bims-polyam 2023-10-15 papers

bims-polyam

Biomed News

on Polyamines

Issue of 2023‒10‒15
seven papers selected by
Sebastian J. Hofer, University of Graz

Polyamines and hormesis: Making sense of a dose response dichotomy.
Polyamines modulate mouse sperm motility.
Intracellular polyamines regulate redox homeostasis with cAMP-PKA signalling during sexual mating/filamentation and pathogenicity of Sporisorium scitamineum.
Metabolic support by macrophages sustains colonic epithelial homeostasis.
Polyamines mediate the inhibitory effect of drought stress on nitrogen reallocation and utilization to regulate the grain number in wheat.
Arbuscular mycorrhizal fungi as an effective approach to enhance the growth and metabolism of soybean plants under thallium (TI) toxicity.
[Exogenous Spermidine Regulates Ryegrass Root System Response to Cd Stress and Its Transcriptome Analysis].

Chem Biol Interact. 2023 Oct 08. pii: S0009-2797(23)00415-5. [Epub ahead of print] 110748

Polyamines and hormesis: Making sense of a dose response dichotomy.

Edward Calabrese, A Wallace Hayes, Peter Pressman, Rachna Kapoor, Gaurav Dhawan, Vittorio Calabrese, Evgenios Agathokleous.

  The diverse biological effects of polyamines (putrescine, spermidine and spermine) were reviewed in the context of hormesis in an integrative manner for the first time. The findings illustrate that each of these polyamines commonly induces hormetic dose responses in a wide range of biological models and types of cells for multiple endpoints in numerous plant species and animal models. Plant studies emphasized preconditioning experimental studies in which the respective polyamines conferred some protection against the damaging effects of a broad range of environmental stressors such as drought, salinity, cold/heat, heavy metals and UV-damage in an hormetic manner. Polyamine-based animal hormesis studies emphasized biomedical endpoints such as longevity and neuroprotection. These findings have important biological and biomedical implications and should guide experimental designs of low dose investigations.

Keywords:  Biphasic dose response; Dose response; Hormesis; Phytomedicine; Polyamines; Sperimidine

DOI:  https://doi.org/10.1016/j.cbi.2023.110748
Syst Biol Reprod Med. 2023 Oct 09. 1-15

Polyamines modulate mouse sperm motility.

Lorena Rodríguez-Páez, Charmina Aguirre-Alvarado, Germán Chamorro-Cevallos, Alcántara-Farfán Veronica, Calderón-Espinosa Sandra Irel, Castillo-Pérez Hugo, Carlos Armando García-Pérez, Guadalupe Elizabeth Jiménez-Gutiérrez, Joaquín Cordero-Martínez.

  Polyamines are polycationic molecules which contains two or more amino groups (-NH3+) highly charged at physiological pH, and among them we found spermine, spermidine, putrescine, and cadaverine. They interact with proteins, nucleic acids, modulate Ca2+, K+, and Na+ channels, and protect sperm from oxidative stress. In this work, we evaluate the effect of spermine, spermidine, and putrescine on the total, progressive and kinematic parameters of motility, capacitation, acrosome reaction, also in presence and absence of the dbcAMP, an analogue of the cAMP, and the IBMX, a phosphodiesterase inhibitor. In addition, we evaluated the intracellular concentrations of cAMP [cAMP]i, and performed an in silico analysis between polyamines and the sAC from mouse to predict the possible interaction among them. Our results showed that all polyamines decrease drastically the total, progressive and the kinetic parameters of sperm motility, decrease the capacitation, and only spermidine and putrescine impeded the acquisition of acrosome reaction. Moreover, the effect of polyamines was attenuated but not countered by the addition of db-cAMP and IBMX, suggesting a possible inhibition of the sAC. Also, the presence of polyamines induced a decrease of the [cAMP]i, and the in silico analysis predicted a strong interaction among polyamines and the sAC. Overall, the evidence suggests that probably the polyamines interact and inhibit the activity of the sAC.

Keywords:  Spermatozoa; acrosome reaction; capacitation; motility; soluble adenylyl cyclase

DOI:  https://doi.org/10.1080/19396368.2023.2262714
Mol Plant Pathol. 2023 Oct 09.

Intracellular polyamines regulate redox homeostasis with cAMP-PKA signalling during sexual mating/filamentation and pathogenicity of Sporisorium scitamineum.

Kai Yin, Guobing Cui, Xinping Bi, Meiling Liang, Zhijian Hu, Yi Zhen Deng.

  Sugarcane smut caused by Sporisorium scitamineum seriously impairs sugarcane production and quality. Sexual mating/filamentation is a critical step of S. scitamineum pathogenesis, yet the regulatory mechanisms are not fully understood. In this study, we identified the SsAGA, SsODC, and SsSAMDC genes, which are involved in polyamine biosynthesis in S. scitamineum. Deletion of SsODC led to complete loss of filamentous growth after sexual mating, and deletion of SsAGA or SsSAMDC caused reduced filamentation. Double deletion of SsODC and SsSAMDC resulted in auxotrophy for putrescine (PUT) and spermidine (SPD) when grown on minimal medium (MM), indicating that these two genes encode enzymes that are critical for PUT and SPD biosynthesis. We further showed that low PUT concentrations promoted S. scitamineum filamentation, while high PUT concentrations suppressed filamentation. Disrupted fungal polyamine biosynthesis also resulted in a loss of pathogenicity and reduced fungal biomass within infected plants at the early infection stage. SPD formed a gradient from the diseased part to nonsymptom parts of the cane stem, suggesting that SPD is probably favourable for fungal virulence. Mutants of the cAMP-PKA (SsGPA3-SsUAC1-SsADR1) signalling pathway displayed up-regulation of the SsODC gene and elevated intracellular levels of PUT. SsODC directly interacted with SsGPA3, and sporidia of the ss1uac1ΔodcΔ mutant displayed abundant pseudohyphae. Furthermore, we found that elevated PUT levels caused accumulation of intracellular reactive oxygen species (ROS), probably by suppressing transcription of ROS-scavenging enzymes, while SPD played the opposite role. Overall, our work proves that polyamines play important roles in the pathogenic development of sugarcane smut fungus, probably by collaboratively regulating intracellular redox homeostasis with the cAMP-PKA signalling pathway.

Keywords:   Sporisorium scitamineum ; cAMP-PKA signalling pathway; pathogenesis; polyamines; redox; sexual mating/filamentation

DOI:  https://doi.org/10.1111/mpp.13393
Cell Metab. 2023 Sep 29. pii: S1550-4131(23)00341-8. [Epub ahead of print]

Metabolic support by macrophages sustains colonic epithelial homeostasis.

Stephanie Deborah Fritsch, Nyamdelger Sukhbaatar, Karine Gonzales, Alishan Sahu, Loan Tran, Andrea Vogel, Mario Mazic, Jayne Louise Wilson, Stephan Forisch, Hannah Mayr, Raimund Oberle, Jakob Weiszmann, Martin Brenner, Roeland Vanhoutte, Melanie Hofmann, Sini Pirnes-Karhu, Christoph Magnes, Torben Kühnast, Wolfram Weckwerth, Christoph Bock, Kristaps Klavins, Markus Hengstschläger, Christine Moissl-Eichinger, Gernot Schabbauer, Gerda Egger, Eija Pirinen, Steven H L Verhelst, Thomas Weichhart.

  The intestinal epithelium has a high turnover rate and constantly renews itself through proliferation of intestinal crypt cells, which depends on insufficiently characterized signals from the microenvironment. Here, we showed that colonic macrophages were located directly adjacent to epithelial crypt cells in mice, where they metabolically supported epithelial cell proliferation in an mTORC1-dependent manner. Specifically, deletion of tuberous sclerosis complex 2 (Tsc2) in macrophages activated mTORC1 signaling that protected against colitis-induced intestinal damage and induced the synthesis of the polyamines spermidine and spermine. Epithelial cells ingested these polyamines and rewired their cellular metabolism to optimize proliferation and defense. Notably, spermine directly stimulated proliferation of colon epithelial cells and colon organoids. Genetic interference with polyamine production in macrophages altered global polyamine levels in the colon and modified epithelial cell proliferation. Our results suggest that macrophages act as "commensals" that provide metabolic support to promote efficient self-renewal of the colon epithelium.

Keywords:  arginase-1; homeostasis; immunometabolism; intestine; mTOR; mTORC1; macrophages; polyamines; spermine

DOI:  https://doi.org/10.1016/j.cmet.2023.09.010
J Exp Bot. 2023 Oct 09. pii: erad393. [Epub ahead of print]

Polyamines mediate the inhibitory effect of drought stress on nitrogen reallocation and utilization to regulate the grain number in wheat.

Juan Li, Qi Li, Nian Guo, Qinglin Xian, Bing Lan, Nangia Vinay, Fei Mo, Yang Liu.

  Drought stress poses a serious threat to wheat grain formation. Nitrogen (N) plays crucial roles in plant organ development. However, the physiological mechanisms by which drought stress affects plant N availability and mediates the formation of grains in spikes of winter wheat are still unclear. Here, we revealed that pre-reproductive drought stress significantly reduced the number of fertile florets and inhibited the formation of grain numbers. Transcriptome analysis demonstrated that this was related to N metabolism, arginine (main precursor for polyamine (PA) synthesis) and proline metabolism pathways. Continuous drought stress restricted plant N accumulation and reallocation rates, but plants preferentially allocated more N to spike development. However, as the activities of amino acid biosynthesis enzymes and catabolic enzymes were inhibited, more free amino acids accumulated in young spikes. Unfortunately, the expression of PA synthase genes was downregulated, and catabolic enzyme-encoding gene expression was enhanced under drought stress, resulting in reductions in endogenous spermidine and putrescine. Importantly, exogenous spermidine treatment optimized N allocation in young spikes and leaves, which greatly alleviated adverse effects reducing the number of grains per spike. Overall, pre-reproductive drought stress affected wheat grain numbers by regulating N redistribution and PA metabolism.

Keywords:  Fertile floret; RNA-Seq; Triticum aestivum; amino acid; nitrogen allocation; nitrogen use efficiency; spermidine; water deficit

DOI:  https://doi.org/10.1093/jxb/erad393
Plant Physiol Biochem. 2023 Oct 06. pii: S0981-9428(23)00588-0. [Epub ahead of print]203 108077

Arbuscular mycorrhizal fungi as an effective approach to enhance the growth and metabolism of soybean plants under thallium (TI) toxicity.

Mohamed Abdel-Mawgoud, Nahla Alsayd Bouqellah, Shereen Magdy Korany, Ahmed Mohamed Reyad, Abdelrahim H A Hassan, Emad A Alsherif, Hamada AbdElgawad.

  Thallium (TI) is a toxic metal that can trigger harmful impacts on growth and metabolism of plants. Utilizing arbuscular mycorrhizal fungi (AMF) proves to be an effective strategy for alleviating heavy metal toxicity in plants. To this end, AMF were applied to mitigate TI toxic effects on the growth, primary and secondary metabolism of soybean plants. Here, TI stress inhibited the growth and photosynthetic parameters of soybean plants. It also increased the oxidative damage as demonstrated by increased levels of oxidative markers, (MDA and lipoxygenase (LOX) activity). However, AMF could mitigate the reduction in growth and photosynthesis induced by TI, as well as the induction of oxidative damage. To overcome TI toxicity, AMF increased the levels and metabolism of osmolytes such as proline in soybean plants. This was in line with the increased activities of key enzymes that involved in proline biosynthesis (e.g., P5CS (pyrroline-5-carboxylate synthetase), P5CR (pyrroline-5-carboxylate reductase) and OAT (ornithine aminotransferase) under the AMF and/or TI treatments. Furthermore, soybean plants could benefit from the synergism between AMF and TI to enhance the contents of individual (e.g., spermine and spermidine) and total polyamines as well as their metabolic enzymes (e.g., arginine decarboxylase and ornithine decarboxylase). Overall, the combined application of AMF emerges as a viable approach for alleviating TI toxicity in soybean plants.

Keywords:  Arbuscular mycorrhizal fungi; Mineral balance; Polyamines; Proline metabolism; Sucrose metabolism; Thallium

DOI:  https://doi.org/10.1016/j.plaphy.2023.108077
Huan Jing Ke Xue. 2023 Oct 08. 44(10): 5746-5756

[Exogenous Spermidine Regulates Ryegrass Root System Response to Cd Stress and Its Transcriptome Analysis].

Zhi-Qiang Yu, Jia-Yuan Hu, Shang-Ke Li, Wei-Lin Shi, Guang-Yu Shi.

  The application of exogenous growth-regulating substances is an effective technique to enhance plant stress tolerance. Here, a hydroponic experiment was conducted to investigate the effects of exogenous basal application of 0.1 mmol·L-1 spermidine (Spd) on both the physiology and molecular biology of ryegrass root systems under varying degrees (0, 5, and 10 mg·L-1) of cadmium (Cd) stress using ryegrass as the test plants. The results of physiological studies revealed that Cd stress significantly reduced the physiological functions of the ryegrass root system, whereas the addition of Spd effectively alleviated the negative effects caused by Cd. The most significant effect was on the root soluble protein content, which increased by 90.91% and 158.35% compared with 5 mg·L-1and 10 mg·L-1 Cd alone. Spd also inhibited the accumulation of oxidative stress products malondialdehyde (MDA) and hydrogen peroxide (H2O2) by increasing the ascorbic acid (ASA) and glutathione (GSH) content and peroxidase (POD) activity, whereas the effects on root activity and superoxide dismutase (SOD) activity were not significant. The results of molecular biology studies demonstrated that 10 mg·L-1 Cd stress caused differential expression of a large number of genes in ryegrass roots, and the number of differentially expressed genes, differential significance, and differential multiplicity were significantly reduced after the application of exogenous Spd. The most significant part of the GO enrichment analysis shifted from responding to organic cyclic compounds and aldehyde/ketone group transferase activity to responding to trivalent iron ions and 2'-deoxymugineic-acid 2'-dioxygenase activity. Single gene expression heat map analysis revealed that exogenous Spd upregulated the expression of genes encoding zinc-iron transporter protein and 2'-deoxymugineic-acid 2'-dioxygenase, which improved the uptake and utilization of iron by the root system. In conclusion, the application of certain concentrations of Spd could effectively regulate the response of ryegrass roots to Cd stress, enhance its tolerance physiology, and mitigate the toxic effects of Cd.

Keywords:  cadmium(Cd); regulatory mechanism; ryegrass; spermidine(Spd); transcriptomics

DOI:  https://doi.org/10.13227/j.hjkx.202210060