The circadian-controlled PIF8–BBX28 module regulates petal senescence in rose flowers by governing mitochondrial ROS homeostasis at night

Abstract

Reactive oxygen species (ROS) are unstable reactive molecules that are toxic to cells. Regulation of ROS homeostasis is crucial to protect cells from dysfunction, senescence and death. In plant leaves, ROS are mainly generated from chloroplasts and are tightly temporally restricted by the circadian clock. However, little is known about how ROS homeostasis is regulated in non-photosynthetic organs, such as petals. Here, we showed that H2O2 levels exhibit typical circadian rhythmicity in rose (Rosa hybrida) petals, consistent with the measured respiratory rate. RNA-seq and functional screening identified a B-box gene, RhBBX28, whose expression was associated with H2O2 rhythms. Silencing RhBBX28 accelerated flower senescence and promoted H2O2 accumulation at night in petals, while overexpression of RhBBX28 had the opposite effects. RhBBX28 influenced the expression of various genes related to respiratory metabolism, including the TCA cycle and glycolysis, and directly repressed the expression of SUCCINATE DEHYDROGENASE 1, which plays a central role in mitochondrial ROS homeostasis. We also found that PHYTOCHROME INTERACTING FACTOR8 (RhPIF8) could activate RhBBX28 expression to control H2O2 levels in petals and thus flower senescence. Our results indicate that the circadian- controlled RhPIF8-RhBBX28 module is a critical player that controls flower senescence by governing mitochondrial ROS homeostasis in rose.

Stable Reference Gene Selection for qRT-PCR Normalization in Strawberry (Fragaria × ananassa) Leaves under Different Stress and Light-Quality Conditions

“…FaBBX28 is a member of the BBX gene family containing the B-box conserved domain [45]. A recent study proposed a relationship between ROS homeostasis and RhBBX28, which is a homologue of FaBBX28 in rose (Rosa hybrida) [46]. Moreover, an expression peak of FaBBX28 in the root tissue of strawberry seedlings was found in our previous results, which led to speculation that the expression level could potentially change in response to drought stress.…”

Apple SINA E3 ligase MdSINA3 negatively mediates JA‐triggered leaf senescence by ubiquitinating and degrading the MdBBX37 protein

“…B‐box (BBX) proteins mediate many aspects of plant growth and development, including flowering, photomorphogenesis, the biosynthesis of secondary metabolites and the shade avoidance response, as well as biotic and abiotic stresses (Bursch et al., 2020; Crocco & Botto, 2013; Gangappa & Botto, 2014; Khanna et al., 2009). Although several studies have revealed that the BBX protein is involved in the modulation of leaf senescence (An et al., 2021d; Liu et al., 2019; Zhang et al., 2021), its molecular mechanism remains to be fully defined. Here, we found that MdBBX37 was induced during leaf senescence (Figure 1a), suggesting that MdBBX37 may play a role in the modulation of leaf senescence.…”

“…MdBBX22 acts by weakening the transcriptional activity of its interacting protein MdABI5, while conversely inhibiting the expression of MdABI5 through MdHY5 (An et al., 2021d). In the genus Rosa (rose), the inhibition of RhBBX28 contributes to flower senescence by promoting the accumulation of reactive oxygen species (ROS) (Zhang et al., 2021). Although the involvement of BBXs in leaf senescence has been reported, the molecular mechanism by which BBX proteins mediate leaf senescence remains unclear.…”

Spatially specific mechanisms and functions of the plant circadian clock

“…Several studies have examined clock expression in specific parts of the plant using a combination of tissue dissection and RNA-seq/microarrays ( Endo et al, 2014 ; Xing et al, 2019 ; Cramer et al, 2020 ; Zhang et al, 2021b ) or RT-qPCR ( Shimizu et al, 2015 ; Bordage et al, 2016 ; Li et al, 2020 ). RNA-seq in particular allows global measurement of transcripts in a single sample.…”