A Novel Gene, <i>OZONE-RESPONSIVE APOPLASTIC PROTEIN1</i>, Enhances Cell Death in Ozone Stress in Rice

Ueda, Yoshiaki; Siddique, Shahid; Frei, Michael

doi:10.1104/pp.15.00956

Cited by 47 publications

(42 citation statements)

References 99 publications

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“…This principle was confirmed in a study by Ueda, Frimpong et al. () and Ueda, Siddique, and Frei (), in which more than 300 genotypes of rice were screened for ozone response, and yield losses were positively correlated with the number of days to maturity. In general, breeding fast‐maturing crop varieties may produce substantial synergies, reducing the impacts of growing seasons characterized by high incidence of other stresses, such as drought, heat, nutrient or biotic stresses.…”

Section: Resultsmentioning

confidence: 54%

“…Breeding for ozone tolerance could thus keep plants from inducing PCD despite the presence of apoplastic ROS. This idea is supported by a study in rice, in which the disruption of the pathogen and ozone responsive apoplastic protein OsORAP1 , which is involved in cell death, led to enhanced ozone tolerance (Ueda, Frimpong et al., ; Ueda, Siddique, & Frei, ). The potential interference of this strategy with pathogen tolerance in crops is obvious, but it is currently unclear whether a synergistic or rather antagonistic relationship would occur with different classes of pathogens, that is biotrophic vs. necrotrophic ones (Huysmans et al., ).…”

Section: Resultsmentioning

confidence: 89%

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Closing the global ozone yield gap: Quantification and cobenefits for multistress tolerance

Mills

Sharps

Simpson

et al. 2018

Global Change Biology

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191

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Increasing both crop productivity and the tolerance of crops to abiotic and biotic stresses is a major challenge for global food security in our rapidly changing climate. For the first time, we show how the spatial variation and severity of tropospheric ozone effects on yield compare with effects of other stresses on a global scale, and discuss mitigating actions against the negative effects of ozone. We show that the sensitivity to ozone declines in the order soybean > wheat > maize > rice, with genotypic variation in response being most pronounced for soybean and rice. Based on stomatal uptake, we estimate that ozone (mean of 2010-2012) reduces global yield annually by 12.4%, 7.1%, 4.4% and 6.1% for soybean, wheat, rice and maize, respectively (the "ozone yield gaps"), adding up to 227 Tg of lost yield. Our modelling shows that the highest ozone-induced production losses for soybean are in North and South America whilst for wheat they are in India and China, for rice in parts of India, Bangladesh, China and Indonesia, and for maize in China and the United States. Crucially, we also show that the same areas are often also at risk of high losses from pests and diseases, heat stress and to a lesser extent aridity and nutrient stress. In a solution-focussed analysis of these results, we provide a crop ideotype with tolerance of multiple stresses (including ozone) and describe how ozone effects could be included in crop breeding programmes. We also discuss altered crop management approaches that could be applied to reduce ozone impacts in the shorter term. Given the severity of ozone effects on staple food crops in areas of the world that are also challenged by other stresses, we recommend increased attention to the benefits that could be gained from addressing the ozone yield gap.

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Section: Resultsmentioning

confidence: 54%

Section: Resultsmentioning

confidence: 89%

Closing the global ozone yield gap: Quantification and cobenefits for multistress tolerance

Mills

Sharps

Simpson

et al. 2018

Global Change Biology

Self Cite

191

142

View full text Add to dashboard Cite

show abstract

“…However, it is important to note that the action of AO gene products may extend beyond the effects exerted through direct changes in AO activity. For example, the expression of the rice (Oryza sativa) AO protein, OsORAP1, which is localized in the apoplast but has no AO activity, enhances cell death in leaves exposed to ozone or pathogens (Ueda et al, 2015). OsORAP1, whose expression was highest in photosynthetic tissues with the highest stomatal conductance, influences JA pathway signaling to mitigate ozone symptoms by unknown mechanisms (Ueda et al, 2015).…”

Section: Discussionmentioning

confidence: 99%

Redox Control of Aphid Resistance through Altered Cell Wall Composition and Nutritional Quality

et al. 2017

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The mechanisms underpinning plant perception of phloem-feeding insects, particularly aphids, remain poorly characterized. Therefore, the role of apoplastic redox state in controlling aphid infestation was explored using transgenic tobacco (Nicotiana tabacum) plants that have either high (PAO) or low (TAO) ascorbate oxidase (AO) activities relative to the wild type. Only a small number of leaf transcripts and metabolites were changed in response to genotype, and cell wall composition was largely unaffected. Aphid fecundity was decreased significantly in TAO plants compared with other lines. Leaf sugar levels were increased and maximum extractable AO activities were decreased in response to aphids in all genotypes. Transcripts encoding the Respiratory Burst Oxidase Homolog F, signaling components involved in ethylene and other hormonemediated pathways, photosynthetic electron transport components, sugar, amino acid, and cell wall metabolism, were increased significantly in the TAO plants in response to aphid perception relative to other lines. The levels of galactosylated xyloglucan were decreased significantly in response to aphid feeding in all the lines, the effect being the least in the TAO plants. Similarly, all lines exhibited increases in tightly bound (1→4)-b-galactan. Taken together, these findings identify AO-dependent mechanisms that limit aphid infestation.

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“…Ascorbate oxidases regulate the redox state of apoplastic ascorbate by oxidizing ascorbate to monodehydroascorbate without generating ROS (Pignocchi and Foyer, 2003). However, not all proteins encoded by genes annotated as ascorbate oxidase have ascorbate oxidase activity (Ueda et al, 2015), and further studies are needed to resolve the function of the proteins encoded by these genes in spruce. GC-MS analysis additionally indicated altered ascorbate metabolism, with tartaric acid (a precursor for ascorbate biosynthesis) as well as oxalic acid and threonic acid (ascorbate breakdown products) belonging to the most discriminating metabolites between lignin-forming and non-lignin-forming cell cultures (Supplemental Fig.…”

Section: Discussionmentioning

confidence: 99%

A Key Role for Apoplastic H₂O₂ in Norway Spruce Phenolic Metabolism

et al. 2017

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Apoplastic events such as monolignol oxidation and lignin polymerization are difficult to study in intact trees. To investigate the role of apoplastic hydrogen peroxide (H 2 O 2 ) in gymnosperm phenolic metabolism, an extracellular lignin-forming cell culture of Norway spruce (Picea abies) was used as a research model. Scavenging of apoplastic H 2 O 2 by potassium iodide repressed lignin formation, in line with peroxidases activating monolignols for lignin polymerization. Time-course analyses coupled to candidate substrate-product pair network propagation revealed differential accumulation of low-molecular-weight phenolics, including (glycosylated) oligolignols, (glycosylated) flavonoids, and proanthocyanidins, in lignin-forming and H 2 O 2 -scavenging cultures and supported that monolignols are oxidatively coupled not only in the cell wall but also in the cytoplasm, where they are coupled to other monolignols and proanthocyanidins. Dilignol glycoconjugates with reduced structures were found in the culture medium, suggesting that cells are able to transport glycosylated dilignols to the apoplast. Transcriptomic analyses revealed that scavenging of apoplastic H 2 O 2 resulted in remodulation of the transcriptome, with reduced carbon flux into the shikimate pathway propagating down to monolignol biosynthesis. Aggregated coexpression network analysis identified candidate enzymes and transcription factors for monolignol oxidation and apoplastic H 2 O 2 production in addition to potential H 2 O 2 receptors. The results presented indicate that the redox state of the apoplast has a profound influence on cellular metabolism.

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A Novel Gene, OZONE-RESPONSIVE APOPLASTIC PROTEIN1, Enhances Cell Death in Ozone Stress in Rice

Cited by 47 publications

References 99 publications

Closing the global ozone yield gap: Quantification and cobenefits for multistress tolerance

Closing the global ozone yield gap: Quantification and cobenefits for multistress tolerance

Redox Control of Aphid Resistance through Altered Cell Wall Composition and Nutritional Quality

A Key Role for Apoplastic H₂O₂ in Norway Spruce Phenolic Metabolism

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A Novel Gene, OZONE-RESPONSIVE APOPLASTIC PROTEIN1, Enhances Cell Death in Ozone Stress in Rice

Cited by 47 publications

References 99 publications

Closing the global ozone yield gap: Quantification and cobenefits for multistress tolerance

Closing the global ozone yield gap: Quantification and cobenefits for multistress tolerance

Redox Control of Aphid Resistance through Altered Cell Wall Composition and Nutritional Quality

A Key Role for Apoplastic H2O2 in Norway Spruce Phenolic Metabolism

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Product

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A Key Role for Apoplastic H₂O₂ in Norway Spruce Phenolic Metabolism