The Role of Polyamines in Plant Disease Resistance

Takahashi, Yoshihiro

doi:10.2525/ecb.54.17

Cited by 23 publications

(17 citation statements)

References 57 publications

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“…Polyamines are present in all life forms and are involved in a plethora of cellular processes including growth, development, stress response, and pathogenesis (reviewed in Valdes-Santiago et al, 2012; Minocha et al, 2014; Miller-Fleming et al, 2015; Takahashi, 2016; Pal and Janda, 2017). Consequently, the PA metabolic pathway in the host plant as well as in the pathogen has been the target of a number of studies to improve disease resistance in plants.…”

Section: Discussionmentioning

confidence: 99%

“…As Orn is synthesized from Glu, which serves both as an entry point for N, and a major precursor for several other AAs in plants, alterations in PA metabolism can impact AA levels in living cells (Mohapatra et al, 2010; Majumdar et al, 2013, 2016). The role of PAs in plant disease resistance is highly evident from several studies that involved alteration of tissue PA concentrations through genetic manipulations or exogenous application of PAs (reviewed in Jiménez-Bremont et al, 2014; Takahashi, 2016; Pal and Janda, 2017). Over-expression of a human SAMDC gene in tobacco resulted in increased accumulation of free and conjugated PAs and conferred tolerance to Verticillium dahliae and Fusarium oxysporum (Waie and Rajam, 2003).…”

Section: Introductionmentioning

confidence: 99%

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Contribution of Maize Polyamine and Amino Acid Metabolism Toward Resistance Against Aspergillus flavus Infection and Aflatoxin Production

et al. 2019

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Polyamines (PAs) are ubiquitous polycations found in plants and other organisms that are essential for growth, development, and resistance against abiotic and biotic stresses. The role of PAs in plant disease resistance depends on the relative abundance of higher PAs [spermidine (Spd), spermine (Spm)] vs. the diamine putrescine (Put) and PA catabolism. With respect to the pathogen, PAs are required to achieve successful pathogenesis of the host. Maize is an important food and feed crop, which is highly susceptible to Aspergillus flavus infection. Upon infection, the fungus produces carcinogenic aflatoxins and numerous other toxic secondary metabolites that adversely affect human health and crop value worldwide. To evaluate the role of PAs in aflatoxin resistance in maize, in vitro kernel infection assays were performed using maize lines that are susceptible (SC212) or resistant (TZAR102, MI82) to aflatoxin production. Results indicated significant induction of both PA biosynthetic and catabolic genes upon A. flavus infection. As compared to the susceptible line, the resistant maize lines showed higher basal expression of PA metabolism genes in mock-inoculated kernels that increased upon fungal infection. In general, increased biosynthesis and conversion of Put to Spd and Spm along with their increased catabolism was evident in the resistant lines vs. the susceptible line SC212. There were higher concentrations of amino acids such as glutamate (Glu), glutamine (Gln) and γ-aminobutyric acid (GABA) in SC212. The resistant lines were significantly lower in fungal load and aflatoxin production as compared to the susceptible line. The data presented here demonstrate an important role of PA metabolism in the resistance of maize to A. flavus colonization and aflatoxin contamination. These results provide future direction for the manipulation of PA metabolism in susceptible maize genotypes to improve aflatoxin resistance and overall stress tolerance.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Contribution of Maize Polyamine and Amino Acid Metabolism Toward Resistance Against Aspergillus flavus Infection and Aflatoxin Production

et al. 2019

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“…Polyamines are common to both plants and fungal pathogens, and their metabolism can play significant roles in host defense as well as successful pathogenesis and mycotoxin production during compatible host-pathogen interactions ( Gardiner et al, 2009 , 2010 ; Valdés-Santiago and Ruiz-Herrera, 2013 ; reviewed in Takahashi, 2016 ). It was demonstrated that the fungus Tapesia yallundae , rendered avirulent due to inactivation of the odc gene, had virulence restored upon re-introduction back into plants, possibly due to the uptake of PAs from the host thus compensating for PA depletion in the pathogen ( Mueller et al, 2001 ).…”

Section: Introductionmentioning

confidence: 99%

The Aspergillus flavus Spermidine Synthase (spds) Gene, Is Required for Normal Development, Aflatoxin Production, and Pathogenesis During Infection of Maize Kernels

et al. 2018

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Aspergillus flavus is a soil-borne saprophyte and an opportunistic pathogen of both humans and plants. This fungus not only causes disease in important food and feed crops such as maize, peanut, cottonseed, and tree nuts but also produces the toxic and carcinogenic secondary metabolites (SMs) known as aflatoxins. Polyamines (PAs) are ubiquitous polycations that influence normal growth, development, and stress responses in living organisms and have been shown to play a significant role in fungal pathogenesis. Biosynthesis of spermidine (Spd) is critical for cell growth as it is required for hypusination-mediated activation of eukaryotic translation initiation factor 5A (eIF5A), and other biochemical functions. The tri-amine Spd is synthesized from the diamine putrescine (Put) by the enzyme spermidine synthase (Spds). Inactivation of spds resulted in a total loss of growth and sporulation in vitro which could be partially restored by addition of exogenous Spd. Complementation of the Δspds mutant with a wild type (WT) A. flavus spds gene restored the WT phenotype. In WT A. flavus, exogenous supply of Spd (in vitro) significantly increased the production of sclerotia and SMs. Infection of maize kernels with the Δspds mutant resulted in a significant reduction in fungal growth, sporulation, and aflatoxin production compared to controls. Quantitative PCR of Δspds mutant infected seeds showed down-regulation of aflatoxin biosynthetic genes in the mutant compared to WT A. flavus infected seeds. Expression analyses of PA metabolism/transport genes during A. flavus-maize interaction showed significant increase in the expression of arginine decarboxylase (Adc) and S-adenosylmethionine decarboxylase (Samdc) genes in the maize host and PA uptake transporters in the fungus. The results presented here demonstrate that Spd biosynthesis is critical for normal development and pathogenesis of A. flavus and pre-treatment of a Δspds mutant with Spd or Spd uptake from the host plant, are insufficient to restore WT levels of pathogenesis and aflatoxin production during seed infection. The data presented here suggest that future studies targeting spermidine biosynthesis in A. flavus, using RNA interference-based host-induced gene silencing approaches, may be an effective strategy to reduce aflatoxin contamination in maize and possibly in other susceptible crops.

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“…In this study, along with the increased vegetative growth and earlier flowering in the transgenic lines, ectopic expression of GhSAMDC 1 increased total polyamines and spermine, and reduced spermidine. Expression analysis of NtSPDS [1][2][3][4][5] and NtSPMS demonstrated that NtSPDS 4 and NtSPMS were downregulated and upregulated, respectively, in the transgenic lines ( Fig. 1), indicating that the conversion of spermidine to spermine might be regulated by NtSPDS 4 and NtSPMS in tobacco.…”

Section: Discussionmentioning

confidence: 99%

Ectopic expression of GhSAMDC1 improved plant vegetative growth and early flowering through conversion of spermidine to spermine in tobacco

Zhu

Tian

Zhu

et al. 2020

Sci Rep

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Polyamines play essential roles in plant development and various stress responses. In this study, one of the cotton S-adenosylmethionine decarboxylase (SAMDC) genes, GhSAMDC 1 , was constructed in the pGWB17 vector and overexpressed in tobacco. Leaf area and plant height increased 25.9-36.6% and 15.0-27.0%, respectively, compared to the wild type, and flowering time was advanced by 5 days in transgenic tobacco lines. polyamine and gene expression analyses demonstrated that a decrease in spermidine and an increase in total polyamines and spermine might be regulated by NtSPDS 4 and NtSPMS in transgenic plants. Furthermore, exogenous spermidine, spermine and spermidine synthesis inhibitor dicyclohexylamine were used for complementary tests, which resulted in small leaves and dwarf plants, big leaves and early flowering, and big leaves and dwarf plants, respectively. these results indicate that spermidine and spermine are mainly involved in the vegetative growth and early flowering stages, respectively. Expression analysis of flowering-related genes suggested that NtSOC 1 , NtAP 1 , NtNFL 1 and NtFT 4 were upregulated in transgenic plants. In conclusion, ectopic GhSAMDC 1 is involved in the conversion of spermidine to spermine, resulting in rapid vegetative growth and early flowering in tobacco, which could be applied to genetically improve plants. Polyamines, including putrescine (diamine), spermidine (triamine), and spermine (tetraamine), play various roles in plants 1,2. Many reports indicate that polyamines are affect the fluidity of the lipid membrane and participate in the biotic and abiotic stress responses 3-9. Furthermore, polyamines have been reported to be involved in various physiological processes 9-14. The polyamine metabolic pathways have been elucidated in plants 15. Putrescine originates from ornithine or arginine, catalysed by ornithine decarboxylase, or arginine decarboxylase, agmatine iminohydrolase and N-carbamoyl putrescine amidohydrolase. Spermidine and spermine are derived from putrescine and are catalysed by spermidine and spermine synthases, respectively. S-adenosylmethionine decarboxylases (SAMDCs) catalyse the S-adenosylmethionine decarboxylation reaction and provide an aminopropyl group, which is involved in spermidine and spermine synthesis. SAMDC transcripts have been analysed in a wide variety of plant species, often with higher transcript levels detected in reproductive than vegetative organs 16-21. Further evidence that polyamines are required for growth and development comes from analysing the Arabidopsis thalian bud2 mutant. This mutant has an inactivated AtSAMDC 4 gene and an enlarged vascular phenotype 22. Moreover, AtSAMDC 1 is involved in an interaction between beet severe curly top virus and Arabidopsis plants 23. Numerous studies have reported upregulation of SAMDC in response to various stressors, including drought, salt, high or low

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The Role of Polyamines in Plant Disease Resistance

Cited by 23 publications

References 57 publications

Contribution of Maize Polyamine and Amino Acid Metabolism Toward Resistance Against Aspergillus flavus Infection and Aflatoxin Production

Contribution of Maize Polyamine and Amino Acid Metabolism Toward Resistance Against Aspergillus flavus Infection and Aflatoxin Production

The Aspergillus flavus Spermidine Synthase (spds) Gene, Is Required for Normal Development, Aflatoxin Production, and Pathogenesis During Infection of Maize Kernels

Ectopic expression of GhSAMDC1 improved plant vegetative growth and early flowering through conversion of spermidine to spermine in tobacco

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