Specificity of H2O2 signaling in leaf senescence: is the ratio of H2O2 contents in different cellular compartments sensed in Arabidopsis plants?

Abstract

Leaf senescence is an integral part of plant development and is driven by endogenous cues such as leaf or plant age. Developmental senescence aims to maximize the usage of carbon, nitrogen and mineral resources for growth and/or for the sake of the next generation. This requires efficient reallocation of the resources out of the senescing tissue into developing parts of the plant such as new leaves, fruits and seeds. However, premature senescence can be induced by severe and long-lasting biotic or abiotic stress conditions. It serves as an exit strategy to guarantee offspring in an unfavorable environment but is often combined with a trade-off in seed number and quality. In order to coordinate the very complex process of developmental senescence with environmental signals, highly organized networks and regulatory cues have to be in place. Reactive oxygen species, especially hydrogen peroxide (H2O2), are involved in senescence as well as in stress signaling. Here, we want to summarize the role of H2O2 as a signaling molecule in leaf senescence and shed more light on how specificity in signaling might be achieved. Altered hydrogen peroxide contents in specific compartments revealed a differential impact of H2O2 produced in different compartments. Arabidopsis lines with lower H2O2 levels in chloroplasts and cytoplasm point to the possibility that not the actual contents but the ratio between the two different compartments is sensed by the plant cells.

ROS production and signalling in chloroplasts: cornerstones and evolving concepts

“…The consensus of opinion has shifted to focus on the beneficial roles of ROS in many essential plant processes, particularly cell to cell communication, cell proliferation, growth and stress responses (Huang et al., 2019; Mhamdi & Van Breusegem, 2018), functions which demonstrate that ROS are essential markers or signals of living cells (Mittler, 2017; Van Breusegem et al., 2018). ROS signals have been implicated in the regulation of numerous development processes from root development (Mase & Tsukagoshi, 2021) and the transition to flowering (Huang et al., 2021) to leaf senescence (Zentgraf et al., 2022). Within this context, chloroplast‐derived ROS not only regulate supply and demand in energy metabolism (Foyer et al., 2017; Noctor & Foyer, 2016), but they also contribute to the elicitation of genetic and epigenetic responses that allow acclimation and adaptation to metabolic, developmental and environmental triggers (Mhamdi & Van Breusegem, 2018; Mittler, 2017).…”

Integrated transcriptomics and miRNAomics provide insights into the complex multi-tiered regulatory networks associated with coleoptile senescence in rice

“…Functionally, AQPs are involved in plant senescence as the suppression of TIP1;1, a member of tonoplast AQPs, compromised carbohydrate transport, had excessive water loss and accelerated leaf senescence ( Ma et al., 2004 ), while overexpression of the cotton TIP1;1-like protein in Arabidopsis promoted premature bolting and delayed senescence of rosette leaves ( Cheng et al., 2022 ). AQPs promote diffusion of H 2 O 2 across the membranes during senescence which may act as a signal for triggering senescence in the adjoining cells ( Zentgraf et al., 2022 ). During senescence, generation of ROS, especially H 2 O 2 is one of the early responses and it acts as a potent signaling reactive oxygen species.…”

Proteomic Analysis Reveals a Critical Role of the Glycosyl Hydrolase 17 Protein in Panax ginseng Leaves under Salt Stress

“…The accumulation of ROS during salinity stress causes damage to the plant cells [ 25 , 26 ]. In this study, a time-dependent accumulation of H 2 O 2 and a membrane peroxidation product, MDA, was observed in ginseng leaves in response to salt stress ( Figure 1 B,C).…”