Skip to main content
SpringerLink
Log in
Book cover

Non-canonical Cyclic Nucleotides pp 87–103Cite as

Cyclic Nucleotide Monophosphates in Plants and Plant Signaling

  • Chapter
  • First Online:

Part of the book series: Handbook of Experimental Pharmacology ((HEP,volume 238))

Abstract

Cyclic nucleotide monophosphates (cNMPs) and the enzymes that can generate them are of increasing interest in the plant sciences. Arguably, the major recent advance came with the release of the complete Arabidopsis thaliana genome that has enabled the systematic search for adenylate (ACs) or guanylate cyclases (GCs) and did eventually lead to the discovery of a number of GCs in higher plants. Many of these proteins have complex domain architectures with AC or GC centers moonlighting within cytosolic kinase domains. Recent reports indicated the presence of not just the canonical cNMPs (i.e., cAMP and cGMP), but also the noncanonical cCMP, cUMP, cIMP, and cdTMP in plant tissues, and this raises several questions. Firstly, what are the functions of these cNMPs, and, secondly, which enzymes can convert the substrate triphosphates into the respective noncanonical cNMPs? The first question is addressed here by comparing the reactive oxygen species (ROS) response of cAMP and cGMP to that elicited by the noncanonical cCMP or cIMP. The results show that particularly cIMP can induce significant ROS production. To answer, at least in part, the second question, we have evaluated homology models of experimentally confirmed plant GCs probing the substrate specificity by molecular docking simulations to determine if they can conceivably catalytically convert substrates other than ATP or GTP. In summary, molecular modeling and substrate docking simulations can contribute to the evaluation of cyclases for noncanonical cyclic mononucleotides and thereby further our understanding of the molecular mechanism that underlie cNMP-dependent signaling in planta.

This is a preview of subscription content, log in via an institution.

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   229.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   299.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   299.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

References

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  CAS  PubMed  Google Scholar 

  • Bastian R, Dawe A, Meier S, Ludidi N, Bajic VB, Gehring C (2010) Gibberelic acid and cGMP-dependent transcriptional regulation in Arabidopsis thaliana. Plant Signal Behav 5:224–232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Berkowitz GA, Gehring C, Irving HR, Kwezi L (2011) Reply to Ashton: the putative guanylyl cyclase domain of AtPepR1 and similar plant receptors. Proc Natl Acad Sci U S A 108:E97–E98

    Article  CAS  PubMed Central  Google Scholar 

  • Beste KY, Seifert R (2013) cCMP, cUMP, cTMP, cIMP and cXMP as possible second messengers: development of a hypothesis based on studies with soluble guanylyl cyclase α(1)β(1). Biol Chem 394:261–270

    Article  CAS  PubMed  Google Scholar 

  • Beste KY, Burhenne H, Kaever V, Stasch J-P, Seifert R (2012) Nucleotidyl cyclase activity of soluble guanylyl cyclase α1β1. Biochemistry 51:194–204

    Article  CAS  PubMed  Google Scholar 

  • 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. Plant J 78:31–43

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bolwell GP (1995) Cyclic-AMP, the reluctant messenger in plants. Trends Biochem Sci 20:492–495

    Article  CAS  PubMed  Google Scholar 

  • Chen Z, Zhang X, Ying L, Dou D, Li Y, Bai Y, Liu J, Liu L, Feng H, Yu X, Leung SW, Vanhoutte PM, Gao Y (2014) cIMP synthesized by sGC as a mediator of hypoxic contraction of coronary arteries. Am J Physiol Heart Circ Physiol 307:H328–H336

    Article  CAS  PubMed  Google Scholar 

  • Choudhury S, Panda P, Sahoo L, Panda SK (2013) Reactive oxygen species signaling in plants under abiotic stress. Plant Signal Behav 8, e23681

    Article  PubMed  Google Scholar 

  • Cochaux P, Van Sande J, Dumont JE (1982) Inhibition of the cyclic AMP-adenylate cyclase system and of secretion by high concentrations of adenosine in the dog thyroid. Biochem Pharmacol 31:3763–3767

    Article  CAS  PubMed  Google Scholar 

  • Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Mol Plant 8:506–520

    Article  CAS  PubMed  Google Scholar 

  • Donaldson L, Ludidi N, Knight MR, Gehring C, Denby K (2004) Salt and osmotic stress cause rapid increases in Arabidopsis thaliana cGMP levels. FEBS Lett 569:317–320

    Article  CAS  PubMed  Google Scholar 

  • Durner J, Wendehenne D, Klessig DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. Proc Natl Acad Sci U S A 95:10328–10333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Facette MR, Shen Z, Bjornsdottir FR, Briggs SP, Smith LG (2013) Parallel proteomic and phosphoproteomic analyses of successive stages of maize leaf development. Plant Cell 25:2798–2812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Florio VA, Ross EM (1983) Regulation of the catalytic component of adenylate cyclase. Potentiative interaction of stimulatory ligands and 2',5'-dideoxyadenosine. Mol Pharmacol 24:195–202

    CAS  PubMed  Google Scholar 

  • Freihat L, Muleya V, Manallack DT, Wheeler JI, Irving HR (2014) Comparison of moonlighting guanylate cyclases: roles in signal direction? Biochem Soc Trans 42:1773–1779

    Article  CAS  PubMed  Google Scholar 

  • Gehring C (2010) Adenyl cyclases and cAMP in plant signaling – past and present. Cell Commun Signal 8:15

    Article  PubMed  PubMed Central  Google Scholar 

  • Hartwig C, Bähre H, Wolter S, Beckert U, Kaever V, Seifert R (2014) cAMP, cGMP, cCMP and cUMP concentrations across the tree of life: high cCMP and cUMP levels in astrocytes. Neurosci Lett 579:183–187

    Article  CAS  PubMed  Google Scholar 

  • Igarashi D, Tsuda K, Katagiri F (2012) The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J 71:194–204

    Article  CAS  PubMed  Google Scholar 

  • Irving HR, Gehring C (2013) Molecular methods for the study of signal transduction in plants. Methods Mol Biol 1016:1–11

    Article  CAS  PubMed  Google Scholar 

  • Irving HR, Kwezi L, Wheeler J, Gehring C (2012) Moonlighting kinases with guanylate cyclase activity can tune regulatory signal networks. Plant Signal Behav 7:201–204

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Isner JC, Nühse T, Maathuis FJ (2012) The cyclic nucleotide cGMP is involved in plant hormone signalling and alters phosphorylation of Arabidopsis thaliana root proteins. J Exp Bot 63:3199–3205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Isoni CA, Borges EA, Veloso CA, Mattos RT, Chaves MM, Nogueira-Machado JA (2009) cAMP activates the generation of reactive oxygen species and inhibits the secretion of IL-6 in peripheral blood mononuclear cells from type 2 diabetic patients. Oxid Med Cell Longev 2:317–321

    Article  PubMed  PubMed Central  Google Scholar 

  • Klessig DF, Durner J, Noad R, Navarre DA, Wendehenne D, Kumar D, Zhou JM, Shah J, Zhang S, Kachroo P, Trifa Y, Pontier D, Lam E, Silva H (2000) Nitric oxide and salicylic acid signaling in plant defense. Proc Natl Acad Sci U S A 97:8849–8855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kwezi L, Meier S, Mungur L, Ruzvidzo O, Irving H, Gehring C (2007) The Arabidopsis thaliana brassinosteroid receptor (AtBRI1) contains a domain that functions as a guanylyl cyclase in vitro. PLoS One 2, e449

    Article  PubMed  PubMed Central  Google Scholar 

  • 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. J Biol Chem 286:22580–22588

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lemtiri-Chlieh F, Thomas L, Marondedze C, Irving H, Gehring C (2011) Cyclic nucleotides and nucleotide cyclases in plant stress responses. In: Shanker A, Venkateswarlu B (eds) Abiotic stress response in plants – physiological, biochemical and genetic perspectives. InTech, Rijeka Croatia, pp 137–182. www.intechopen.com

    Google Scholar 

  • Liu Y, Ruoho AE, Rao VD, Hurley JH (1997) Catalytic mechanism of the adenylyl and guanylyl cyclases: modeling and mutational analysis. Proc Natl Acad Sci U S A 94:13414–13419

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ludidi N, Gehring C (2003) Identification of a novel protein with guanylyl cyclase activity in Arabidosis thaliana. J Biol Chem 278:6490–6494

    Article  CAS  PubMed  Google Scholar 

  • Maathuis FJ (2006) cGMP modulates gene transcription and cation transport in Arabidopsis roots. Plant J 45:700–711

    Article  CAS  PubMed  Google Scholar 

  • Marondedze C, Turek I, Parrott B, Thomas L, Jankovic B, Lilley KS, Gehring C (2013) Structural and functional characteristics of cGMP-dependent methionine oxidation in Arabidopsis thaliana proteins. Cell Commun Signal 11:1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCue LA, McDonough KA, Lawrence CE (2000) Functional classification of cNMP-binding proteins and nucleotide cyclases with implications for novel regulatory pathways in Mycobacterium tuberculosis. Genome Res 10:204–219

    Article  CAS  PubMed  Google Scholar 

  • Meier S, Seoighe C, Kwezi L, Irving H, Gehring C (2007) Plant nucleotide cyclases: an increasingly complex and growing family. Plant Signal Behav 2:536–539

    Article  PubMed  PubMed Central  Google Scholar 

  • 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, e8904

    Article  PubMed  PubMed Central  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  CAS  PubMed  Google Scholar 

  • Mosher S, Seybold H, Rodriguez P, Stahl M, Davies KA, Dayaratne S, Morillo SA, Wierzba M, Favery B, Keller H, Tax FE, Kemmerling B (2013) The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner. Plant J 73:469–482

    Article  CAS  PubMed  Google Scholar 

  • Moutinho A, Hussey PJ, Trewavas AJ, Malho R (2001) cAMP acts as a second messenger in pollen tube growth and reorientation. Proc Natl Acad Sci U S A 98:10481–10486

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mulaudzi T, Ludidi N, Ruzvidzo O, Morse M, Hendricks N, Iwuoha E, Gehring C (2011) Identification of a novel Arabidopsis thaliana nitric oxide-binding molecule with guanylate cyclase activity in vitro. FEBS Lett 585:2693–2697

    Article  CAS  PubMed  Google Scholar 

  • Muleya V, Wheeler JI, Ruzvidzo O, Freihat L, Manallack DT, Gehring C, Irving HR (2014) Calcium is the switch in the moonlighting dual function of the ligand-activated receptor kinase phytosulfokine receptor 1. Cell Commun Signal 12:60

    Article  PubMed  PubMed Central  Google Scholar 

  • Munne-Bosch S, Queval G, Foyer CH (2013) The impact of global change factors on redox signaling underpinning stress tolerance. Plant Physiol 161:5–19

    Article  CAS  PubMed  Google Scholar 

  • Newton RP, Smith CJ (2004) Cyclic nucleotides. Phytochemistry 65:2423–2437

    Article  CAS  PubMed  Google Scholar 

  • Newton RP, Chiatante D, Ghosh D, Brenton AG, Walton TJ, Harris FM, Brown EG (1989) Identification of cyclic-nucleotide constituents of meristematic and non-meristematic tissue of Pisum sativum roots. Phytochemistry 28:2243–2254

    Article  CAS  Google Scholar 

  • Newton RP, Roef L, Witters E, Van Onckelen H (1999) Tansley review No. 106 – cyclic nucleotides in higher plants: the enduring paradox. New Phytol 143:427–455

    Article  CAS  Google Scholar 

  • Nogueira-Machado JA, Limae Silva FC, Cunha EP, Calsolari MR, Costa DC, Perilo CS, Horta BC, Ferreira IC, Chaves MM (2006) Modulation of the production of reactive oxygen species (ROS) by cAMP-elevating agents in granulocytes from diabetic patients: an Akt/PKB-dependent phenomenon. Diabetes Metab 32:331–335

    Article  CAS  PubMed  Google Scholar 

  • O’Brien JA, Daudi A, Butt VS, Bolwell GP (2012) Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta 236:765–779

    Article  PubMed  Google Scholar 

  • Ordoñez NM, Marondedze C, Thomas L, Pasqualini S, Shabala L, Shabala S, Gehring C (2014) Cyclic mononucleotides modulate potassium and calcium flux responses to H2O2 in Arabidopsis roots. FEBS Lett 588:1008–1015

    Article  PubMed  Google Scholar 

  • Pasqualini S, Meier S, Gehring C, Madeo L, Fornaciari M, Romano B, Ederli L (2009) Ozone and nitric oxide induce cGMP-dependent and -independent transcription of defence genes in tobacco. New Phytol 181:860–870

    Article  CAS  PubMed  Google Scholar 

  • 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. Plant Cell 8:2325–2333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, Meng EC, Ferrin TE (2004) UCSF chimera – a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612

    Article  CAS  PubMed  Google Scholar 

  • Pharmawati M, Shabala SN, Newman IA, Gehring CA (1999) Natriuretic peptides and cGMP modulate K+, Na+, and H+ fluxes in Zea Mays roots. Mol Cell Biol Res Commun 2:53–57

    Article  CAS  PubMed  Google Scholar 

  • 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. Proc Natl Acad Sci U S A 107:21193–21198

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Roelofs J, Meima M, Schaap P, Van Haastert PJ (2001) The dictyostelium homologue of mammalian soluble adenylyl cyclase encodes a guanylyl cyclase. EMBO J 20:4341–4348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ruiz-Stewart I, Tiyyagura SR, Lin JE, Kazerounian S, Pitari GM, Schulz S, Martin E, Murad F, Waldman SA (2004) Guanylyl cyclase is an ATP sensor coupling nitric oxide signaling to cell metabolism. Proc Natl Acad Sci U S A 101:37–42

    Article  CAS  PubMed  Google Scholar 

  • Sali A, Blundell TL (1993) Comparative protein modelling by satisfaction of spatial restraints. J Mol Biol 234:779–815

    Article  CAS  PubMed  Google Scholar 

  • Schaap P (2005) Guanylyl cyclases across the tree of life. Front Biosci 10:1485–1498

    Article  CAS  PubMed  Google Scholar 

  • Seifert R (2014) Is cIMP a second messenger with functions opposite to those of cGMP? Naunyn Schmiedebergs Arch Pharmacol 387:897–899

    Article  CAS  PubMed  Google Scholar 

  • Seifert R (2015) cCMP and cUMP: emerging second messengers. Trends Biochem Sci 40:8–15

    Article  CAS  PubMed  Google Scholar 

  • Seifert R, Schneider EH, Bahre H (2015) From canonical to non-canonical cyclic nucleotides as second messengers: pharmacological implications. Pharmacol Ther 148:154–184

    Article  CAS  PubMed  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:26

    Google Scholar 

  • Shen Y, Diener AC (2013) Arabidopsis thaliana resistance to Fusarium oxysporum 2 implicates tyrosine-sulfated peptide signaling in susceptibility and resistance to root infection. PLoS Genet 9, e1003525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sunahara RK, Beuve A, Tesmer JJ, Sprang SR, Garbers DL, Gilman AG (1998) Exchange of substrate and inhibitor specificities between adenylyl and guanylyl cyclases. J Biol Chem 273:16332–16338

    Article  CAS  PubMed  Google Scholar 

  • Sürmeli NB, Müskens FM, Marletta MA (2015) The influence of nitric oxide on soluble guanylate cyclase regulation by nucleotides: the role of pseudosymmetric site. J Biol Chem 19: 15570–15580

    Google Scholar 

  • Suwastika IN, Gehring CA (1999) The plasma membrane H+-ATPase from tradescantia stem and leaf tissue is modulated in vitro by cGMP. Arch Biochem Biophys 367:137–139

    Article  CAS  PubMed  Google Scholar 

  • Talke IN, Blaudez D, Maathuis FJ, Sanders D (2003) CNGCs: prime targets of plant cyclic nucleotide signalling? Trends Plant Sci 8:286–293

    Article  CAS  PubMed  Google Scholar 

  • Trott O, Olson AJ (2010) AutoDock vina: improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J Comput Chem 31:455–461

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tucker CL, Hurley JH, Miller TR, Hurley JB (1998) Two amino acid substitutions convert a guanylyl cyclase, RetGC-1, into an adenylyl cyclase. Proc Natl Acad Sci U S A 95:5993–5997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wheeler JI, Freihat L, Irving HR (2013) A cyclic nucleotide sensitive promoter reporter system suitable for bacteria and plant cells. BMC Biotechnol 13:97

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong A, Gehring C (2013a) The Arabidopsis thaliana proteome harbors undiscovered multi-domain molecules with functional guanylyl cyclase catalytic centers. Cell Commun Signal 11:48

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wong A, Gehring C (2013b) Computational identification of candidate nucleotide cyclases in higher plants. Methods Mol Biol 1016:195–205

    Article  CAS  PubMed  Google Scholar 

  • Wong A, Gehring C, Irving HR (2015) Conserved functional motifs and homology modelling to predict hidden moonlighting functional sites. Front Bioeng Biotechnol 3:82

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoshida T, Mogami J, Yamaguchi-Shinozaki K (2015) Omics approaches toward defining the comprehensive abscisic acid signaling network in plants. Plant Cell Physiol 56:1043–1052

    Article  CAS  PubMed  Google Scholar 

  • Zelman AK, Dawe A, Gehring C, Berkowitz GA (2012) Evolutionary and structural perspectives of plant cyclic nucleotide-gated cation channels. Front Plant Sci 3:95

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhang G, Liu Y, Ruoho AE, Hurley JH (1997) Structure of the adenylyl cyclase catalytic core. Nature 386:247–253

    Article  CAS  PubMed  Google Scholar 

  • Zhou H, Yu M, Fukuda K, Im J, Yao P, Cui W, Bulek K, Zepp J, Wan Y, Kim TW, Yin W, Ma V, Thomas J, Gu J, Wang JA, DiCorleto PE, Fox PL, Qin J, Li X (2013) IRAK-M mediates toll-like receptor/IL-1R-induced NFkappaB activation and cytokine production. EMBO J 32:583–596

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biochemistry, Cambridge Centre for Proteomics, University of Cambridge, Cambridge, UK

    Claudius Marondedze

  2. Division of Biological and Environmental Science and Engineering, King Abdullah University of Science and Technology, Thuwal, Kingdom of Saudi Arabia

    Aloysius Wong & Chris Gehring

  3. Proteomics Core Laboratory, King Abdullah University of Science and Technology, Thuwal, Kingdom of Saudi Arabia

    Ludivine Thomas

  4. Drug Discovery Biology, Monash Institute of Pharmaceutical Sciences, Monash University, Melbourne, Australia

    Helen Irving

Authors
  1. Claudius Marondedze
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Aloysius Wong
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Ludivine Thomas
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Helen Irving
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Chris Gehring
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chris Gehring .

Editor information

Editors and Affiliations

  1. Medical School of Hannover Insitute of Pharmakology, Hannover, Niedersachsen, Germany

    Roland Seifert

Rights and permissions

Reprints and permissions

Copyright information

© 2015 Springer International Publishing Switzerland

About this chapter

Cite this chapter

Marondedze, C., Wong, A., Thomas, L., Irving, H., Gehring, C. (2015). Cyclic Nucleotide Monophosphates in Plants and Plant Signaling. In: Seifert, R. (eds) Non-canonical Cyclic Nucleotides. Handbook of Experimental Pharmacology, vol 238. Springer, Cham. https://doi.org/10.1007/164_2015_35

Download citation

Publish with us

Policies and ethics

Search

Navigation