Regulation of the NADPH Oxidase RBOHD During Plant Immunity

Abstract

Pathogen recognition induces the production of reactive oxygen species (ROS) by NADPH oxidases in both plants and animals. ROS have direct antimicrobial properties, but also serve as signaling molecules to activate further immune outputs. However, ROS production has to be tightly controlled to avoid detrimental effects on host cells, but yet must be produced in the right amount, at the right place and at the right time upon pathogen perception. Plant NADPH oxidases belong to the respiratory burst oxidase homolog (RBOH) family, which contains 10 members in the model plant Arabidopsis thaliana. The perception of pathogen-associated molecular patterns (PAMPs) by pattern recognition receptors (PRRs) leads to a rapid, specific and strong production of ROS, which is dependent on RBOHD. RBOHD is mainly controlled by Ca(2+) via direct binding to EF-hand motifs and phosphorylation by Ca(2+)-dependent protein kinases. Recent studies have, however, revealed a critical role for a Ca(2+)-independent regulation of RBOHD. The plasma membrane-associated cytoplasmic kinase BIK1 (BOTRYTIS-INDUCED KINASE1), which is a direct substrate of the PRR complex, directly interacts with and phosphorylates RBOHD upon PAMP perception. Impairment of these phosphorylation events completely abolishes the function of RBOHD in immunity. These results suggest that RBOHD activity is tightly controlled by multilayered regulations. In this review, we summarize recent advances in our understanding of the regulatory mechanisms controlling RBOHD activation.

Reactive Oxygen Species in the Regulation of Stomatal Movements

“…Together, the results suggested Ca 2+ -independent phosphorylation of this site. Thus, the authors suggested that BIK1-mediated, Ca 2+ -independent phosphorylation occurred upstream of Ca 2+ and primed AtRBOHD for Ca 2+ regulation (Kadota et al, 2014(Kadota et al, , 2015. This model is also in agreement with the observation that in HEK cells Ca 2+ stimulation did not lead to RBOH activation in the presence of a kinase inhibitor (Kimura et al, 2012).…”

“…FLAGELLIN-SENSITIVE2 (FLS2) and EF-TU RECEPTOR, which recognize flg22 and elf18, associate in a complex with the Leu-rich repeat receptor-like kinase (LRR-RLK) BRASSINOSTEROID INSENSITIVE1-ASSOCIATED RECEPTOR KINASE (BAK1) and receptor-like cytoplasmic kinases such as BOTRYTIS-INDUCED KINASE1 (BIK1; Fig. 1; for review, see Kadota et al, 2015).…”

Plasma Membrane Microdomains Are Essential for Rac1-RbohB/H-Mediated Immunity in Rice

“…Recent reports also showed that the dynamics of AtRbohD are regulated by PM microdomains (Hao et al, 2014). At-RbohD has been shown to play an important role in innate immunity in Arabidopsis (Kadota et al, 2015) and belongs to same clade with Os-RbohB and Os-RbohH (Supplemental Figure 11A). Taken together with the data that OsRbohB contributes to resistance to rice blast fungus infection, simultaneous localization of Os-Rac1 and Os-RbohB/H to PM microdomains in response to chitin is likely to be necessary for the activation of Os-RbohB/H by activated Os-Rac1.…”

A Cysteine-Rich Protein Kinase Associates with a Membrane Immune Complex and the Cysteine Residues Are Required for Cell Death

“…For example, FLS2-mediated flg22 perception and signaling requires transphosphorylation events that occur in the receptor complex (Macho et al, 2015). In addition, the transmembrane protein RBOHD, an NADPH oxidase responsible for the production of extracellular ROS, is activated through transphosphorylation by the receptor-like cytoplasmic kinase BIK1 and calcium-dependent protein kinases (Kadota et al, 2015). Mutation of the conserved Lys residue in the kinase domain of the Ser/Thr protein kinases is known to abolish kinase activity and thereby signaling Lin et al, 2015).…”