Role of Hormonal and Developmental Signaling in Plant-Cyst Nematode Interaction

Plant-parasitic cyst nematodes are one of the most destructive root parasites that cause severe yield losses in many crop plants. These obligate parasites induce a specialized multi-nucleate feeding site called syncytium. This study was conducted to explore the roles of phytohormones particularly auxin and ethylene, and miRNA-mediated crosstalk between development and defense responses in establishing the compatible interaction between Arabidopsis and Heterodera schachtii. Using yeast two-hybrid assay, a complete protein-protein interaction map between Auxin/indole-3-acetic acid (Aux/IAA) proteins and auxin response factors (ARFs) was generated. In addition, gene co-expression profiles of ARFs and Aux/IAAs were incorporated with protein-protein interaction data. Together, these analyses revealed the biological significance of the ARFs and Aux/IAA interactions in the differentiation and development of various plant tissues and organs, including H. schachtii–induced syncytium. Our analyses also provided evidence for the roles of ETHYLENE RESPONSE 1 and ETHYLENE INSENSITIVE 3/ETHYLENE INSENSITIVE LIKE 1 in regulating Arabidopsis responses to H. schachtii infection. The role of miRNAs in mediating the coordination between developmental signaling and defense response is emerging. Functional characterization of miR858 and its MYB83 target gene pointed into novel cooperative regulatory functions of this regulatory module in syncytium transcriptome reprogramming during cyst nematode parasitism of Arabidopsis. We discovered that miR858-mediated silencing of MYB83 is tightly regulated through a feedback loop that may ensure proper expression levels of more than a thousand of MYB83-regulated genes in the syncytium. Finally, the direct targets of Growth Regulating Factor 1 (GRF1) and 3, master regulators of syncytium differentiation, were identified. Specific and the shared cis-binding elements of GRF1 and GRF3 were identified, providing unprecedented understanding of the mechanism of their functional redundancy. GRF1 and GRF3 directly target genes associated with cell cycle regulation, cytoskeleton organization, phytohormone biosynthesis and signaling, and defense responses, key cellular processes that determine the outcomes of plant-cyst nematode interactions. The analysis also provided intriguing evidence for the involvement of GRF1/3 in mediating the trade-off between plant growth and stress signaling. Understanding the molecular mechanisms underlying the coordinated interactions between plant growth and defense signaling will open new avenues for enhancing plant growth and stress response simultaneously.