Correlation-based network analysis of metabolite and enzyme profiles reveals a role of citrate biosynthesis in modulating N and C metabolism in Zea mays

To investigate the natural variability of leaf metabolism and enzymatic activity in a maize inbred population, statistical and network analyses were employed on metabolite and enzyme profiles. The test of coefficient of variation showed that sugars and amino acids displayed opposite trends in their...

Full description

Bibliographic Details
Main Authors: David Toubiana, Wentao Xue, Nengyi Zhang, Karl Kremling, Amit Gur, Shai Pilosof, Yves Gibon, Mark Stitt, Edward Buckler, Alisdair Fernie, Aaron Fait
Format: Article
Language:English
Published: Frontiers Media S.A. 2016-07-01
Series:Frontiers in Plant Science
Subjects:
Online Access:http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01022/full
id doaj-7b2900ee10b644f1a6b890abbdf9fd13
record_format Article
spelling doaj-7b2900ee10b644f1a6b890abbdf9fd132020-11-24T23:48:49ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2016-07-01710.3389/fpls.2016.01022190904Correlation-based network analysis of metabolite and enzyme profiles reveals a role of citrate biosynthesis in modulating N and C metabolism in Zea maysDavid Toubiana0Wentao Xue1Wentao Xue2Nengyi Zhang3Karl Kremling4Amit Gur5Amit Gur6Shai Pilosof7Shai Pilosof8Yves Gibon9Yves Gibon10Mark Stitt11Edward Buckler12Alisdair Fernie13Aaron Fait14Ben Gurion UniversityBen Gurion UniversityGuizhou UniversityCornell UniversityCornell UniversityCornell UniversityIsraeli Agricultural Research OrganizationBen Gurion UniversityUniversity of ChicagoMax Planck Institute of Molecular Plant PhysiologyUniversité de BordeauxMax Planck Institute of Molecular Plant PhysiologyCornell UniversityMax Planck Institute of Molecular Plant PhysiologyBen Gurion UniversityTo investigate the natural variability of leaf metabolism and enzymatic activity in a maize inbred population, statistical and network analyses were employed on metabolite and enzyme profiles. The test of coefficient of variation showed that sugars and amino acids displayed opposite trends in their variance within the population, consistently with their related enzymes. The overall higher CV values for metabolites as compared to the tested enzymes are indicative for their greater phenotypic plasticity. H2 tests revealed galactinol (1) and asparagine (0.91) as the highest scorers among metabolites and nitrate reductase (0.73), NAD-glutamate dehydrogenase (0.52), and phosphoglucomutase (0.51) among enzymes. The overall low H2 scores for metabolites and enzymes are suggestive for a great environmental impact or gene-environment interaction. Correlation-based network generation followed by community detection analysis, partitioned the network into three main communities and one dyad, (i) reflecting the different levels of phenotypic plasticity of the two molecular classes as observed for the CV values and (ii) highlighting the concerted changes between classes of chemically related metabolites. Community 1 is composed mainly of enzymes and specialized metabolites, community 2’ is enriched in N-containing compounds and phosphorylated-intermediates. The third community contains mainly organic acids and sugars. Cross-community linkages are supported by aspartate, by the photorespiration amino acids glycine and serine, by the metabolically related GABA and putrescine, and by citrate. The latter displayed the strongest node-betweenness value (185.25) of all nodes highlighting its fundamental structural role in the connectivity of the network by linking between different communities and to the also strongly connected enzyme aldolase.http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01022/fullMetabolic Networks and PathwaysMetabolismZea maysEnzymatic ProcessesTCA cyclecorrelation-based network analysis
collection DOAJ
language English
format Article
sources DOAJ
author David Toubiana
Wentao Xue
Wentao Xue
Nengyi Zhang
Karl Kremling
Amit Gur
Amit Gur
Shai Pilosof
Shai Pilosof
Yves Gibon
Yves Gibon
Mark Stitt
Edward Buckler
Alisdair Fernie
Aaron Fait
spellingShingle David Toubiana
Wentao Xue
Wentao Xue
Nengyi Zhang
Karl Kremling
Amit Gur
Amit Gur
Shai Pilosof
Shai Pilosof
Yves Gibon
Yves Gibon
Mark Stitt
Edward Buckler
Alisdair Fernie
Aaron Fait
Correlation-based network analysis of metabolite and enzyme profiles reveals a role of citrate biosynthesis in modulating N and C metabolism in Zea mays
Frontiers in Plant Science
Metabolic Networks and Pathways
Metabolism
Zea mays
Enzymatic Processes
TCA cycle
correlation-based network analysis
author_facet David Toubiana
Wentao Xue
Wentao Xue
Nengyi Zhang
Karl Kremling
Amit Gur
Amit Gur
Shai Pilosof
Shai Pilosof
Yves Gibon
Yves Gibon
Mark Stitt
Edward Buckler
Alisdair Fernie
Aaron Fait
author_sort David Toubiana
title Correlation-based network analysis of metabolite and enzyme profiles reveals a role of citrate biosynthesis in modulating N and C metabolism in Zea mays
title_short Correlation-based network analysis of metabolite and enzyme profiles reveals a role of citrate biosynthesis in modulating N and C metabolism in Zea mays
title_full Correlation-based network analysis of metabolite and enzyme profiles reveals a role of citrate biosynthesis in modulating N and C metabolism in Zea mays
title_fullStr Correlation-based network analysis of metabolite and enzyme profiles reveals a role of citrate biosynthesis in modulating N and C metabolism in Zea mays
title_full_unstemmed Correlation-based network analysis of metabolite and enzyme profiles reveals a role of citrate biosynthesis in modulating N and C metabolism in Zea mays
title_sort correlation-based network analysis of metabolite and enzyme profiles reveals a role of citrate biosynthesis in modulating n and c metabolism in zea mays
publisher Frontiers Media S.A.
series Frontiers in Plant Science
issn 1664-462X
publishDate 2016-07-01
description To investigate the natural variability of leaf metabolism and enzymatic activity in a maize inbred population, statistical and network analyses were employed on metabolite and enzyme profiles. The test of coefficient of variation showed that sugars and amino acids displayed opposite trends in their variance within the population, consistently with their related enzymes. The overall higher CV values for metabolites as compared to the tested enzymes are indicative for their greater phenotypic plasticity. H2 tests revealed galactinol (1) and asparagine (0.91) as the highest scorers among metabolites and nitrate reductase (0.73), NAD-glutamate dehydrogenase (0.52), and phosphoglucomutase (0.51) among enzymes. The overall low H2 scores for metabolites and enzymes are suggestive for a great environmental impact or gene-environment interaction. Correlation-based network generation followed by community detection analysis, partitioned the network into three main communities and one dyad, (i) reflecting the different levels of phenotypic plasticity of the two molecular classes as observed for the CV values and (ii) highlighting the concerted changes between classes of chemically related metabolites. Community 1 is composed mainly of enzymes and specialized metabolites, community 2’ is enriched in N-containing compounds and phosphorylated-intermediates. The third community contains mainly organic acids and sugars. Cross-community linkages are supported by aspartate, by the photorespiration amino acids glycine and serine, by the metabolically related GABA and putrescine, and by citrate. The latter displayed the strongest node-betweenness value (185.25) of all nodes highlighting its fundamental structural role in the connectivity of the network by linking between different communities and to the also strongly connected enzyme aldolase.
topic Metabolic Networks and Pathways
Metabolism
Zea mays
Enzymatic Processes
TCA cycle
correlation-based network analysis
url http://journal.frontiersin.org/Journal/10.3389/fpls.2016.01022/full
work_keys_str_mv AT davidtoubiana correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT wentaoxue correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT wentaoxue correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT nengyizhang correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT karlkremling correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT amitgur correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT amitgur correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT shaipilosof correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT shaipilosof correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT yvesgibon correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT yvesgibon correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT markstitt correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT edwardbuckler correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT alisdairfernie correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
AT aaronfait correlationbasednetworkanalysisofmetaboliteandenzymeprofilesrevealsaroleofcitratebiosynthesisinmodulatingnandcmetabolisminzeamays
_version_ 1725484356537942016