Involvement of the xyloglucan endotransglycosylase/hydrolases encoded by celery XTH1 and Arabidopsis XTH33 in the phloem response to aphids.

During infestation, phloem-feeding insects induce transcriptional reprogramming in plants that may lead to protection. Transcripts of the celery XTH1 gene, encoding a xyloglucan endotransglycosylase/hydrolase (XTH), were previously found to accumulate systemically in celery (Apium graveolens) phloem, following infestation with the generalist aphid Myzus persicae. XTH1 induction was specific to the phloem but was not correlated with an increase in xyloglucan endotransglycosylase (XET) activity in the phloem. XTH1 is homologous to the Arabidopsis thaliana XTH33 gene. XTH33 expression was investigated following M. persicae infestation. The pattern of XTH33 expression is tightly controlled during development and indicates a possible role in cell expansion. An xth33 mutant was assayed for preference assay with M. persicae. Aphids settled preferentially on the mutant rather than on the wild type. This suggests that XTH33 is involved in protecting plants against aphids; therefore, that cell wall modification can alter the preference of aphids for a particular plant. Nevertheless, the ectopic expression of XTH33 in phloem tissue was not sufficient to confer protection, demonstrating that modifying the expression of this single gene does not readily alter plant-aphid interactions.

Systemic response to aphid infestation by Myzus persicae in the phloem of Apium graveolens.

Little is known about the molecular processes involved in the phloem response to aphid feeding. We investigated molecular responses to aphid feeding on celery (Apium graveolenscv. Dulce) plants infested with the aphid Myzus persicae, as a means of identifying changes in phloem function. We used celery as our model species as it is easy to separate the phloem from the surrounding tissues in the petioles of mature leaves of this species. We generated a total of 1187 expressed sequence tags (ESTs), corresponding to 891 non-redundant genes. We analysed these ESTs in silico after cDNA macroarray hybridisation. Aphid feeding led to significant increase in RNA accumulation for 126 different genes. Different patterns of deregulation were observed, including transitory or stable induction 3 or 7 days after infestation. The genes affected belonged to various functional categories and were induced systemically in the phloem after infestation. In particular, genes involved in cell wall modification, water transport, vitamin biosynthesis, photosynthesis, carbon assimilation and nitrogen and carbon mobilisation were up-regulated in the phloem. Further analysis of the response in the phloem or xylem suggested that a component of the response was developed more specifically in the phloem. However, this component was different from the stress responses in the phloem driven by pathogen infection. Our results indicate that the phloem is actively involved in multiple adjustments, recruiting metabolic pathways and in structural changes far from aphid feeding sites. However, they also suggest that the phloem displays specific mechanisms that may not be induced in other tissues.

Jasmonate and salicylate induce expression of herbivore cytochrome P450 genes.

Jasmonate and salicylate are plant-produced signals that activate plant defence genes after herbivory or pathogen attack. Amplification of these signals, evoked by either enemy attack or experimental manipulation, leads to an increase in the synthesis of toxic compounds (allelochemicals) and defence proteins in the plants. Although the jasmonate and salicylate signal cascades activate different sets of plant defence genes, or even act antagonistically, there is substantial communication between the pathways. Jasmonate and salicylate also contribute to protecting plants against herbivores by causing plants that experience insect damage to increase their production of volatile molecules that attract natural enemies of herbivorous insects. In response to plant defences, herbivores increase their production of enzymes that detoxify allelochemicals, including cytochrome P450s (refs 15, 16). But herbivores are potentially vulnerable to toxic allelochemicals in the duration between ingesting toxins and induction of detoxification systems. Here we show that the corn earworm Helicoverpa zea uses jasmonate and salicylate to activate four of its cytochrome P450 genes that are associated with detoxification either before or concomitantly with the biosynthesis of allelochemicals. This ability to 'eavesdrop' on plant defence signals protects H. zea against toxins produced by host plants.