Key role of reactive oxygen species-scavenging system in nitric oxide and hydrogen sulfide crosstalk-evoked thermotolerance in maize seedlings

Abstract

Nitric oxide (NO) and hydrogen sulfide (H2S) are novel signaling molecules, which participate in plant growth, development, and response to stress. In this study root-irrigation with 0.15 mM sodium nitroprusside (SNP, NO donor) up-regulated gene expression of L-CYSTEINE DESULFHYDRASE1 (LCD1), activities of L-cysteine desulfhydrase (LCD) and D-cysteine desulfhydrase (DCD), as well as an endogenous H2S level, compared to control seedlings. The SNP-up-regulated effects were enhanced by 0.5 mM sodium hydrosulfide (NaHS, H2S donor), but weakened by NO scavenger 2-(4-carboxyphenyl)-4,4,5,5-tetramethylimidazoline-1-oxyl-3-oxide (cPTIO) and H2S scavenger hypotaurine (HT) alone. NaHS had no significant effect on gene expression and activity of nitrate reductase (NR, a NO candidate producing enzyme). These data indicate that NO could trigger the LCD/H2S signaling pathway in maize seedlings. To further investigate the effect of NO and H2S crosstalk on thermotolerance in maize seedlings, thermotolerance parameters and reactive oxygen species (ROS)-scavenging system were estimated. The results show that SNP increased survival rate and tissue viability, decreased malondialdehyde (MDA) accumulation, and electrolyte leakage in maize seedlings under heat stress (HS), implying NO could improve thermotolerance in maize seedlings. The NO-improved thermotolerance was impaired by H2S inhibitor DL-propargylglycine (PAG) and scavenger HT alone. Similarly, SNP up-regulated the gene expression of DEHYDROASCORBATE REDUCTASE (DHAR) and GLUTATHIONE REDUCTASE1 (GR1); activities of ascorbate peroxidase, glutathione reductase, and catalase; as well as levels of ascorbic acid, glutathione, flavonoids, carotenoids, and total phenols. SNP also reduced hydrogen peroxide and superoxide radical accumulation in maize seedlings under HS compared to the control. The effects of SNP on ROS and their scavenger system were weakened by PAG and HT alone. These data hint that NO could evoke thermotolerance in maize seedlings by triggering the LCD/H2S signaling pathway, and the ROS-scavenging system played a key role in the NO and H2S crosstalk-evoked thermotolerance.

The role of nitric oxide and hydrogen sulfide in regulation of redox homeostasis at extreme temperatures in plants

“…In Zea mays plants, an increase in ascorbate peroxidase activity under normal conditions and under heat stress has been shown by treatment with the NO donor SNP ( Sun et al., 2022 ). However, the nitric oxide donor did not affect APX1 gene expression.…”

“…However, there is also evidence that hydrogen sulfide mediates the effects of nitric oxide. For example, the treatment of maize seedlings with a nitric oxide donor, which induced the development of heat tolerance, was accompanied by increased expression of the gene encoding L-cysteine desulfhydrase ( LCD1 ) and increased enzyme activity ( Sun et al., 2022 ). Wherein, the hydrogen sulfide scavenger hypotaurine abolished the effect of the NO donor on L-cysteine desulfhydrase and the development of heat resistance in maize seedlings.…”

The Essential Role of H2S-ABA Crosstalk in Maize Thermotolerance through the ROS-Scavenging System

“…The suitable concentrations were dated according to the preliminary experiments and previous references [48,50,51]. And then, the irrigated seedlings were subjected to HS at 46 • C for 16 h. Finally, before and after HS, the mesocotyls (which is the most sensitive organ that responds to HS [52]) of the seedlings were selected and used to determine the physiological, biochemical, and molecular parameters according to the following methods, respectively.…”

“….− ) and hydrogen peroxide (H 2 O 2 ) content in seedlings irrigated with NaHS and ABA alone or in combination was determined according to the titanium sulfate method [53] and Na,3 -[1-[(phenylamino)-carbonyl]-3, 4-tetrazolium] (4-methoxy-6-nitro) benzene sulfonic acid hydrate (XTT) method [52]. The O 2…”

Gasotransmitter ammonia accelerates seed germination, seedling growth, and thermotolerance acquirement in maize

“…Finally, the survival rate was counted according to the previous methods. 9 Experiments were repeated at least three times, and the data was assessed as per one-way analysis of variance and the least significant difference. Asterisk (*) and double asterisks (**) in figures represent significant difference ( P < .05) and very significant difference ( P < .01) compared with the control without NH 3.…”