Plant Natriuretic Peptides

Abstract

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.
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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.

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Gehring, Chris(Nov 2019) Plant Natriuretic Peptides. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028907]