Abstract
The plant cell cuticle serves as the first barrier protecting plants from mechanical injury and invading pathogens. The cuticle can be breached by cutinase-producing pathogens and the degradation products may activate pathogenesis signals in the invading pathogens. Cuticle degradation products may also trigger the plant’s defense responses. Botrytis cinerea is an important plant pathogen, capable of attacking and causing disease in a wide range of plant species. Arabidopsis thaliana shn1-1D is a gain-of-function mutant, which has a modified cuticular lipid composition. We used this mutant to examine the effect of altering the whole-cuticle metabolic pathway on plant responses to B. cinerea attack. Following infection with B. cinerea, the shn1-1D mutant discolored more quickly, accumulated more H2O2, and showed accelerated cell death relative to wild-type (WT) plants. Whole transcriptome analysis of B. cinerea-inoculated shn1-1D vs. WT plants revealed marked upregulation of genes associated with senescence, oxidative stress and defense responses on the one hand, and genes involved in the magnitude of defense-response control on the other. We propose that altered cutin monomer content and composition of shn1-1D plants triggers excessive reactive oxygen species accumulation and release which leads to a strong, unique and uncontrollable defense response, resulting in plant sensitivity and death.
Highlights
Plants encounter a wide range of pathogens and insects in their natural environment
We discovered that shn1-1D plants generate excess reactive oxygen species (ROS) and exhibit strong activation of defense responses, yet these plants were more susceptible to the necrotrophic fungus B. cinerea than the WT
In accordance with the resistance found when shn1–1D cutin monomers were supplemented to the inoculation suspension (Figure 6A), we found these genes to be moderately upregulated in WT plants 72 h after inoculation with B. cinerea suspension supplemented with shn1–1D cutin monomers, as compared to their expression in shn1–1D plants inoculated with B. cinerea alone, and even to their expression in inoculated WT plants (Figure 6B)
Summary
Plants encounter a wide range of pathogens and insects in their natural environment. Some of these are responsible for annual worldwide economic damage due to losses in important agricultural crops. The second barrier protecting plants from pathogenic attack is a set of biochemical reactions, which lead to hypersensitive and acquired immune responses These constitutive and inducible defense events depend largely on the perception of signaling molecules [2,3,4,5,6], some of which can be activated by cuticle-degradation products. The observed differences in the effects of permeable or altered cuticles on pathogenesis by diverse fungal pathogens suggest that other, yet to be discovered mechanisms may be involved in triggering the plant response and plant-induced resistance during cuticular disruption by invading pathogens. We propose that shn1-1D plants exhibit accelerated ROS generation, which leads to overstimulated activation of genes involved in the defense response that cannot be controlled, resulting in plant sensitivity and death
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