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Interplay between hydrogen sulfide and methylglyoxal initiates thermotolerance in maize seedlings by modulating reactive oxidative species and osmolyte metabolism

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Abstract

Hydrogen sulfide (H2S) and methylglyoxal (MG) were supposed to be novel signaling molecules in plants. However, whether interplay between H2S and MG can initiate thermotolerance in maize seedlings and in relation to metabolism of reactive oxygen species (ROS) and osmolytes is little known. In this study, watering with MG and NaHS (H2S donor) alone or in combination elevated survival and tissue vigor of maize seedlings under heat stress and coped with an increase in the biomembrane injury (as indicated in membrane lipid peroxidation and electrolyte leakage). The above-mentioned effects were separately weakened by MG scavengers (N-acetyl cysteine: NAC; aminoguanidine: AG) and H2S inhibitor (DL-propargylglycine, PAG) and scavenger (hypotaurine, HT). These suggested that the interplay between H2S and MG initiated the thermotolerance in maize seedlings. The further data indicated that, under non-heat stress and heat stress conditions, MG and NaHS alone or in combination modulated ROS metabolism by regulating the activities of antioxidant enzymes (catalase, ascorbate peroxidase, guaiacol peroxidase, glutathione reductase, monodehydroascorbate reductase, and dehydroascorbate reductase) and the contents of non-enzymatic antioxidants (ascorbic acid, glutathione, flavonoids, and carotenoids) in maize seedlings. In addition, MG and NaHS alone or in combination also separately modulated the metabolism of osmolytes (proline, trehalose, glycine betaine, and total soluble sugar), H2S (L-cysteine desulfhydrase and O-acetylserine (thione) lyase), and MG (glyoxalase I, glyoxalase II, and MG reductase). These physiological effects also were separately impaired by NAC, AG, PAG, and HT. The current data illustrated that the interplay between H2S and MG initiated the thermotolerance in maize seedlings by modulating ROS, osmolyte, H2S, and MG metabolism.

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Funding

This work is funded by National Natural Science Foundation of China (31760069, 31360057).

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Author notes

  1. Xin-Yu Ye and Xue-Mei Qiu contributed equally to this work.

Authors and Affiliations

  1. School of Life Sciences, Yunnan Normal University, Kunming, 650092, People’s Republic of China

    Xin-Yu Ye, Xue-Mei Qiu, Yu-Ying Sun & Zhong-Guang Li

  2. Engineering Research Center of Sustainable Development and Utilization of Biomass Energy, Ministry of Education, Kunming, 650092, People’s Republic of China

    Xin-Yu Ye, Xue-Mei Qiu, Yu-Ying Sun & Zhong-Guang Li

  3. Key Laboratory of Biomass Energy and Environmental Biotechnology, Yunnan Normal University, Kunming, 650092, Yunnan Province, People’s Republic of China

    Xin-Yu Ye, Xue-Mei Qiu, Yu-Ying Sun & Zhong-Guang Li

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  1. Xin-Yu Ye
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  2. Xue-Mei Qiu
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ZGL conceived and designed experiments and wrote manuscript, XYY performed experiments and wrote manuscript, XMQ and YYS assisted the whole experiment process. All authors have approved the final version of the manuscript.

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Correspondence to Zhong-Guang Li.

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Ye, XY., Qiu, XM., Sun, YY. et al. Interplay between hydrogen sulfide and methylglyoxal initiates thermotolerance in maize seedlings by modulating reactive oxidative species and osmolyte metabolism. Protoplasma 257, 1415–1432 (2020). https://doi.org/10.1007/s00709-020-01516-x

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