PECTIN ACETYLESTERASE9 Affects the Transcriptome and Metabolome and Delays Aphid Feeding

Abstract

The plant cell wall plays an important role in damage-associated molecular pattern-induced resistance to pathogens and herbivorous insects. Our current understanding of cell wall-mediated resistance is largely based on the degree of pectin methylesterification. However, little is known about the role of pectin acetylesterification in plant immunity. This study describes how one pectin-modifying enzyme, <i>PECTIN ACETYLESTERASE 9</i> (<i>PAE9</i>), affects the Arabidopsis (<i>Arabidopsis thaliana</i>) transcriptome, secondary metabolome, and aphid performance. Electro-penetration graphs showed that <i>Myzus persicae</i> aphids established phloem feeding earlier on <i>pae9</i> mutants. Whole-genome transcriptome analysis revealed a set of 56 differentially expressed genes (DEGs) between uninfested <i>pae9-2</i> mutants and wild-type plants. The majority of the DEGs were enriched for biotic stress responses and down-regulated in the <i>pae9-2</i> mutant, including <i>PAD3</i> and <i>IGMT2</i>, involved in camalexin and indole glucosinolate biosynthesis, respectively. Relative quantification of more than 100 secondary metabolites revealed decreased levels of several compounds, including camalexin and oxylipins, in two independent <i>pae9</i> mutants. In addition, absolute quantification of phytohormones showed that jasmonic acid (JA), jasmonoyl-Ile, salicylic acid, abscisic acid, and indole-3-acetic acid were compromised due to PAE9 loss of function. After aphid infestation, however, <i>pae9</i> mutants increased their levels of camalexin, glucosinolates, and JA, and no long-term effects were observed on aphid fitness. Overall, these data show that PAE9 is required for constitutive up-regulation of defense-related compounds, but that it is not required for aphid-induced defenses. The signatures of phenolic antioxidants, phytoprostanes, and oxidative stress-related transcripts indicate that the processes underlying PAE9 activity involve oxidation-reduction reactions.