Nitric Oxide and Its Interaction with Hydrogen Peroxide Enhance Plant Tolerance to Low Temperatures by Improving the Eff

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Nitric Oxide and Its Interaction with Hydrogen Peroxide Enhance Plant Tolerance to Low Temperatures by Improving the Efficiency of the Calvin Cycle and the Ascorbate–Glutathione Cycle in Cucumber Seedlings Pei Wu1,2 · Chunyan Xiao1,2 · Jinxia Cui1,2 · Baoyu Hao1,2 · Wenbo Zhang1,2 · Zhifeng Yang1,2 · Golam Jalal Ahammed3 · Huiying Liu1,2 · Huimei Cui1,2 Received: 1 August 2020 / Accepted: 2 October 2020 © Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract The present study was aimed to assess the effect of nitric oxide (NO) and the interaction of NO with hydrogen peroxide ­(H2O2) on plant tolerance to low temperatures in cucumber seedlings. Exogenous NO significantly increased the endogenous NO content, initial and total activities of ribulose-1,5-bisphosphate carboxylase/oxygenase (RuBisCO), RuBisCO carboxylation rate (Vc,max), RuBP regeneration rate (Jmax) and the transcript levels of related genes in cucumber seedlings under low temperatures (11 °C/7 °C); however, the effect of NO was blocked by PTIO (NO scavenger). In addition, the SNP treatment significantly improved the contents of glucose, fructose, sucrose, starch, and the activities of sucrose phosphate synthase (SPS), acid invertase (AI), sucrose synthase (SS), as well as the expression levels of SUCROSE PHOSPHATE SYNTHASE 1&2 (SPS1, SPS2), SUCROSE TRANSPORTER 1&2 (SUT2, SUT4), β-starch hydrolase (BAM), and invertase gene (INVERTASE) in cucumber leaves under low temperatures, and the positive effect of NO was impaired by PTIO. Furthermore, we found that the ­H2O2, induced by NO, participated in NO-induced elevation of ascorbic acid (AsA), glutathione (GSH), and increased activities of related enzymes in the AsA-GSH cycle at low temperatures. However, the positive effect of NO was blocked by l-NAME (NOS inhibitor), PTIO, DPI (inhibitor of NADPH oxidase), and DMTU (reactive oxygen species scavenger). Taken together, our findings indicate that NO increased the low temperature tolerance of cucumber seedlings via ­H2O2 by improving the efficiency of the Calvin cycle, which in turn increased the carbohydrates content and accelerated the AsA-GSH cycle to enhance ROS scavenging. Keywords  Cucumber · Low temperature · Nitric oxide · Sucrose · Calvin cycle · Ascorbate–glutathione

Introduction

Pei Wu and Chunyan Xiao contributed equally to this study. * Jinxia Cui [email protected] 1



Department of Horticulture, Agricultural College, Shihezi University, Shihezi 832000, Xinjiang, PR China

2



Key Laboratory of Special Fruits and Vegetables Cultivation Physiology and Germplasm Resources Utilization of Xinjiang Production and Construction Crops, Shihezi 832000, Xinjiang, PR China

3

College of Forestry, Henan University of Science and Technology, Luoyang 471023, PR China



Most tropical and subtropical plant species lack the ability to cope with low temperatures and are typically injured by temperatures below 15 °C. Cucumber (Cucumis sativus L.) is a typical subtropical plant, which is susceptible to low temperature stress, partic