Ethylene-Induced Flavonol Accumulation in Guard Cells Suppresses Reactive Oxygen Species and Moderates Stomatal Aperture

Article (PDF Available)inPlant physiology 164(4) · March 2014with45 Reads
DOI: 10.1104/pp.113.233528 · Source: PubMed
Guard cell swelling controls the aperture of stomata, pores that facilitate gas exchange and water loss from leaves. The hormone abscisic acid (ABA) has a central role in regulation of stomatal closure through synthesis of second messengers, which include reactive oxygen species (ROS). ROS accumulation must be minimized by antioxidants to keep concentrations from reaching damaging levels within the cell. Flavonols are plant metabolites that have been implicated as antioxidants; however, their antioxidant activity in planta has been debated. Flavonols accumulate in guard cells of Arabidopsis thaliana, but not surrounding pavement cells, as visualized with a flavonol-specific dye. The expression of a reporter driven by the promoter of CHALCONE SYNTHASE (CHS), a gene encoding a flavonol biosynthetic enzyme, in guard cells, but not pavement cells, suggests guard cell specific flavonoid synthesis. Increased levels of ROS were detected using a fluorescent ROS sensor in guard cells of tt4-2, which has a null mutation in CHS and therefore synthesizes no flavonol antioxidants. Guard cells of tt4-2 show more rapid ABA-induced closure than wild-type, suggesting flavonols may dampen the ABA-dependent ROS burst that drives stomatal closing. The levels of flavonols are positively regulated in guard cells by ethylene treatment in wild-type, but not in the ethylene-insensitive2-5 (ein2-5) mutant. Additionally, in both ethylene-overproducing1 (eto1) and ethylene-treated wild-type plants, elevated flavonols lead to decreasing ROS and slower ABA-mediated stomatal closure. These results are consistent with flavonols suppressing ROS accumulation and decreasing the rate of ABA-dependent stomatal closure, with ethylene-induced increases in guard cell flavonols modulating these responses.

Full-text (PDF)

Available from: Gloria K Muday, Oct 19, 2014
    • "In this study, the dynamic changes of many flavonoids (and their conjugated derivatives) were measured in guard cells under elevated CO 2 . The results suggest potential involvement of flavonoids as ROS scavengers (Watkins et al., 2014) in CO 2 induced stomatal closure. "
    [Show abstract] [Hide abstract] ABSTRACT: Foliar stomatal movements are critical for regulating plant water loss and gas exchange. Elevated carbon dioxide (CO2) levels are known to induce stomatal closure. However, the current knowledge on CO2 signal transduction in stomatal guard cells is limited. Here we report metabolomic responses of Brassica napus guard cells to elevated CO2 using three hyphenated metabolomics platforms: gas chromatography (GC)-mass spectrometry (MS), liquid chromatography (LC)-multiple reaction monitoring (MRM)-MS, and ultra high-performance LC (UHPLC)-quadrupole time-of-flight (QToF)-MS. A total of 358 metabolites from guard cells were quantified in a time-course response to elevated CO2 level. Most metabolites increased under elevated CO2, showing the most significant differences at 10 minutes. In addition, reactive oxygen species (ROS) production increased and stomatal aperture decreased with time. Major alterations in flavonoid, organic acid, sugar, fatty acid, phenylpropanoid, and amino acid metabolic pathways indicated changes in both primary and specialized metabolic pathways in guard cells. Most interestingly, the jasmonic acid (JA) biosynthesis pathway was significantly altered in the course of elevated CO2 treatment. Together with results obtained from JA biosynthesis and signaling mutants as well as CO2 signaling mutants, we discovered that CO2 induced stomatal closure is mediated by JA signaling. This article is protected by copyright. All rights reserved.
    Full-text · Article · Aug 2016
    • "Flavonoids, another class of ROS scavengers, have also been found to be upregulated in AM‐mediated resistance to drought in plants (Abbaspour et al., 2012). Flavonols, a group of low molecular antioxidant com­ pounds, also regulate the level of oxidative stress in plants subsequently regulating the aperture of guard cells (Watkins et al., 2014). "
    [Show abstract] [Hide abstract] ABSTRACT: Sustainable agriculture is vital in today's world as it offers the potential to meet our ever-increasing agricultural needs, something that conventional agriculture fails to do. Drought stress is considered to be one of the most important abiotic factors limiting plant growth and yield. A significant decrease in crop yield has been reported in both temperate and tropical parts of various continents under drought-induced stress. Among the various approaches employed to date, mycorrhizal association marks an important step in enhancing drought stress tolerance. In a mycorrhizal association, the fungus colonizes the host plant's roots, either intracellularly as in arbuscular mycorrhizal fungi (AMF or AM), or extracellularly as in ectomycorrhizal fungi. Plants in association with mycorrhiza are found to be more resistant to infections and diseases, including soil-borne pathogens. AMF has also been significantly correlated with soil biological fertility variables such as soil fungi and soil bacteria, including soil diseases. Furthermore, AMF also associates itself with physical soil variables, but only with water level and not with aggregate stability. AMF is also variable with the effects of drought. Several ecophysiological studies reveal that AM symbiosis can regulate the rate of water movement into, through and out of the host plants, thereby affecting tissue hydration and plant physiology. Drought tolerance in plants by AM symbiosis has been demonstrated to be a cumulative effect of physical, nutritional, physiological, and cellular aspects. This chapter summarizes various aspects of AM symbiosis and their mechanisms that protect host plants against the detrimental effects of water deficiency, gaining an understanding toward sustainable agriculture.
    Full-text · Chapter · Jun 2016 · Frontiers in Physiology
    • "Each metabolite could belong to multiple pathways (Figure 5). The phenolic compounds play diverse and important functions in plant development and defense as reactive oxygen species scavengers, disease resistance inducer (Moreno et al., 1994; Murphy et al., 2000; Mustafa and Verpoorte, 2007; Watkins et al., 2014). In our study, C6C1-, C6C3-, and C6C3C6-compounds comprised 3.58, 51.81, and 44.60% of total phenolic compounds, respectively. "
    [Show abstract] [Hide abstract] ABSTRACT: Phenolic compounds belong to a class of secondary metabolites and are implicated in a wide range of responsive mechanisms in plants triggered by both biotic and abiotic elicitors. In this study, we approached the combinational effects of ethylene and MeJA (methyl jasmonate) on phenolic compounds profiles and gene expressions in the medicinal plant Catharanthus roseus. In virtue of a widely non-targeted metabolomics method, we identified a total of 34 kinds of phenolic compounds in the leaves, composed by 7 C6C1-, 11 C6C3-, and 16 C6C3C6 compounds. In addition, 7 kinds of intermediates critical for the biosynthesis of phenolic compounds and alkaloids were identified and discussed with phenolic metabolism. The combinational actions of ethylene and MeJA effectively promoted the total phenolic compounds, especially the C6C1 compounds (such as salicylic acid, benzoic acid) and C6C3 ones (such as cinnamic acid, sinapic acid). In contrast, the C6C3C6 compounds displayed a notably inhibitory trend in this case. Subsequently, the gene-to-metabolite networks were drawn up by searching for correlations between the expression profiles of 5 gene tags and the accumulation profiles of 41 metabolite peaks. Generally, we provide an insight into the controlling mode of ethylene-MeJA combination on phenolic metabolism in C. roseus leaves.
    Full-text · Article · May 2016
Show more