CLE effector peptide signaling in plant-nematode interactions

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Plant-parasitic nematodes are a major impediment to meeting the challenge of feeding a population projected to reach 9 billion by 2050. These nematodes cause billions of dollars in yield losses annually worldwide. The unavailability or limited genetic base of commercially acceptable resistant cultivars, genotypic variability in nematode field populations, as well as the emergence of new species, pose a continued threat to crop production by this group of agriculturally important pests. The most economically important plant-parasitic nematodes include the cyst forming nematodes. Cyst nematodes form parasitic relationships with their plant hosts by establishing a permanent feeding site within the root, which serves as a nutrient sink to support growth and development of the nematode. This project will provide new insights into how plants recognize and respond to nematode-secreted molecules to form unique and essential feeding cells within host roots, which may, in turn, translate into novel strategies to bioengineer crops with robust resistance to pathogenic cyst nematodes. The investigators seek to understand the detailed molecular mechanisms and pathways by which plant-parasitic cyst nematodes co-opt host developmental programs for feeding cell formation. Feeding cell development and maintenance is dependent on stylet-secreted effector proteins produced in the esophageal gland cells of cyst nematodes. However, our understanding of signaling processes directing the process of host cell transformation by nematode-secreted effectors is largely lacking. Among the stylet-secreted effectors are small signaling peptides sharing similarity with plant CLAVATA3/ENDOSPERM SURROUNDING REGION-related (CLE) peptides. The investigators have demonstrated that these nematode-secreted peptide signals are required for successful infection, but their exact role in developmental reprogramming of root cells for feeding cell formation remains unclear. The project focuses on elucidating the function of nematode-secreted CLE peptides in modulating the plant cellular program for feeding cell formation. Molecular, genetic, genomic, and biochemical analyses will be used to characterize the role of nematode CLE peptides in feeding cell formation. Once delivered into host cells, CLE proteins are retargeted to the apoplast via a novel post-translational trafficking mechanism. The trafficking pathway will be investigated through subcellular localization and analyses of host-interacting proteins. In the apoplast, CLE peptides are perceived by plant receptors. Receptor localization will be characterized and deletion and mutagenesis studies will be used to evaluate receptor binding specificity to nematode CLE peptides. The hypothesis that CLE peptides act to modulate phytohormone and defense signaling pathways will be tested through cell-specific studies of mutants, reporter lines, and other related assays including nematode infection assays and in vitro peptide application assays. The data generated will provide information about a class of pathogen effectors unique to plant-parasitic cyst nematodes and the first example of a pathogen secreting a protein mimic of a plant peptide hormone. Beyond the cyst nematode-plant interaction, the data generated will contribute to an understanding of CLE signaling and potentially novel protein trafficking pathways in plants. The project will integrate research activities with education and training of female and underrepresented minority undergraduate students in plant molecular genetics and cell biology through outreach programs targeting K-5 focused on applications of plant science and technology for society.