Physiological and Transcriptome Analysis of Exogenous L-Arginine in the Alleviation of High-Temperature Stress in Gracilariopsis lemaneiformis

Abstract

Gracilariopsis lemaneiformis (G. lemaneiformis) is an important marine red macroalgae with high economic and ecological value all over the world. To date, global warming is a key issue that has a great impact on all living organisms, such as macroalgae. L-arginine (Arg) is a precursor of nitric oxide (NO) and polyamines (PAs), which can induce stress defense responses in land plants. However, its role in inducing algae resistance at high temperature (HT) is unclear. In this study, G. lemaneiformis thalli were treated with different concentrations of Arg to investigate its effect and the mechanism on the tolerance of G. lemaneiformis against HT stress. It turned out that exogenous Arg significantly alleviated the HT-induced oxidative damage as indicated by a markedly decrease in malondialdehyde (MDA) content. Notably, Arg remarkably improved the relative growth rate (RGR) and phycobiliprotein (PBP) contents of G. lemaneiformis at HT. Moreover, Arg significantly elevated the activities of antioxidant enzymes, such as superoxide dismutase (SOD), peroxidase (POD), and catalase (CAT), to efficiently scavenge reactive oxygen species (ROS). In addition, it also promoted the accumulation of free amino acids (AAs) as compared to those in the control treatment (CK) group under HT conditions. To investigate the mechanism of G. lemaneiformis to Arg, a transcriptome analysis was performed and revealed 1,414 and 3,825 differentially expressed genes (DEGs) in Arg-treated groups as compared to CK groups at 24 and 48 h of HT stress, respectively. Results showed that Arg significantly upregulated the expression of genes encoding antioxidant enzymes, heat shock proteins, and triggered transcription factors (TFs) signaling during HT stress. Moreover, Arg enhanced the DEGs involved in arginine and proline (Pro) metabolism, AAs biosynthesis, glycolysis, tricarboxylic acid (TCA) cycle, and oxidative phosphorylation. These results may help in understanding the role of Arg in G. lemaneiformis resistance to HT and provide a practical viewpoint for obtaining heat-tolerant G. lemaneiformis to further promote the development of the cultivated seaweed industry in the future.

Characterization of Spermidine Synthase (SPDS) Gene and RNA−Seq Based Identification of Spermidine (SPD) and Spermine (SPM) Involvement in Improving High Temperature Stress Tolerance in Gracilariopsis lemaneiformis (Rhodophyta)

“…Since the PA synthetic gene GlSPDS markedly response to high temperature, we aimed to reveal the role of exogenous PA [spermidine (SPD) and spermine (SPM)] on G. lemaneiformis under high temperature. As our previous study indicated, RGR of G. lemaneiformis at 30/30°C was significantly decreased compared with 23/23°C (Zhang et al, 2021). In the present study, we first examined whether SPD and SPM could alleviate HT-induced growth decline of G. lemaneiformis.…”

“…As is known, the wild G. lemaneiformis can growth prolifically under the temperature range of 10°C to 23°C, once beyond the upper limit its production may be reduced or even cease (Lv et al, 2019). Many studies showed high temperature (HT) stress could induce overaccumulation of reactive oxygen species (ROS) in algae, which oxidizes cellular components of lipids, proteins, and nucleic acids, and brings damage to cellmembranes (Zhang et al, 2020;Zhang et al, 2021). Under these circumstances, algae and plants may upregulate the activities of antioxidant enzymes to decrease the malondialdehyde (MDA) content and thereby reduce membrane damage (Mittler et al, 2004;Wang et al, 2018b).…”

Comparative Transcriptome Analysis Provides Insights Into the Mechanism by Which 2,4-Dichlorophenoxyacetic Acid Improves Thermotolerance in Lentinula edodes

“…As previously reported, heat stress could down-regulate energy metabolisms, decreasing the intermediate product of glycolysis and TCA cycle in the response of L. edodes to heat stress ( Zhao et al, 2019 ). Exogenous L-Arginine was reported to enrich the DEGs involved in glycolysis, TCA cycle, and oxidative phosphorylation in Gracilariopsis lemaneiformis under heat stress ( Zhang et al, 2021b ). In the present study, 2,4-D could remarkably enhance the energy metabolism by activating the expression of genes encoding the TCA cycle (e.g., pyruvate dehydrogenase, citrate synthase, phosphoenolpyruvate carboxykinase, and fumarate reductase) and electron transport chain NADH dehydrogenase, cytochrome c reductase, cytochrome c oxidase, and ATPase ( Figures 2B , 3 ) under thermal stress, it can provide energy for subsequent mycelial regeneration.…”

Versatile roles of polyamines in improving abiotic stress tolerance of plants

“…Exogenously applied arginine significantly improves the tolerance against abiotic stress damages in various crops ( Nasibi et al., 2013 ; Karpets et al., 2018 ; Silveira et al., 2021 ). Similarly, arginine is significant in combating a non-conducive environment through arginine-derived stress-related substances under high-temperature stress in G. lemaneiformis ( Zhang et al., 2021 ) ( Figure 3 ).…”

“… A model diagram for Arg-induced high temperature tolerance in G. lemaneiformis attributed to physiological and transcriptional alterations. PE, phycoerythrin; PC, phycocyanin; MDA, malondialdehyde; SOD, superoxide dismutase; APX, ascorbate peroxidase; TRX, thioredoxin; MDAR, monodehydroascorbate reductase; PRXR, peroxiredoxins; OAT, ornithine–oxo-acid transaminase; P5CR, pyrroline-5-carboxylate reductase; SAMDC, S-adenosylmethionine decarboxylase; GABA, γ-aminobutyric acid; PAO, polyamine oxidases; NAD+, aldehyde dehydrogenase; Asp, aspartate; His, histidine; Gly, glycine; Cys, cystine; Ser, serine; Thr, threonine; Val, valine; Ala, Alanine; PK, pyruvate kinase; PDH, pyruvate dehydrogenase; ENO, enolase; TCA, tricarboxylic acid; IDH, isocitrate dehydrogenase; CSY, citrate synthase; αKGDH, 2-oxoglutarate dehydrogenase ( Zhang et al., 2021 ). …”