Table 2.
RCP (aaa) | Plant-associated organism | Host plant (relationship with host) | Repeat featuresb | Localization in planta | Part of an RCP effector family? | References |
---|---|---|---|---|---|---|
ATR1Emoy2 (311) | Hyaloperonospora arabidopsidis (plant-pathogenic oomycete) | Arabidopsis thaliana (causes downy mildew disease) | Two amphipathic degenerate tandem WY domain repeats of 83 and 100 aa identified by structural analysis that adopt a five-helix bundle fold | Host cell cytoplasm | Yes | Rehmany et al., 2005; Sohn et al., 2007; Krasileva et al., 2010; Chou et al., 2011; Steinbrenner et al., 2015 |
Biological function: ATR1 from isolate Emoy2 (ATR1Emoy2) contributes to pathogen virulence, although its specific function is unknown. ATR1Emoy2 is directly recognized by the RPP1NdA and RPP1WsB immune receptors of A. thaliana. One and two aa residues in ATR1Emoy2 associated with the recognition of this effector by RPP1NdA and RPP1WsB, respectively, are located on the surface of repeat unit one. Other aa residues, as identified by gain-of-(RPP1NdA)-recognition mutagenesis screens using traditionally non-recognized ATR1 alleles are also located on the surface of repeat unit one | ||||||
ATR13 (187) | H. arabidopsidis | Six hydrophilic degenerate tandem leucine/isoleucine repeats of 7 aa, followed by 4 hydrophilic imperfect tandem repeats of 11 aa. Repeats are located in a disordered region of the protein | Host cell nucleolus | No | Allen et al., 2004, 2008; Sohn et al., 2007; Leonelli et al., 2011 | |
Biological function: ATR13 contributes to pathogen virulence, possibly by suppressing host immune responses, although its specific function is unknown. ATR13 is recognized by the RPP13Nd immune receptor of A. thaliana. Mutations cannot be made to particular leucine or isoleucine residues within the 7-aa repeats of ATR13 without altering recognition by RPP13Nd. The 11-aa repeats of ATR13 are required for nucleolar localization. Alleles of ATR13 carrying only one of the four 11-aa repeats do not localize to the nucleolus. However, when the three missing repeats are added to these alleles, nucleolar localization is observed | ||||||
AvrM-A (343) | Melampsora lini (plant-pathogenic fungus) | Flax (causes leaf rust disease) | Two hydrophilic degenerate tandem repeats of 68 aa identified by structural analysis that adopt a four-helix bundle fold. Repeats share some similarity in the overall architecture to the WY domain of several oomycete effectors | Host cell cytoplasm | Yes | Catanzariti et al., 2006, 2010; Rafiqi et al., 2010; Ve et al., 2013 |
Biological function: AvrM-A function unknown. AvrM is directly recognized by the M immune receptor of flax. Several residues of AvrM required for recognition by M are located on the surface of repeat unit two | ||||||
CBEL (268) | Phytophthora parasitica var. nicotianae (plant-pathogenic oomycete) | Tobacco (causes black shank root and crown rot disease) | Two amphipathic imperfect near-tandem repeats of 113 and 114 aa comprising a carbohydrate-binding module family 1 (CBM1)/fungal-type cellulose-binding domain (CBD) linked to a PAN/APPLE domain | Cyst surface and hyphal cell wall | No | Séjalon-Delmas et al., 1997; Villalba Mateos et al., 1997; Gaulin et al., 2002, 2006; Khatib et al., 2004 |
Biological function: the CBDs of CBEL play a role in the adhesion of mycelia to cellulosic substrates, including plant cell walls, and in the organized deposition of the P. parasitica var. nicotianae cell wall polysaccharide, β-glucan. However, knockdown transformants do not display significantly reduced virulence. CBEL also elicits strong host immune responses when infiltrated into tobacco, as well as various non-host plants, including A. thaliana. These immune responses require the binding of CBEL to the plant cell wall, as mediated through the CBDs | ||||||
Cin1c (523) | Venturia inaequalis (plant-pathogenic fungus) | Apple (causes scab disease) | Eight hydrophilic imperfect tandem repeats of 52–64 aa that adopt a core helix-loop-helix motif as part of a three-helix bundle fold | Unknown | Yes | Kucheryava et al., 2008; Mesarich et al., 2012 |
Biological function: Cin1 function unknown. Cin1 gene expression is induced in planta | ||||||
CTP1 (171) | Melampsora larici-populina (plant-pathogenic fungus) | Poplar (causes leaf rust disease) | Two amphipathic imperfect near-tandem repeats of 64 aa | Host cell chloroplast (stroma) and mitochondria | Yes | Petre et al., 2015a,b |
Biological function: CTP1 function unknown. Repeat unit one overlaps with a predicted chloroplast transit peptide | ||||||
Ecp6 (222) | Cladosporium fulvum (plant-pathogenic fungus) | Tomato (causes leaf mold disease) | Three amphipathic degenerate near-tandem lysin motif (LysM) domain repeats of 44 or 45 aa that adopt a βααβ-fold | Host apoplast | No | Bolton et al., 2008; de Jonge et al., 2010; Thomma et al., 2011; Sánchez-Vallet et al., 2013 |
Biological function: Ecp6 perturbs chitin-triggered immunity in tomato by sequestering chitin oligosaccharides released from the fungal cell wall. More specifically, LysM1 and LysM3 domain repeats out-compete host chitin receptors for the binding of chitin oligosaccharides. The LysM2 domain repeat may perturb chitin-triggered immunity through a yet unknown mechanism. Ecp6 is recognized by the Cf-Ecp6 immune receptor of tomato | ||||||
Hum3 (828) | Ustilago maydis (plant-pathogenic fungus) | Maize (causes smut disease) | Seventeen amphipathic imperfect tandem repeats of 31–36 aa. Fourteen repeats are separated by putative Kex2 processing motifs | Unknown | No | (Teertstra et al., 2006; Müller et al., 2008) |
Biological function: Hum3 function unknown. Deletion of Hum3 alone does not affect virulence of U. maydis on maize. However, the pathogenic development of a Hum3/Rsp1 double knock-out mutant is halted in planta shortly after penetration. The Hum3 repeat domain is followed by a hydrophobin domain | ||||||
Rep1 (652) | U. maydis | Twelve amphipathic imperfect mostly tandem repeats of 34–55 aa. Repeats are separated by Kex2 sites, and are proteolytically processed into 10 small amphipathic peptides (Rep1-1–Rep1-10) of 35–53 aa, and one of 228 aa (Rep1-11) | Hyphal cell wall | No | Wösten et al., 1996; Teertstra et al., 2006, 2009; Müller et al., 2008 | |
Biological function: Rep1 is a repellent protein. Following the proteolytic processing of Rep1 by Kex2, processed repellent peptides form surface-active amyloid-like fibrils at the hyphal surface that play a role in cellular attachment to hydrophobic surfaces (e.g., the host surface) and in the formation of aerial hyphae. Rep1 does not appear to be required for the virulence of U. maydis on maize | ||||||
Rsp1 (260) | U. maydis | Eleven hydrophilic imperfect tandem repeats of 18 or 21 aa. Repeats are separated by putative Kex2 processing motifs | Unknown | No | Müller et al., 2008 | |
Biological function: Rsp1 function unknown. Deletion of Rsp1 alone does not affect virulence of U. maydis on maize. However, the pathogenic development of a Hum3/Rsp1 double knock-out mutant is halted in planta shortly after penetration | ||||||
SP7 (499)d | Rhizophagus irregularis (arbuscular mycorrhizal fungus) | Broad host range (mutualistic symbiont of plant roots) | Up to 10 hydrophilic imperfect repeats of 6–16 aa, separated by four hydrophilic imperfect repeats of 7 or 8 aa | Host cell nucleus | Yes | Kloppholz et al., 2011 |
Biological function: SP7 interacts with the pathogenesis-related ethylene-responsive host transcription factor ERF19 to promote symbiotic biotrophy. Possibly counteracts ERF19-regulated host defense responses |
Protein length in amino acids (aa).
Repeat hydropathy profiles were determined using the Expasy ProtScale server (http://web.expasy.org/protscale/), with default server settings.
Cin1 is a candidate effector of V. inaequalis (Kucheryava et al., 2008).
The length of SP7 remains unclear due to differential transcript splicing, with five versions of the mRNA transcript found at different developmental stages (Kloppholz et al., 2011).