshell’.Crossref | GoogleScholarGoogle Scholar |

Nan WB, Wang XM, Yang L, Hu YF, Wei YT, Liang XL, Mao LN, Bi YR (2014) Cyclic GMP is involved in auxin signalling during Arabidopsis root growth and development. Journal of Experimental Botany 65, 1571–1583.
Cyclic GMP is involved in auxin signalling during Arabidopsis root growth and development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXltFKisLw%3D&md5=7c300ae6684c4aad384b249732b58b1aCAS |

Neill SJ, Desikan R, Clarke A, Hancock JT (2002) Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells. Plant Physiology 128, 13–16.
Nitric oxide is a novel component of abscisic acid signaling in stomatal guard cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XmvVSluw%3D%3D&md5=390fec6bed4ddba92c44cdd5fd91fe41CAS |

Neill S, Barros R, Bright J, Desikan R, Hancock J, Harrison J, Morris P, Ribeiro D, Wilson I (2008) Nitric oxide, stomatal closure, and abiotic stress. Journal of Experimental Botany 59, 165–176.
Nitric oxide, stomatal closure, and abiotic stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXjsVamt70%3D&md5=dcf59f11ae884657b6a2c5a8b70d25e8CAS |

Newton RP, Smith CJ (2004) Cyclic nucleotides. Phytochemistry 65, 2423–2437.
Cyclic nucleotides.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnslKhsrc%3D&md5=3e367f54fc72b4143af9c72eb772b912CAS |

Ordoñez NM, Marondedze C, Ludivine T, Pasqualini S, Shabala L, Shabala S, Gehring C (2014) Cyclic mononucleotides modulate potassium and calcium flux responses to H2O2 in Arabidopsis roots. FEBS Letters 588, 1008–1015.
Cyclic mononucleotides modulate potassium and calcium flux responses to H2O2 in Arabidopsis roots.Crossref | GoogleScholarGoogle Scholar |

Pagnussat GC, Lanteri ML, Lamattina L (2003) Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process. Plant Physiology 132, 1241–1248.
Nitric oxide and cyclic GMP are messengers in the indole acetic acid-induced adventitious rooting process.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXlsFGhtLw%3D&md5=f33df12d4b237e35b3c30592b8fa8278CAS |

Pagnussat GC, Lanteri ML, Lombardo MC, Lamattina L (2004) Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiology 135, 279–286.
Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXkt12nurk%3D&md5=7d0fcf606414568670fca29b7e32f7b5CAS |

Penson SP, Schuurink RC, Fath A, Gubler F, Jacobsen JV, Jones RL (1996) cGMP is required for gibberellic acid-induced gene expression in barley aleurone. The Plant Cell 8, 2325–2333.
cGMP is required for gibberellic acid-induced gene expression in barley aleurone.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2sXisl2rsw%3D%3D&md5=b1f66da26022e7be5d0e615328d3b548CAS |

Pharmawati M, Billington T, Gehring CA (1998) Stomatal guard cell responses to kinetin and natriuretic peptides are cGMP-dependent. Cellular and Molecular Life Sciences 54, 272–276.
Stomatal guard cell responses to kinetin and natriuretic peptides are cGMP-dependent.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXisVOjs74%3D&md5=33a6a07304f64160ae8e825e649725aeCAS |

Pharmawati M, Maryani MM, Nikolakopoulos T, Gehring CA, Irving HR (2001) Cyclic GMP modulates stomatal opening induced by natriuretic peptides and immunoreactive analogues. Plant Physiology and Biochemistry 39, 385–394.
Cyclic GMP modulates stomatal opening induced by natriuretic peptides and immunoreactive analogues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktlSit78%3D&md5=9f91b2559b6d33defa6b25864d5be290CAS |

Qi Z, Verma R, Gehring C, Yamaguchi Y, Zhao YC, Ryan CA, Berkowitz GA (2010) Ca2+ signaling by plant Arabidopsis thaliana Pep peptides depends on AtPepR1, a receptor with guanylyl cyclase activity, and cGMP-activated Ca2+ channels. Proceedings of the National Academy of Sciences of the United States of America 107, 21193–21198.
Ca2+ signaling by plant Arabidopsis thaliana Pep peptides depends on AtPepR1, a receptor with guanylyl cyclase activity, and cGMP-activated Ca2+ channels.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFyls7fP&md5=efe8f4a83c861e5daba84dfc56efd9d9CAS |

Rubio F, Flores P, Navarro JM, Martinez V (2003) Effects of Ca2+, K+ and cGMP on Na+ uptake in pepper plants. Plant Science 165, 1043–1049.
Effects of Ca2+, K+ and cGMP on Na+ uptake in pepper plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsVagtrs%3D&md5=45fd97d7e6c31332ce3e04e4f9062a6aCAS |

Sauter M (2015) Phytosulfokine peptide signalling. Journal of Experimental Botany 66, 5161–5169.
Phytosulfokine peptide signalling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXitVWht77E&md5=aa31a815ab4a1f74278be9d573c053b2CAS |

Strack R (2016) Yes to genetically encoded NO center dot sensors. Nature Methods 13, 288
Yes to genetically encoded NO center dot sensors.Crossref | GoogleScholarGoogle Scholar |

Szmidt-Jaworska A, Jaworski K, Zienkiewicz A, Lenartowska M, Kopcewicz J (2009) Guanylyl cyclase activity during photoperiodic flower induction in Pharbitis nil. Plant Growth Regulation 57, 173–184.
Guanylyl cyclase activity during photoperiodic flower induction in Pharbitis nil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlGnsL0%3D&md5=b4edd3c61cc9691abc3117f8cd7369cfCAS |

Talke IN, Blaudez D, Maathuis FJM, Sanders D (2003) CNGCs: prime targets of plant cyclic nucleotide signalling? Trends in Plant Science 8, 286–293.
CNGCs: prime targets of plant cyclic nucleotide signalling?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXksF2hurs%3D&md5=ed2c844c597f57fd8f76f15973e86e71CAS |

Teng Y, Xu WZ, Ma M (2010) cGMP is required for seed germination in Arabidopsis thaliana. Journal of Plant Physiology 167, 885–889.
cGMP is required for seed germination in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXpt1Citbc%3D&md5=96f9b01aaf4e5669188b4725eee2bf73CAS |

Turek I, Gehring C (2016) The plant natriuretic peptide receptor is a guanylyl cyclase and enables cGMP-dependent signaling. Plant Molecular Biology 91, 275–286.
The plant natriuretic peptide receptor is a guanylyl cyclase and enables cGMP-dependent signaling.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XjvVGitLc%3D&md5=4280657792bfded5618d0a464d62e105CAS |

Turek I, Marondedze C, Wheeler JI, Gehring C, Irving HR (2014) Plant natriuretic peptides induce proteins diagnostic for an adaptive response to stress. Frontiers in Plant Science 5, 1–11.
Plant natriuretic peptides induce proteins diagnostic for an adaptive response to stress.Crossref | GoogleScholarGoogle Scholar |

Van Damme T, Blancquaert D, Couturon P, Van Der Straeten D, Sandra P, Lynen F (2014) Wounding stress causes rapid increase in concentration of the naturally occurring 2ʹ,3ʹ-isomers of cyclic guanosine- and cyclic adenosine monophosphate (cGMP and cAMP) in plant tissues. Phytochemistry 103, 59–66.
Wounding stress causes rapid increase in concentration of the naturally occurring 2ʹ,3ʹ-isomers of cyclic guanosine- and cyclic adenosine monophosphate (cGMP and cAMP) in plant tissues.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXmtFakt74%3D&md5=915d6f11293794195ec32ebde58dc982CAS |

Wang HC, Ngwenyama N, Liu YD, Walker JC, Zhang SQ (2007) Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. The Plant Cell 19, 63–73.
Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Wang YH, Gehring C, Irving HR (2011) Plant natriuretic peptides are apoplastic and paracrine stress response molecules. Plant & Cell Physiology 52, 837–850.
Plant natriuretic peptides are apoplastic and paracrine stress response molecules.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtFymsr8%3D&md5=e28ac2d355fbfee7617e2c5e472c2043CAS |

Wang YF, Munemasa S, Nishimura N, Ren HM, Robert N, Han M, Puzorjova I, Kollist H, Lee S, Mori I, Schroeder JI (2013) Identification of cyclic GMP-activated nonselective Ca2+-permeable cation channels and associated CNGC5 and CNGC6 genes in Arabidopsis guard cells. Plant Physiology 163, 578–590.
Identification of cyclic GMP-activated nonselective Ca2+-permeable cation channels and associated CNGC5 and CNGC6 genes in Arabidopsis guard cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Ojs7fO&md5=551774920ea59b8d4f2c19965432ffdcCAS |

Wheeler JI, Irving HR (2010) Evolutionary advantages of secreted peptide signalling molecules in plants. Functional Plant Biology 37, 382–394.
Evolutionary advantages of secreted peptide signalling molecules in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXlsFKnu7c%3D&md5=481c87319f1eccf12c393265d59c330bCAS |

Wheeler JI, Freihat L, Irving HR (2013) A cyclic nucleotide sensitive promoter reporter system suitable for bacteria and plant cells. BMC Biotechnology 13, 97
A cyclic nucleotide sensitive promoter reporter system suitable for bacteria and plant cells.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhvVans7nF&md5=0c79a72d0062a02c47acfbdd763a9e5bCAS |

Wu MZ, Wang FQ, Zhang C, Xie YJ, Han B, Huang JJ, Shen WB (2013) Heme oxygenase-1 is involved in nitric oxide- and cGMP-induced α-Amy2/54 gene expression in GA-treated wheat aleurone layers. Plant Molecular Biology 81, 27–40.
Heme oxygenase-1 is involved in nitric oxide- and cGMP-induced α-Amy2/54 gene expression in GA-treated wheat aleurone layers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhvV2ks7rP&md5=3c208d2584c8e0259743adc08ea8fb97CAS |

Zhao YC, Qi Z, Berkowitz GA (2013) Teaching an old hormone new tricks: cytosolic Ca2+ elevation involvement in plant brassinosteroid signal transduction cascades. Plant Physiology 163, 555–565.
Teaching an old hormone new tricks: cytosolic Ca2+ elevation involvement in plant brassinosteroid signal transduction cascades.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Ojs7bL&md5=5ae2f84de861ed729e0b86f0afdbdb4cCAS |