Resistance to Botrytis cinerea in sitiens, an Abscisic Acid-Deficient Tomato Mutant, Involves Timely Production of Hydrogen Peroxide and Cell Wall Modifications in the Epidermis

Abstract

Plant defense mechanisms against necrotrophic pathogens, such as Botrytis cinerea, are considered to be complex and to differ from those that are effective against biotrophs. In the abscisic acid-deficient sitiens tomato (Solanum lycopersicum) mutant, which is highly resistant to B. cinerea, accumulation of hydrogen peroxide (H 2 O 2 ) was earlier and stronger than in the susceptible wild type at the site of infection. In sitiens, H 2 O 2 accumulation was observed from 4 h postinoculation (hpi), specifically in the leaf epidermal cell walls, where it caused modification by protein cross-linking and incorporation of phenolic compounds. In wildtype tomato plants, H 2 O 2 started to accumulate 24 hpi in the mesophyll layer and was associated with spreading cell death. Transcript-profiling analysis using TOM1 microarrays revealed that defense-related transcript accumulation prior to infection was higher in sitiens than in wild type. Moreover, further elevation of sitiens defense gene expression was stronger than in wild type 8 hpi both in number of genes and in their expression levels and confirmed a role for cell wall modification in the resistant reaction. Although, in general, plant defense-related reactive oxygen species formation facilitates necrotrophic colonization, these data indicate that timely hyperinduction of H 2 O 2 -dependent defenses in the epidermal cell wall can effectively block early development of B. cinerea.

Dual Roles of Reactive Oxygen Species and NADPH Oxidase RBOHD in an Arabidopsis-Alternaria Pathosystem

“…7C). Single-cell H 2 O 2 accumulation followed by cell death was reported in various plant-fungus interactions (Thordal-Christensen et al, 1997;Asselbergh et al, 2007;Vorwerk et al, 2007). Cells of inoculated AtrbohD leaves, on the contrary, did not exhibit extracellular H 2 O 2 accumulation but showed H 2 O 2 -specific DAB polymer precipitation in the chloroplasts.…”

The multifaceted role of ABA in disease resistance

“…After successful penetration, pathogens face the second barrier of early post-invasive defense (Phase II). This includes early cellular responses at the infection sites, such as formation of papillae and rapid accumulation of ROS (not shown) [20]. Early postinvasive penetration defense is followed by transcriptomic and metabolomic reprogramming, which can result from a hypersensitive response.…”

“…Throughout Phase II, it promotes callose deposition in response to infection by fungi and oomycetes. However, in certain cases, ABA production can suppress early ROS production and cause increased susceptibility, as observed during the interaction between tomato and Botrytis cinerea [20]. By contrast, components in the ABA response pathway can suppress bacteria-induced callose deposition and, therefore, contribute negatively to resistance [14,16].…”

“…Recently, it was demonstrated that this resistance is based on increased accumulation of ROS during the early stages of tissue penetration [20]. Pre-treatment with the callose synthesis blocker 2-deoxy-D-glucose has no influence on the sitiensinduced resistance but reduces the basal resistance of wildtype plants.…”

“…Hence, increased ROS production in sitiens precedes callose-mediated defense against B. cinerea. Based on the finding that application of the antioxidant ascorbate can restore susceptibility to B. cinerea [20], it is tempting to speculate that sitiens-induced resistance is caused by an interaction between the xanthophyll cycle and the ROS-buffering ascorbate-gluthatione cycle (Figure 3). In support of this, a mechanistic link between ABA biosynthesis and ascorbate has been demonstrated [21], which showed that low ascorbate in the Arabidopsis vtc1 (vitamin C1) mutant stimulates ABA production.…”