S-adenosylmethionine synthetase 1 confers drought and salt tolerance in transgenic tomato

doi:10.1016/j.envexpbot.2020.104226

Environmental and Experimental Botany

Volume 179, November 2020, 104226

https://doi.org/10.1016/j.envexpbot.2020.104226 Get rights and content

Highlights

•
Tomato SAMS1 was a multiple stress-induced gene.
•
Overexpression of SlSAMS1 enhanced tomato drought and salt tolerance.
•
PAs, H₂O₂ and ABA signals was involved in SlSAMS1 positively regulating tomato tolerance to drought and salt tolerance.

Abstract

Environmental stresses, like drought and salt, seriously threaten the productivity of tomato (Solanum lycopersicum L.). S-adenosylmethionine synthetase (SAMS) is responsible for synthesis of SAM that plays important roles in regulating plant-environment interactions. In this study, we analyzed the function of tomato SAMS1 (SlSAMS1) gene under drought and salt stresses. Promoter analysis showed that the promoter region of SlSAMS1 had several stress-related cis-regulatory elements. Expression pattern analysis indicated that SlSAMS1 was induced by salt, drought, low temperature and abscisic acid (ABA) treatments. Overexpression of SlSAMS1 in tomato improved drought and salt stresses tolerance. Under drought and salt stresses, water-retention capacity and photosynthetic capacity were significantly enhanced in transgentc lines. In addition, overexpression of SlSAMS1 significantly reduced the accumulation of superoxide, hydrogen peroxide (H₂O₂) and malondialdehyde, and enhanced ABA content and reactive oxygen species scavenging enzymes (superoxide dismutase, catalase and ascorbate peroxidase) activities. Furthermore, drought and salt treatment enlarged the influences caused by overexpressing SlSAMS1 in polyamines (PAs) synthesis and ethylene emission. Interestingly, water loss assay indicated that SlSAMS1 modulated the generation of PAs and H₂O₂, not ethylene, to maintain a better water homeostasis in transgenic plants. Moreover, ABA induced the expression of PAs and ethylene synthesis related genes to change PAs contents and ethylene emission. Importantly, compared with wild type plants, transgenic plants reduced water loss under ABA treatment. Collectively, these results suggested that SlSAMS1 involved in tomato drought and salt tolerance mainly through mediated PAs, H₂O₂ and ABA signals.

Introduction

Crop productivity was significantly limited by environmental changes, especially drought and soil salinity (Zhu, 2016). About 6 % of the land area are under high salt concentration and worldwide climate change triggers water shortage (Yang et al., 2010; Zhang et al., 2020a). These problems are becoming more and more serious. Drought and soil salinity led to plant cells in hyperosmotic stress, which was resulted from water shortage (Maathuis, 2014). Under this hyperosmotic stress, phytohormone abscisic acid (ABA) was induced in plant cells to adapt environmental changes (Zhu, 2002). In addition, reactive oxygen species (ROS) could excessively accumulate in plant cells, resulting in cell components damage and lipid peroxidation accumulation (Mailloux and Harper, 2011). However, ROS, as signal molecules, also participated in stomatal closure, influenced ion channels and induced specific stress response (Moschou et al., 2008). The accumulation of ROS and ROS scavengers were regulated by polyamines (PAs) that was mainly composed of putrescine (Put), spermidine (Spd) and spermine (Spm) (Ma et al., 2017; Saha et al., 2015). For instance, diamine oxidases (DAO) and PA oxidases (PAOs) catabolized PAs to generate hydrogen peroxide (H₂O₂) (Pottosin and Shabala, 2014). Spd induced NADPH-oxidase to accumulate superoxide (O^2˙−) (Pal et al., 2015). However, O₂^˙− was converted to H₂O₂ by spontaneous or enzymatic manner (Andronis et al., 2014). In addition, Put could form a positively feedback loop with ABA under abiotic stress (Takahashi et al., 2010). Because ROS and ABA strongly affected plant respond to environmental changes, controlling the synthesis of PAs, as a strategy, has been applied to improve plant resistance to environment stresses (Pal et al., 2015).

As a precursor of PAs biosynthesis, SAM was synthesized by SAM synthetase (SAMS) (Roje, 2006). Previous studies showed that SAMSs could be induced by multiple stress treatment and played important roles in regulating plant tolerance to environmental changes, especially soil salinity and drought. For example, SAMSs of Suaeda salsa and Medicago sativa positively regulated the resistance to salt stress in transgenic tobacco plants (Hua et al., 2012; Qi et al., 2010). The ectopic expression of potato SAMS in Arabidopsis could enhance salt and drought tolerance (Kim et al., 2015). It was also reported that ectopic expressing sugar beet SAMS in Arabidopsis increased salt and H₂O₂ tolerance (Ma et al., 2017). In addition, previous research also indicated that overexpressing MfSAMS1 in tobacco plants enhanced cold tolerance through regulated PAs and H₂O₂ cross-linked networks (Guo et al., 2014). This regulatory mechanism was also found in tomato response to alkali stress using overexpressing SlSAMS1 transgenic lines (Gong et al., 2014b, 2016). These studies suggested that SAMS genes have multiple adjustment functions in plant against environment stresses.

Tomato (Solanum lycopersicum L.) has great nutritional value and is an important model plant for studying gene function. However, saline soil and drought seriously affected tomato growth and development, then limited the productivity. A total of four tomato SAMS genes were identified in tomato genome, and SlSAMS1 and SlSAMS3 were induced by salt, ABA and mannitol treatments (Espartero et al., 1994). Although we have evaluated the regulatory mechanism of SlSAMS1 mediated alkali tolerance in previous studies (Gong et al., 2014b, 2016), whether SlSAMS1 participate in tomato drought and salt tolerance remains unclear. Here, the cis-regulatory elements were analyzed in SlSAMS1 promoter. Then, the expression levels of SlSAMS1 were examined under salt, drought, low temperature and ABA conditions. After that, SlSAMS1 overexpression (OE) tomato plants were used to evaluate the function of SlSAMS1 under drought and salt conditions. Meanwhile, a series of physiological characteristics were compared between OE lines and the wild type (WT) plants under drought and salt conditions. Furthermore, possible regulatory mechanisms were analyzed by water loss assay and exogenous application ABA assay. Overall, this study not only clarified a basic understanding for SlSAMS1 mediated mechanism tomato drought and salt stresses, but also provided a novel insight into the further study of biological function of SAMS genes.

Section snippets

Plant materials and treatment conditions

Tomato (Solanum lycopersicum L.) plants were grown in a growth chamber with a 16 h light (28 °C) / 8 h dark (22 °C) (Zhang et al., 2020b). The compound of Hoagland nutrient solution was based on previously described (Yan et al., 2019). For analysis of the SlSAMS1 expression levels under drought, salt, low temperature and ABA stresses, four-week-old WT tomato plants were treated with 5 % PEG 8000, 150 mM NaCl, 4 °C and 10 μmol ABA, respectively. Then, the treated leaves were collected at 0, 12,

SlSAMS1 promoter analysis and SlSAMS1 expression patterns under different stresses

To study the biological functions of SlSAMS1, we analyzed stress related cis-regulatory elements in the promoter regions 2.0-kb upstream of SlSAMS1 gene. As shown in Fig.1A, three ABA response elements, two defense and stress response elements and one salicylic acid (SA) response element were found in SlSAMS1 promoter region.

For investigating whether SlSAMS1 participate in ABA related osmotic stresses, the expression profiles of SlSAMS1 were tested under salt, drought, low temperature and ABA

Discussion

SAMS family genes have been identified in Arabidopsis (Shen et al., 2002), tomato (Gong et al., 2014b), rice (Li et al., 2011), soybean (Hua et al., 2012), Suaeda salsa (Qi et al., 2010), Medicago sativa (Hua et al., 2012) and sugar beet (Ma et al., 2017). In the past decade, extensively studies have reported the functions of SAMS genes in regulating plants responded to abiotic stress (Gong et al., 2014b; Guo et al., 2014; Ma et al., 2017; Qi et al., 2010). Although we have revealed that the

Conclusions

In summary, SlSAMS1, as a multiple stress-induced gene, positively regulated tomato drought and salt resistance in three ways: (I). Improving water-retention and photosynthesis capacity in transgenic tomato; (II). Maintaining strong ROS-scavenging ability and higher content of osmolytes in transgenic tomato to reduce the damage of oxidative stress; (III). Decreasing water loss in transgenic tomato mainly through PAs, H₂O₂ and ABA signals.

Author contributions

QS and BG designed the experiments. BG and XZ performed the experiments. XZ analyzed the data and wrote the manuscript. ZB revised the manuscript.

Declaration of Competing Interest

The authors declare that they have no conflict of interest.

Acknowledgements

This work was supported by the National Natural Science Foundation of China (U1903105, U1906205and 31872954); the National Key Research and Development Program of China (2018YFD1000800); Major Agricultural Application Technology Innovation Project of Shandong Province (2018); the Project of Shandong “Double-First-Class” (SYL2017YSTD06); Shandong Upgraded Project of “Bohai Granary” Science and Technology Demonstration Engineering (2019BHLC005); the Project of State Key Laboratory of Crop Biology

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View full text

S-adenosylmethionine synthetase 1 confers drought and salt tolerance in transgenic tomato

Highlights

Abstract

Introduction

Section snippets

Plant materials and treatment conditions

SlSAMS1 promoter analysis and SlSAMS1 expression patterns under different stresses

Discussion

Conclusions

Author contributions

Declaration of Competing Interest

Acknowledgements

Peroxisomal polyamine oxidase and NADPH-oxidase cross-talk for ROS homeostasis which affects respiration rate in Arabidopsis thaliana

Front. Plant Sci.

Exogenous spermidine affects polyamine metabolism in salinity-stressed Cucumis sativus roots and enhances short-term salinity tolerance

J. Plant Physiol.

Differential accumulation of S-adenosylmethionine synthetase transcripts in response to salt stress

Plant Mol. Biol.

Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants

Plant Physiol. Biochem.

Sodic alkaline stress mitigation by interaction of nitric oxide and polyamines involves antioxidants and physiological strategies in Solanum lycopersicum

Free Radic. Biol. Med.

Overexpression of S-adenosyl-L-methionine synthetase increased tomato tolerance to alkali stress through polyamine metabolism

Plant Biotechnol. J.

S-nitrosoglutathione reductase-modulated redox signaling controls sodic alkaline stress responses in Solanum lycopersicum L

Plant Cell Physiol.

Overexpression of S-adenosylmethionine synthetase 1 enhances tomato callus tolerance to alkali stress through polyamine and hydrogen peroxide cross-linked networks

Plant Cell Tissue Organ Cult.

Expression of wheat Na(+)/H(+) antiporter TNHXS1 and H(+)- pyrophosphatase TVP1 genes in tobacco from a bicistronic transcriptional unit improves salt tolerance

Plant Mol. Biol.

Abscisic acid, H2O2 and nitric oxide interactions mediated cold-induced S-adenosylmethionine synthetase in Medicago sativa subsp. Falcata that confers cold tolerance through up-regulating polyamine oxidation

Plant Biotechnol. J.

The formation of ACC and competition between polyamines and ethylene for SAM

Annual Plant Reviews

Effect of exogenous spermidine on polyamine content and metabolism in tomato exposed to salinity-alkalinity mixed stress

Plant Physiol. Biochem.

Stress-inducible expression of GsSAMS2 enhances salt tolerance in transgenic Medicago sativa

Afr. J. Biotechnol.

Expression of potato S-adenosyl-L-methionine synthase (SbSAMS) gene altered developmental characteristics and stress responses in transgenic Arabidopsis plants

Plant Physiol. Biochem.

A chloroplast-targeted DnaJ protein contributes to maintenance of photosystem II under chilling stress

J. Exp. Bot.

Polyamines induce adaptive responses in water deficit stressed cucumber roots

J. Plant Res.

Polyamines and plant adaptation to saline environments

Stomatal size, speed, and responsiveness impact on photosynthesis and water use efficiency

Plant Physiol.

PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences

Nucleic Acids Res.

The important roles of reactive oxygen species in the relationship between ethylene and polyamines in leaves of spring wheat seedlings under root osmotic stress

Plant Sci.

Knockdown of SAMS genes encoding S-adenosyl-l-methionine synthetases causes methylation alterations of DNAs and histones and leads to late flowering in rice

J. Plant Physiol.

Overexpression of tomato enhancer of SOS3-1 (LeENH1) in tobacco enhanced salinity tolerance by excluding Na+ from the cytosol

Plant Physiol. Biochem.

Sodic alkaline stress mitigation by exogenous melatonin in tomato needs nitric oxide as a downstream signal

J. Plant Physiol.

Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method

Methods

Overexpression of S-adenosyl-L-methionine synthetase 2 from sugar beet M14 increased Arabidopsis tolerance to salt and oxidative stress

Int. J. Mol. Sci.

Sodium in plants: perception, signalling, and regulation of sodium fluxes

J. Exp. Bot.

Uncoupling proteins and the control of mitochondrial reactive oxygen species production

Free Radic. Biol. Med.

FERONIA receptor kinase interacts with S-adenosylmethionine synthetase and suppresses S-adenosylmethionine production and ethylene biosynthesis in Arabidopsis

Plant Cell Environ.

Oxidative stress, antioxidants and stress tolerance

Trends Plant Sci.

Abscisic acid, H₂O₂ and nitric oxide interactions mediated cold-induced S-adenosylmethionine synthetase in Medicago sativa subsp. Falcata that confers cold tolerance through up-regulating polyamine oxidation

Overexpression of tomato enhancer of SOS3-1 (LeENH1) in tobacco enhanced salinity tolerance by excluding Na⁺ from the cytosol

Analysis of relative gene expression data using real-time quantitative PCR and the 2^−ΔΔCT method