Negative regulation of ABA signaling by WRKY33 is critical for Arabidopsis immunity towards Botrytis cinerea 2100

Abstract

The Arabidopsis mutant wrky33 is highly susceptible to Botrytis cinerea. We identified >1680 Botrytis-induced WRKY33 binding sites associated with 1576 Arabidopsis genes. Transcriptional profiling defined 318 functional direct target genes at 14 hr post inoculation. Comparative analyses revealed that WRKY33 possesses dual functionality acting either as a repressor or as an activator in a promoter-context dependent manner. We confirmed known WRKY33 targets involved in hormone signaling and phytoalexin biosynthesis, but also uncovered a novel negative role of abscisic acid (ABA) in resistance towards B. cinerea 2100. The ABA biosynthesis genes NCED3 and NCED5 were identified as direct targets required for WRKY33-mediated resistance. Loss-of-WRKY33 function resulted in elevated ABA levels and genetic studies confirmed that WRKY33 acts upstream of NCED3/NCED5 to negatively regulate ABA biosynthesis. This study provides the first detailed view of the genome-wide contribution of a specific plant transcription factor in modulating the transcriptional network associated with plant immunity.

DOI: http://dx.doi.org/10.7554/eLife.07295.001

eLife digest

Crop yields can be badly affected by diseases caused by some fungi and other microbes. One fungus called Botrytis cinerea is able to infect many different species of crop plants—including tomatoes and grapes—and can cause severe damage both before and after harvest. This fungus belongs to a group of microbes that kill the plant cells they invade and then extract the nutrients from the dead cells.

Some plants are able to resist infection by B. cinerea and researchers have identified several proteins that are involved in this resistance. One such protein is called WRKY33, which is able to bind to DNA to regulate the activity of particular genes. However, it was not clear exactly which genes were involved in the response to B. cinerea.

Arabidopsis thaliana is a small flowering plant that is often used in research. Mutant A. thaliana plants lacking WRKY33 are very susceptible to infection with B. cinerea. Here, Liu et al. use several genetic techniques to find out which genes WRKY33 regulates when A. thaliana plants are exposed to the fungus. The experiments indicate that WRKY33 can alter the activity of over 300 genes. Some of these genes had previously been shown to be targets of WRKY33 and are involved in cell responses to plant hormones and the production of an antimicrobial molecule called camalexin.

Liu et al. also show that two genes called NCED3 and NCED5—which are required for the production of a plant hormone called abscisic acid—are repressed by WRKY33. Mutant plants lacking WRKY33 had increased levels of abscisic acid and further experiments suggested that the repression of NCED3 and NCED5 by WRKY33 is important to resistance against the fungus.

Liu et al.'s findings provide the first detailed view of which genes in A. thaliana are regulated by WRKY33 when the plant is exposed to B. cinerea. A future challenge is to understand how blocking the production of abscisic acid protects plants against B. cinerea and other similar fungi.

DOI: http://dx.doi.org/10.7554/eLife.07295.002