Abstract
During the last decades, an increasing number of plant signaling peptides have been discovered and it appears that many of them are specific ligands for interacting receptor molecules. These receptors can enable the formation of second messengers which in turn transmit the ligand-induced stimuli into complex and tunable downstream responses. In order to perform such complex tasks, receptor proteins often contain several distinct domains such as a kinase and/or adenylate cyclase (AC) or guanylate cyclase (GC) domains. ACs catalyze the conversion of ATP to 3′,5′-cyclic adenosine monophosphate (cAMP) while GCs catalyze the reaction of GTP to 3′,5′-cyclic guanosine monophosphate (cGMP). Both cAMP and cGMP are now recognized as essential components of many plant responses, including responses to peptidic hormones. Here we describe the approach that led to the discovery of the Plant Natriuretic Peptide Receptor (PNP receptor), including a protocol for the identification of currently undiscovered peptidic interactions, and the subsequent application of computational methods for the identification of AC and/or GC domains in such interacting receptor candidates.
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References
Qi Z, Verma R, Gehring C, Yamaguchi Y, Zhao Y, 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(49):21193–21198. https://doi.org/10.1073/pnas.1000191107
Wheeler JI, Irving HR (2010) Evolutionary advantages of secreted peptide signalling. Funct Plant Biol 37:382–394
Matsubayashi Y (2014) Posttranslationally modified small-peptide signals in plants. Annu Rev Plant Biol 65:385–413. https://doi.org/10.1146/annurev-arplant-050312-120122
Turek I, Gehring C (2016) The plant natriuretic peptide receptor is a guanylyl cyclase and enables cGMP-dependent signaling. Plant Mol Biol 91(3):275–286. https://doi.org/10.1007/s11103-016-0465-8
Hirakawa Y, Torii KU, Uchida N (2017) Mechanisms and strategies shaping plant peptide hormones. Plant Cell Physiol 58(8):1313–1318. https://doi.org/10.1093/pcp/pcx069
Turek I, Wheeler J, Bartels S, Szczurek J, Wang YH, Taylor P, Gehring C, Irving H (2020) A natriuretic peptide from Arabidopsis thaliana (AtPNP-A) can modulate catalase 2 activity. Sci Rep 10(1):19632. https://doi.org/10.1038/s41598-020-76676-0
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(25):22580–22588. https://doi.org/10.1074/jbc.M110.168823
Gehring C, Turek IS (2017) Cyclic nucleotide monophosphates and their cyclases in plant signaling. Front Plant Sci 8:1704. https://doi.org/10.3389/fpls.2017.01704
Wheeler JI, Wong A, Marondedze C, Groen AJ, Kwezi L, Freihat L, Vyas J, Raji MA, Irving HR, Gehring C (2017) The brassinosteroid receptor BRI1 can generate cGMP enabling cGMP-dependent downstream signaling. Plant J 91(4):590–600. https://doi.org/10.1111/tpj.13589
Kwezi L, Wheeler JI, Marondedze C, Gehring C, Irving HR (2018) Intramolecular crosstalk between catalytic activities of receptor kinases. Plant Signal Behav 13(2):e1430544. https://doi.org/10.1080/15592324.2018.1430544
Muleya V, Marondedze C, Wheeler JI, Thomas L, Mok YF, Griffin MD, Manallack DT, Kwezi L, Lilley KS, Gehring C, Irving HR (2016) Phosphorylation of the dimeric cytoplasmic domain of the phytosulfokine receptor, PSKR1. Biochem J 473(19):3081–3098. https://doi.org/10.1042/BCJ20160593
Donaldson L, Meier S, Gehring C (2016) The Arabidopsis cyclic nucleotide interactome. Cell Commun Signal 14(1):10. https://doi.org/10.1186/s12964-016-0133-2
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(4):860–870. https://doi.org/10.1111/j.1469-8137.2008.02711.x
Ludidi N, Gehring C (2003) Identification of a novel protein with guanylyl cyclase activity in Arabidopsis thaliana. J Biol Chem 278(8):6490–6494. https://doi.org/10.1074/jbc.M210983200
Gehring C (2010) Adenyl cyclases and cAMP in plant signaling - past and present. Cell Commun Signal 8:15. https://doi.org/10.1186/1478-811X-8-15
Al-Younis I, Wong A, Lemtiri-Chlieh F, Schmockel S, Tester M, Gehring C, Donaldson L (2018) The Arabidopsis thaliana K+-uptake permease 5 (AtKUP5) contains a functional cytosolic adenylate cyclase essential for K+ transport. Front Plant Sci 9:1645. https://doi.org/10.3389/fpls.2018.01645
Al-Younis I, Moosa B, Kwiatkowski M, Jaworski K, Wong A, Gehring C (2021) Functional crypto-adenylate cyclases operate in complex plant proteins. Front Plant Sci 12:711749. https://doi.org/10.3389/fpls.2021.711749
Wong A, Tian X, Gehring C, Marondedze C (2018) Discovery of novel functional centers with rationally designed amino acid motifs. Comput Struct Biotechnol J 16:70–76. https://doi.org/10.1016/j.csbj.2018.02.007
Gottig N, Garavaglia BS, Daurelio LD, Valentine A, Gehring C, Orellano EG, Ottado J (2008) Xanthomonas axonopodis pv. citri uses a plant natriuretic peptide-like protein to modify host homeostasis. Proc Natl Acad Sci U S A 105(47):18631–18636. https://doi.org/10.1073/pnas.0810107105
Wang YH, Gehring C, Irving HR (2011) Plant natriuretic peptides are apoplastic and paracrine stress response molecules. Plant Cell Physiol 52(5):837–850. https://doi.org/10.1093/pcp/pcr036
Laemmli UK (1970) Cleavage of structural proteins during the assemby of the head of bacteriophage T4. Nature 227:680–685
Zhou W, Chi W, Shen W, Dou W, Wang J, Tian X, Gehring C, Wong A (2021) Computational identification of functional centers in complex proteins: a step-by-step guide with examples. Frontiers. Bioinformatics 1. https://doi.org/10.3389/fbinf.2021.652286
Wong A, Gehring C (2013) The Arabidopsis thaliana proteome harbors undiscovered multi-domain molecules with functional guanylyl cyclase catalytic centers. Cell Commun Signal 11(48). https://doi.org/10.1186/1478-811X-11-48
Xu N, Fu D, Li S, Wang Y, Wong A (2018) GCPred: a web tool for guanylyl cyclase functional Centre prediction from amino acid sequence. Bioinformatics 34(12):2134–2135. https://doi.org/10.1093/bioinformatics/bty067
Morse M, Pironcheva G, Gehring C (2004) AtPNP-A is a systemically mobile natriuretic peptide immunoanalogue with a role in Arabidopsis thaliana cell volume regulation. FEBS Lett 556(1–3):99–103. https://doi.org/10.1016/s0014-5793(03)01384-x
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(5):e449. https://doi.org/10.1371/journal.pone.0000449
Keller A, Nesvizhskii AI, Kolker E, Aebersold R (2002) Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal Chem 74(20):5383–5393
Nesvizhskii AI, Keller A, Kolker E, Aebersold R (2003) A statistical model for identifying proteins by tandem mass spectrometry. Anal Chem 75(17):4646–4658
Domingo-Almenara X, Montenegro-Burke JR, Ivanisevic J, Thomas A, Sidibe J, Teav T, Guijas C, Aisporna AE, Rinehart D, Hoang L, Nordstrom A, Gomez-Romero M, Whiley L, Lewis MR, Nicholson JK, Benton HP, Siuzdak G (2018) XCMS-MRM and METLIN-MRM: a cloud library and public resource for targeted analysis of small molecules. Nat Methods 15(9):681–684. https://doi.org/10.1038/s41592-018-0110-3
Adams KJ, Pratt B, Bose N, Dubois LG, St John-Williams L, Perrott KM, Ky K, Kapahi P, Sharma V, MacCoss MJ, Moseley MA, Colton CA, MacLean BX, Schilling B, Thompson JW, Alzheimer's Disease Metabolomics C (2020) Skyline for small molecules: a unifying software package for quantitative metabolomics. J Proteome Res 19(4):1447–1458. https://doi.org/10.1021/acs.jproteome.9b00640
Acknowledgments
The authors thank the KAUST Analytical and Bioscience Core Laboratories for supporting this project. I.T. was supported by a scholarship from King Abdullah University of Science and Technology.
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Turek, I., Gehring, C. (2024). Peptide-Mediated Cyclic Nucleotide Signaling in Plants: Identification and Characterization of Interactor Proteins with Nucleotide Cyclase Activity. In: Schaller, A. (eds) Plant Peptide Hormones and Growth Factors. Methods in Molecular Biology, vol 2731. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-3511-7_14
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DOI: https://doi.org/10.1007/978-1-0716-3511-7_14
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