MYB30 Links the Reactive Oxygen Species Wave to Systemic Acclimation

Stress signals trigger systemic signaling and acclimation. The propagation of reactive oxygen species (ROS) from the tissues that initially sense the stress stimuli to distant ones or to the entire plant is known as the ROS wave and is key to plant acclimation to adverse conditions (Suzuki et al., 2013). Recent work from the Mittler lab showed that this cell-to-cell communication is dependent on the function of RESPIRATORY BURST OXIDASE HOMOLOG D (RBOHD) and is accompanied by extensive transcriptional reprogramming in a context of stress (Zandalinas et al., 2019, 2020).

The ROS wave-associated transcripts constitute a set of transcription factors including an R2R3 MYB, MYB30. Earlier reports identified MYB30 as a key factor mediating hormone and stress responses in plants (Li et al., 2009; Liao et al., 2017; Mabuchi et al., 2018; Maki et al., 2019; Yan et al., 2020). Yet, the network of MYB30 and the roles in ROS and systemic signaling are not known.

In this issue of Plant Physiology, Fichman et al. (2020) determined the interactions between MYB30, the ROS wave, and systemic acquired acclimation in Arabidopsis (Arabidopsis thaliana). When subjected to high light, the myb30 mutants display enhanced rates of ROS wave propagation and their local tissues were able to acclimate to the excess light. However, they were unable to mount an acclimation response in their systemic tissues, suggesting that MYB30 is required to couple the ROS wave and systemic acclimation (Fig. 1). These phenotypes were specific to excess light, as the myb30 responses to wounding or heat stress were not different from those of the wild type.

Figure 1.

MYB30 links the ROS wave to systemic acquired acclimation in the context of high-light stress. Left, Imaging at 10 and 30 min of whole-plant ROS accumulation in the wild type (WT) and MYB30 loss-of-function lines triggered by local (L) excess light (stress was applied to leaf L only and followed in the whole rosette including systemic [S] leaves). Right, Scheme showing the roles of MYB30 in systemic signaling and acclimation. MYB30 is induced by ROS and is required to trigger systemic acclimation in response to high light (HL). MYB30 functions are linked to GATA8 and GDSL and could be mediated by PHYTOCHROME-INTERACTING FACTORS such as PIF4 (Yan et al., 2020). Fichman et al. (2020) propose that MYB30 could be required to suppress the ROS wave during its propagation (feedback signals indicated by ?) or even at the local initiation site. Adapted from Fichman et al. (2020), Figs. 1 and 4.

In response to excess light in local leaves, myb30 plants showed a strong transcriptomic response. However, consistent with the observed defect in systemic acclimation, systemic leaves displayed a much weaker transcriptomic response relative to wild-type plants. Furthermore, the authors identified a subset of genes that were associated with the ROS wave (Zandalinas et al., 2019), induced in the wild type but not in myb30, that contained MYB-binding motifs in their promoters. Fichman et al. (2020) hypothesized that the corresponding proteins (e.g. GATA8 and the GDSL esterase/lipase) may possibly be involved in suppressing the ROS wave and that their functions could be linked to MYB30 (Fig. 1). In agreement with this scenario, the authors demonstrated that, similar to MYB30, mutations in GATA8 and GDSL enhance ROS wave propagation and delay or suppress the expression of MYB30, respectively. Additionally, network and coexpression analyses as well as thorough mining of a large number of transcriptomic data sets allowed the authors to identify direct targets of MYB30 that are dependent on RBOHD.

Collectively, the analyses by Fichman and colleagues (2020) define MYB30 as a key factor that mediates systemic acquired acclimation to light stress and regulates the intensity of initiation or propagation of the ROS wave. This work sets the ground for future experimental validation that should yield a comprehensive overview of the interactions between MYB30 and its targets and reveal new routes for the propagation and integration of the ROS wave that convey specificity to the systemic response.