Extensive reprogramming of primary and secondary metabolism by fungal elicitor or infection in parsley cells

Abstract

The transcription rates of numerous plant genes have previously been shown to be strongly affected by pathogen infection or elicitor treatment. Here we estimate the extent and complexity of this response by analyzing the patterns of mRNA induction in fungal elicitor-treated parsley cells (Petroselinum crispum) for several representatives from various primary and secondary metabolic pathways, cytosolic as well as plastidic. As a reference, we use the biphasic accumulation curve for the coordinately induced mRNAs encoding the three core enzymes of general phenylpropanoid metabolism, phenylalanine ammonia-lyase, cinnamate 4-hydroxylase and 4-coumarate:CoA ligase. Coincidence with this curve was observed for the mRNA induction kinetics of several, but not all, phenylpropanoid branch pathway-related reactions, whereas seven selected mRNAs from the pentose phosphate, glycolytic and shikimate pathways, including various cytosolic and plastidic isoforms, were induced with great differences in timing. Likewise unique and dissimilar from the reference curve were the induction patterns for various mRNAs encoding enzymes or proteins that are either more distantly or not at all related to phenylpropanoid metabolism. None of over 40 mRNAs tested so far remained unaffected. Using one strongly elicitor-responsive mRNA from carbohydrate metabolism, encoding a cytosolic glucose 6-phosphate dehydrogenase, for in situ RNA/RNA hybridization in fungus-infected parsley leaf tissue, we observed again the previously reported, close simulation of metabolic changes in true plant/fungus interactions by elicitor treatment of cultured cells. In addition to demonstrating extensive, highly complex functional, temporal and spatial patterns of changes in gene expression in infected plant cells, these results provide valuable information for the identification of pathogen-responsive promoters suitable for gene technology-assisted resistance breeding.