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Peptides and the Regulation of Plant Homeostasis

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Plant Signaling Peptides

Part of the book series: Signaling and Communication in Plants ((SIGCOMM,volume 16))

Abstract

Homeostasis defines the property of living organisms to keep a stable internal environment despite considerable external fluctuations, and this process is of considerable importance to plants as they are trapped unmoving in their changing surroundings. In addition to plant hormones, signaling peptides also have role(s) in maintaining plant homeostasis. Plant natriuretic peptides (PNPs) modulate ion channels and water uptake and have been implicated as compounds important in maintaining homeostasis. PNP and molecular mimics produced by pathogens modulate photosynthesis and the chloroplast proteome, thus indicating that PNP has widespread effects on homeostasis and could be considered a prototype homeostatic peptide. We propose that other peptides such as phytosulfokines (PSKs) and rapid alkalinization factors (RALFs) that have recognized roles in development and defense also have functions in plant homeostasis.

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References

  • Baena-Gonzalez E, Sheen J (2008) Convergent energy and stress signaling. Trends Plant Sci 13:474–482

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Billington T, Pharmawati M, Gehring CA (1997) Isolation and immunoaffinity purification of biologically active plant natriuretic peptide. Biochem Biophys Res Commun 235:722–725

    Article  PubMed  CAS  Google Scholar 

  • Blatt MR (1992) K+ channels of stomatal guard cells – characteristics of the inward rectifier and its control by pH. J Gen Physiol 99:615–644

    Article  PubMed  CAS  Google Scholar 

  • Blatt MR, Armstrong F (1993) K+ channels of stomatal guard cells – abscisic-acid-evoked control of the outward rectifier mediated by cytoplasmic pH. Planta 191:330–341

    Article  CAS  Google Scholar 

  • Boudart G, Jamet E, Rossignol M, Lafitte C, Borderies G, Jauneau A, Esquerre-Tugaye M, Pont-Lezica R (2004) Cell wall proteins in apoplastic fluids of Arabidopsis thaliana rosettes: identification by mass spectrometry and bioinformatics. Proteomics 5:212–221

    Article  Google Scholar 

  • Bowler C, Neuhaus G, Yamagata H, Chua N-H (1994) Cyclic GMP and calcium mediate phytochrome phototransduction. Cell 77:73–81

    Article  PubMed  CAS  Google Scholar 

  • Chen CC, England S, Akopian AN, Wood JN (1998) A sensory neuron-specific, proton-gated ion channel. Proc Natl Acad Sci USA 95:10240–10245

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Fromm J, Lautner S (2007) Electrical signals and their physiological significance in plants. Plant Cell Environ 30:249–257

    Article  PubMed  CAS  Google Scholar 

  • Gamble RL, Coonfield ML, Schaller GE (1998) Histidine kinase activity of the ETR1 ethylene receptor from Arabidopsis. Proc Natl Acad Sci USA 95:7825–7829

    Article  PubMed  CAS  Google Scholar 

  • Garavaglia BS, Thomas L, Zimaro T, Gottig N, Daurelio LD, Ndimba B, Orellano EG, Ottado J, Gehring C (2010a) A plant natriuretic peptide-like molecule of the pathogen Xanthomonas axonopodis pv. citri causes rapid changes in the proteome of its citrus host. BMC Plant Biol 10:51

    Article  PubMed  Google Scholar 

  • Garavaglia BS, Thomas L, Gottig N, Dunger G, Garofalo CG, Daurelio LD, Ndimba B, Orellano EG, Gehring C, Ottado J (2010b) A eukaryotic-acquired gene by a biotrophic phytopathogen allows prolonged survival on the host by counteracting the shut-down of plant photosynthesis. PLoS One 5:e8950

    Article  PubMed  Google Scholar 

  • Gehring CA, Irving HR (2003) Natriuretic peptides – a class of heterologous molecules in plants. Int J Biochem Cell Biol 35:1318–1322

    Article  PubMed  CAS  Google Scholar 

  • Gehring CA, Khalid KM, Toop T, Donald JA (1996) Rat natriuretic peptide binds specifically to plant membranes and induces stomatal opening. Biochem Biophys Res Commun 228:739–744

    Article  PubMed  CAS  Google Scholar 

  • Germain H, Chevalier E, Caron S, Matton DP (2005) Characterization of five RALF-like genes from Solanum chacoense provides support for a developmental role in plants. Planta 220:447–454

    Article  PubMed  CAS  Google Scholar 

  • 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 USA 105:18631–18636

    Article  PubMed  CAS  Google Scholar 

  • Gottig N, Garavaglia BS, Daurelio LD, Valentine A, Gehring C, Orellano EG, Ottado J (2009) Modulating host homeostasis as a strategy in the plant-pathogen arms race. Commun Integr Biol 2:89–90

    PubMed  CAS  Google Scholar 

  • Hanai H, Nakayama D, Yang H, Matsubayashi Y, Hirota Y, Sakagami Y (2000) Existence of a plant tyrosylprotein sulfotransferase: novel plant enzyme catalyzing tyrosine O-sulfation of preprophytosulfokine variants in vitro. FEBS Lett 470:97–101

    Article  PubMed  CAS  Google Scholar 

  • Haruta M, Constabel CP (2003) Rapid alkalinization factors in poplar cell cultures. Peptide isolation, cDNA cloning, and differential expression in leaves and methyl jasmonate-treated cells. Plant Physiol 131:814–823

    Article  PubMed  CAS  Google Scholar 

  • Haruta M, Monshausen G, Gilroy S, Sussman MR (2008) A cytoplasmic Ca2+ functional assay for identifying and purifying endogenous cell signaling peptides in Arabidopsis seedlings: identification of AtRALF1 peptide. Biochemistry 47:6311–6321

    Article  PubMed  CAS  Google Scholar 

  • Ilan N, Schwartz A, Moran N (1994) External pH effects on the depolarization-activated K-channels in guard cell protoplasts of Vicia faba. J Gen Physiol 103:807–831

    Article  PubMed  CAS  Google Scholar 

  • Ito Y, Nakanoyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H (2006) Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313:842–845

    Article  PubMed  CAS  Google Scholar 

  • Kaplan B, Sherman T, Fromm H (2007) Cyclic nucleotide-gated channels in plants. FEBS Lett 581:2237–2246

    Article  PubMed  CAS  Google Scholar 

  • Kende H, Zeevaart J (1997) The five “classical” plant hormones. Plant Cell 9:1197–1210

    Article  PubMed  CAS  Google Scholar 

  • Kende H, Bradford K, Brummell D, Cho HT, Cosgrove D, Fleming A, Gehring C, Lee Y, McQueen-Mason S, Rose J, Voesenek LA (2004) Nomenclature for members of the expansin superfamily of genes and proteins. Plant Mol Biol 55:311–314

    Article  PubMed  CAS  Google Scholar 

  • Kuhn M (2005) Cardiac and intestinal natriuretic peptides: insights from genetically modified mice. Peptides 26:1078–1085

    Article  PubMed  CAS  Google Scholar 

  • Kutschmar A, Rzewuski G, Stuhrwohldt N, Beemster GT, Inze D, Sauter M (2009) PSK-alpha promotes root growth in Arabidopsis. New Phytol 181:820–831

    Article  PubMed  CAS  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 signalling in plants. J Biol Chem 286:22580–22588

    Article  PubMed  CAS  Google Scholar 

  • Leng Q, Mercier RW, Yao W, Berkowitz GA (1999) Cloning and first functional characterization of a plant cyclic nucleotide-gated cation channel. Plant Physiol 121:753–761

    Article  PubMed  CAS  Google Scholar 

  • Lorbiecke R, Sauter M (2002) Comparative analysis of PSK peptide growth factor precursor homologs. Plant Sci 163:321–332

    Article  CAS  Google Scholar 

  • Ludidi NN, Heazlewood JL, Seoighe C, Irving HR, Gehring CA (2002) Expansin-like molecules: novel functions derived from common domains. J Mol Evol 54:587–594

    Article  PubMed  CAS  Google Scholar 

  • Ludidi N, Morse M, Sayed M, Wherrett T, Shabala S, Gehring C (2004) A recombinant plant natriuretic peptide causes rapid and spatially differentiated K+, Na+ and H+ flux changes in Arabidopsis thaliana roots. Plant Cell Physiol 45:1093–1098

    Article  PubMed  CAS  Google Scholar 

  • Ma W, Yoshioka K, Gehring C, Berkowitz G (2010) The function of cyclic nucleotide-gated channels in biotic stress. In: Demidchik V, Maathuis F (eds) Ion channels and plant stress responses, signaling and communication in plants. Springer, Berlin, pp 159–174

    Chapter  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Maryani MM, Shabala SN, Gehring CA (2000) Plant natriuretic peptide immunoreactants modulate plasma-membrane H(+) gradients in Solanum tuberosum L. leaf tissue vesicles. Arch Biochem Biophys 376:456–458

    Article  PubMed  CAS  Google Scholar 

  • Maryani MM, Bradley G, Cahill DM, Gehring CA (2001) Natriuretic peptides and immunoreactants modify osmoticum-dependent volume changes in Solanum tuberosum L. mesophyll cell protoplasts. Plant Sci 161:443–452

    Article  CAS  Google Scholar 

  • Matsubayashi Y, Sakagami Y (1996) Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc Natl Acad Sci USA 93:7623–7627

    Article  PubMed  CAS  Google Scholar 

  • Matsubayashi Y, Takagi L, Omura N, Morita A, Sakagami Y (1999) The endogenous sulfated pentapeptide phytosulfokine-alpha stimulates tracheary element differentiation of isolated mesophyll cells of zinnia. Plant Physiol 120:1043–1048

    Article  PubMed  CAS  Google Scholar 

  • Matsubayashi Y, Ogawa M, Morita A, Sakagami Y (2002) An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296:1470–1472

    Article  PubMed  CAS  Google Scholar 

  • Matsubayashi Y, Ogawa M, Kihara H, Niwa M, Sakagami Y (2006) Disruption and overexpression of Arabidopsis phytosulfokine receptor gene affects cellular longevity and potential for growth. Plant Physiol 142:45–53

    Article  PubMed  CAS  Google Scholar 

  • McGurl B, Pearce G, Ryan CA (1994) Polypeptide signalling for plant defence genes. Biochem Soc Symp 60:149–154

    PubMed  CAS  Google Scholar 

  • Meier S, Bastian R, Donaldson L, Murray S, Bajic V, Gehring C (2008) Co-expression and promoter content analyses assign a role in biotic and abiotic stress responses to plant natriuretic peptides. BMC Plant Biol 8:24

    Article  PubMed  Google 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 Signal Behav 4:307–309

    Article  PubMed  CAS  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  Google Scholar 

  • Mingossi FB, Matos JL, Rizzato AP, Medeiros AH, Falco MC, Silva-Filho MC, Moura DS (2010) SacRALF1, a peptide signal from the grass sugarcane (Saccharum spp.), is potentially involved in the regulation of tissue expansion. Plant Mol Biol 73:271–281

    Article  PubMed  CAS  Google Scholar 

  • 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 556:99–103

    Article  PubMed  CAS  Google Scholar 

  • Motose H, Iwamoto K, Endo S, Demura T, Sakagami Y, Matsubayashi Y, Moore KL, Fukuda H (2009) Involvement of phytosulfokine in the attenuation of stress response during the transdifferentiation of Zinnia mesophyll cells into tracheary elements. Plant Physiol 150:437–447

    Article  PubMed  CAS  Google Scholar 

  • Navarro B, Kirichok Y, Clapham DE (2007) KSper, a pH-sensitive K+ current that controls sperm membrane potential. Proc Natl Acad Sci USA 104:7688–7692

    Article  PubMed  CAS  Google Scholar 

  • Nembaware V, Seoighe C, Sayed M, Gehring C (2004) A plant natriuretic peptide-like gene in the bacterial pathogen Xanthomonas axonopodis may induce hyper-hydration in the plant host: a hypothesis of molecular mimicry. BMC Evol Biol 4:10

    Article  PubMed  Google Scholar 

  • Pandey S, Wang R-S, Wilson L, Li S, Zhao Z, Gookin TE, Assmann SM, Albert R (2010) Boolean modeling of transcriptome data reveals novel modes of heterotrimeric G-protein action. Mol Syst Biol 6:372

    Article  PubMed  Google Scholar 

  • Pearce G, Strydom D, Johnson S, Ryan CA (1991) A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science 253:895–898

    Article  PubMed  CAS  Google Scholar 

  • Pearce G, Moura DS, Stratmann J, Ryan CA Jr (2001) RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc Natl Acad Sci USA 98:12843–12847

    Article  PubMed  CAS  Google Scholar 

  • Pearce G, Munske G, Yamaguchi Y, Ryan CA (2010) Structure-activity studies of GmSubPep, a soybean peptide defense signal derived from an extracellular protease. Peptides 31:2159–2164

    Article  PubMed  CAS  Google Scholar 

  • Peuke AD, Windt C, Van As H (2006) Effects of cold-girdling on flows in the transport phloem in Ricinus communis: is mass flow inhibited? Plant Cell Environ 29:15–25

    Article  PubMed  Google Scholar 

  • Pharmawati M, Gehring CA, Irving HR (1998a) An immunoaffinity purified plant natriuretic peptide analogue modulates cGMP levels in the Zea mays root stele. Plant Sci 137:107–115

    Article  CAS  Google Scholar 

  • Pharmawati M, Billington T, Gehring CA (1998b) Stomatal guard cell responses to kinetin and natriuretic peptides are cGMP-dependent. Cell Mol Life Sci 54:272–276

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Pharmawati M, Maryani MM, Nikolakopoulos T, Gehring CA, Irving HR (2001) Cyclic GMP modulates stomatal opening induced by natriuretic peptides and immunoreactive analogues. Plant Physiol Biochem 39:385–394

    Article  CAS  Google Scholar 

  • Potter LR, Abbey-Hosch S, Dickey DM (2006) Natriuretic peptides, their receptors, and cyclic guanosine monophosphate-dependent signaling functions. Endocr Rev 27:47–72

    Article  PubMed  CAS  Google Scholar 

  • 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 USA 107:21193–21198

    Article  PubMed  CAS  Google Scholar 

  • Rafudeen S, Gxaba G, Makgoke G, Bradley G, Pironcheva G, Raitt L, Irving H, Gehring C (2003) A role for plant natriuretic peptide immuno-analogues in NaCl- and drought-stress responses. Physiol Planta 119:554–562

    Article  CAS  Google Scholar 

  • Ruzvidzo O, Donaldson L, Valentine A, Gehring C (2011) The Arabidopsis thaliana natriuretic peptide AtPNP-A is a systemic regulator of leaf dark respiration and signals via the phloem. J Plant Physiol 168:1710–1714

    Article  PubMed  CAS  Google Scholar 

  • Srivastava R, Liu JX, Howell SH (2008) Proteolytic processing of a precursor protein for a growth-promoting peptide by a subtilisin serine protease in Arabidopsis. Plant J 56:219–227

    Article  PubMed  CAS  Google Scholar 

  • Srivastava R, Liu JX, Guo H, Yin Y, Howell SH (2009) Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis. Plant J 59:930–939

    Article  PubMed  CAS  Google Scholar 

  • Suwastika I, Gehring C (1998) Natriuretic peptide hormones promote radial water movements from the xylem of Tradescantia shoots. Cell Mol Life Sci 54:1161–1167

    Article  CAS  Google Scholar 

  • Suwastika IN, Toop T, Irving HR, Gehring CA (2000) In situ and in vitro binding of natriuretic peptide hormones in Tradescantia multiflora. Plant Biol 2:1–3

    Article  CAS  Google Scholar 

  • Toop T, Donald JA (2004) Comparative aspects of natriuretic peptide physiology in non-mammalian vertebrates: a review. J Comp Physiol B 174:189–204

    Article  PubMed  CAS  Google Scholar 

  • Vesely DL, Giordano AT (1991) Atrial natriuretic peptide hormonal system in plants. Biochem Biophys Res Commun 179:695–700

    Article  PubMed  CAS  Google Scholar 

  • Vesely DL, Gower WR Jr, Giordano AT (1993) Atrial natriuretic peptides are present throughout the plant kingdom and enhance solute flow in plants. Am J Physiol 265:E465–E477

    PubMed  CAS  Google Scholar 

  • Wang YH, Irving HR (2011) Developing a model of plant hormone interactions. Plant Signal Behav 6:494–500

    Article  PubMed  CAS  Google Scholar 

  • Wang YH, Gehring C, Cahill DM, Irving HR (2007) Plant natriuretic peptide active site determination and effects on cGMP and cell volume regulation. Funct Plant Biol 34:645–653

    Article  CAS  Google Scholar 

  • Wang YH, Ahmar H, Irving HR (2010) Induction of apoptosis by plant natriuretic peptides in rat cardiomyoblasts. Peptides 31:1213–1218

    Article  PubMed  CAS  Google Scholar 

  • Wang YH, Gehring C, Irving HR (2011a) Plant natriuretic peptides are apoplastic and paracrine stress response molecules. Plant Cell Physiol 52:837–850

    Article  PubMed  CAS  Google Scholar 

  • Wang YH, Donaldson L, Gehring C, Irving HR (2011b) Plant natriuretic peptides: control of synthesis and systemic effects. Plant Signal Behav 6:1606–1608

    Article  PubMed  CAS  Google Scholar 

  • Wu J, Kurten EL, Monshausen G, Hummel GM, Gilroy S, Baldwin IT (2007) NaRALF, a peptide signal essential for the regulation of root hair tip apoplastic pH in Nicotiana attenuata, is required for root hair development and plant growth in native soils. Plant J 52:877–890

    Article  PubMed  CAS  Google Scholar 

  • Yang H, Matsubayashi Y, Nakamura K, Sakagami Y (1999) Oryza sativa PSK gene encodes a precursor of phytosulfokine-alpha, a sulfated peptide growth factor found in plants. Proc Natl Acad Sci USA 96:13560–13565

    Article  PubMed  CAS  Google Scholar 

  • Yang H, Matsubayashi Y, Nakamura K, Sakagami Y (2001) Diversity of Arabidopsis genes encoding precursors for phytosulfokine, a peptide growth factor. Plant Physiol 127:842–851

    Article  PubMed  CAS  Google Scholar 

  • Yu L, Moshelion M, Moran N (2001) Extracellular protons inhibit the activity of inward-rectifying potassium channels in the motor cells of Samanea saman pulvini. Plant Physiol 127:1310–1322

    Article  PubMed  CAS  Google Scholar 

  • Zeng X-H, Yang C, Kim ST, Lingle CJ, Xia X-M (2011) Deletion of the Slo3 gene abolishes alkalization-activated K(+) current in mouse spermatozoa. Proc Natl Acad Sci USA 108:5879–5884

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This work was supported by the Australian Research Council’s Discovery project funding scheme (DP0557561, DP0878194).

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Correspondence to Chris Gehring .

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Gehring, C., Irving, H.R. (2012). Peptides and the Regulation of Plant Homeostasis. In: Irving, H., Gehring, C. (eds) Plant Signaling Peptides. Signaling and Communication in Plants, vol 16. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-27603-3_10

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