Crip21: Alert from Dodder to Crops

Abstract

Together with pathogenic microbes and herbivorous insects, parasitic plants are emerging as aggressive threats on agriculture worldwide. Among them, Cuscuta (dodder), a stem holoparasite, extracts nutrients and water from host plants through phloem feeding. Dodder is parasitic on a very wide variety of plants, including a number of important agricultural and horticultural crops such as alfalfa, clover, tomatoes, and potatoes. Dodder infestations cause major economic concerns, including crop yield reduction and cost increase of crop harvesting. Understanding resistance mechanisms against dodder can provide potential solutions to effectively control dodder infestations. A recent study from the Markus Albert laboratory and their collaborators demonstrated that a cell wall protein from dodder can be specifically recognized by a tomato receptor Cuscuta receptor 1 (CuRe1) (Hegenauer et al., 2020Hegenauer V. Slaby P. Körner M. Bruckmüller J.-A. Burggraf R. Albert I. Kaiser B. Löffelhardt B. Droste-Borel I. Sklenar J. et al.The tomato receptor CuRe1 senses a cell wall protein to identify Cuscuta as a pathogen.Nat. Commun. 2020; 11: 5299Crossref PubMed Scopus (7) Google Scholar). Previous work from the same laboratory revealed that plasma-membrane-localized CuRe1 is a critical component in detecting Cuscuta reflexa (C. reflexa) (Hegenauer et al., 2016Hegenauer V. Fürst U. Kaiser B. Smoker M. Zipfel C. Felix G. Stahl M. Albert M. Detection of the plant parasite Cuscuta reflexa by a tomato cell surface receptor.Science. 2016; 353: 478-481Crossref PubMed Scopus (63) Google Scholar). To further illuminate how host plant recognizes C. reflexa, researchers purified and identified the Cuscuta factor from the cell wall extract of C. reflexa, which triggers defense responses in cultivated tomato (Solanum lycopersicum) (Hegenauer et al., 2020Hegenauer V. Slaby P. Körner M. Bruckmüller J.-A. Burggraf R. Albert I. Kaiser B. Löffelhardt B. Droste-Borel I. Sklenar J. et al.The tomato receptor CuRe1 senses a cell wall protein to identify Cuscuta as a pathogen.Nat. Commun. 2020; 11: 5299Crossref PubMed Scopus (7) Google Scholar). Using LC-MS/MS, Cuscuta factor is identified as a glycine-rich protein (GRP) of C. reflexa (CrGRP) consisting of 116 amino acids. Expressing CrGRP in Nicotiana benthamiana leaves results in hypersensitive cell death when CuRe1 is present, indicating CrGRP is recognized by CuRe1 to trigger defense responses (Figure 1). Direct interaction between a 29-amino-acid (aa)-long peptide (crip29) of CrGRP and CuRe1 receptor was confirmed by affinity-crosslinking experiments in N. benthamiana leaves. Further analyses identified a 21-aa-peptide (crip21) as the minimal epitope of CrGRP to trigger defense responses. Individual site-mutagenesis analysis showed that four cysteine residues at positions 7, 17, 20, and 21 contribute to CuRe1 activation. Interestingly, based on the comparison of crip21 and its homologous sequences in other plants, researchers further showed that a single amino acid change from alanine 11 to tyrosine in crip21 completely abolishes CuRe1-dependent crip21 activity. Plant GRPs have been shown to possess diverse functions including in cell wall stabilization (Mangeon et al., 2010Mangeon A. Junqueira R.M. Sachetto-Martins G. Functional diversity of the plant glycine-rich proteins superfamily.Plant Signal. Behav. 2010; 5: 99-104Crossref PubMed Scopus (168) Google Scholar). The discovery of crip21 as a molecular pattern recognized by plant surface receptor CuRe1 significantly boosts the understanding of interactions between host and parasitic plants. Further studies on the crip21-CuRe1 pathway can potentially guide resistance engineering against parasitic plants. No conflict of interest declared.