Hydrogen sulfide enhances rice tolerance to nickel through the prevention of chloroplast damage and the improvement of nitrogen metabolism under excessive nickel

Muhammad Rizwan; Mohammad Golam Mostofa; Muhammad Zulfiqar Ahmad; Yaoyu Zhou; Muhammad Adeel; Sajid Mehmood; Muhammad Arslan Ahmad; Rabia Javed; Muhammad Imtiaz; Omar Aziz; Muhammad Ikram; Shuxin Tu; Yongxian Liu

doi:10.1016/j.plaphy.2019.02.023

Hydrogen sulfide enhances rice tolerance to nickel through the prevention of chloroplast damage and the improvement of nitrogen metabolism under excessive nickel

Plant Physiol Biochem. 2019 May:138:100-111. doi: 10.1016/j.plaphy.2019.02.023. Epub 2019 Mar 2.

Authors

Affiliations

¹ Microelement Research Center, College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, China; Hubei Collaborative Innovation Center for Grain Industry, Jingzhou, 434023, China.
² Department of Biochemistry and Molecular Biology, Bangabandhu Sheikh Mujibur Rahman Agricultural University, Gazipur, 1706, Bangladesh.
³ Department of Plant Breeding & Genetics, Faculty of Agriculture, Gomal University, Dera Ismail Khan, K.P, Pakistan.
⁴ College of Resources and Environment, Hunan Agricultural University, Changsha, 410128, China.
⁵ Beijing Key Laboratory of Farmland Soil Pollution Prevention and Remediation, College of Resources and Environmental Sciences, China Agricultural University, Beijing, 100193, China.
⁶ School of Civil Engineering, Guangzhou University, Guangzhou, 51006, PR China.
⁷ Key Lab of Eco-restoration of Regional Contaminated Environment (Shenyang University), Ministry of Education, Shenyang, 11044, China.
⁸ Department of Multidisciplinary Studies, National University of Medical Sciences, Rawalpindi, 46000, Pakistan.
⁹ Microelement Research Center, College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, China.
¹⁰ Statistical Genomics Lab, College of Plant Science and Technology, Huazhong Agricultural University, Wuhan, 430070, China.
¹¹ Microelement Research Center, College of Resources and Environment, Huazhong Agricultural University, Wuhan, 430070, China; Hubei Collaborative Innovation Center for Grain Industry, Jingzhou, 434023, China. Electronic address: stu@mail.hzau.edu.cn.
¹² Guangxi Academy of Agricultural Sciences, Nanning, 530007, China.

PMID: 30856414
DOI: 10.1016/j.plaphy.2019.02.023

Abstract

Hydrogen sulfide (H₂S) modulates plant tolerance to abiotic stresses, but its regulatory effects on nitrogen metabolism and chloroplast protection under nickel (Ni) stress in crop plants remain elusive. Taking this into account, we investigated the potential roles of sodium hydrosulfide (NaHS), a H₂S generator, in the improvement of growth performance of rice plants under Ni stress. Results showed that NaHS successfully reversed the adverse effects of Ni, as reflected in plant growth and biomass, and photosynthesis attributes including photosynthetic rates, stomatal conductance, transpiration rate, internal CO₂ concentration and photosynthetic pigment contents. NaHS generated H₂S plays a crucial role in controlling the photosynthetic machinery of rice as evidenced by the ultrastructure of chloroplast viewed under transmission electron microscope (TEM). The reduced content of Ni in roots and leaves of NaHS-supplemented Ni-stressed plants has revealed the restricted uptake and accumulation of Ni. A rescue of NaHS to the Ni-induced decline in nitrate (NO₃^-) content and the activities NO₃^- biosynthesizing enzymes nitrate reductase, nitrite reductase, glutamate synthase, glutamate oxaloacetate transaminase, glutamine synthetase, and glutamate pyruvate transaminase in leaves indicated a positive role of H₂S on NO₃^- metabolism in rice under Ni stress. NaHS application also reverted Ni-mediated increases in ammonium (NH₄⁺) content and glutamate dehydrogenase activity, implying H₂S-induced alleviation of NH₄⁺ toxicity. The regulatory effects of H₂S on nitrogen metabolism was further confirmed by increased and decreased transcript abundance of NO₃^- and NH₄⁺ metabolism associated genes, respectively. Our study suggests a decisive role of H₂S in controlling Ni toxicity as elucidated by the novel findings such as enhanced gas exchanged parameters, Ni homeostasis and chloroplast protection. Moreover, this article highlights the significance of H₂S in controlling chloroplast biogenesis and nitrogen metabolism in rice crop under Ni stress.

Keywords: Chloroplast; Genes expressions; Hydrogen sulfide; Nickel toxicity; Nitrogen metabolism; Photosynthesis; Rice.

MeSH terms

Chloroplast Proteins / biosynthesis
Chloroplasts / metabolism*
Hydrogen Sulfide / pharmacology*
Nickel / toxicity*
Nitrogen / metabolism*
Oryza / growth & development*

Substances

Chloroplast Proteins
Nickel
Nitrogen
Hydrogen Sulfide