Role of mannitol metabolism in the pathogenicity of the necrotrophic fungus Alternaria brassicicola

In this study, the physiological functions of fungal mannitol metabolism in the pathogenicity and protection against environmental stresses were investigated in the necrotrophic fungus Alternaria brassicicola. Mannitol metabolism was examined during infection of Brassica oleracea leaves by sequentia...

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Published in:Frontiers in plant science Vol. 4; p. 131
Main Authors: Calmes, Benoit, Guillemette, Thomas, Teyssier, Lény, Siegler, Benjamin, Pigné, Sandrine, Landreau, Anne, Iacomi, Béatrice, Lemoine, Rémi, Richomme, Pascal, Simoneau, Philippe
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Abstract In this study, the physiological functions of fungal mannitol metabolism in the pathogenicity and protection against environmental stresses were investigated in the necrotrophic fungus Alternaria brassicicola. Mannitol metabolism was examined during infection of Brassica oleracea leaves by sequential HPLC quantification of the major soluble carbohydrates and expression analysis of genes encoding two proteins of mannitol metabolism, i.e., a mannitol dehydrogenase (AbMdh), and a mannitol-1-phosphate dehydrogenase (AbMpd). Knockout mutants deficient for AbMdh or AbMpd and a double mutant lacking both enzyme activities were constructed. Their capacity to cope with various oxidative and drought stresses and their pathogenic behavior were evaluated. Metabolic and gene expression profiling indicated an increase in mannitol production during plant infection. Depending on the mutants, distinct pathogenic processes, such as leaf and silique colonization, sporulation, survival on seeds, were impaired by comparison to the wild-type. This pathogenic alteration could be partly explained by the differential susceptibilities of mutants to oxidative and drought stresses. These results highlight the importance of mannitol metabolism with respect to the ability of A. brassicicola to efficiently accomplish key steps of its pathogenic life cycle.
AbstractList In this study, the physiological functions of fungal mannitol metabolism in the pathogenicity and protection against environmental stresses were investigated in the necrotrophic fungus Alternaria brassicicola . Mannitol metabolism was examined during infection of Brassica oleracea leaves by sequential HPLC quantification of the major soluble carbohydrates and expression analysis of genes encoding two proteins of mannitol metabolism, i.e., a mannitol dehydrogenase ( AbMdh ), and a mannitol-1-phosphate dehydrogenase ( AbMpd ). Knockout mutants deficient for AbMdh or AbMpd and a double mutant lacking both enzyme activities were constructed. Their capacity to cope with various oxidative and drought stresses and their pathogenic behavior were evaluated. Metabolic and gene expression profiling indicated an increase in mannitol production during plant infection. Depending on the mutants, distinct pathogenic processes, such as leaf and silique colonization, sporulation, survival on seeds, were impaired by comparison to the wild-type. This pathogenic alteration could be partly explained by the differential susceptibilities of mutants to oxidative and drought stresses. These results highlight the importance of mannitol metabolism with respect to the ability of A. brassicicola to efficiently accomplish key steps of its pathogenic life cycle.
In this study, the physiological functions of fungal mannitol metabolism in the pathogenicity and protection against environmental stresses were investigated in the necrotrophic fungus Alternada brassicicola. Mannitol metabolism was examined during infection of Brass/ca oleracea leaves by sequential HPLC quantification of the major soluble carbohydrates and expression analysis of genes encoding two proteins of mannitol metabolism, i.e., a mannitol dehydrogenase (AbMdh), and a mannito1-1-phosphate dehydrogenase (AbMpd). Knockout mutants deficient for AbMdf7 or AbMpd and a double mutant lacking both enzyme activities were constructed. Their capacity to cope with various oxidative and drought stresses and their pathogenic behavior were evaluated. Metabolic and gene expression profiling indicated an increase in mannitol production during plant infection. Depending on the mutants, distinct pathogenic processes, such as leaf and silique colonization, sporulation, survival on seeds, were impaired by comparison to the wild-type. This pathogenic alteration could be partly explained by the differential susceptibilities of mutants to oxidative and drought stresses. These results highlight the importance of mannitol metabolism with respect to the ability of A. brassicrcola to efficiently accomplish key steps of its pathogenic life cycle.
In this study, the physiological functions of fungal mannitol metabolism in the pathogenicity and protection against environmental stresses were investigated in the necrotrophic fungus Alternaria brassicicola. Mannitol metabolism was examined during infection of Brassica oleracea leaves by sequential HPLC quantification of the major soluble carbohydrates and expression analysis of genes encoding two proteins of mannitol metabolism, i.e. a mannitol dehydrogenase (AbMdh), and a mannitol-1-phosphate dehydrogenase (AbMpd). Knockout mutants deficient for AbMdh or AbMpd and a double mutant lacking both enzyme activities were constructed. Their capacity to cope with various oxidative and drought stresses and their pathogenic behaviour were evaluated. Metabolic and gene expression profiling indicated an increase in mannitol production during plant infection. Depending on the mutants, distinct pathogenic processes, such as leaf and silique colonization, sporulation, survival on seeds, were impaired by comparison to the wild-type. This pathogenic alteration could be partly explained by the differential susceptibilities of mutants to oxidative and drought stresses. These results highlight the importance of mannitol metabolism with respect to the ability of A. brassicicola to efficiently accomplish key steps of its pathogenic life cycle.
In this study, the physiological functions of fungal mannitol metabolism in the pathogenicity and protection against environmental stresses were investigated in the necrotrophic fungus Alternaria brassicicola. Mannitol metabolism was examined during infection of Brassica oleracea leaves by sequential HPLC quantification of the major soluble carbohydrates and expression analysis of genes encoding two proteins of mannitol metabolism, i.e., a mannitol dehydrogenase (AbMdh), and a mannitol-1-phosphate dehydrogenase (AbMpd). Knockout mutants deficient for AbMdh or AbMpd and a double mutant lacking both enzyme activities were constructed. Their capacity to cope with various oxidative and drought stresses and their pathogenic behavior were evaluated. Metabolic and gene expression profiling indicated an increase in mannitol production during plant infection. Depending on the mutants, distinct pathogenic processes, such as leaf and silique colonization, sporulation, survival on seeds, were impaired by comparison to the wild-type. This pathogenic alteration could be partly explained by the differential susceptibilities of mutants to oxidative and drought stresses. These results highlight the importance of mannitol metabolism with respect to the ability of A. brassicicola to efficiently accomplish key steps of its pathogenic life cycle.
Author Simoneau, Philippe
Iacomi, Béatrice
Lemoine, Rémi
Siegler, Benjamin
Landreau, Anne
Guillemette, Thomas
Calmes, Benoit
Pigné, Sandrine
Richomme, Pascal
Teyssier, Lény
AuthorAffiliation 1 SFR 4207 QUASAV, UMR 1345 IRHS, Université d'Angers Angers Cedex, France
6 USAMV Bucharest, Romania
3 SFR 4207 QUASAV, Agrocampus-Ouest, UMR 1345 IRHS Angers Cedex, France
4 Plateforme d'Ingénierie et Analyses Moléculaires, Université d'Angers Angers Cedex, France
2 SFR 4207 QUASAV, INRA, UMR 1345 IRHS Angers Cedex, France
5 SONAS EA 921, SFR 4207, QUASAV UFR des Sciences Pharmaceutiques et d'Ingénierie de la Santé, Université d'Angers Angers Cedex, France
7 Ecologie, Biologie des Interactions, UMR 7267 CNRS/Université de Poitiers Poitiers, France
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ContentType Journal Article
Copyright Distributed under a Creative Commons Attribution 4.0 International License
Copyright © 2013 Calmes, Guillemette, Teyssier, Siegler, Pigné, Landreau, Iacomi, Lemoine, Richomme and Simoneau. 2013
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– notice: Copyright © 2013 Calmes, Guillemette, Teyssier, Siegler, Pigné, Landreau, Iacomi, Lemoine, Richomme and Simoneau. 2013
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Keywords brassicicolin A
pathogenicity
Alternaria brassicicola
null mutants
isothiocyanates
oxidative and drought stress
mannitol
CHAIN DEHYDROGENASES
ASPERGILLUS-NIGER
BOTRYTIS-CINEREA
ANTIFUNGAL ACTIVITY
FILAMENTOUS FUNGI
GENE
STAGONOSPORA-NODORUM
BIOSYNTHESIS
CRYPTOCOCCUS-NEOFORMANS
STRESS TOLERANCE
Language English
License Distributed under a Creative Commons Attribution 4.0 International License: http://creativecommons.org/licenses/by/4.0
This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in other forums, provided the original authors and source are credited and subject to any copyright notices concerning any third-party graphics etc.
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content type line 23
Edited by: Adi Avni, Tel Aviv University, Israel
Reviewed by: Mary B. Mudgett, Stanford University, USA; Jane Glazebrook, University of Minnesota-Twin Cities, USA
This article was submitted to Frontiers in Plant-Microbe Interaction, a specialty of Frontiers in Plant Science.
ORCID 0000-0002-5649-974X
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References 21251090 - Mol Microbiol. 2011 Mar;79(5):1305-24
12912888 - Eukaryot Cell. 2003 Aug;2(4):690-8
7549480 - Plant Cell. 1995 Aug;7(8):1221-33
20136633 - Biochem J. 2010 Mar 29;427(2):323-32
17219185 - Planta. 2007 Jun;226(1):251-65
12231996 - Plant Physiol. 1993 Nov;103(3):1001-1008
17317242 - Fungal Genet Biol. 2007 Oct;44(10):965-78
12781675 - Fungal Genet Biol. 2003 Jul;39(2):168-75
9112772 - Plant Physiol. 1997 Apr;113(4):1177-83
28947 - Eur J Biochem. 1978 Aug 1;88(2):607-12
20305000 - Eukaryot Cell. 2010 Sep;9(9):1398-402
16404948 - Mol Plant Microbe Interact. 2006 Jan;19(1):7-15
7742302 - Biochemistry. 1995 May 9;34(18):6003-13
12223821 - Plant Physiol. 1997 Oct;115(2):527-532
20507491 - Mol Plant Pathol. 2007 Mar;8(2):195-208
18355747 - C R Biol. 2008 Apr;331(4):255-61
17092745 - Fungal Genet Biol. 2007 Apr;44(4):258-68
22571391 - Plant Methods. 2012 May 09;8(1):16
11335726 - J Biol Chem. 2001 Jul 20;276(29):27555-61
20569383 - Mol Plant Pathol. 2003 Jul 1;4(4):225-36
11319072 - Appl Environ Microbiol. 2001 May;67(5):1987-94
20812995 - Cell Microbiol. 2011 Jan;13(1):62-80
21299839 - FEBS J. 2011 Apr;278(8):1264-76
19223049 - Phytochemistry. 2009 Feb;70(3):394-402
15037621 - J Biol Chem. 2004 Jun 11;279(24):25075-84
9112783 - Plant Physiol. 1997 Apr;113(4):1427-35
9844027 - Proc Natl Acad Sci U S A. 1998 Dec 8;95(25):15129-33
17442575 - Trends Microbiol. 2007 Jun;15(6):257-62
15465386 - Fungal Genet Biol. 2004 Nov;41(11):973-81
9148737 - Biochem J. 1997 Mar 15;322 ( Pt 3):681-92
18549402 - FEMS Microbiol Lett. 2008 Aug;285(1):122-9
19500266 - New Phytol. 2009;183(4):1149-62
16859492 - Biochem J. 2006 Oct 15;399(2):231-9
8621921 - J Immunol. 1996 May 15;156(10):3836-40
15720079 - Mol Plant Microbe Interact. 2005 Feb;18(2):110-5
16987106 - Biochem J. 2006 Oct 15;399(2):e3-5
23134520 - Mol Plant Microbe Interact. 2012 Dec;25(12 ):1628-38
12366799 - Plant J. 2002 Oct;32(1):41-9
20569213 - Biotechniques. 2010 May;48(5):399-404
17631523 - Plant Physiol. 2007 Sep;145(1):62-74
16392246 - Mycologia. 2005 May-Jun;97(3):580-8
19011080 - Appl Environ Microbiol. 2009 Jan;75(1):127-34
16441347 - Plant J. 2006 Feb;45(4):523-39
19726575 - Plant Physiol. 2009 Nov;151(3):1459-75
15618426 - Plant Physiol. 2005 Jan;137(1):190-8
17488238 - Plant J. 2007 Jul;51(1):47-59
8936320 - Microbiology. 1996 Apr;142 ( Pt 4):937-43
19233304 - Fungal Genet Biol. 2009 May;46(5):381-9
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SubjectTerms Alternaria brassicicola
Isothiocyanates
Life Sciences
Mannitol
null mutants
oxidative and drought stress
pathogenicity
Plant Science
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Title Role of mannitol metabolism in the pathogenicity of the necrotrophic fungus Alternaria brassicicola
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