Plant Natriuretic Peptides


Plant natriuretic peptides (PNPs) belong to a growing number of plant peptide hormones. PNPs were first immuno‐affinity purified from ivy with an antibody against the vertebrate atrial natriuretic peptide (ANP) and were shown to affect a number of physiological responses, including stomatal movements and abiotic and biotic stress responses. PNPs are secreted into the apoplastic space and are systemically mobile. They act at nanomolar concentrations and in a 3′,5′‐cyclic guanosine monophosphate (cGMP)‐dependent manner. The Arabidopsis thaliana PNP (AtPNP‐A) is distantly related to expansins, but it does not contain a wall‐binding domain consistent with its systemic mode of action. The first AtPNP‐A receptor (AtPNP‐R1) is a novel leucine‐rich repeat receptor kinase located in the cell membrane and harbours a functional guanylyl cyclase in the cytosolic part essential for cGMP‐dependent responses. Finally, PNPs have also been acquired by several plant pathogens through ancient horizontal gene transfer and interfere with host defences to the detriment of their hosts.

Key Concepts

  • Most currently established plant hormones are small molecules that can act on the site of synthesis or at a distance from their site of synthesis, within or between plants.
  • Plant peptide hormones are a new and rapidly expanding class of plant hormones that have important roles in growth, development and responses to the environment and in particular the defence against pathogens.
  • Plant peptide hormones, including plant natriuretic peptides (PNPs), are systemically mobile and can signal through membrane‐associated receptor kinases some of which harbour functional guanylyl cyclase catalytic centres capable of converting GTP to cGMP.
  • cGMP, in turn, is a key messenger in plant responses to the environment that enables and modulates downstream responses including cGMP‐dependent protein phosphorylation and the activation of cyclic nucleotide‐gated channels (CNGCs).
  • Animal natriuretic peptides (ANPs), although not orthologs of PNPs, can trigger similar responses in plants, and both can act as ligands for their membrane‐associated receptors that harbour guanylyl cyclases capable of generating cGMP from GTP.
  • PNPs have been acquired by some plant pathogens through ancient horizontal gene transfer (HGT). These pathogens make use of the plant peptide hormones to interfere with host defences to their advantage and the detriment of the host.
  • The use of horizontally acquired PNPs in plant pathogens can afford new insights into host‐pathogen biology and may inform novel approaches to pest control.

Keywords: plant peptide hormones; plant natriuretic peptides (PNPs); plant peptide hormone receptors; leucine‐rich repeat (LRR) receptor kinases; guanylyl cyclase; second messengers; 3′,5′‐cyclic guanosine monophosphate (cGMP); 3′,5′‐cyclic adenosine monophosphate (cAMP); horizontal gene transfer (HGT); plant stress responses

Figure 1. Overview of the cellular processes modulated by PNP. PNP (At2g18660) is perceived by a leucine‐rich receptor kinase that contains a cytosolic guanylyl cyclase domain (pGC) (At1g33612) capable of generating cGMP from GTP. PNP‐induced cGMP transients affect many processes, notably cyclic nucleotide‐gated channels (CNGCs), directly or indirectly cGMP‐dependent kinases, the phosphorylation of aquaporins (AQPs) and the transcription of genes. There is increasing evidence that cGMP also affects both chloroplast and mitochondrial functions. PNP in its unprocessed cytosolic configuration may also specifically and directly modulate the activity of enzymes.
Figure 2. Domain organisation of the PNPs (a) and alignment of PNPs from different species (b). (a) PNPs contain a signal peptide (SP) that directs the molecule into the apoplastic (extracellular) space, and an active domain (red) that is necessary and sufficient for the currently known physiological responses. The C‐terminus contains a lytic transglycosylase domain (Pfam 03330) that remains biologically uncharacterised. (b) Sequence alignment of the Arabidopsis thaliana PNP AtPNP‐A(AY142603, At2g18660): the Citrus clementina PNP CcPNP (XP_006453480): the PNP of the bacterial plant pathogen Xanthomonas axonopodis PNP XacPNP (WP_078560788): the PNP of the fungal plant pathogen Verticillium dahlia avirulence protein (AEZ51498.1): and the PNP of the silver whitefly Bemisia tabaci (XP_018915441.1). The active region in AtPNP‐A is marked in red.
Figure 3. Schematic representation of the domain organisation of AtPNP‐R1 (a) and models of the receptor (b). (a) The extracellular portion of the AtPNP‐R1 protein contains a signal peptide (SP) and LRR N‐terminal domain (LRRNT 2: in grey harbours the predicted AtPNP‐A binding region), while the intracellular part consists of a predicted protein kinase (PK) domain and a guanylyl cyclase (GC) catalytic centre (blue). TM indicates the predicted transmembrane domain. The functionally assigned residues of the GC catalytic centre are in red, the aa substitutions are in square brackets ([]), ‘X’ stands for any amino acid, and the gap size is marked in curly brackets ({}). (b) The AtPNP‐R1 models. Ribbon (left) and surface (middle) model of AtPNP‐R1(26‐455) with the AtPNP‐A(33‐66) docked (right). AtPNP‐A(33‐66) is indicated with pink, the LRRNT 2 domain is marked grey, and blue marks the designated GC catalytic centre. Turek and Gehring . Reproduced with permission of Springer Nature.


de Bold AJ, Borenstein HB, Veress AT and Sonnenberg H (1981) A rapid and potent natriuretic response to intravenous injection of atrial myocardial extract in rats. Life Sciences 28: 89–94.

Boudart G, Jamet E, Rossignol M, et al. (2004) Cell wall proteins in apoplastic fluids of Arabidopsis thaliana rosettes: identification by mass spectrometry and bioinformatics. Proteomics 5: 212–221.

Chinkers M, Garbers DL, Chang M‐S, et al. (1989) A membrane form of guanylate cyclase is an atrial natriuretic peptide receptor. Nature 338: 78–83.

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

Donaldson L, Meier S and Gehring C (2016) The arabidopsis cyclic nucleotide interactome. Cell Communication and Signaling 14: 10.

Ficarra FA, Grandellis C, Garavaglia BS, Gottig N and Ottado J (2018) Bacterial and plant natriuretic peptides improve plant defence responses against pathogens. Molecular Plant Pathology 19: 801–811.

Garavaglia BS, Thomas L, Zimaro T, et al. (2010) 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 Biology 10: 51.

Gehring CA (1999) Natriuretic Peptides—A new class of plant hormone? Annals of Botany 83: 329–334.

Gehring C and Irving H (2003) Natriuretic peptides—a class of heterologous molecules in plants. International Journal of Biochemistry and Cell Biology 35: 1318–1322.

Gehring C and Turek IS (2017) Cyclic nucleotide monophosphates and their cyclases in plant signaling. Frontiers in Plant Science 8: 1704.

Gottig N, Garavaglia BS, Daurelio LD, et al. (2008) Xanthomonas axonopodis pv. citri uses a plant natriuretic peptide‐like protein to modify host homeostasis. Proceedings of the National Academy of Sciences USA 105: 18631–18636.

Hirakawa Y, Torii KU and Uchida N (2017) Mechanisms and strategies shaping plant peptide hormones. Plant Cell Physiology 58: 1313–1318.

Irving HR, Kwezi L, Wheeler JI and Gehring C (2012) Moonlighting kinases with guanylate cyclase activity can tune regulatory signal networks. Plant Signaling and Behaviour 2: 201–204.

de Jonge R, Peter van Esse H, Maruthachalam K, et al. (2012) Tomato immune receptor Ve1 recognizes effector of multiple fungal pathogens uncovered by genome and RNA sequencing. Proceedings of the National Academy of Sciences USA 109: 5110–5115.

Kende H and Zeevaart JAD (1997) The five classical plant hormones. Plant Cell 9: 1197–1210.

Kende H, Bradford K, Brummell D, et al. (2004) Nomenclature for members of the expansin superfamily of genes and proteins. Plant Molecular Biology 55: 311–314.

Kwezi L, Ruzvidzo O, Wheeler JI, et al. (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.

Kwezi L, Wheeler JI, Marondedze C, Gehring C and Irving HR (2018) Intramolecular crosstalk between catalytic activities of receptor kinases. Plant Signaling and Behaviour 13: e1430544.

Lee KP, Liu K, Kim EY, et al. (2019) PLANT NATRIURETIC PEPTIDE A antagonizes salicylic acid‐primed cell death. BioRxiv 2019: 592881.

Lindsey K (2001) Plant peptide hormones: the long and the short of it. Current Biology 11: 741–743.

Lori M, Van Verk MC, Hander T, et al. (2015) Evolutionary divergence of the plant elicitor peptides (Peps) and their receptors: Interfamily incompatibility of perception but compatibility of downstream signalling. Journal of Experimental Botany 66: 5315–5325.

Ludidi NN, Heazlewood JL, Seoighe C, Irving HR and Gehring C (2002) Expansin‐like molecules: novel functions derived from common domains. Journal of Molecular Evolution 54: 587–594.

Ludidi N, Morse M, Sayed M, et al. (2004) A recombinant plant natriuretic peptide causes rapid and spatially differentiated K+, Na+ and H+ flux changes in Arabidopsis thaliana roots. Plant Cell Physiology 45: 1093–1098.

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

Meier S, Bastian R, Donaldson L, et al. (2008) Co‐expression and promoter content analyses assign a role in biotic and abiotic stress responses to plant natriuretic peptides. BMC Plant Biology 8: 24.

Muleya V, Marondedze C, Wheeler JI, et al. (2016) Phosphorylation of the dimeric cytoplasmic domain of the phytosulfokine receptor, PSKR1. Biochemical Journal 473: 3081–3098.

Nembaware V, Seoighe C, Sayed M and 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 Evolutionary Biology 4: 10.

Pearce G, Strydom D, Johnson S and Ryan CA (1991) A polypeptide from tomato leaves induces wound‐inducible proteinase inhibitor proteins. Science 253: 895–897.

Pearce G, Moura DS, Stratmann J and Ryan CA (2001) Production of multiple plant hormones from a single polyprotein precursor. Nature 411: 817–820.

Qi Z, Verma R, Gehring C, et al. (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 USA 107: 21193–21198.

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

Simon R and Dresselhaus T (2015) Peptides take centre stage in plant signalling. Journal of Experimental Botany 66: 5135–5138.

Song Y, Liu L, Wang Y, et al. (2018) Transfer of tomato immune receptor Ve1 confers Ave 1‐dependent Verticillium resistance in tobacco and cotton. Plant Biotechnology Journal 16: 638–648.

Stührwohldt N and Schaller A (2019) Regulation of plant peptide hormones and growth factors by post‐translational modification. Plant Biology 21: 49–63.

Subramanian H, Froese A, Jönsson P, et al. (2018) Distinct submembrane localisation compartmentalises cardiac NPR1 and NPR2 signalling to cGMP. Nature Communications 9: 2446.

Turek I and Gehring C (2016) The plant natriuretic peptide receptor is a guanylyl cyclase and enables cGMP‐dependent signaling. Plant Molecular Biology 91: 275–286.

Vesely DL and Giordano AT (1991) Atrial natriuretic peptide hormonal system in plants. Biochemical and Biophysical Research Communications 179: 695–700.

De Vito P (2014) Atrial natriuretic peptide: an old hormone or a new cytokine? Peptides 58: 108–116.

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

Zhang H, Han Z, Song W and Chai J (2016) Structural insight into recognition of plant peptide hormones by receptors. Molecular Plant 9: 1454–1463.

Further Reading

Cook DE, Mesarich CH and Thomma BPHJ (2015) Understanding plant immunity as a surveillance system to detect invasion. Annual Review of Phytopathology 53: 541–563.

Depuydt S and Hardtke CS (2011) Hormone signalling crosstalk in plant growth regulation. Current Biology 21: 365–373.

Ghorbani S, Fernandez A, Hilson P and Beekman T (2014) Signaling peptides in plants. Cell and Developmental Biology 3: 98–101.

Potter LR (2011) Natriuretic peptide metabolism, clearance and degradation. FEBS Journal 278: 1808–1817.

Soucy SM, Huang J and Gogarten JP (2015) Horizontal gene transfer: building the web of life. Nature Reviews Genetics 16: 472.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Gehring, Chris(Nov 2019) Plant Natriuretic Peptides. In: eLS. John Wiley & Sons Ltd, Chichester. [doi: 10.1002/9780470015902.a0028907]