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...
Saved in:
Published in: | Frontiers in plant science Vol. 4; p. 131 |
---|---|
Main Authors: | , , , , , , , , , |
Format: | Journal Article |
Language: | English |
Published: |
Switzerland
Frontiers
2013
Frontiers Media S.A |
Subjects: | |
Online Access: | Get full text |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
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 |
AuthorAffiliation_xml | – name: 5 SONAS EA 921, SFR 4207, QUASAV UFR des Sciences Pharmaceutiques et d'Ingénierie de la Santé, Université d'Angers Angers Cedex, France – name: 6 USAMV Bucharest, Romania – name: 7 Ecologie, Biologie des Interactions, UMR 7267 CNRS/Université de Poitiers Poitiers, France – name: 3 SFR 4207 QUASAV, Agrocampus-Ouest, UMR 1345 IRHS Angers Cedex, France – name: 2 SFR 4207 QUASAV, INRA, UMR 1345 IRHS Angers Cedex, France – name: 1 SFR 4207 QUASAV, UMR 1345 IRHS, Université d'Angers Angers Cedex, France – name: 4 Plateforme d'Ingénierie et Analyses Moléculaires, Université d'Angers Angers Cedex, France |
Author_xml | – sequence: 1 givenname: Benoit surname: Calmes fullname: Calmes, Benoit organization: SFR 4207 QUASAV, UMR 1345 IRHS, Université d'Angers Angers Cedex, France ; SFR 4207 QUASAV, INRA, UMR 1345 IRHS Angers Cedex, France ; SFR 4207 QUASAV, Agrocampus-Ouest, UMR 1345 IRHS Angers Cedex, France – sequence: 2 givenname: Thomas surname: Guillemette fullname: Guillemette, Thomas – sequence: 3 givenname: Lény surname: Teyssier fullname: Teyssier, Lény – sequence: 4 givenname: Benjamin surname: Siegler fullname: Siegler, Benjamin – sequence: 5 givenname: Sandrine surname: Pigné fullname: Pigné, Sandrine – sequence: 6 givenname: Anne surname: Landreau fullname: Landreau, Anne – sequence: 7 givenname: Béatrice surname: Iacomi fullname: Iacomi, Béatrice – sequence: 8 givenname: Rémi surname: Lemoine fullname: Lemoine, Rémi – sequence: 9 givenname: Pascal surname: Richomme fullname: Richomme, Pascal – sequence: 10 givenname: Philippe surname: Simoneau fullname: Simoneau, Philippe |
BackLink | https://www.ncbi.nlm.nih.gov/pubmed/23717316$$D View this record in MEDLINE/PubMed https://hal.science/hal-01210006$$DView record in HAL |
BookMark | eNpdksFrHCEUxqWkNMk2597KHNvDbnR0nPFSWEKbBBYKpYXexHWeOwZHp-oE8t_XyaYhqQeV9773e0_5ztGJDx4Q-kDwhtJOXJrJpU2NCd3gspE36IxwztaM179PXtxP0UVKd7isBmMh2nfotKYtaSnhZ0j_CA6qYKpReW9zcNUIWe2Ds2msrK_yANWk8hAO4K22-WHRLkEPOoYcwzRYXZnZH-ZUbV2G6FW0qtpHlVIp0MGp9-itUS7BxdO5Qr--ff15dbPefb--vdru1poJmtctbxtNjai1UFBDS2qjmeqZ6bHWoulMRxXX3FDcko4SURPeAAXKSgZYU9MVuj1y-6Du5BTtqOKDDMrKx0CIB6littqBpISZTnfQE94zqkxHMKaa7HtKmsKGwvpyZE3zfoReg89RuVfQ1xlvB3kI95LyMkmZb4U-HwHDf2U3251cYpjUpSnm96RoPz01i-HPDCnL0SYNzikPYU6S0IaLhgmGi_TyKC2_n1IE88wmWC6ukIsr5OIK-eiKUvHx5Uue9f88QP8CWbm2Bg |
CitedBy_id | crossref_primary_10_1007_s00425_022_03925_z crossref_primary_10_1094_PDIS_11_22_2712_RE crossref_primary_10_1371_journal_pone_0101008 crossref_primary_10_3389_fmicb_2015_01019 crossref_primary_10_1007_s11274_017_2285_7 crossref_primary_10_1093_mtomcs_mfaa010 crossref_primary_10_1038_s41598_017_16401_6 crossref_primary_10_1073_pnas_2107994119 crossref_primary_10_13080_z_a_2018_105_012 crossref_primary_10_1016_j_ibiod_2017_05_011 crossref_primary_10_3390_plants10102212 crossref_primary_10_1038_s41467_022_32394_x crossref_primary_10_1371_journal_pone_0169441 crossref_primary_10_3389_fpls_2018_00928 crossref_primary_10_1016_j_tplants_2016_01_006 crossref_primary_10_1371_journal_pone_0075143 crossref_primary_10_1016_j_fgb_2015_09_009 crossref_primary_10_1038_s41598_019_48823_9 crossref_primary_10_1128_aem_01034_23 crossref_primary_10_1186_s12866_015_0462_0 crossref_primary_10_3389_fmicb_2020_00834 crossref_primary_10_3390_jof8030298 crossref_primary_10_3389_fmicb_2022_1019800 crossref_primary_10_3390_jof8070667 crossref_primary_10_1186_s12866_019_1667_4 crossref_primary_10_1016_j_ram_2016_05_004 crossref_primary_10_3389_ffgc_2024_1379791 crossref_primary_10_1111_tpj_12454 crossref_primary_10_1128_mBio_02660_18 crossref_primary_10_1093_femsle_fnx223 |
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 |
Copyright_xml | – notice: Distributed under a Creative Commons Attribution 4.0 International License – notice: Copyright © 2013 Calmes, Guillemette, Teyssier, Siegler, Pigné, Landreau, Iacomi, Lemoine, Richomme and Simoneau. 2013 |
DBID | NPM AAYXX CITATION 7X8 1XC VOOES 5PM DOA |
DOI | 10.3389/fpls.2013.00131 |
DatabaseName | PubMed CrossRef MEDLINE - Academic Hyper Article en Ligne (HAL) Hyper Article en Ligne (HAL) (Open Access) PubMed Central (Full Participant titles) Directory of Open Access Journals |
DatabaseTitle | PubMed CrossRef MEDLINE - Academic |
DatabaseTitleList | PubMed |
Database_xml | – sequence: 1 dbid: DOA name: Directory of Open Access Journals url: http://www.doaj.org/ sourceTypes: Open Website |
DeliveryMethod | fulltext_linktorsrc |
Discipline | Botany |
EISSN | 1664-462X |
EndPage | 131 |
ExternalDocumentID | oai_doaj_org_article_314f8c8ed16d43af81003c1bd315831e oai_HAL_hal_01210006v1 10_3389_fpls_2013_00131 23717316 |
Genre | Journal Article |
GroupedDBID | 5VS 9T4 AAFWJ AAKDD ACGFO ACGFS ACXDI ADBBV ADRAZ AENEX ALMA_UNASSIGNED_HOLDINGS AOIJS BCNDV EBD ECGQY GROUPED_DOAJ GX1 HYE IAO IEA IGS IPNFZ ISR KQ8 M48 M~E NPM OK1 PGMZT RIG RNS RPM AAYXX CITATION 7X8 1XC VOOES 5PM AFPKN |
ID | FETCH-LOGICAL-c493t-7675c3f92c9ae2e712fc4ad4fd0cc958f83a6c6f307183192165e3e348f8e4523 |
IEDL.DBID | RPM |
ISSN | 1664-462X |
IngestDate | Tue Oct 22 15:10:13 EDT 2024 Tue Sep 17 20:49:30 EDT 2024 Tue Oct 15 15:17:28 EDT 2024 Fri Oct 25 07:29:47 EDT 2024 Thu Nov 21 20:43:26 EST 2024 Tue Oct 15 23:47:08 EDT 2024 |
IsDoiOpenAccess | true |
IsOpenAccess | true |
IsPeerReviewed | true |
IsScholarly | true |
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. |
LinkModel | DirectLink |
MergedId | FETCHMERGED-LOGICAL-c493t-7675c3f92c9ae2e712fc4ad4fd0cc958f83a6c6f307183192165e3e348f8e4523 |
Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 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 0000-0002-3890-9848 0000-0001-7788-2556 |
OpenAccessLink | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3652318/ |
PMID | 23717316 |
PQID | 1356954940 |
PQPubID | 23479 |
PageCount | 1 |
ParticipantIDs | doaj_primary_oai_doaj_org_article_314f8c8ed16d43af81003c1bd315831e pubmedcentral_primary_oai_pubmedcentral_nih_gov_3652318 hal_primary_oai_HAL_hal_01210006v1 proquest_miscellaneous_1356954940 crossref_primary_10_3389_fpls_2013_00131 pubmed_primary_23717316 |
PublicationCentury | 2000 |
PublicationDate | 2013-00-00 |
PublicationDateYYYYMMDD | 2013-01-01 |
PublicationDate_xml | – year: 2013 text: 2013-00-00 |
PublicationDecade | 2010 |
PublicationPlace | Switzerland |
PublicationPlace_xml | – name: Switzerland |
PublicationTitle | Frontiers in plant science |
PublicationTitleAlternate | Front Plant Sci |
PublicationYear | 2013 |
Publisher | Frontiers Frontiers Media S.A |
Publisher_xml | – name: Frontiers – name: Frontiers Media S.A |
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 |
References_xml | |
SSID | ssj0000500997 |
Score | 2.2030504 |
Snippet | In this study, the physiological functions of fungal mannitol metabolism in the pathogenicity and protection against environmental stresses were investigated... |
SourceID | doaj pubmedcentral hal proquest crossref pubmed |
SourceType | Open Website Open Access Repository Aggregation Database Index Database |
StartPage | 131 |
SubjectTerms | Alternaria brassicicola Isothiocyanates Life Sciences Mannitol null mutants oxidative and drought stress pathogenicity Plant Science |
SummonAdditionalLinks | – databaseName: Directory of Open Access Journals dbid: DOA link: http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwrV07j9QwELbgREGDeJPjIYMoaKJbx4_E5R7caQtEwUOis7wTm42UjVeXLBL_nplkb3WBgoaUjmUn840zM_bkG8beCgmmAO1zUWudK7xyX1Iyja8LG6Jde0n_O6--lJ--Vx8uiCbnWOqLcsImeuBJcGdSqFhBFWphaiV9rATqIYh1LYWupAjj13dhbgRTE6s3uT7lxOWDUZg9i7uW2LkFEZoKKWZmaGTrR-OyoVzIvx3NP_Mlbxigy_vs3sFz5MvpiR-wW6F7yO6cJ_Tufj1i8Dm1gafIt1SEaEgt34YBAW6bfsubjqOfx6n6cEKFaQBdb-pLjR36jWm4SrtNAxyt3I99z5ftuE2IuskxmO5p6wP1xT9m3y4vvr5f5YcCCjkoK4eciFpARluA9aEIpSgiKF-rWC8ArK5iJb0BE3Gd48omZjSjgwxS4Z2gMER9wk661IVnjMcAOlo07oCA-HWwGqKBAIqAWZsiY--u5el2E0-Gw_iCRO9I9I5E70bRZ-yc5H3sRgTXYwPC7g6wu3_BnrE3iNZsjNXyo6M2YqkjK_wTZ3p9DabDVUNHIb4Lad87IbWhA061yNjTCdzjWIWkzARhMlbOYJ9NNr_TNZuRmVsaFJqoTv_HGz5nd4ux9AZt97xgJ8PVPrxkt_t6_2rU9d_dYASY priority: 102 providerName: Directory of Open Access Journals |
Title | Role of mannitol metabolism in the pathogenicity of the necrotrophic fungus Alternaria brassicicola |
URI | https://www.ncbi.nlm.nih.gov/pubmed/23717316 https://search.proquest.com/docview/1356954940 https://hal.science/hal-01210006 https://pubmed.ncbi.nlm.nih.gov/PMC3652318 https://doaj.org/article/314f8c8ed16d43af81003c1bd315831e |
Volume | 4 |
hasFullText | 1 |
inHoldings | 1 |
isFullTextHit | |
isPrint | |
link | http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lj9MwELboigMXxJvwWBnEgUu269jO49hddtUDIMRD4ma5E3sbKY-qSZH498w4zaqFGzk6jm35G2dm7PE3jL0TEtIEtI1FqXWs8IltRsE0tkwK54uVlXTfefkt-_wz_3BFNDl6ugsTgvZhVZ21dXPWVusQW7lpYD7Fic2_fLqUKbpPIp_P2AxtwwMXfST0JqsnG2l80AEr5n5TEzG3IC5TISk3TCLp8JlynB8oo8DZjypmTRGR_5qbf0dNHqih6wfs_t5-5ItxnA_ZHdc-YncvOrTxfj9m8LWrHe88bygV0dDVvHEDwlxXfcOrlqO1xykHcYdiUwEa4FSXClu0Hrth223WFXDUdTe7ni_qsFmIEsrRpe5pAwSlxj5hP66vvl8u430ahRhUIYeY6FpA-iKBwrrEZSLxoGypfHkOUOjc59KmkHpc7bi-iR8t1U46qfCNUzjTT9lJ27XuOePegfYFqniQQtmVKzT4FBwoV4p0lSYRez_Np9mMbBkGvQxCwRAKhlAwAYWIXdB831YjmutQ0G1vzB5sg734HHJqvVTS-lzgTwjEqpRC41BdxN4iWkdtLBcfDZURVx3p4l_Y05sJTINrhw5EbOu6XW-E1Ckdc6rziD0bwb1taxKRiGVHsB91dvwGxTXwc-_F88V_f_mS3UtC1g3a6XnFTobtzr1ms77cnYY9g9Mg8X8Av3AGZQ |
link.rule.ids | 230,315,729,782,786,866,887,2106,4028,27932,27933,27934,53800,53802 |
linkProvider | National Library of Medicine |
linkToHtml | http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwnV1Lb9QwELZoQYIL70d4GsSBS7rrOM7juC2tFrGtEBSJm-VM7G6kPFabLBL_nplkU-3CrTnajp1kPntm7Mk3jH0UEqIAlPFFrpQf4uWbmIJpTB6k1qWZkfS_8_xHfPEr-XxKNDlq_BemD9qHrDiqy-qoLpZ9bOWqgskYJzb5dn4iI3SfRDI5YLdxvk6nO076QOlNdk88EPmgC5ZO3Kokam5BbKZCUnaYQNLxM2U531FHPWs_KpklxUT-b3D-Gze5o4jOHtzwFR6y-1vLk8-G6kfslq0fszvHDVqHf54w-N6UljeOV5TEqGtKXtkOAVIWbcWLmqOdyCl7cYOAKwBNd2pLhTXanU23blbLAjhqyatNy2dlv82I2ObojLe0dYJ4M0_Zz7PTy5O5v03A4EOYys4noheQLg0gNTawsQgchCYPXT4FSFXiEmkiiByuE7gyELNapKy0MsQaG-ILPmOHdVPbF4w7C8qlaByAFKHJbKrARWAhtLmIsijw2KdRDno18Gxo9E9Iepqkp0l6upeex45JTtfNiCC7L2jWV3r7jTWO4hJIqPc8lMYlApcvEFkuhcJHtR77gFLe62M-W2gqI5Y70uK_caT3Iwg0zjo6SjG1bTatFlJFdEAaTj32fADFdV8jtDwW78Flb7D9GkRJz-y9RcXLG9_5jt2dX54v9OLLxddX7F7Q5-6g_aLX7LBbb-wbdtDmm7f9fPkLOHEa9A |
linkToPdf | http://sdu.summon.serialssolutions.com/2.0.0/link/0/eLvHCXMwpV1Lj9MwELbYBSEuyxvC0yAOXLKp4zyP3UdVxLJa8ZC4Wc7E3kbKS026Ev-emaStWrhBjo5jx5nPnhl78g1jH4SEyIdQuyIPQzfAy9UxBdPo3E-NTTMt6X_n-bf48mdydk40OdtUX0PQPmTFcV1Wx3WxGGIr2wq8TZyYd_XlVEboPonEa3PrHbDbOGcn_o6jPtJ6k-0Tj2Q-6Ialnm1LoucWxGgqJGWI8SUdQVOm8x2VNDD3o6JZUFzk30bnn7GTO8podv8_hvGAHa0tUD4dqzxkt0z9iN05adBK_PWYwdemNLyxvKJkRn1T8sr0CJSy6Cpe1BztRU5ZjBsEXgFowlNdKqzR_mz6ZdMuCuCoLa9XHZ-Ww3YjYpyjU97RFgriTj9hP2bn30_n7joRgwtBKnuXCF9A2tSHVBvfxMK3EOg8sPkEIA0Tm0gdQWRxvcAVghjWotBIIwO8YwIc5FN2WDe1ec64NRDaFI0EkCLQmUlDsBEYCEwuoizyHfZxIwvVjnwbCv0UkqAiCSqSoBok6LATktW2GhFlDwXN8lqtv7PCXmwCCbWeB1LbROAyBiLLpQjxVY3D3qOk99qYTy8UlRHbHWnzG-zp3QYICmcfHano2jSrTgkZRnRQGkwc9mwExratDbwcFu9BZq-z_TuIlIHhe42MF__85Ft29-pspi4-XX5-ye75QwoP2jZ6xQ775cq8ZgddvnozTJnfDwEddA |
openUrl | ctx_ver=Z39.88-2004&ctx_enc=info%3Aofi%2Fenc%3AUTF-8&rfr_id=info%3Asid%2Fsummon.serialssolutions.com&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Ajournal&rft.genre=article&rft.atitle=Role+of+mannitol+metabolism+in+the+pathogenicity+of+the+necrotrophic+fungus+Alternaria+brassicicola&rft.jtitle=Frontiers+in+plant+science&rft.au=Calmes%2C+Benoit&rft.au=Guillemette%2C+Thomas&rft.au=Teyssier%2C+L%C3%A9ny&rft.au=Siegler%2C+Benjamin&rft.date=2013&rft.issn=1664-462X&rft.eissn=1664-462X&rft.volume=4&rft.spage=131&rft.epage=131&rft_id=info:doi/10.3389%2Ffpls.2013.00131&rft.externalDBID=NO_FULL_TEXT |
thumbnail_l | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/lc.gif&issn=1664-462X&client=summon |
thumbnail_m | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/mc.gif&issn=1664-462X&client=summon |
thumbnail_s | http://covers-cdn.summon.serialssolutions.com/index.aspx?isbn=/sc.gif&issn=1664-462X&client=summon |