Phytochrome B regulates reactive oxygen signaling during abiotic and biotic stress in plants

Abstract

Plants are essential for life on Earth converting light into chemical energy in the form of sugars. To adjust for changes in light intensity and quality, and to become as efficient as possible in harnessing light, plants utilize multiple light receptors, signaling, and acclimation mechanisms. In addition to altering plant metabolism, development and growth, light cues sensed by some photoreceptors, such as phytochromes, impact on many plant responses to biotic and abiotic stresses. Central for plant responses to different stresses are reactive oxygen species (ROS) that function as key signaling molecules. Recent studies demonstrated that respiratory burst oxidase homolog (RBOH) proteins that reside at the plasma membrane and produce ROS at the apoplast play a key role in plant responses to different biotic and abiotic stresses. Here we reveal that phytochrome B (phyB) and RBOHs function as part of a key regulatory module that controls ROS production, transcript expression, and plant acclimation to excess light stress. We further show that phyB can regulate ROS production during stress even if it is restricted to the cytosol, and that phyB, RBOHD and RBOHF co-regulate thousands of transcripts in response to light stress. Surprisingly, we found that phyB is also required for ROS accumulation in response to heat, wounding, cold, and bacterial infection. Taken together, our findings reveal that phyB plays a canonical role in plant responses to biotic and abiotic stresses, regulating ROS production, and that phyB and RBOHs function in the same pathway.Significant StatementAbiotic and biotic stresses cause extensive losses to agricultural production and threaten global food security. Augmenting plant resilience to stressful conditions requires understanding of how plants sense stress. Here we report that the sensing of different abiotic and biotic stresses that result in the production of the key stress-response signaling molecules, reactive oxygen species, requires the plant photoreceptor protein phytochrome B. We further show that in contrast to its many nuclear functions, phytochrome B regulates reactive oxygen production by plasma membrane-localized respiratory burst oxidase homologs while localized to the cytosol. Our findings reveal the existence of a rapid stress response regulatory mechanism requiring phytochrome B and reactive oxygen species, essential for plant acclimation to stress.

ROS are evolutionary conserved cell-to-cell signals

“…All organisms, outside of the mammalian cells, were fumigated with 50 µM H2DCFDA (Millipore-Sigma, St. Louis, MO, USA) in 0.05 M Phosphate buffer pH 7.4 with 0.01% Silwet L-77. Fumigation was carried out for 30 min using nebulizers (Punasi Direct, Hong Kong, China) [20][21][22][23][24]37,38 . For mammalian cells 10 µM H2DCFDA (final concentration) was applied to the medium and incubated for 30 min.…”

“…The findings that rapid systemic ROS signals are conserved among many land plants (Figures 1 and 2) 20,22,24,33 prompted us to test whether they can also be found in multicellular (Chara vulgaris) and unicellular (Chlamydomonas reinhardtii) algae. Multicellular and unicellular algae are known to use extracellular ROS as signals and contain NOX/RBOH enzymes 40,41 .…”

“…Polyclonal anti-sHSP17.1 antibodies from rabbit were used to identify the proteins on the membrane as described previously 24,25 .…”

“…The ROS wave was also recently shown to spread from one plant to another, when plants physically touch each other and conditions are sufficiently humid 22 . In addition to plasma membrane-localized RBOHs, the ROS wave requires the function of PDlocalized proteins, different calcium channels, calcium signaling proteins, phytochrome B, and the plasma membrane (PM)-localized apoplastic ROS receptor H2O2-induced Ca 2+ increases 1 (HPCA1) protein 21,23,24 .…”

“…Numerous studies have shown that the ROS wave is linked to cell-to-cell calcium and electric signaling and that it is required for plant acclimation to stress (e.g., 17,21,[24][25][26][27] ).…”