The function of plant PR1 and other members of the CAP protein superfamily in plant-pathogen interactions

Abstract

The pathogenesis-related (PR) proteins of plants have originally been identified as proteins that are strongly induced upon biotic and abiotic stress. These proteins fall into 17 distinct classes (PR1-PR17). The mode of action of most of these PR proteins has been well characterized, except for PR1, which belongs to a widespread superfamily of proteins that share a common CAP domain. Proteins of this family are not only expressed in plants but also in humans and in many different pathogens, including phytopathogenic nematodes and fungi. These proteins are associated with a diverse range of physiological functions. However, their precise mode of action has remained elusive. The importance of these proteins in immune defence is illustrated by the fact that PR1 overexpression in plants results in increased resistance against pathogens. However, PR1-like CAP proteins are also produced by pathogens and deletion of these genes results in reduced virulence, suggesting that CAP proteins can exert both defensive and offensive functions. Recent progress has revealed that plant PR1 is proteolytically cleaved to release a C-terminal CAPE1 peptide, which is sufficient to activate an immune response. The release of this signalling peptide is blocked by pathogenic effectors to evade immune defence. Moreover, plant PR1 forms complexes with other PR family members, including PR5, also known as thaumatin, and PR14, a lipid transfer protein, to enhance the host's immune response. Here, we discuss possible functions of PR1 proteins and their interactors, particularly in light of the fact that these proteins can bind lipids, which have important immune signalling functions.

Keywords: effector proteins; fungal CAPs; nematode VALs/VAPs; pathogen virulence; plant PR1; plant immunity; sperm-coating proteins (SCPs).

FIGURE 1

Structural conservation of the CAP domain. (a) Sequence alignment of CAP family members from Arabidopsis thaliana (AtPR1), from the potato cyst nematode Globodera rostochiensis (GrVAP1), from the phytopathogenic fungus Cytospora chrysosperma (CcCAP1), and from the yeast Saccharomyces cerevisiae (PRY1). The CAP1–4 signature motifs are boxed in blue. The highly conserved histidine and glutamic acid residues that constitute the conserved tetrad residues are indicated in red. The four alpha‐helices (α1–α4) are shown as wavy lines. The conserved aromatic amino acids (ØXØXXXXØ) that define the caveolin‐binding motif (CBM) in the flexible loop that connects helix α3 with α4 is highlighted in a purple box. The three cysteines that are highly conserved in all four proteins are indicated in orange. (b) Tertiary structure of the CAP domain from AtPR1. Conserved elements as determined by ConSurf (Ashkenazy et al., 2016) are indicated in red and the highly conserved histidine and glutamic acid residues are indicated, as is the CBM, the CAPE1 motif, and the fatty acid (FA) binding pocket formed by helices α1, α3, and α4. Key residues Ala40, Val96, and Val123 in the FA binding pocket are indicated. The structure is represented by a ribbon diagram and as a space‐filling model.

FIGURE 2

Docking of the CAP domain of AtPR1 with SsCP1. Protein docking was performed by UCSF Chimera (Pettersen et al., 2004). Conserved elements as determined by ConSurf (Ashkenazy et al., 2016) are indicated in red, and the CBM domain and CAPE1 motif are indicated. The SsCP1 peptide (amino acids 48–71) involved in binding with AtPR1 is shown in yellow. The structure is represented by a ribbon diagram and as a space‐filling model.

FIGURE 3

Comparison of sterol structures between fungi, mammals, and plants. The structural properties of the fungal ergosterol, mammalian cholesterol, the β‐phytosterols stigmasterol, sitosterol, and campesterol, and the plant signalling steroid brassinolide are shown. Note that the three phytosterols share the same tetracyclic ring structure with the mammalian cholesterol but differ in their aliphatic side chains. Also shown is the structure of eugenol, an allylbenzene class of aliphatic compounds that can also be bound by PR1 proteins.

FIGURE 4

Possible model of PR1 function in the apoplastic space. In this schematic model, the PR1 protein, shown as a space‐filling model, perceives the presence of small lipid ligands such as sterols or oxylipids in the apoplastic space to facilitate release of the C‐terminal CAPE1 signalling peptide. Binding of PR1 by various pathogen effectors blocks the release of CAPE1 and hence suppresses the host's immune response. Once released, CAPE1 induces plant immunity and upregulation of PR proteins, particularly PR1, PR5, and PR14. PR1 can then interact with PR5 and/or PR14 in the extracellular space to amplify immunity by increasing the antimicrobial activity of the PR1 protein complex itself and/or through the release of more CAPE1. PR1‐like proteins secreted by various pathogens may either sequester the lipidic ligand to suppress perception of the initial signal or sequester the interactors of PR1 such as PR1 itself, PR5, and/or PR14.