Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming
During compatible interactions with their host plants, biotrophic plant pathogens subvert host metabolism to ensure the sustained provision of nutrient assimilates by the colonized host cells. To investigate, whether common motifs can be revealed in the response of primary carbon and nitrogen metabo...
| Main Authors: | , , , , , , , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2011-08-01
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| Series: | Frontiers in Plant Science |
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| Online Access: | http://journal.frontiersin.org/Journal/10.3389/fpls.2011.00039/full |
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| author | Lars Matthias Voll Robin Jonathan Horst Anna Maria Voitsik Doreen eZajic Birgit eSamans Jörn ePons-Kühnemann Gunther eDoehlemann Steffen eMünch Ramon eWahl Alexandra eMolitor Jörg eHofmann Alfred eSchmiedl Frank eWaller Holger Bruno Deising Ragine eKahmann Jörg eKämper Karl-Heinz eKogel Uwe eSonnewald |
| author_facet | Lars Matthias Voll Robin Jonathan Horst Anna Maria Voitsik Doreen eZajic Birgit eSamans Jörn ePons-Kühnemann Gunther eDoehlemann Steffen eMünch Ramon eWahl Alexandra eMolitor Jörg eHofmann Alfred eSchmiedl Frank eWaller Holger Bruno Deising Ragine eKahmann Jörg eKämper Karl-Heinz eKogel Uwe eSonnewald |
| author_sort | Lars Matthias Voll |
| collection | DOAJ |
| description | During compatible interactions with their host plants, biotrophic plant pathogens subvert host metabolism to ensure the sustained provision of nutrient assimilates by the colonized host cells. To investigate, whether common motifs can be revealed in the response of primary carbon and nitrogen metabolism towards colonization with biotrophic fungi in cereal leaves, we have conducted a combined metabolome and transcriptome study of three quite divergent pathosystems, the barley powdery mildew fungus (Blumeria graminis f.sp. hordei), the corn smut fungus Ustilago maydis and the maize anthracnose fungus Colletotrichum graminicola, the latter being a hemibiotroph that only exhibits an initial biotrophic phase during its establishment.Based on the analysis of 42 water-soluble metabolites, we were able to separate early biotrophic from late biotrophic interactions by hierarchical cluster analysis and principal component analysis, irrespective of the plant host. Interestingly, the corresponding transcriptome dataset could not discriminate between these stages of biotrophy, irrespective, of whether transcript data for genes of central metabolism or the entire transcriptome dataset was used. Strong differences in the transcriptional regulation of photosynthesis, glycolysis, the TCA cycle, lipid biosynthesis, and cell wall metabolism were observed between the pathosystems. Increased contents of Gln, Asn, and glucose as well as diminished contents of PEP and 3-PGA were common to early post-penetration stages of all interactions. On the transcriptional level, genes of the TCA cycle, nucleotide energy metabolism and amino acid biosynthesis exhibited consistent trends among the compared biotrophic interactions, identifying the requirement for metabolic energy and the rearrangement of amino acid pools as common transcriptional motifs during early biotrophy. Both metabolome and transcript data were employed to generate models of leaf primary metabolism during early biotrophy. |
| first_indexed | 2024-12-10T22:49:38Z |
| format | Article |
| id | doaj.art-7037640886ba4e03a05970b04c8d2ef0 |
| institution | Directory Open Access Journal |
| issn | 1664-462X |
| language | English |
| last_indexed | 2024-12-10T22:49:38Z |
| publishDate | 2011-08-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Plant Science |
| spelling | doaj.art-7037640886ba4e03a05970b04c8d2ef02022-12-22T01:30:28ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2011-08-01210.3389/fpls.2011.0003911791Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogrammingLars Matthias Voll0Robin Jonathan Horst1Anna Maria Voitsik2Doreen eZajic3Birgit eSamans4Jörn ePons-Kühnemann5Gunther eDoehlemann6Steffen eMünch7Ramon eWahl8Alexandra eMolitor9Jörg eHofmann10Alfred eSchmiedl11Frank eWaller12Holger Bruno Deising13Ragine eKahmann14Jörg eKämper15Karl-Heinz eKogel16Uwe eSonnewald17Friedrich-Alexander-University Erlangen-NurembergUniversity of WashingtonFriedrich-Alexander-University Erlangen-NurembergFriedrich-Alexander-University Erlangen-NurembergJustus Liebig UniversityJustus Liebig UniversityMax Planck Institute for Terrestrial MicrobiologyMartin-Luther-University Halle-WittenbergUniversity of KarlsruheJustus Liebig UniversityFriedrich-Alexander-University Erlangen-NurembergFriedrich-Alexander-University Erlangen-NurembergJulius-Maximilians-Universität WürzburgMartin-Luther-University Halle-WittenbergMax Planck Institute for Terrestrial MicrobiologyUniversity of KarlsruheJustus Liebig UniversityFriedrich-Alexander-University Erlangen-NurembergDuring compatible interactions with their host plants, biotrophic plant pathogens subvert host metabolism to ensure the sustained provision of nutrient assimilates by the colonized host cells. To investigate, whether common motifs can be revealed in the response of primary carbon and nitrogen metabolism towards colonization with biotrophic fungi in cereal leaves, we have conducted a combined metabolome and transcriptome study of three quite divergent pathosystems, the barley powdery mildew fungus (Blumeria graminis f.sp. hordei), the corn smut fungus Ustilago maydis and the maize anthracnose fungus Colletotrichum graminicola, the latter being a hemibiotroph that only exhibits an initial biotrophic phase during its establishment.Based on the analysis of 42 water-soluble metabolites, we were able to separate early biotrophic from late biotrophic interactions by hierarchical cluster analysis and principal component analysis, irrespective of the plant host. Interestingly, the corresponding transcriptome dataset could not discriminate between these stages of biotrophy, irrespective, of whether transcript data for genes of central metabolism or the entire transcriptome dataset was used. Strong differences in the transcriptional regulation of photosynthesis, glycolysis, the TCA cycle, lipid biosynthesis, and cell wall metabolism were observed between the pathosystems. Increased contents of Gln, Asn, and glucose as well as diminished contents of PEP and 3-PGA were common to early post-penetration stages of all interactions. On the transcriptional level, genes of the TCA cycle, nucleotide energy metabolism and amino acid biosynthesis exhibited consistent trends among the compared biotrophic interactions, identifying the requirement for metabolic energy and the rearrangement of amino acid pools as common transcriptional motifs during early biotrophy. Both metabolome and transcript data were employed to generate models of leaf primary metabolism during early biotrophy.http://journal.frontiersin.org/Journal/10.3389/fpls.2011.00039/fullMaizebarleypowdery mildewtranscriptome analysisColletotrichum graminicolacompatible interaction |
| spellingShingle | Lars Matthias Voll Robin Jonathan Horst Anna Maria Voitsik Doreen eZajic Birgit eSamans Jörn ePons-Kühnemann Gunther eDoehlemann Steffen eMünch Ramon eWahl Alexandra eMolitor Jörg eHofmann Alfred eSchmiedl Frank eWaller Holger Bruno Deising Ragine eKahmann Jörg eKämper Karl-Heinz eKogel Uwe eSonnewald Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming Frontiers in Plant Science Maize barley powdery mildew transcriptome analysis Colletotrichum graminicola compatible interaction |
| title | Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming |
| title_full | Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming |
| title_fullStr | Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming |
| title_full_unstemmed | Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming |
| title_short | Common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming |
| title_sort | common motifs in the response of cereal primary metabolism to fungal pathogens are not based on similar transcriptional reprogramming |
| topic | Maize barley powdery mildew transcriptome analysis Colletotrichum graminicola compatible interaction |
| url | http://journal.frontiersin.org/Journal/10.3389/fpls.2011.00039/full |
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