Dual roles for the variable domain in protein trafficking and host‐specific recognition of Heterodera glycines CLE effector proteins

Abstract

Summary• Soybean cyst nematodes (Heterodera glycines) produce secreted effector proteins that function as peptide mimics of plant CLAVATA3 ⁄ ESR (CLE)-like peptides probably involved in the developmental reprogramming of root cells to form specialized feeding cells called syncytia.• The site of action and mechanism of delivery of CLE effectors to host plant cells by the nematode, however, have not been established. In this study, immunologic, genetic and biochemical approaches were used to reveal the localization and site of action of H. glycines-secreted CLE proteins in planta.• We present evidence indicating that the nematode CLE propeptides are delivered to the cytoplasm of syncytial cells, but ultimately function in the apoplast, consistent with their proposed role as ligand mimics of plant CLE peptides. We determined that the nematode 12-amino-acid CLE motif peptide is not sufficient for biological activity in vivo, pointing to an important role for sequences upstream of the CLE motif in function.• Genetic and biochemical analysis confirmed the requirement of the variable domain in planta for host-specific recognition and revealed a novel role in trafficking cytoplasmically delivered CLEs to the apoplast in order to function as ligand mimics.

SNPs of CLAVATA receptors in tomato, in the context of root-knot nematode infection

“…Another CLE-like nematode gene, 16D10, was isolated from a cDNA library derived from the esophageal gland cells of the root-knot nematode Meloidogyne incognita at the parasitic stage (Huang et al, 2006a, b). Furthermore, Arabidopsis mutants of CLV3 receptors, clv2 and crn/sol2, showed obvious resistance to nematode infection (Replogle et al, 2010). These results indicate that the CLV3 signaling molecules are responsible for successful nematode infection in plants.…”

“…Mutations of CLV2 and CRN/SOL2 in Arabidopsis conferred resistance against plant parasitic nematode infection; their products CLV2 and CRN/SOL2 are known as CLV3 peptide hormone receptors (Replogle et al, 2010). CLV1 and RPK2 are also known as CLV3 receptors (Miwa et al, 2008;Kinoshita et al, 2010;Betsuyaku et al, 2011).…”

“…In general, parasitic effector proteins produced in the esophageal gland cells of nematodes are secreted from the nematode through its stylet into the plant tissue (Davis et al, 2000;Davis et al, 2008). Attempts to target secretory proteins from the esophageal gland cells of the soybean cyst nematode Heterodera glycines at the parasitic stage identified HgCLE1 (formerly known as 2B10 and identical to Hg-SYV46) and HgCLE2 (known as 4G12), which encode a protein that harbors the C-terminal CLE domain (Wang et al, 2001;Gao et al, 2003;Wang et al, 2010). Members of the CLE gene family encode small (about 100 amino-acid) proteins that share a conserved structure of a putative N-terminus secretory signal peptide and a conserved 14-amino-acid CLE domain at the C-terminus (Cock and McCormick, 2001;Sharma et al, 2003;Sharma et al, 2005;Strabala et al, 2006;Sawa et al, 2006;Kinoshita et al, 2007;Sawa et al, 2008;Miwa et al, 2009a, b;Sawa and Tabata, 2011;Tabata and Sawa, 2011).…”

“…CLE genes have been found in many plants; however, so far in the animal kingdom, the CLD genes have been found only the plant-parasitic nematode. HgCLE genes in the nematode encode proteins of about 140 aminoacids with N-terminal signal peptides and their 12-aminoacid CLE domains (Wang et al, 2001;Gao et al, 2003;Wang et al, 2010). Another CLE-like nematode gene, 16D10, was isolated from a cDNA library derived from the esophageal gland cells of the root-knot nematode Meloidogyne incognita at the parasitic stage (Huang et al, 2006a, b).…”

Impact des changements climatiques sur les interactions moléculaires entre le nématode à kyste du soya (Heterodera glycines) et son hôte principal, le soya (Glycine max)

“…À la suite de la sélection par le stade J2 d'une cellule initiale servant au développe-ment du syncytium, le NKS produit et injecte d'autres effecteurs qui lui permettent de compléter son cycle de vie. Ces effecteurs servent à (i) dissoudre les parois des cellules adjacentes afin d'optimiser le détour-nement des ressources nutritives de la plante et (ii) favoriser l'ubiquitination (dégradation) de certaines protéines produites par la plante afin d'interférer avec les diverses voies métaboliques et d'ainsi affaiblir le système de défense de l'hôte (Gao et al 2003(Gao et al , 2004Haegeman et al 2010Haegeman et al , 2012Ithal et al 2007;Wang et al 2010).…”