SWEETs of aging plants: Role of OsSweet1b in plant senescence is explained

This is the authors' abstract. We don't add key points for this paper.

Most of us adore the autumn scenery where deciduous trees are covered with colorful leaves, waiting to be swept by the wind. While this romantic display is entertaining for our eyes, it is part of a critical phenomenon for plant life known as senescence. Plant senescence is the last stage of plant development. Although most of us are familiar with the tissue-level senescence, for example leaf senescence, certain plant species go through an entire-plant senescence at the end of their life cycle, known as monocarpic senescence. During monocarpic senescence, the vegetative organs of the plants and their photosynthetic machinery systematically die, followed by massive remobilization of nutrients from senescing organs to developing seeds (Distelfeld et al. 2014). The nutrient remobilization rate and efficiency from senescing organs to developing grains significantly impact grain quality and yield in cereal crops, making plant senescence a central process for world agriculture (Gregersen et al. 2008). Multiple factors play a role in the process of senescence such as the developmental age of the plant, environmental stressors, or the plant`s nutrient status (Balazadeh and Mueller-Roeber 2018). For plant senescence to occur seamlessly, mechanisms that sense the age of the plant cells and organs must exist and harmoniously integrate signals from other biotic and abiotic factors to drive an irreversible degeneration process, making the regulation of plant senescence highly complex (Woo et al. 2018). Sugars Will Eventually be Exported Transporters (SWEETs) are sugar transporters that are commonly studied in plants, but their role in plant senescence is understudied. In this issue of Plant Physiology, Chen et al. (2024) explored the role of a sugar transporter, OsSWEET1b, in leaf senescence in rice. Previously, the authors created mutants for 19 SWEET genes in rice and showed that the ossweet1b mutant has accelerated leaf senescence at the heading stage (Li et al. 2022). To follow up on this finding, in this study, they generated transgenic plants and further characterized the role of OsSWEET1b sugar transporter in leaf senescence. During senescence in cereals, the photosynthetic machinery in leaves systematically degrades; as a result, plant leaves lose their chloroplasts and turn yellow. At the molecular level, these changes are also represented in the efficiency of photosynthesis, leakage of electrons, and expression of senescence associated genes (SAGs) (Have et al. 2016). Chen et al. (2024) first showed that transgenic plants overexpressing OsSWEET1b (OsSWEET1b-OE) are delayed in senescence compared to wild type and the ossweet1b mutant based on multiple physiological indicators of leaf senescence such as chlorophyll content, electron leakage analysis, and photosynthesis rate. The differences in senescence patterns were more evident in later stages of plant life; the senescing flag leaf of ossweet1b mutant was completely yellow at the grain-filling stage, while OsSWEET1b-OE and wild type were still completely green. The authors complemented these physiological observations with further molecular analysis. Reactive oxygen species (ROS) homeostasis is one of the earliest responses of plant cells to senescence, and diaminobenzidine (DAB) staining results indicated ossweet1b mutants have more accumulation of H2O2 in their flag leaves compared to OsSWEET1b-OE and wild type. Significant changes were observed in the expression of multiple SAGs, including chlorophyll genes involved in synthesis and degradation, between wild type, OsSWEET1b-OE, ossweet1b mutant. Overall, these results further confirmed that OsSWEET1b is involved in leaf senescence in rice. Since OsSWEET1b was predicted to be a sugar transporter, Chen et al. (2024) further characterized this protein in senescence. They tracked the expression patterns of OsSWEET1b in multiple tissues throughout the plant growth. OsSWEET1b expression was higher in leaves and sheaths than in other tissues starting from the vegetative growth stage, and its expression decreased throughout senescence. They also showed that OsSWEET1b is localized on plasma membrane and is a hexose transporter using Xenopus oocytes. Furthermore, they provided in planta evidence for OsSWEET1b`s activity in hexose transportation by measuring the amount of various sugars in the flag leaf at different stages of growth. The flag leaf is the immediate leaf below the spike. Due to its proximity, flag leaves are the primary source of nutrients for developing grains (Biswal and Kohli 2013). Glucose and galactose levels were higher in OsSWEET1b-OE plants from tillering to grain filling stage. OsSWEET1b-OE plants also accumulated more starch in flag leaves, which provides further evidence for OsSWEET1b’s role in sugar transport during senescence. Taken together, these results indicate that ossweet1b mutant has an accelerated senescence most likely due to attenuated glucose and galactose transport. Changes in plant senescence can significantly impact the agronomic quality of grains. Authors planted OsSWEET1b-OE, ossweet1b mutant and wild-type plants in the field and compared their agronomic performance by assessing several agronomic parameters. ossweet1b mutants showed decreased plant height, tiller number, and panicle length. Furthermore, grain number per panicle was decreased by around 50% in ossweet1b mutants compared to wild type, which caused around 30% decrease in 1000-grain weight. Along these lines, OsSWEET1b-OE had significantly increased grain number per panicle compared to wild type. Overall, Chen et al. (2024) is providing comprehensive evidence of the role of a new sugar transporter in the senescence process in rice. In light of their previous findings, the authors propose the OsWRKY53 as dual regulator of both SWEET transporters and ABA metabolism in rice leaves (Xie et al. 2022) (Fig.). Findings from Chen et al. add to our increasing understanding of molecular mechanisms regulating plant senescence in cereal crops. Further studies along these lines will provide opportunities to improve the agronomic performance of cereal crops by delaying senescence or increasing its efficiency. Proposed working model of OsWRKY53-regulated senescence. OsWRKY53 binds and suppresses the expressions of OsSWEET1b and OsABA8ox1 or OsABA8ox2, causing decreased sugar accumulation and increased ABA accumulation in leaf cells, respectively. The attenuated sugar content and enhanced ABA level coordinately promote leaf senescence (adapted from Chen et al 2024). B.A. wishes to thank Plant Physiology for the opportunity to act as an Assistant Features Editor. No new data were generated or analyzed in support of this research.