Metabolic Profiling of a Mapping Population Exposes New Insights in the Regulation of Seed Metabolism and Seed, Fruit, and Plant Relations
To investigate the regulation of seed metabolism and to estimate the degree of metabolic natural variability, metabolite profiling and network analysis were applied to a collection of 76 different homozygous tomato introgression lines (ILs) grown in the field in two consecutive harvest seasons. Factorial ANOVA confirmed the presence of 30 metabolite quantitative trait loci (mQTL). Amino acid contents displayed a high degree of variability across the population, with similar patterns across the two seasons, while sugars exhibited significant seasonal fluctuations. Upon integration of data for tomato pericarp metabolite profiling, factorial ANOVA identified the main factor for metabolic polymorphism to be the genotypic background rather than the environment or the tissue. Analysis of the coefficient of variance indicated greater phenotypic plasticity in the ILs than in the M82 tomato cultivar. Broad-sense estimate of heritability suggested that the mode of inheritance of metabolite traits in the seed differed from that in the fruit. Correlation-based metabolic network analysis comparing metabolite data for the seed with that for the pericarp showed that the seed network displayed tighter interdependence of metabolic processes than the fruit. Amino acids in the seed metabolic network were shown to play a central hub-like role in the topology of the network, maintaining high interactions with other metabolite categories, i.e., sugars and organic acids. Network analysis identified six exceptionally highly co-regulated amino acids, Gly, Ser, Thr, Ile, Val, and Pro. The strong interdependence of this group was confirmed by the mQTL mapping. Taken together these results (i) reflect the extensive redundancy of the regulation underlying seed metabolism, (ii) demonstrate the tight co-ordination of seed metabolism with respect to fruit metabolism, and (iii) emphasize the centrality of the amino acid module in the seed metabolic network. Finally, the study highlights the added value of integrating metabolic network analysis with mQTL mapping.
Vyšlo v časopise:
Metabolic Profiling of a Mapping Population Exposes New Insights in the Regulation of Seed Metabolism and Seed, Fruit, and Plant Relations. PLoS Genet 8(3): e32767. doi:10.1371/journal.pgen.1002612
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.pgen.1002612
Souhrn
To investigate the regulation of seed metabolism and to estimate the degree of metabolic natural variability, metabolite profiling and network analysis were applied to a collection of 76 different homozygous tomato introgression lines (ILs) grown in the field in two consecutive harvest seasons. Factorial ANOVA confirmed the presence of 30 metabolite quantitative trait loci (mQTL). Amino acid contents displayed a high degree of variability across the population, with similar patterns across the two seasons, while sugars exhibited significant seasonal fluctuations. Upon integration of data for tomato pericarp metabolite profiling, factorial ANOVA identified the main factor for metabolic polymorphism to be the genotypic background rather than the environment or the tissue. Analysis of the coefficient of variance indicated greater phenotypic plasticity in the ILs than in the M82 tomato cultivar. Broad-sense estimate of heritability suggested that the mode of inheritance of metabolite traits in the seed differed from that in the fruit. Correlation-based metabolic network analysis comparing metabolite data for the seed with that for the pericarp showed that the seed network displayed tighter interdependence of metabolic processes than the fruit. Amino acids in the seed metabolic network were shown to play a central hub-like role in the topology of the network, maintaining high interactions with other metabolite categories, i.e., sugars and organic acids. Network analysis identified six exceptionally highly co-regulated amino acids, Gly, Ser, Thr, Ile, Val, and Pro. The strong interdependence of this group was confirmed by the mQTL mapping. Taken together these results (i) reflect the extensive redundancy of the regulation underlying seed metabolism, (ii) demonstrate the tight co-ordination of seed metabolism with respect to fruit metabolism, and (iii) emphasize the centrality of the amino acid module in the seed metabolic network. Finally, the study highlights the added value of integrating metabolic network analysis with mQTL mapping.
Zdroje
1. LiuJPCongBTanksleySD 2003 Generation and analysis of an artificial gene dosage series in tomato to study the mechanisms by which the cloned quantitative trait locus fw2.2 controls fruit size. Plant Physiol 132 292 299
2. SchauerNSemelYRoessnerUGurABalboI 2006 Comprehensive metabolic profiling and phenotyping of interspecific introgression lines for tomato improvement. Nat Biotechnol 24 447 454
3. MoftahAEAl-RedhaimanKN 2006 Effects of preharvest foliar spray of ‘Limewash’ on water relations, quantity, quality, and shelf life of bell pepper under water deficit conditions. Eur J Hortic Sci 71 78 83
4. GilbertLAlhagdowMNunes-NesiAQuemenerBGuillonF 2009 GDP-d-mannose 3,5-epimerase (GME) plays a key role at the intersection of ascorbate and non-cellulosic cell-wall biosynthesis in tomato. Plant J 60 499 508
5. MaloneyGSKochevenkoATiemanDMTohgeTKriegerU 2010 Characterization of the Branched-Chain Amino Acid Aminotransferase Enzyme Family in Tomato. Plant Physiol 153 925 936
6. GiovannoniJ 2001 Molecular biology of fruit maturation and ripening. Annual Review of Plant Phys 52 725 749
7. LippmanZBSemelYZamirD 2007 An integrated view of quantitative trait variation using tomato interspecific introgression lines. Curr Opin Genet Dev 17 545 552
8. BradfordKJChenFCooleyMBDahalPDownieB 2000 Gene expression prior to radicle emergence in imbibed tomato seeds. BlackMJBradfordKJVazquez-RamosJ Seed Biology: Advances and Applications Oxfordshire, UK CABI 231 251
9. HilhorstHWMGrootSPCBinoRJ 1998 The tomato seed as a model system to study seed development and germination. Acta Bot Neerl 47 169 183
10. MartinRCPluskotaWENonogakiH 2010 Seed Germination. Eng-ChongPDaveyMR Plant Developmental Biology - Biotechnological Perspectives, Vol 1. 1st ed Heidelberg, Germany Springer 383 404
11. FraryANesbittTCGrandilloSvan der KnaapECongB 2000 fw2.2: A quantitative trait locus key to the evolution of tomato fruit size. Science 289 85 88
12. FernieARWillmitzerL 2004 Carbohydrate metabolism. ChristouPKleeHK Handbook of Plant Biotechnology Chichester, UK Wiley
13. TanksleySDMcCouchSR 1997 Seed banks and molecular maps: Unlocking genetic potential from the wild. Science 277 1063 1066
14. McCouchS 2004 Diversifying selection in plant breeding. PLoS Biol 2 e347 doi:10.1371/journal.pbio.0020347
15. DoebleyJFGautBSSmithBD 2006 The molecular genetics of crop domestication. Cell 127 1309 1321
16. FernieARTadmorYZamirD 2006 Natural genetic variation for improving crop quality. Curr Opin Plant Biol 9 196 202
17. GresselJ 2008 Genetic glass ceilings: transgenics for crop biodiversity Baltimore, US The Johns Hopkins University Press
18. DoebleyJ 1989 Molecular evidence for a missing relative of maize and the introgression of its chloroplast genome into Zea-Perennis. Evolution 43 1555 1559
19. RottenbergAZoharyDNevoE 1996 Isozyme relationships between cultivated artichoke and the wild relatives. Genet Resour Crop Ev 43 59 62
20. SalaminiFOzkanHBrandoliniASchafer-PreglRMartinW 2002 Genetics and geography of wild cereal domestication in the Near East. Nat Rev Genet 3 429 441
21. JohalGSBalint-KurtiPWellCF 2008 Mining and Harnessing Natural Variation: A Little MAGIC. Crop Sci 48 2066 2073
22. UdallJAQuijadaPALambertBOsbornTC 2006 Quantitative trait analysis of seed yield and other complex traits in hybrid spring rapeseed (Brassica napus L.): 2. Identification of alleles from unadapted germplasm. Theor Appl Genet 113 597 609
23. MarzaFBaiGHCarverBFZhouWC 2006 Quantitative trait loci for yield and related traits in the wheat population Ning7840×Clark. Theor Appl Genet 112 688 698
24. AshikariMMatsuokaM 2006 Identification, isolation and pyramiding of quantitative trait loci for rice breeding. Trends Plant Sci 11 344 350
25. SeptiningsihEMPrasetiyonoJLubisETaiTHTjubaryatT 2003 Identification of quantitative trait loci for yield and yield components in an advanced backcross population derived from the Oryza sativa variety IR64 and the wild relative O-rufipogon. Theor Appl Genet 107 1419 1432
26. PillenKZachariasALeonJ 2003 Advanced backcross QTL analysis in barley (Hordeum vulgare L.). Theor Appl Genet 107 340 352
27. ConcibidoVCLa ValleeBMcLairdPPinedaNMeyerJ 2003 Introgression of a quantitative trait locus for yield from Glycine soja into commercial soybean cultivars. Theor Appl Genet 106 575 582
28. BriggsWHMcMullenMDGautBSDoebleyJ 2007 Linkage mapping of domestication loci in a large maize-teosinte backcross resource. Genetics 177 1915 1928
29. BlairMWIriarteGBeebeS 2006 QTL analysis of yield traits in an advanced backcross population derived from a cultivated Andean×wild common bean (Phaseolus vulgaris L.) cross. Theor Appl Genet 112 1149 1163
30. RaoGUBen ChaimABorovskyYParanI 2003 Mapping of yield-related QTLs in pepper in an interspecific cross of Capsicum annuum and C-frutescens. Theor Appl Genet 106 1457 1466
31. ParanIZamirD 2003 Quantitative traits in plants: beyond the QTL. Trends Genet 19 303 306
32. KoornneefMAlonso-BlancoCVreugdenhilD 2004 Naturally occurring genetic variation in Arabidopsis thaliana. Annu Rev Plant Biol 55 141 172
33. SalviSTuberosaR 2005 To clone or not to clone plant QTLs: present and future challenges. Trends Plant Sci 10 297 304
34. KusanoMFukushimaAKobayashiMHayashiNJonssonP 2007 Application of a metabolomic method combining one-dimensional and two-dimensional gas chromatography-time-of-flight/mass spectrometry to metabolic phenotyping of natural variants in rice. J Chromatgr B 855 71 79
35. SchauerNSemelYBalboISteinfathMRepsilberD 2008 Mode of inheritance of primary metabolic traits in tomato. Plant Cell 20 509 523
36. KeurentjesJJBBentsinkLAlonso-BlancoCHanhartCJVriesHBD 2007 Development of a near-isogenic line population of Arabidopsis thaliana and comparison of mapping power with a recombinant inbred line population. Genetics 175 891 905
37. Alonso-BlancoCBentsinkLHanhartCJVriesHBEKoornneefM 2003 Analysis of natural allelic variation at seed dormancy loci of Arabidopsis thaliana. Genetics 164 711 729
38. BentsinkLJowettJHanhartCJKoornneefM 2006 Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc Natl Acad Sci USA 103 17042 17047
39. ClerkxEJMEl-LithyMEVierlingERuysGJBlankestijin-De VriesH 2004 Analysis of natural allelic variation of Arabidopsis seed germination and seed longevity traits between the accessions Landsberg erecta and Shakdara, using a new recombinant inbred line population. Plant Physiol 135 432 443
40. BetteyMFinch-SavageWEKingGJLynnJR 2000 Quantitative genetic analysis of seed vigour and pre-emergence seedling growth traits in Brassica oleracea. New Phytol 148 277 286
41. QuesadaVGarcia-MartinezSPiquerasPPonceMRMicolJL 2002 Genetic architecture of NaCl tolerance in Arabidopsis. Plant Physiol 130 951 963
42. RousseauxMCJonesCMAdamsDChetelatRBennettA 2005 QTL analysis of fruit antioxidants in tomato using Lycopersicon pennellii introgression lines. Theor Appl Genet 111 1396 1408
43. FraryAGolDKelesDOkmenBPinarH 2010 Salt tolerance in Solanum pennellii: antioxidant response and related QTL. Bmc Plant Biol 10
44. StevensRPageDGoubleBGarcheryCZamirD 2008 Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant Cell Environ 31 1086 1096
45. WobusUWeberH 1999 Seed maturation: genetic programmes and control signals. Curr Opin Plant Biol 2 33 38
46. GutierrezRALejayLVDeanAChiaromonteFShashaDE 2007 Qualitative network models and genome-wide expression data define carbon/nitrogen-responsive molecular machines in Arabidopsis. Genome Biol 8
47. AngeloviciRGaliliGFernieARFaitA 2010 Seed desiccation: a bridge between maturation and germination. Trends Plant Sci 15 211 218
48. BentsinkLAlonso-BlancoCVreugdenhilDTesnierKGrootSPC 2000 Genetic analysis of seed-soluble oligosaccharides in relation to seed storability of Arabidopsis. Plant Physiol 124 1595 1604
49. KoornneefMBentsinkLHilhorstH 2002 Seed dormancy and germination. Curr Opin Plant Biol 5 33 36
50. HuangXQSchmittJDornLGriffithCEffgenS 2010 The earliest stages of adaptation in an experimental plant population: strong selection on QTLS for seed dormancy. Mol Ecol 19 1335 1351
51. KeurentjesJJBFuJYde VosCHRLommenAHallRD 2006 The genetics of plant metabolism. Nat Genet 38 842 849
52. KeurentjesJJBSulpiceRGibonYSteinhauserMCFuJY 2008 Integrative analyses of genetic variation in enzyme activities of primary carbohydrate metabolism reveal distinct modes of regulation in Arabidopsis thaliana. Genome Biol 9
53. BaudSLepiniecL 2009 Regulation of de novo fatty acid synthesis in maturing oilseeds of Arabidopsis. Plant Physiol Bioch (Paris) 47 448 455
54. RolletschekHStangelmayerABorisjukL 2009 Methodology and Significance of Microsensor-based Oxygen Mapping in Plant Seeds - an Overview. Sensors 9 3218 3227
55. HoldsworthMJBentsinkLSoppeWJJ 2008 Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy and germination. New Phytol 179 33 54
56. FinkelsteinRReevesWAriizumiTSteberC 2008 Molecular aspects of seed dormancy. Annu Rev Plant Biol 59 387 415
57. HarriganGGStorkLGRiordanSGReynoldsTLRidleyWP 2007 Impact of genetics and environment on nutritional and metabolite components of maize grain. J Agr Food Chem 55 6177 6185
58. DoPTPrudentMSulpiceRCausseMFernieAR 2010 The influence of fruit load on the tomato pericarp metabolome in a Solanum chmielewskii introgression line population. Plant Physiol 154 1128 1142
59. EshedYZamirD 1995 An introgression line population of Lycopersicon Pennellii in the cultivated tomato enables the identification and fine mapping of yield-associated QTL. Genetics 141 1147 1162
60. RoessnerULuedemannABrustDFiehnOLinkeT 2001 Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. Plant Cell 13 11 29
61. LisecJSchauerNKopkaJWillmitzerLFernieAR 2006 Gas chromatography mass spectrometry-based metabolite profiling in plants. Nat Protoc 1 387 396
62. FaitAFrommHWalterDGaliliGFernieAR 2008 Highway or byway: the metabolic role of the GABA shunt in plants. Trends Plant Sci 13 14 19
63. ChanEKFRoweHCHansenBGKliebensteinDJ 2010 The Complex Genetic Architecture of the Metabolome. PLoS Genet 6 e1001198 doi:10.1371/journal.pgen.1001198
64. ElowitzMBLevineAJSiggiaEDSwainPS 2002 Stochastic gene expression in a single cell. Science 297 1183 1186
65. RaserJMO'SheaEK 2004 Control of stochasticity in eukaryotic gene expression. Science 304 1811 1814
66. KliebensteinDJ 2008 A Role for Gene Duplication and Natural Variation of Gene Expression in the Evolution of Metabolism. PLoS ONE 3 e1838 doi:10.1371/journal.pone.0001838
67. BasselGWLanHGlaabEGibbsDJGerjetsT 2011 Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc Natl Acad Sci USA 108 9709 9714
68. EnricoBasselGWGMarquezJuliettaHoldsworthMichaelJBacarditJaume 2011 Functional network construction in Arabidopsis using rule-based machine Learning on large-scale data sets. Plant Cell 17
69. SteinhauserMCSteinhauserDKoehlKCarrariFGibonY 2010 Enzyme Activity Profiles during Fruit Development in Tomato Cultivars and Solanum pennellii. Plant Physiol 153 80 98
70. KolbeAOliverSNFernieARStittMvan DongenJT 2006 Combined transcript and metabolite profiling of Arabidopsis leaves reveals fundamental effects of the thiol-disulfide status on plant metabolism. Plant Physiol 141 412 422
71. FrommerWBHummelSUnseldMNinnemannO 1995 Seed and vascular expression of a high-affinity transporter for cationic amino acids in Arabidopsis. Proc Natl Acad Sci USA 92 12036 12040
72. RiveraCGVakilRBaderJS 2010 NeMo: Network Module identification in Cytoscape. Bmc Bioinformatics 11
73. FaitAAngeloviciRLessHOhadIUrbanczyk-WochniakE 2006 Arabidopsis seed development and germination is associated with temporally distinct metabolic switches. Plant Physiol 142 839 854
74. FaitAHanhinevaKBeleggiaRDaiNRogachevI 2008 Reconfiguration of the achene and receptacle metabolic networks during strawberry fruit development. Plant Physiol 148 730 750
75. WeigeltKKusterHRadchukRMullerMWeichertH 2008 Increasing amino acid supply in pea embryos reveals specific interactions of N and C metabolism, and highlights the importance of mitochondrial metabolism. Plant J 55 909 926
76. AngeloviciRFaitAZhuXHSzymanskiJFeldmesserE 2009 Deciphering Transcriptional and Metabolic Networks Associated with Lysine Metabolism during Arabidopsis Seed Development. Plant Physiol 151 2058 2072
77. AngeloviciRFaitAFernieARGaliliG 2011 A seed high-lysine trait is negatively associated with the TCA cycle and slows down Arabidopsis seed germination. New Phytol 189 148 159
78. FaitANunes-NesiAAngeloviciRLehmanMPhamP 2011 Targeted enhancement of glutamate to γ-aminobutyrate conversion in Arabidopsis seeds affects C-N balance and storage reserves in a development-dependent manner. Plant Physiol 157 1026 1042
79. BorisjukLWangTLRolletschekHWobusUWeberH 2002 A pea seed mutant affected in the differentiation of the embryonic epidermis is impaired in embryo growth and seed maturation. Development 129 1595 1607
80. BorisjukLRolletschekHRadchukRWeschkeWWobusU 2004 Seed development and differentiation: A role for metabolic regulation. Plant Biol 6 375 386
81. WeberHBorisjukLWobusU 2005 Molecular physiology of legume seed development. Annu Rev Plant Biol 56 253 279
82. RoweHCHansenBGHalkierBAKliebensteinDJ 2008 Biochemical networks and epistasis shape the Arabidopsis thaliana metabolome. Plant Cell 20 1199 1216
83. Urbanczyk-WochniakELuedemannAKopkaJSelbigJRoessner-TunaliU 2003 Parallel analysis of transcript and metabolic profiles: a new approach in systems biology. Embo Rep 4 989 993
84. RoessnerUWillmitzerLFernieAR 2001 High-resolution metabolic phenotyping of genetically and environmentally diverse potato tuber systems. Identification of phenocopies. Plant Physiol 127 749 764
85. WentzellAMKliebensteinDJ 2008 Genotype, age, tissue, and environment regulate the structural outcome of glucosinolate activation. Plant Physiol 147 415 428
86. LalondeSBolesEHellmannHBarkerLPatrickJW 1999 The dual function of sugar carriers: Transport and sugar sensing. Plant Cell 11 707 726
87. TonsorSJAlonso-BlancoCKoornneefM 2005 Gene function beyond the single trait: natural variation, gene effects, and evolutionary ecology in Arabidopsis thaliana. Plant Cell Environ 28 2 20
88. GuLPJonesADLastRL 2010 Broad connections in the Arabidopsis seed metabolic network revealed by metabolite profiling of an amino acid catabolism mutant. Plant J 61 579 590
89. LessHGaliliG 2009 Coordinations between gene modules control the operation of plant amino acid metabolic networks. Bmc Syst Biol 3
90. LessHAngeloviciRTzinVGaliliG 2010 Principal transcriptional regulation and genome-wide system interactions of the Asp-family and aromatic amino acid networks of amino acid metabolism in plants. Amino Acids 39 1023 1028
91. KanehisaMGotoS 2000 KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res 28 27 30
92. KanehisaMGotoSHattoriMAoki-KinoshitaKFItohM 2006 From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 34 D354 D357
93. KanehisaMGotoSFurumichiMTanabeMHirakawaM 2010 KEGG for representation and analysis of molecular networks involving diseases and drugs. Nucleic Acids Res 38 D355 D360
94. StittMFernieAR 2003 From measurements of metabolites to metabolomics: an ‘on the fly’ perspective illustrated by recent studies of carbon-nitrogen interactions. Curr Opin Biotech 14 136 144
95. Nunes-NesiAFernieARStittM 2010 Metabolic and Signaling Aspects Underpinning the Regulation of Plant Carbon Nitrogen Interactions. Mol Plant 3 973 996
96. NakabayashiKOkamotoMKoshibaTKamiyaYNambaraE 2005 Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J 41 697 709
97. Roessner-TunaliUHegemannBLytovchenkoACarrariFBruedigamC 2003 Metabolic profiling of transgenic tomato plants overexpressing hexokinase reveals that the influence of hexose phosphorylation diminishes during fruit development. Plant Physiol 133 84 99
98. AssenovYRamirezFSchelhornSELengauerTAlbrechtM 2008 Computing topological parameters of biological networks. Bioinformatics 24 282 284
99. SteuerRLopezGZ 2008 Global Network Properties. JunkerBHSchreiberF Analysis of Biological Networks New Jersey, US Wiley Series 29 59
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Genetika Reprodukčná medicínaČlánok vyšiel v časopise
PLOS Genetics
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