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1.  H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses 
Journal of Experimental Botany  2014;65(15):4371-4383.
Brassinosteroids induce H2O2 accumulation from RBOH1-NADPH oxidase, which first induces ABA biosynthesis and stress tolerance, in turn leading to prolonged H2O2 production in both apoplast and chloroplast and stress tolerances.
The production of H2O2 is critical for brassinosteroid (BR)- and abscisic acid (ABA)-induced stress tolerance in plants. In this study, the relationship between BR and ABA in the induction of H2O2 production and their roles in response to heat and paraquat (PQ) oxidative stresses were studied in tomato. Both BR and ABA induced increases in RBOH1 gene expression, NADPH oxidase activity, apoplastic H2O2 accumulation, and heat and PQ stress tolerance in wild-type plants. BR could only induced transient increases in these responses in the ABA biosynthetic mutant notabilis (not), whereas ABA induced strong and prolonged increases in these responses in the BR biosynthetic mutant d ^im compared with wild-type plants. ABA levels were reduced in the BR biosynthetic mutant but could be elevated by exogenous BR. Silencing of RBOH1 compromised BR-induced apoplastic H2O2 production, ABA accumulation, and PQ stress responses; however, ABA-induced PQ stress responses were largely unchanged in the RBOH1-silenced plants. BR induces stress tolerance involving a positive feedback mechanism in which BR induces a rapid and transient H2O2 production by NADPH oxidase. The process in turn triggers increased ABA biosynthesis, leading to further increases in H2O2 production and prolonged stress tolerance. ABA induces H2O2 production in both the apoplastic and chloroplastic compartments.
PMCID: PMC4112640  PMID: 24899077
Abscisic acid; brassinosteroid; hydrogen peroxide; NADPH oxidase; Solanum lycopersicum; VIGS.
2.  Chloroplastic thioredoxin-f and thioredoxin-m1/4 play important roles in brassinosteroids-induced changes in CO2 assimilation and cellular redox homeostasis in tomato 
Journal of Experimental Botany  2014;65(15):4335-4347.
Virus-induced gene silencing (VIGS) was used in this study to characterize the role of thioredoxin-f and thioredoxin-m1/4 in brassinosteroid-induced changes in CO2 assimilation and cellular redox homeostasis in tomato.
Chloroplast thioredoxins (TRXs) and glutathione function as redox messengers in the regulation of photosynthesis. In this work, the roles of chloroplast TRXs in brassinosteroids (BRs)-induced changes in cellular redox homeostasis and CO2 assimilation were studied in the leaves of tomato plants. BRs-deficient d ^im plants showed decreased transcripts of TRX-f, TRX-m2, TRX-m1/4, and TRX-x, while exogenous BRs significantly induced CO2 assimilation and the expression of TRX-f, TRX-m2, TRX-m1/4, and TRX-x. Virus-induced gene silencing (VIGS) of the chloroplast TRX-f, TRX-m2, TRX-m1/4, and TRX-y genes individually increased membrane lipid peroxidation and accumulation of 2-Cys peroxiredoxin dimers, and decreased the activities of the ascorbate–glutathione cycle enzymes and the ratio of reduced glutathione to oxidized glutathione (GSH/GSSG) in the leaves. Furthermore, partial silencing of TRX-f, TRX-m2, TRX-m1/4, and TRX-y resulted in decreased expression of genes involved in the Benson–Calvin cycle and decreased activity of the associated enzymes. Importantly, the BRs-induced increase in CO2 assimilation and the increased expression and activities of antioxidant- and photosynthesis-related genes and enzymes were compromised in the partially TRX-f- and TRX-m1/4-silenced plants. All of these results suggest that TRX-f and TRX-m1/4 are involved in the BRs-induced changes in CO2 assimilation and cellular redox homeostasis in tomato.
PMCID: PMC4112637  PMID: 24847092
Antioxidant; Benson–Calvin cycle; chloroplast; 2-Cys peroxiredoxin; glutathione; photosynthesis.
3.  RBOH1-dependent H2O2 production and subsequent activation of MPK1/2 play an important role in acclimation-induced cross-tolerance in tomato 
Journal of Experimental Botany  2013;65(2):595-607.
H2O2 and mitogen-activated protein kinase (MAPK) cascades play important functions in plant stress responses, but their roles in acclimation response remain unclear. This study examined the functions of H2O2 and MPK1/2 in acclimation-induced cross-tolerance in tomato plants. Mild cold, paraquat, and drought as acclimation stimuli enhanced tolerance to more severe subsequent chilling, photooxidative, and drought stresses. Acclimation-induced cross-tolerance was associated with increased transcript levels of RBOH1 and stress- and defence-related genes, elevated apoplastic H2O2 accumulation, increased activity of NADPH oxidase and antioxidant enzymes, reduced glutathione redox state, and activation of MPK1/2 in tomato. Virus-induced gene silencing of RBOH1, MPK1, and MPK2 or MPK1/2 all compromised acclimation-induced cross-tolerance and associated stress responses. Taken together, these results strongly suggest that acclimation-induced cross-tolerance is largely attributed to RBOH1-dependent H2O2 production at the apoplast, which may subsequently activate MPK1/2 to induce stress responses.
PMCID: PMC3904713  PMID: 24323505
Cross-tolerance; hydrogen peroxide; mitogen-activated protein kinase; reactive oxygen species; Respiratory burst oxidase homologue 1; signal transduction; Solanum lycopersicum.
4.  The Role of Hydrogen Peroxide and Nitric Oxide in the Induction of Plant-Encoded RNA-Dependent RNA Polymerase 1 in the Basal Defense against Tobacco Mosaic Virus 
PLoS ONE  2013;8(9):e76090.
Plant RNA-dependent RNA Polymerase 1 (RDR1) is an important element of the RNA silencing pathway in the plant defense against viruses. RDR1 expression can be elicited by viral infection and salicylic acid (SA), but the mechanisms of signaling during this process remains undefined. The involvement of hydrogen peroxide (H2O2) and nitric oxide (NO) in RDR1 induction in the compatible interactions between Tobacco mosaic tobamovirus (TMV) and Nicotiana tabacum, Nicotiana benthamiana, and Arabidopsis thaliana was examined. TMV inoculation onto the lower leaves of N. tabacum induced the rapid accumulation of H2O2 and NO followed by the increased accumulation of RDR1 transcripts in the non-inoculated upper leaves. Pretreatment with exogenous H2O2 and NO on upper leaf led to increased RDR1 expression and systemic TMV resistance. Conversely, dimethylthiourea (an H2O2 scavenger) and 2-(4-carboxyphenyl)- 4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (an NO scavenger) partly blocked TMV- and SA-induced RDR1 expression and increased TMV susceptibility, whereas pretreatment with exogenous H2O2 and NO failed to diminish TMV infection in N. benthamiana plants with naturally occurring RDR1 loss-of-function. Furthermore, in N. tabacum and A. thaliana, TMV-induced H2O2 accumulation was NO-dependent, whereas NO generation was not affected by H2O2. These results suggest that, in response to TMV infection, H2O2 acts downstream of NO to mediate induction of RDR1, which plays a critical role in strengthening RNA silencing to restrict systemic viral infection.
PMCID: PMC3786905  PMID: 24098767
5.  Hydrogen peroxide functions as a secondary messenger for brassinosteroids-induced CO2 assimilation and carbohydrate metabolism in Cucumis sativus *  
Brassinosteroids (BRs) are potent regulators of photosynthesis and crop yield in agricultural crops; however, the mechanism by which BRs increase photosynthesis is not fully understood. Here, we show that foliar application of 24-epibrassinolide (EBR) resulted in increases in CO2 assimilation, hydrogen peroxide (H2O2) accumulation, and leaf area in cucumber. H2O2 treatment induced increases in CO2 assimilation whilst inhibition of the H2O2 accumulation by its generation inhibitor or scavenger completely abolished EBR-induced CO2 assimilation. Increases of light harvesting due to larger leaf areas in EBR- and H2O2-treated plants were accompanied by increases in the photochemical efficiency of photosystem II (ΦPSII) and photochemical quenching coefficient (q P). EBR and H2O2 both activated carboxylation efficiency of ribulose-1,5-bisphosphate oxygenase/carboxylase (Rubisco) from analysis of CO2 response curve and in vitro measurement of Rubisco activities. Moreover, EBR and H2O2 increased contents of total soluble sugar, sucrose, hexose, and starch, followed by enhanced activities of sugar metabolism such as sucrose phosphate synthase, sucrose synthase, and invertase. Interestingly, expression of transcripts of enzymes involved in starch and sugar utilization were inhibited by EBR and H2O2. However, the effects of EBR on carbohydrate metabolisms were reversed by the H2O2 generation inhibitor diphenyleneodonium (DPI) or scavenger dimethylthiourea (DMTU) pretreatment. All of these results indicate that H2O2 functions as a secondary messenger for EBR-induced CO2 assimilation and carbohydrate metabolism in cucumber plants. Our study confirms that H2O2 mediates the regulation of photosynthesis by BRs and suggests that EBR and H2O2 regulate Calvin cycle and sugar metabolism via redox signaling and thus increase the photosynthetic potential and yield of crops.
PMCID: PMC3468824  PMID: 23024048
Metabolism; Photosynthesis; Reactive oxygen species; Rubisco; Sucrose
6.  Effects of nitrogen form on growth, CO2 assimilation, chlorophyll fluorescence, and photosynthetic electron allocation in cucumber and rice plants*  
Cucumber and rice plants with varying ammonium (NH4 +) sensitivities were used to examine the effects of different nitrogen (N) sources on gas exchange, chlorophyll (Chl) fluorescence quenching, and photosynthetic electron allocation. Compared to nitrate (NO3 −)-grown plants, cucumber plants grown under NH4 +-nutrition showed decreased plant growth, net photosynthetic rate, stomatal conductance, intercellular carbon dioxide (CO2) level, transpiration rate, maximum photochemical efficiency of photosystem II, and O2-independent alternative electron flux, and increased O2-dependent alternative electron flux. However, the N source had little effect on gas exchange, Chl a fluorescence parameters, and photosynthetic electron allocation in rice plants, except that NH4 +-grown plants had a higher O2-independent alternative electron flux than NO3 −-grown plants. NO3 − reduction activity was rarely detected in leaves of NH4 +-grown cucumber plants, but was high in NH4 +-grown rice plants. These results demonstrate that significant amounts of photosynthetic electron transport were coupled to NO3 − assimilation, an effect more significant in NO3 −-grown plants than in NH4 +-grown plants. Meanwhile, NH4 +-tolerant plants exhibited a higher demand for the reduced form of nicotinamide adenine dinucleotide phosphate (NADPH) for NO3 − reduction, regardless of the N form supplied, while NH4 +-sensitive plants had a high water-water cycle activity when NH4 + was supplied as the sole N source.
PMCID: PMC3030957  PMID: 21265044
Nitrogen form; Photosynthetic electron allocation; Alternative electron flux; Nitrate reductase

Results 1-6 (6)