Lipid peroxide-derived short-chain aldehydes promote programmed cell death in wheat roots under aluminum stress.

Lipid peroxidation is a primary event in plant roots exposed to aluminum (Al) toxicity, which leads to the formation of reactive aldehydes. Current evidence demonstrates that the resultant aldehydes are integrated components of cellular damage in plants. Here, we investigated the roles of aldehydes in mediating Al-induced damage, particularly cell death, using two wheat genotypes with different Al resistances. Aluminum treatment significantly induced cell death, which was accompanied by decreased root activity and cell length. Al-induced cell death displayed granular nuclei and internucleosomal fragmentation of nuclear DNA, suggesting these cells underwent programmed cell death (PCD). During this process, caspase-3-like protease activity was extensively enhanced and showed a significant difference between these two wheat genotypes. Further experiments showed that Al-induced cell death was positively correlated with aldehydes levels. Al-induced representative diagnostic markers for PCD, such as TUNEL-positive nuclei and DNA fragmentation, were further enhanced by the aldehyde donor (E)-2-hexenal, but significantly suppressed by the aldehyde scavenger carnosine. As the crucial executioner of Al-induced PCD, the activity of caspase-3-like protease was further enhanced by (E)-2-hexenal but inhibited by carnosine in wheat roots. These results suggest that reactive aldehydes sourced from lipid peroxidation mediate Al-initiated PCD probably through activating caspase-3-like protease in wheat roots.

Phytomelatonin and plant mineral nutrition.

Plant mineral nutrition is critical for agricultural productivity and for human nutrition; however, the availability of mineral elements is spatially and temporally heterogeneous in many ecosystems and agricultural landscapes. Nutrient imbalances trigger intricate signalling networks that modulate plant acclimation responses. One signalling agent of particular importance in such networks is phytomelatonin, a pleiotropic molecule with multiple functions. Evidence indicates that deficiencies or excesses of nutrients generally increase phytomelatonin levels in certain tissues, and it is increasingly thought to participate in the regulation of plant mineral nutrition. Alterations in endogenous phytomelatonin levels can protect plants from oxidative stress, influence root architecture, and influence nutrient uptake and efficiency of use through transcriptional and post-transcriptional regulation; such changes optimize mineral nutrient acquisition and ion homeostasis inside plant cells and thereby help to promote growth. This review summarizes current knowledge on the regulation of plant mineral nutrition by melatonin and highlights how endogenous phytomelatonin alters plant responses to specific mineral elements. In addition, we comprehensively discuss how melatonin influences uptake and transport under conditions of nutrient shortage.

Short-chain aldehydes increase aluminum retention and sensitivity by enhancing cell wall polysaccharide contents and pectin demethylation in wheat seedlings.

Upon environmental stimuli, aldehydes are generated downstream of reactive oxygen species and thereby contribute to severe cell damage. In this study, using two wheat genotypes differing in aluminum (Al) tolerance, we investigated the effects of lipid peroxidation-derived aldehydes on cell wall composition and subsequent Al-binding capacities. The spatial accumulation of Al along wheat roots was found to the generation of reactive aldehydes, which are highly localized to the apical regions of roots. Elimination of aldehydes by carnosine significantly reduced Al contents in root tips, with a concomitant alleviation of root growth inhibition. In contrast, root growth and Al accumulation were exacerbated by application of the short-chain aldehyde (E)-2-hexenal. We further confirmed that cell wall binding capacity, rather than malate efflux or pH alteration strategies, is associated with the aldehyde-induced accumulation of Al. Scavenging of lipid-derived aldehydes reduced Al accumulation in the pectin and hemicellulose 1 (HC1) fractions of root cell walls, whereas exposure to (E)-2-hexenal promoted a further accumulation of Al, particularly in the cell wall HC1 fraction of the Al-sensitive genotype. Different strategies were introduced by pectin and HC1 to accumulate Al in response to aldehydes in wheat roots. Accumulation in pectin is based on a reduction of methylation levels in response to elevated pectin methylesterase activity and gene expression, whereas that in HC1 is associated with an increase in polysaccharide contents. These findings indicate that aldehydes exacerbate Al phytotoxicity by enhancing Al retention in cell wall polysaccharides.

Indium induces nitro-oxidative stress in roots of wheat (Triticum aestivum).

The entrance of indium, an emerging contaminant from electronics, into the agroecosystem inevitably causes its accumulation in crops and raises exposure risk of humans via food chain. This study investigated indium uptake and toxicological effects in wheat plants under a worst-case scenario. Inhibition of root growth is a primary manifestation of indium toxicity and most absorbed indium accumulated in wheat roots with only a tiny portion reaching the leaves. The enhancement of reactive oxygen species (ROS), lipid peroxidation and protein oxidation in roots suggest that indium caused oxidative stress. Additionally, we found the levels of nitric oxide and peroxyinitrite, two major reactive nitrogen species (RNS), also increased in wheat roots under indium stress. These changes were accompanied by a raise in protein tyrosine nitration, thereby provoking nitrosative stress. The increase in peroxyinitrite and S-nitrosoglutathione content, S-nitrosoglutathione reductase activity as well as a concomitant reduction in glutathione concentrations suggest a rigorous metabolic interplay between ROS and RNS. Moreover, indium simultaneously triggered alteration in protein carbonylation and nitration. Overall, our results suggest that indium induced nitro-oxidative stress which probably contributes to toxicological effects in wheat plants, which are helpful in reducing the potential risk from emerging contaminants analogous to indium to humans.

Lipid Peroxide-Derived Short-Chain Aldehydes are Involved in Aluminum Toxicity of Wheat (Triticum aestivum) Roots.

Lipid peroxidation is a common event during aluminum (Al) toxicity in plants, and it generates an array of aldehyde fragments. The present study investigated and compared the profile and physiological functions of lipid peroxide-derived aldehydes under Al stress in two wheat genotypes that differed in Al resistance. Under Al stress, the sensitive genotype Yangmai-5 suffered more severe plasma membrane damage and accumulated higher levels of aldehydes in roots than the Al-tolerant genotype Jian-864. The complementary use of high-resolution mass spectrometry and standard compounds allowed the identification and quantification of 13 kinds of short-chain aldehydes sourced from lipids in wheat roots. Among these aldehydes, acetaldehyde, isovaldehyde, valeraldehyde, (E)-2-hexenal (HE), heptaldehyde, and nonyl aldehyde were the predominant species. Moreover, it was found that HE in the sensitive genotype was over 2.63 times higher than that in the tolerant genotype after Al treatment. Elimination of aldehydes using carnosine rescued root growth inhibition by 19.59 and 11.63% in Jian-864 and Yangmai-5, respectively, and alleviated Al-induced membrane damage and protein oxidation. Exogenous aldehyde application further inhibited root elongation and exacerbated oxidative injury. The tolerant genotype Jian-864 showed elevated aldehyde detoxifying enzyme activity and transcript levels. These results suggest that lipid peroxide-derived short-chain aldehydes are involved in Al toxicity, and a higher aldehyde-detoxifying capacity may be responsible for Al tolerance.