Protein networks reveal organ-specific defense strategies in maize in response to an aboveground herbivore

Abstract

Many of the proteins and defense pathways in maize that are activated in an organ-specific manner in leaves and roots during aboveground caterpillar attack have not yet been identified. In this study, we examined systemic and organ-specific defenses in the insect-resistant maize genotype, Mp708, when infested aboveground with fall armyworm (FAW, Spodoptera frugiperda). We used proteomic and network biology analyses and then integrated these data with known FAW resistance QTL to create a protein abundance QTL (pQTL) subnetwork. Using 10-plex tandem mass spectrometry tags (TMT) proteomics technique, we identified a total of 4675 proteins in leaves and roots of control and FAW-infested plants. Among the identified proteins, 794 had significant differences in abundance in response to FAW herbivory. Proteins that were upregulated in leaves during FAW infestation included jasmonic acid biosynthetic enzymes, cysteine proteases, protease inhibitors, REDOX-related proteins, and peroxidases. In roots, highly abundant proteins were involved in ET biosynthesis, DNA expression regulation, and pyruvate biosynthesis. We found many proteins that possibly contribute different defense functions to FAW resistance in Mp708. One potential resistance mechanism identified was that trade-offs between growth and defense responses were reduced in Mp708. Some of the proteins involved in this trade-off that were found within the pQTL subnetwork were the Kinesin-like protein (GRMZM2G046186_P01) and Pi starvation-induced protein (GRMZM2G118037_P01). We proposed other mechanisms contributing to resistance that suggest that jasmonic acid and ethylene control the local accumulation of insecticidal cysteine protease (MIR1-CP) in leaves, while ethylene controlled the systemic accumulation of MIR1-CP in roots. Finally, we hypothesized that receptor kinases such as receptor protein kinase 1 (GRMZM2G055678) could be involved in the activation of root-specific defense responses during aboveground insect infestation.