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Zebra chip disease enhances respiration and oxidative stress of potato tubers (Solanum tuberosum L.)

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Abstract

Main conclusion

The physiological phenotype of potato tubers afflicted by zebra chip disease is characterized by increased oxidative stress metabolism and upregulation of systems for its mitigation.

Starch catabolism and extensive buildup of reducing sugars render potatoes infected with zebra chip (ZC) pathogen (Candidatus Liberibacter solanacearum) unsuitable for fresh market and processing into chips/fries. Here we show that the disease inflicts considerable oxidative stress, which likely constitutes a substantial sink for metabolic energy, resulting in increased respiration rate of afflicted tubers. In contrast to healthy tubers, tissue from diseased tubers had greater ability to reduce 2,3,5-triphenyl-tetrazolium chloride to formazan, indicating enhanced dehydrogenase activity, probable disease-induced changes in cellular redox potential, and increased respiratory activity. The respiration rate of diseased tubers (cv. Atlantic) was 2.4-fold higher than healthy tubers and this correlated with increased activities of glucose-6-phosphate and 6-phosphogluconate dehydrogenases, key enzymes responsible for synthesis of cytosolic reducing equivalents. Wound-induced NADPH oxidase activity was greater for ZC than healthy tubers, but the resulting superoxide was rapidly catabolized by higher superoxide dismutase activity in ZC tubers. Peroxidase, catalase, glutathione reductase and ascorbate free radical reductase activities were also higher in diseased tubers, as was malondialdehyde, a biomarker of peroxidative damage and oxidative stress. Upregulation of the glutathione–ascorbate pathway is a direct response to (and indicator of) oxidative stress, which consumes reducing equivalents (NADPH) to catabolize reactive oxygen species and maintain cellular redox homeostasis. ZC disease substantially altered the oxidative metabolism of tubers, resulting in a physiological phenotype defined by metabolic changes directed toward mitigating oxidative stress. Paradoxically, the increased respiration rate of ZC tubers, which fuels the metabolic pathways responsible for attenuating oxidative stress, likely also contributes to oxidative stress.

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Abbreviations

AFR:

Ascorbate free radical reductase

ANOVA:

Analysis of variance

AsA:

Ascorbic acid

CAT:

Catalase

CLso:

Candidatus Liberibacter solanacearum

DPI:

Diphenylene iodonium chloride

G6PDH:

Glucose-6-phosphate dehydrogenase

6PGDH:

6-Phosphogluconate dehydrogenase

GSH:

Reduced glutathione

GSSG:

Oxidized glutathione

MDA:

Malondialdehyde

NBT:

Nitroblue tetrazolium

NOX:

NADPH oxidase

POX:

Peroxidase

PPP:

Pentose phosphate pathway

SOD:

Superoxide dismutase

rboh:

Respiratory burst oxidase homologue

ROS:

Reactive oxygen species

SP:

Starch phosphorylase (α-1,4-glucan phosphorylase)

TTC:

2,3,5-Tetrazolium chloride

ZC:

Zebra chip

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Acknowledgements

We thank Dr. Joseph E. Munyaneza (National Program Leader, USDA-ARS, Beltsville, MD, USA) for providing CLso-infected tuber samples. Financial support was provided by the USDA-ARS, Washington State Potato Commission, and Washington State University Agricultural Research Center to N. R. Knowles.

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  1. Postharvest Physiology and Biochemistry Laboratory, Department of Horticulture, Washington State University, P.O. Box 646414, Pullman, WA, 99164-6414, USA

    G. N. Mohan Kumar, Lisa O. Knowles & N. Richard Knowles

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  1. G. N. Mohan Kumar
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Correspondence to G. N. Mohan Kumar or N. Richard Knowles.

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Kumar, G.N.M., Knowles, L.O. & Knowles, N.R. Zebra chip disease enhances respiration and oxidative stress of potato tubers (Solanum tuberosum L.). Planta 246, 625–639 (2017). https://doi.org/10.1007/s00425-017-2714-8

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