A comparative analysis of transcriptomic, biochemical, and physiological responses to elevated ozone identifies species-specific mechanisms of resilience in legume crops

Yendrek, Craig R.; Koester, Robert P.; Ainsworth, Elizabeth A.

doi:10.1093/jxb/erv404

Cited by 49 publications

(40 citation statements)

References 82 publications

(94 reference statements)

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“…Similar effects of O 3 stress on central metabolism have been reported previously: changes in the activity and expression of genes and pathways involved in detoxification and redox balance (e.g. the aldehyde dehydrogenase ALDH, chloroplastic superoxide dismutase activity, and NADH regeneration) were linked to stomatal closure, decreased photosynthetic activity, and increased mitochondrial respiration Yendrek et al, 2015). However, when herbivory was applied as a second stress, all these initial effects of O 3 stress were reversed, resulting in decreased levels of sugars and amino acids and a reconfiguration of gene expression, including down-regulation of the amino acid transporter AAP2, which promotes nitrogen accumulation in siliques and seed development in Arabidopsis (Hirner et al, 1998;Ortiz-Lopez et al, 2000).…”

Section: O 3 and Herbivory Affect Central Metabolism In Opposite Wayssupporting

confidence: 82%

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

et al. 2016

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Plants have evolved adaptive mechanisms that allow them to tolerate a continuous range of abiotic and biotic stressors. Tropospheric ozone (O 3 ), a global anthropogenic pollutant, directly affects living organisms and ecosystems, including plant-herbivore interactions. In this study, we investigate the stress responses of Brassica nigra (wild black mustard) exposed consecutively to O 3 and the specialist herbivore Pieris brassicae. Transcriptomics and metabolomics data were evaluated using multivariate, correlation, and network analyses for the O 3 and herbivory responses. O 3 stress symptoms resembled those of senescence and phosphate starvation, while a sequential shift from O 3 to herbivory induced characteristic plant defense responses, including a decrease in central metabolism, induction of the jasmonic acid/ethylene pathways, and emission of volatiles. Omics network and pathway analyses predicted a link between glycerol and central energy metabolism that influences the osmotic stress response and stomatal closure. Further physiological measurements confirmed that while O 3 stress inhibited photosynthesis and carbon assimilation, sequential herbivory counteracted the initial responses induced by O 3 , resulting in a phenotype similar to that observed after herbivory alone. This study clarifies the consequences of multiple stress interactions on a plant metabolic system and also illustrates how omics data can be integrated to generate new hypotheses in ecology and plant physiology.

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Section: O 3 and Herbivory Affect Central Metabolism In Opposite Wayssupporting

confidence: 82%

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

et al. 2016

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“…Thus, balancing the interplay of redox homeostasis and PCD pathways is essential for the breeding of ozone‐tolerant crop plants. As a first line of defence against ozone stress, high levels of apoplastic antioxidants such as ascorbate may mitigate ROS formation, a concept that has been confirmed in crop plants such as wheat (Feng, Pang et al., ) and legumes (Yendrek, Koester, & Ainsworth, ). Breeding for high levels of antioxidants is also assumed to cause synergies with other types of abiotic stress tolerance, including for drought and heat, both of which are associated with oxidative stress (Gill & Tuteja, ).…”

Section: Resultsmentioning

confidence: 94%

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

Mills

Sharps

Simpson

et al. 2018

Global Change Biology

187

142

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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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“…; Yendrek et al . ). A recent study in strawberry ( Fragaria × ananassa ) investigating plant responses after treatment with different low, medium and high doses of CO (133–533 ppb), NO x and SO 2 (0.05–0.20 ppm) showed that prolonged exposure to the pollutants resulted in continuous ROS production in leaves, with a negative effect on stomatal closure and photosynthesis (Muneer et al .…”

Section: Plant Physiological and Molecular Responses To Combinations mentioning

confidence: 97%

“…In a recent study on different varieties of legume, Yendrek et al . () combined physiological screening with transcriptomic and metabolic analyses, showing that while O 3 reduced leaf growth and sugar content, it increased the expression of transcripts associated with cellular respiration and GR activity, thus simultaneously inducing higher levels of antioxidant metabolites such as GSH and ascorbic acid (Yendrek et al . ).…”

Section: Plant Physiological and Molecular Responses To Combinations mentioning

confidence: 99%

Dynamics of plant responses to combinations of air pollutants

Papazian

Blande

2019

Plant Biol J

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The focus of this review is on how plants respond to combinations of multiple air pollutants. Global pollution trends, plant physiological responses and ecological perspectives in natural and agricultural systems are all discussed. In particular, we highlight the importance of studying sequential or simultaneous exposure of plants to pollutants, rather than exposure to individual pollutants in isolation, and explore how these responses may interfere with the way plants interact with their biotic community. Air pollutants can alter the normal physiology and metabolic functioning of plants. Here we describe how the phenotypic and molecular changes in response to multiple pollutants can differ compared to those elicited by single pollutants, and how different responses have been observed between plants in the field and in controlled laboratory conditions and between trees and crop plants. From an ecological perspective, we discuss how air pollution can result in greater susceptibility to biotic stressors and in direct or indirect effects on interactions with organisms that occupy higher trophic levels. Finally, we provide an overview of the potential uses of plants to mitigate air pollution, exploring the feasibility for pollution removal via the processes of bio-accumulation and phytoremediation. We conclude by proposing some new directions for future research in the field.

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A comparative analysis of transcriptomic, biochemical, and physiological responses to elevated ozone identifies species-specific mechanisms of resilience in legume crops

Abstract: HighlightPhotosynthesis and leaf longevity were unaffected by growth in elevated [O3] in pea. Resilience to elevated [O3] was supported by transcriptional and biochemical metabolism associated with detoxification and antioxidant metabolism.

Cited by 49 publications

References 82 publications

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

Central Metabolic Responses to Ozone and Herbivory Affect Photosynthesis and Stomatal Closure

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

Dynamics of plant responses to combinations of air pollutants

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