Structural and Functional Diversity of CLAVATA3/ESR (CLE)-Like Genes from the Potato Cyst Nematode Globodera rostochiensis

Abstract

Plant CLAVATA3/ESR-related (CLE) peptides have diverse roles in plant growth and development. Here, we report the isolation and functional characterization of five new CLE genes from the potato cyst nematode Globodera rostochiensis. Unlike typical plant CLE peptides that contain a single CLE motif, four of the five Gr-CLE genes encode CLE proteins with multiple CLE motifs. These Gr-CLE genes were found to be specifically expressed within the dorsal esophageal gland cell of nematode parasitic stages, suggesting a role for their encoded proteins in plant parasitism. Overexpression phenotypes of Gr-CLE genes in Arabidopsis mimicked those of plant CLE genes, and Gr-CLE proteins could rescue the Arabidopsis clv3-2 mutant phenotype when expressed within meristems. A short root phenotype was observed when synthetic GrCLE peptides were exogenously applied to roots of Arabidopsis or potato similar to the overexpression of Gr-CLE genes in Arabidopsis and potato hairy roots. These results reveal that G. rostochiensis CLE proteins with either single or multiple CLE motifs function similarly to plant CLE proteins and that CLE signaling components are conserved in both Arabidopsis and potato roots. Furthermore, our results provide evidence to suggest that the evolution of multiple CLE motifs may be an important mechanism for generating functional diversity in nematode CLE proteins to facilitate parasitism.

Receptor Kinases in Plant-Pathogen Interactions: More Than Pattern Recognition

“…It has long been known that cyst nematodes secrete peptides that are structural and functional mimics of plant CLAVATA3/ENDOSPERM SURROUNDING REGION-related (CLE) peptides (Wang et al, 2001(Wang et al, , 2005Gao et al, 2003;Lu et al, 2009), with the latter being peptide hormones required for meristem maintenance and vascular differentiation (Fiers et al, 2007). The nematode CLE effectors are required for virulence (Patel et al, 2008), apparently by stimulating both the CLV2 and the CLV1 pathways (Replogle et al, 2011(Replogle et al, , 2013.…”

Cellular Signaling Pathways and Posttranslational Modifications Mediated by Nematode Effector Proteins

“…The CLE-like effectors seem to be unique to cyst nematodes, as no other CLElike effectors have been identified outside cyst nematodes so far. The function of cyst nematode CLE-like effectors in mimicking endogenous plant peptides is supported by experimental data showing that overexpression of nematode CLE-like effectors in Arabidopsis produced a WUSCHEL phenotype (premature termination of shoot and floral meristems) similar to that of plant CLE overexpression (Wang et al, 2005Lu et al, 2009). Nematode CLE-like effectors were also able to complement the Arabidopsis clavata3-2 (clv3-2) null mutant (Lu et al, 2009;Wang et al, 2010).…”

“…The function of cyst nematode CLE-like effectors in mimicking endogenous plant peptides is supported by experimental data showing that overexpression of nematode CLE-like effectors in Arabidopsis produced a WUSCHEL phenotype (premature termination of shoot and floral meristems) similar to that of plant CLE overexpression (Wang et al, 2005Lu et al, 2009). Nematode CLE-like effectors were also able to complement the Arabidopsis clavata3-2 (clv3-2) null mutant (Lu et al, 2009;Wang et al, 2010). Genetic and molecular analyses indicated that plant CLE peptides are perceived by various receptor-like kinases (RLKs) to mediate the downstream signaling essential for correct stem cell fate (Guo et al, 2010(Guo et al, , 2011Kinoshita et al, 2010).…”

Plant-nematode Interactions: From Genomics to Metabolomics

“…These cell wall degrading enzymes help the infective J2 nematodes to migrate through the plant roots by softening the cell wall. The effector proteins include CLAVATA3 (CLV3) /ESR (CLE) -like (Wang et al, 2005;Patel et al, 2008;Lu et al, 2009;Wang et al, 2010a;Wang et al, 2010b), SPRY domain-containing (SPRYSEC) effector proteins (Huang et al, 2006;Rehman et al, 2009;Sacco et al, 2009;Postma et al, 2012), Mi-EFF1 (Jaouannet et al, 2012), calreticulin Mi-CRT (Jaubert et al, 2002;Jaubert et al, 2005;Jaouannet et al, 2013), and Hs19C07 (Lee et al, 2011). These proteins are involved in plant-nematode compatible interactions by suppressing the defense mechanisms of host plants in some cases.…”