{"title":"Crosstalk of methylglyoxal and calcium signaling in maize (Zea mays L.) thermotolerance through methylglyoxal-scavenging system","authors":"Ru-Hua Xiang , Jia-Qi Wang , Zhong-Guang Li","doi":"10.1016/j.jplph.2024.154362","DOIUrl":null,"url":null,"abstract":"<div><div>Methylglyoxal (MG) and calcium ion (Ca<sup>2+</sup>) can increase multiple-stress tolerance including plant thermotolerance. However, whether crosstalk of MG and Ca<sup>2+</sup> exists in the formation of maize thermotolerance and underlying mechanism still remain elusive. In this paper, maize seedlings were irrigated with MG and calcium chloride alone or in combination, and then exposed to heat stress (HS). The results manifested that, compared with the survival percentage (SP, 45.3%) of the control seedlings, the SP of MG and Ca<sup>2+</sup> alone or in combination was increased to 72.4%, 74.2%, and 83.4% under HS conditions, indicating that Ca<sup>2+</sup> and MG alone or in combination could upraise seedling thermotolerance. Also, the MG-upraised SP was separately weakened to 42.2%, 40.3%, 52.1%, and 39.4% by Ca<sup>2+</sup> chelator (ethylene glycol tetraacetic acid, EGTA), plasma membrane Ca<sup>2+</sup> channel blocker (lanthanum chloride, LaCl<sub>3</sub>), intracellular Ca<sup>2+</sup> channel blocker (neomycin, NEC), and calmodulin (CaM) antagonist (trifluoperazine, TFP). However, significant effect of MG scavengers N-acetylcysteine (NAC) and aminoguanidine (AG) on Ca<sup>2+</sup>-induced thermotolerance was not observed. Similarly, an endogenous Ca<sup>2+</sup> level in seedlings was increased by exogenous MG under non-HS and HS conditions, while exogenous Ca<sup>2+</sup> had no significant effect on endogenous MG. These data implied that Ca<sup>2+</sup> signaling, at least partly, mediated MG-upraised thermotolerance in maize seedlings. Moreover, the activity and gene expression of glyoxalase system (glyoxalase I, glyoxalase II, and glyoxalase III) and non-glyoxalase system (MG reductase, aldehyde reductase, aldo-keto reductase, and lactate dehydrogenase) were up-regulated to a certain extent by Ca<sup>2+</sup> and MG alone in seedlings under non-HS and HS conditions. The up-regulated MG-scavenging system by MG was enhanced by Ca<sup>2+</sup>, while impaired by EGTA, LaCl<sub>3</sub>, NEC, or TFP. These data suggest that the crosstalk of MG and Ca<sup>2+</sup> signaling in maize thermotolerance through MG-scavenging system. These findings provided a theoretical basis for breeding climate-resilient maize crop and developing smart agriculture.</div></div>","PeriodicalId":16808,"journal":{"name":"Journal of plant physiology","volume":"303 ","pages":"Article 154362"},"PeriodicalIF":4.0000,"publicationDate":"2024-10-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Journal of plant physiology","FirstCategoryId":"99","ListUrlMain":"https://www.sciencedirect.com/science/article/pii/S0176161724001937","RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PLANT SCIENCES","Score":null,"Total":0}
引用次数: 0
Abstract
Methylglyoxal (MG) and calcium ion (Ca2+) can increase multiple-stress tolerance including plant thermotolerance. However, whether crosstalk of MG and Ca2+ exists in the formation of maize thermotolerance and underlying mechanism still remain elusive. In this paper, maize seedlings were irrigated with MG and calcium chloride alone or in combination, and then exposed to heat stress (HS). The results manifested that, compared with the survival percentage (SP, 45.3%) of the control seedlings, the SP of MG and Ca2+ alone or in combination was increased to 72.4%, 74.2%, and 83.4% under HS conditions, indicating that Ca2+ and MG alone or in combination could upraise seedling thermotolerance. Also, the MG-upraised SP was separately weakened to 42.2%, 40.3%, 52.1%, and 39.4% by Ca2+ chelator (ethylene glycol tetraacetic acid, EGTA), plasma membrane Ca2+ channel blocker (lanthanum chloride, LaCl3), intracellular Ca2+ channel blocker (neomycin, NEC), and calmodulin (CaM) antagonist (trifluoperazine, TFP). However, significant effect of MG scavengers N-acetylcysteine (NAC) and aminoguanidine (AG) on Ca2+-induced thermotolerance was not observed. Similarly, an endogenous Ca2+ level in seedlings was increased by exogenous MG under non-HS and HS conditions, while exogenous Ca2+ had no significant effect on endogenous MG. These data implied that Ca2+ signaling, at least partly, mediated MG-upraised thermotolerance in maize seedlings. Moreover, the activity and gene expression of glyoxalase system (glyoxalase I, glyoxalase II, and glyoxalase III) and non-glyoxalase system (MG reductase, aldehyde reductase, aldo-keto reductase, and lactate dehydrogenase) were up-regulated to a certain extent by Ca2+ and MG alone in seedlings under non-HS and HS conditions. The up-regulated MG-scavenging system by MG was enhanced by Ca2+, while impaired by EGTA, LaCl3, NEC, or TFP. These data suggest that the crosstalk of MG and Ca2+ signaling in maize thermotolerance through MG-scavenging system. These findings provided a theoretical basis for breeding climate-resilient maize crop and developing smart agriculture.
期刊介绍:
The Journal of Plant Physiology is a broad-spectrum journal that welcomes high-quality submissions in all major areas of plant physiology, including plant biochemistry, functional biotechnology, computational and synthetic plant biology, growth and development, photosynthesis and respiration, transport and translocation, plant-microbe interactions, biotic and abiotic stress. Studies are welcome at all levels of integration ranging from molecules and cells to organisms and their environments and are expected to use state-of-the-art methodologies. Pure gene expression studies are not within the focus of our journal. To be considered for publication, papers must significantly contribute to the mechanistic understanding of physiological processes, and not be merely descriptive, or confirmatory of previous results. We encourage the submission of papers that explore the physiology of non-model as well as accepted model species and those that bridge basic and applied research. For instance, studies on agricultural plants that show new physiological mechanisms to improve agricultural efficiency are welcome. Studies performed under uncontrolled situations (e.g. field conditions) not providing mechanistic insight will not be considered for publication.
The Journal of Plant Physiology publishes several types of articles: Original Research Articles, Reviews, Perspectives Articles, and Short Communications. Reviews and Perspectives will be solicited by the Editors; unsolicited reviews are also welcome but only from authors with a strong track record in the field of the review. Original research papers comprise the majority of published contributions.