{"title":"通过多胺转运和修饰提高番茄耐盐性。","authors":"Gwendolyn Kirschner","doi":"10.1111/tpj.17161","DOIUrl":null,"url":null,"abstract":"<p>Worldwide, 11% of irrigated land is affected by salinization (Food and Agriculture Organization of the United Nations, <span>2011</span>), limiting crop productivity due to osmotic stress, ion toxicity, and secondary stresses like oxidative and nutritional stress (Zhao et al., <span>2020</span>).</p><p>Recent studies have highlighted the role of polyamines in regulating tolerance to abiotic stress (Alcázar et al., <span>2010</span>). Polyamines, such as putrescine (Put), spermidine (Spd), and spermine (Spm), are low molecular weight aliphatic nitrogenous bases found in higher plants. They often conjugate with phenolic acids to form phenolamides, which act as antioxidants and play a significant role in the salt stress response of plants (Chen et al., <span>2019</span>).</p><p>Jie Yang, a postdoc in Shouchuang Wang's Lab at Hainan University in China and first author of the highlighted publication, is studying the modulation of polyamines in response to various stresses. As a former agricultural college student, he wants to use scientific and technological achievements to help promote agriculture, thereby raising farmers' living standards. Shouchuang Wang's Lab focuses on plant metabolomic research, developing new technologies for detection and using multi-omics tools to study metabolites, including polyamines. For their study, Yang and colleagues characterized the genetic basis of natural variation in polyamine and phenolamide metabolism in tomato (Yang et al., <span>2024</span>).</p><p>Tomatoes are a model plant for studying metabolic pathways due to their rich metabolic resources and well-established research system. However, domestication has led to the loss of disease resistance and abiotic stress tolerance traits, posing challenges to cultivation. Investigating genetic loci influencing tomato resistance is crucial for breeding high-resistance and high-quality varieties (Wang et al., <span>2024</span>).</p><p>Yang et al. used a metabolome-based genome-wide association study (mGWAS) on fruit polyamine data of 276 tomato accessions. They identified 12 loci significantly associated with polyamine accumulation, focusing on one locus on Chromosome 8. This locus included genes encoding a polyamine uptake transporter (<i>SlPUT3</i>), polyphenol oxidases (<i>SlPPOE</i> and <i>SlPPOF</i>), BAHD acyltransferases (<i>SlAT4</i> and <i>SlAT5</i>), and a 4-coumarate-coA ligase (<i>Sl4CL6</i>). Because polyamine synthesis mostly occurs in meristematic and growing tissue (Chen et al., <span>2019</span>) and all six genes were co-expressed in tomato roots, the authors hypothesized that these six genes form a gene cluster responsible for polyamine modification and transport.</p><p>Functional analysis showed that these genes are involved in polyamine modification and phenolamide synthesis. The polyamine transport function of SlPUT3 was confirmed in <i>Xenopus</i> oocytes, and overexpressing <i>SlPUT3</i> in tomatoes led to growth defects when supplemented with polyamines. That SlPUT3 acts as a polyamine uptake transporter was further verified by measuring the uptake of labeled polyamine spermine-(butyl-d8) into <i>SlPUT3</i>-overexpressing tomato lines. Eight hours after feeding, the plants showed higher spermine-(butyl-d8) content, and polyamine and phenolamide metabolites derived from Spm-d8 accumulated earlier. Thus, SlPUT3 facilitates the uptake of Spm into cells, where it is subsequently transformed into other polyamines and phenolamides to maintain polyamine homeostasis.</p><p>As an application of polyamines can enhance plant stress tolerance (Alcázar et al., <span>2010</span>), the authors measured the transcript levels of the genes in the cluster under drought, heat, and salt stress, and found that all transcript levels were elevated under salt stress. Seedlings overexpressing <i>SlPUT3</i>, <i>SlAT5</i>, <i>SlPPOE</i>, or <i>SlPPOF</i> coped better with salt stress than WT or <i>slput3</i> lines. The application of Spm attenuated the inhibitory effects of salt stress in the overexpression lines, and they accumulated more phenolamide under salt and Spm treatment.</p><p>In Arabidopsis, AtPUT3 interacts with the Na<sup>+</sup>/H<sup>+</sup> transporter AtSOS1, influencing transport capacity (Chai et al., <span>2020</span>). The authors hypothesized that SlPUT3 might interact with other transporters. They identified the aquaporin SlPIP2;4 as an interactor of SlPUT3, which transports H<sub>2</sub>O<sub>2</sub> into the cytoplasm. SlPUT3 restricted the transport activity of SlPIP2;4, and overexpression <i>SlPUT3</i> caused local necrosis in <i>Nicotiana benthamiana</i> leaves due to an H<sub>2</sub>O<sub>2</sub> burst and programmed cell death. This effect was also observed in <i>SlPUT3</i> overexpression lines of tomato when Spm was applied, inducing antioxidant enzymes and stress-responsive genes. While Spm effectively increased the expression of salt stress-induced genes, this effect was compromised if the lines were pre-treated with an H<sub>2</sub>O<sub>2</sub> scavenger. This suggests that the Spm-mediated stress response may depend on H<sub>2</sub>O<sub>2</sub> as a second messenger.</p><p>In summary, the authors propose two roles for polyamines in salt stress tolerance (Figure 1): Polyamines are modified by a series of enzymes (such as the gene cluster members <i>SlPPOE</i>, <i>SlPPOF</i>, <i>SlAT4</i>, <i>SlAT5</i> and <i>Sl4CL6</i>) to form phenolamides. In parallel, polyamine-derived H<sub>2</sub>O<sub>2</sub>, as a second messenger activates stress response genes. Both mechanisms enhance antioxidant levels and thereby increase stress tolerance.</p>","PeriodicalId":233,"journal":{"name":"The Plant Journal","volume":"120 5","pages":"1700-1701"},"PeriodicalIF":6.2000,"publicationDate":"2024-12-10","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://onlinelibrary.wiley.com/doi/epdf/10.1111/tpj.17161","citationCount":"0","resultStr":"{\"title\":\"Enhancing tomato salt tolerance through polyamine transport and modification\",\"authors\":\"Gwendolyn Kirschner\",\"doi\":\"10.1111/tpj.17161\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p>Worldwide, 11% of irrigated land is affected by salinization (Food and Agriculture Organization of the United Nations, <span>2011</span>), limiting crop productivity due to osmotic stress, ion toxicity, and secondary stresses like oxidative and nutritional stress (Zhao et al., <span>2020</span>).</p><p>Recent studies have highlighted the role of polyamines in regulating tolerance to abiotic stress (Alcázar et al., <span>2010</span>). Polyamines, such as putrescine (Put), spermidine (Spd), and spermine (Spm), are low molecular weight aliphatic nitrogenous bases found in higher plants. They often conjugate with phenolic acids to form phenolamides, which act as antioxidants and play a significant role in the salt stress response of plants (Chen et al., <span>2019</span>).</p><p>Jie Yang, a postdoc in Shouchuang Wang's Lab at Hainan University in China and first author of the highlighted publication, is studying the modulation of polyamines in response to various stresses. As a former agricultural college student, he wants to use scientific and technological achievements to help promote agriculture, thereby raising farmers' living standards. Shouchuang Wang's Lab focuses on plant metabolomic research, developing new technologies for detection and using multi-omics tools to study metabolites, including polyamines. For their study, Yang and colleagues characterized the genetic basis of natural variation in polyamine and phenolamide metabolism in tomato (Yang et al., <span>2024</span>).</p><p>Tomatoes are a model plant for studying metabolic pathways due to their rich metabolic resources and well-established research system. However, domestication has led to the loss of disease resistance and abiotic stress tolerance traits, posing challenges to cultivation. Investigating genetic loci influencing tomato resistance is crucial for breeding high-resistance and high-quality varieties (Wang et al., <span>2024</span>).</p><p>Yang et al. used a metabolome-based genome-wide association study (mGWAS) on fruit polyamine data of 276 tomato accessions. They identified 12 loci significantly associated with polyamine accumulation, focusing on one locus on Chromosome 8. This locus included genes encoding a polyamine uptake transporter (<i>SlPUT3</i>), polyphenol oxidases (<i>SlPPOE</i> and <i>SlPPOF</i>), BAHD acyltransferases (<i>SlAT4</i> and <i>SlAT5</i>), and a 4-coumarate-coA ligase (<i>Sl4CL6</i>). Because polyamine synthesis mostly occurs in meristematic and growing tissue (Chen et al., <span>2019</span>) and all six genes were co-expressed in tomato roots, the authors hypothesized that these six genes form a gene cluster responsible for polyamine modification and transport.</p><p>Functional analysis showed that these genes are involved in polyamine modification and phenolamide synthesis. The polyamine transport function of SlPUT3 was confirmed in <i>Xenopus</i> oocytes, and overexpressing <i>SlPUT3</i> in tomatoes led to growth defects when supplemented with polyamines. That SlPUT3 acts as a polyamine uptake transporter was further verified by measuring the uptake of labeled polyamine spermine-(butyl-d8) into <i>SlPUT3</i>-overexpressing tomato lines. Eight hours after feeding, the plants showed higher spermine-(butyl-d8) content, and polyamine and phenolamide metabolites derived from Spm-d8 accumulated earlier. Thus, SlPUT3 facilitates the uptake of Spm into cells, where it is subsequently transformed into other polyamines and phenolamides to maintain polyamine homeostasis.</p><p>As an application of polyamines can enhance plant stress tolerance (Alcázar et al., <span>2010</span>), the authors measured the transcript levels of the genes in the cluster under drought, heat, and salt stress, and found that all transcript levels were elevated under salt stress. Seedlings overexpressing <i>SlPUT3</i>, <i>SlAT5</i>, <i>SlPPOE</i>, or <i>SlPPOF</i> coped better with salt stress than WT or <i>slput3</i> lines. The application of Spm attenuated the inhibitory effects of salt stress in the overexpression lines, and they accumulated more phenolamide under salt and Spm treatment.</p><p>In Arabidopsis, AtPUT3 interacts with the Na<sup>+</sup>/H<sup>+</sup> transporter AtSOS1, influencing transport capacity (Chai et al., <span>2020</span>). The authors hypothesized that SlPUT3 might interact with other transporters. They identified the aquaporin SlPIP2;4 as an interactor of SlPUT3, which transports H<sub>2</sub>O<sub>2</sub> into the cytoplasm. SlPUT3 restricted the transport activity of SlPIP2;4, and overexpression <i>SlPUT3</i> caused local necrosis in <i>Nicotiana benthamiana</i> leaves due to an H<sub>2</sub>O<sub>2</sub> burst and programmed cell death. This effect was also observed in <i>SlPUT3</i> overexpression lines of tomato when Spm was applied, inducing antioxidant enzymes and stress-responsive genes. While Spm effectively increased the expression of salt stress-induced genes, this effect was compromised if the lines were pre-treated with an H<sub>2</sub>O<sub>2</sub> scavenger. This suggests that the Spm-mediated stress response may depend on H<sub>2</sub>O<sub>2</sub> as a second messenger.</p><p>In summary, the authors propose two roles for polyamines in salt stress tolerance (Figure 1): Polyamines are modified by a series of enzymes (such as the gene cluster members <i>SlPPOE</i>, <i>SlPPOF</i>, <i>SlAT4</i>, <i>SlAT5</i> and <i>Sl4CL6</i>) to form phenolamides. In parallel, polyamine-derived H<sub>2</sub>O<sub>2</sub>, as a second messenger activates stress response genes. 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Enhancing tomato salt tolerance through polyamine transport and modification
Worldwide, 11% of irrigated land is affected by salinization (Food and Agriculture Organization of the United Nations, 2011), limiting crop productivity due to osmotic stress, ion toxicity, and secondary stresses like oxidative and nutritional stress (Zhao et al., 2020).
Recent studies have highlighted the role of polyamines in regulating tolerance to abiotic stress (Alcázar et al., 2010). Polyamines, such as putrescine (Put), spermidine (Spd), and spermine (Spm), are low molecular weight aliphatic nitrogenous bases found in higher plants. They often conjugate with phenolic acids to form phenolamides, which act as antioxidants and play a significant role in the salt stress response of plants (Chen et al., 2019).
Jie Yang, a postdoc in Shouchuang Wang's Lab at Hainan University in China and first author of the highlighted publication, is studying the modulation of polyamines in response to various stresses. As a former agricultural college student, he wants to use scientific and technological achievements to help promote agriculture, thereby raising farmers' living standards. Shouchuang Wang's Lab focuses on plant metabolomic research, developing new technologies for detection and using multi-omics tools to study metabolites, including polyamines. For their study, Yang and colleagues characterized the genetic basis of natural variation in polyamine and phenolamide metabolism in tomato (Yang et al., 2024).
Tomatoes are a model plant for studying metabolic pathways due to their rich metabolic resources and well-established research system. However, domestication has led to the loss of disease resistance and abiotic stress tolerance traits, posing challenges to cultivation. Investigating genetic loci influencing tomato resistance is crucial for breeding high-resistance and high-quality varieties (Wang et al., 2024).
Yang et al. used a metabolome-based genome-wide association study (mGWAS) on fruit polyamine data of 276 tomato accessions. They identified 12 loci significantly associated with polyamine accumulation, focusing on one locus on Chromosome 8. This locus included genes encoding a polyamine uptake transporter (SlPUT3), polyphenol oxidases (SlPPOE and SlPPOF), BAHD acyltransferases (SlAT4 and SlAT5), and a 4-coumarate-coA ligase (Sl4CL6). Because polyamine synthesis mostly occurs in meristematic and growing tissue (Chen et al., 2019) and all six genes were co-expressed in tomato roots, the authors hypothesized that these six genes form a gene cluster responsible for polyamine modification and transport.
Functional analysis showed that these genes are involved in polyamine modification and phenolamide synthesis. The polyamine transport function of SlPUT3 was confirmed in Xenopus oocytes, and overexpressing SlPUT3 in tomatoes led to growth defects when supplemented with polyamines. That SlPUT3 acts as a polyamine uptake transporter was further verified by measuring the uptake of labeled polyamine spermine-(butyl-d8) into SlPUT3-overexpressing tomato lines. Eight hours after feeding, the plants showed higher spermine-(butyl-d8) content, and polyamine and phenolamide metabolites derived from Spm-d8 accumulated earlier. Thus, SlPUT3 facilitates the uptake of Spm into cells, where it is subsequently transformed into other polyamines and phenolamides to maintain polyamine homeostasis.
As an application of polyamines can enhance plant stress tolerance (Alcázar et al., 2010), the authors measured the transcript levels of the genes in the cluster under drought, heat, and salt stress, and found that all transcript levels were elevated under salt stress. Seedlings overexpressing SlPUT3, SlAT5, SlPPOE, or SlPPOF coped better with salt stress than WT or slput3 lines. The application of Spm attenuated the inhibitory effects of salt stress in the overexpression lines, and they accumulated more phenolamide under salt and Spm treatment.
In Arabidopsis, AtPUT3 interacts with the Na+/H+ transporter AtSOS1, influencing transport capacity (Chai et al., 2020). The authors hypothesized that SlPUT3 might interact with other transporters. They identified the aquaporin SlPIP2;4 as an interactor of SlPUT3, which transports H2O2 into the cytoplasm. SlPUT3 restricted the transport activity of SlPIP2;4, and overexpression SlPUT3 caused local necrosis in Nicotiana benthamiana leaves due to an H2O2 burst and programmed cell death. This effect was also observed in SlPUT3 overexpression lines of tomato when Spm was applied, inducing antioxidant enzymes and stress-responsive genes. While Spm effectively increased the expression of salt stress-induced genes, this effect was compromised if the lines were pre-treated with an H2O2 scavenger. This suggests that the Spm-mediated stress response may depend on H2O2 as a second messenger.
In summary, the authors propose two roles for polyamines in salt stress tolerance (Figure 1): Polyamines are modified by a series of enzymes (such as the gene cluster members SlPPOE, SlPPOF, SlAT4, SlAT5 and Sl4CL6) to form phenolamides. In parallel, polyamine-derived H2O2, as a second messenger activates stress response genes. Both mechanisms enhance antioxidant levels and thereby increase stress tolerance.
期刊介绍:
Publishing the best original research papers in all key areas of modern plant biology from the world"s leading laboratories, The Plant Journal provides a dynamic forum for this ever growing international research community.
Plant science research is now at the forefront of research in the biological sciences, with breakthroughs in our understanding of fundamental processes in plants matching those in other organisms. The impact of molecular genetics and the availability of model and crop species can be seen in all aspects of plant biology. For publication in The Plant Journal the research must provide a highly significant new contribution to our understanding of plants and be of general interest to the plant science community.