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

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...

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Main Authors: Rajtilak Majumdar, Rakesh Minocha, Matthew D. Lebar, Kanniah Rajasekaran, Stephanie Long, Carol Carter-Wientjes, Subhash Minocha, Jeffrey W. Cary
Format: Article
Language:English
Published: Frontiers Media S.A. 2019-05-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/article/10.3389/fpls.2019.00692/full
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author Rajtilak Majumdar
Rakesh Minocha
Matthew D. Lebar
Kanniah Rajasekaran
Stephanie Long
Carol Carter-Wientjes
Subhash Minocha
Jeffrey W. Cary
author_facet Rajtilak Majumdar
Rakesh Minocha
Matthew D. Lebar
Kanniah Rajasekaran
Stephanie Long
Carol Carter-Wientjes
Subhash Minocha
Jeffrey W. Cary
author_sort Rajtilak Majumdar
collection DOAJ
description 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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spelling doaj.art-8f01ffc105ff411e8c40c9359c0dd78d2022-12-22T01:39:03ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2019-05-011010.3389/fpls.2019.00692453984Contribution of Maize Polyamine and Amino Acid Metabolism Toward Resistance Against Aspergillus flavus Infection and Aflatoxin ProductionRajtilak Majumdar0Rakesh Minocha1Matthew D. Lebar2Kanniah Rajasekaran3Stephanie Long4Carol Carter-Wientjes5Subhash Minocha6Jeffrey W. Cary7Food and Feed Safety Research Unit, Southern Regional Research Center, United States Department of Agriculture, Agricultural Research Service, New Orleans, LA, United StatesUnited States Department of Agriculture Forest Service, Northern Research Station, Durham, NH, United StatesFood and Feed Safety Research Unit, Southern Regional Research Center, United States Department of Agriculture, Agricultural Research Service, New Orleans, LA, United StatesFood and Feed Safety Research Unit, Southern Regional Research Center, United States Department of Agriculture, Agricultural Research Service, New Orleans, LA, United StatesUnited States Department of Agriculture Forest Service, Northern Research Station, Durham, NH, United StatesFood and Feed Safety Research Unit, Southern Regional Research Center, United States Department of Agriculture, Agricultural Research Service, New Orleans, LA, United StatesDepartment of Biological Sciences, University of New Hampshire, Durham, NH, United StatesFood and Feed Safety Research Unit, Southern Regional Research Center, United States Department of Agriculture, Agricultural Research Service, New Orleans, LA, United StatesPolyamines (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.https://www.frontiersin.org/article/10.3389/fpls.2019.00692/fullAspergillus flavuss-adenosylmethionine decarboxylasepolyamine oxidasemycotoxinpolyamine uptakeamino acids
spellingShingle Rajtilak Majumdar
Rakesh Minocha
Matthew D. Lebar
Kanniah Rajasekaran
Stephanie Long
Carol Carter-Wientjes
Subhash Minocha
Jeffrey W. Cary
Contribution of Maize Polyamine and Amino Acid Metabolism Toward Resistance Against Aspergillus flavus Infection and Aflatoxin Production
Frontiers in Plant Science
Aspergillus flavus
s-adenosylmethionine decarboxylase
polyamine oxidase
mycotoxin
polyamine uptake
amino acids
title Contribution of Maize Polyamine and Amino Acid Metabolism Toward Resistance Against Aspergillus flavus Infection and Aflatoxin Production
title_full Contribution of Maize Polyamine and Amino Acid Metabolism Toward Resistance Against Aspergillus flavus Infection and Aflatoxin Production
title_fullStr Contribution of Maize Polyamine and Amino Acid Metabolism Toward Resistance Against Aspergillus flavus Infection and Aflatoxin Production
title_full_unstemmed Contribution of Maize Polyamine and Amino Acid Metabolism Toward Resistance Against Aspergillus flavus Infection and Aflatoxin Production
title_short Contribution of Maize Polyamine and Amino Acid Metabolism Toward Resistance Against Aspergillus flavus Infection and Aflatoxin Production
title_sort contribution of maize polyamine and amino acid metabolism toward resistance against aspergillus flavus infection and aflatoxin production
topic Aspergillus flavus
s-adenosylmethionine decarboxylase
polyamine oxidase
mycotoxin
polyamine uptake
amino acids
url https://www.frontiersin.org/article/10.3389/fpls.2019.00692/full
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