Protein degradation - an alternative respiratory substrate for stressed plants

Trends in Plant Science

Volumn 16, Issue 9, 2011, Pages 489-498

  Araújo, Wagner L ^a   Tohge, Takayuki ^a   Ishizaki, Kimitsune ^b,c   Leaver, Christopher J ^c   Fernie, Alisdair R ^a  

^a MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^b KYOTO UNIVERSITY   (Japan)

^c UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID; CHLOROPHYLL; ELECTRON TRANSFERRING FLAVOPROTEIN; PROTEASOME; VEGETABLE PROTEIN;

AUTOPHAGY; CELL RESPIRATION; CITRIC ACID CYCLE; ELECTRON TRANSPORT; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MITOCHONDRION; OXIDATIVE STRESS; PLANT; PLANT GENE; REVIEW; UBIQUITINATION;

AMINO ACIDS; AUTOPHAGY; CELL RESPIRATION; CHLOROPHYLL; CITRIC ACID CYCLE; ELECTRON TRANSPORT; ELECTRON-TRANSFERRING FLAVOPROTEINS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; MITOCHONDRIA; OXIDATIVE STRESS; PLANT PROTEINS; PLANTS; PROTEASOME ENDOPEPTIDASE COMPLEX; TRANSCRIPTION, GENETIC; UBIQUITINATION;

EID: 80052334837     PISSN: 13601385     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tplants.2011.05.008     Document Type: Review

References (135)

1. Tcherkez G., et al. In vivo respiratory metabolism of illuminated leaves. Plant Physiol. 2005, 138:1596-1606.
2. Nunes-Nesi A., et al. The enigmatic contribution of mitochondrial function in photosynthesis. J. Exp. Bot. 2008, 59:1675-1684.
3. Carrari F., et al. Reduced expression of aconitase results in an enhanced rate of photosynthesis and marked shifts in carbon partitioning in illuminated leaves of wild species tomato. Plant Physiol. 2003, 133:1322-1335.
4. Fernie A.R., et al. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr. Opin. Plant Biol. 2004, 7:254-261.
5. Sweetlove L.J., et al. The mitochondrion: an integration point of cellular metabolism and signalling. Crit. Rev. Plant Sci. 2007, 26:17-43.
6. Rasmusson A.G., et al. The multiplicity of dehydrogenases in the electron transport chain of plant mitochondria. Mitochondrion 2008, 8:47-60.
7. McDonald A.E., et al. Alternative oxidase in animals: unique characteristics and taxonomic distribution. J. Exp. Biol. 2009, 212:2627-2634.
8. Plaxton W.C., Podesta F.E. The functional organization and control of plant respiration. Crit. Rev. Plant Sci. 2006, 25:159-198.
9. Ishizaki K., et al. The critical role of Arabidopsis electron-transfer flavoprotein:ubiquinone oxidoreductase during dark-induced starvation. Plant Cell 2005, 17:2587-2600.
10. Kunz H.H., et al. The ABC transporter PXA1 and peroxisomal beta-oxidation are vital for metabolism in mature leaves of Arabidopsis during extended darkness. Plant Cell 2009, 21:2733-2749.
11. Vierstra R.D. The ubiquitin-26S proteasome system at the nexus of plant biology. Nat. Rev. Mol. Cell Biol. 2009, 10:385-397.
12. Hörtensteiner S., Kräutler B. Chlorophyll breakdown in higher plants. Biochim. Biophys. Acta 2011, 1807:977-988.
13. Urade R. Cellular response to unfolded proteins in the endoplasmic reticulum of plants. FEBS J. 2007, 274:1152-1171.
14. Tajima H., et al. Endoplasmic reticulum stress response and regulated intramembrane proteolysis in plants. Plant Biotech. 2008, 25:271-278.
15. Vitale A., Boston R.S. Endoplasmic reticulum quality control and the unfolded protein response: insights from plants. Traffic 2008, 9:1581-1588.
16. Stuttmann J., et al. COP9 signalosome- and 26S proteasome-dependent regulation of SCFTIR1 accumulation in Arabidopsis. J. Biol. Chem. 2009, 284:7917-7927.
17. Moon J., et al. The ubiquitin-proteasome pathway and plant development. Plant Cell 2004, 16:3181-3195.
18. Wang H., et al. Regulatory features underlying pollination-dependent and -independent tomato fruit set revealed by transcript and primary metabolite profiling. Plant Cell 2009, 21:1428-1452.
19. An F.Y., et al. Ethylene-induced stabilization of ETHYLENE INSENSITIVE3 and EIN3-LIKE1 is mediated by proteasomal degradation of EIN3 binding F-Box 1 and 2 that requires EIN2 in Arabidopsis. Plant Cell 2010, 22:2384-2401.
20. Negi S., et al. Inhibition of the ubiquitin-proteasome pathway alters cellular levels of nitric oxide in tomato seedlings. Mol. Plant 2010, 3:854-869.
21. Xiong Y., et al. AtATG18a is required for the formation of autophagosomes during nutrient stress and senescence in Arabidopsis thaliana. Plant J. 2005, 42:535-546.
22. Diaz-Troya S., et al. The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy 2008, 4:851-865.
23. Liu Y.M., Bassham D.C. TOR Is a negative regulator of autophagy in Arabidopsis thaliana. PloS ONE 2010, 5:e11883.
24. Schieke S.M., Finkel T. Mitochondrial signaling, TOR, and life span. Biol. Chem. 2006, 387:1357-1361.
25. Leiber R.M., et al. The TOR pathway modulates the structure of cell walls in Arabidopsis. Plant Cell 2010, 22:1898-1908.
26. Kapahi P., et al. With TOR, less is more: a key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metab. 2010, 11:453-465.
27. Deprost D., et al. The Arabidopsis TOR kinase links plant growth, yield, stress resistance and mRNA translation. EMBO Rep. 2007, 8:864-870.
28. Mahfouz M.M., et al. Arabidopsis TARGET OF RAPAMYCIN interacts with RAPTOR, which regulates the activity of S6 kinase in response to osmotic stress signals. Plant Cell 2006, 18:477-490.
29. Dinkova T.D., et al. Dissecting the TOR-S6K signal transduction pathway in maize seedlings: relevance on cell growth regulation. Physiol. Plant 2007, 130:1-10.
30. Noda T., Ohsumi Y. TOR, a phosphatidylinositol kinase homologue, controls autophagy in yeast. J. Biol. Chem. 1998, 273:3963-3966.
31. Bassham D.C. Plant autophagy-more than a starvation response. Curr. Opin. Plant Biol. 2007, 10:587-593.
32. Downes B., Vierstra R.D. Post-translational regulation in plants employing a diverse set of polypeptide tags. Biochem. Soc. Trans. 2005, 33:393-399.
33. Smalle J., Vierstra R.D. The ubiquitin 26S proteasome proteolytic pathway. Annu. Rev. Plant Biol. 2004, 55:555-590.
34. Wilkinson K.D. Ubiquitination and deubiquitination: Targeting of proteins for degradation by the proteasome. Semin. Cell Dev. Biol. 2000, 11:141-148.
35. Doherty F.J., et al. The ubiquitin-proteasome pathway of intracellular proteolysis. Essays Biochem. 2002, 38:51-63.
36. Hicke L. Protein regulation by monoubiquitin. Nat. Rev. Mol. Cell Biol. 2001, 2:195-201.
37. Woo H.R., et al. ORE9, an F-box protein that regulates leaf senescence in Arabidopsis. Plant Cell 2001, 13:1779-1790.
38. Sullivan J.A., et al. The diverse roles of ubiquitin and the 26S proteasome in the life of plants. Nat. Rev. Genet. 2003, 4:948-958.
39. Bachmair A., et al. Ubiquitylation in plants: a post-genomic look at a post-translational modification. Trends Plant Sci. 2001, 6:463-470.
40. Brouquisse R., et al. Induction of a carbon-starvation-related proteolysis in whole maize plants submitted to light/dark cycles and to extended darkness. Plant Physiol. 1998, 117:1281-1291.
41. Vierstra R.D. Proteolysis in plants: mechanisms and functions. Plant Mol. Biol. 1996, 32:275-302.
42. Schnell J.D., Hicke L. Non-traditional functions of ubiquitin and ubiquitin-binding proteins. J. Biol. Chem. 2003, 278:35857-35860.
43. Titapiwatanakun B., Murphy A.S. Post-transcriptional regulation of auxin transport proteins: cellular trafficking, protein phosphorylation, protein maturation, ubiquitination, and membrane composition. J. Exp. Bot. 2009, 60:1093-1107.
44. Hanna J., et al. Deubiquitinating enzyme Ubp6 functions noncatalytically to delay proteasomal degradation. Cell 2006, 127:99-111.
45. Sridhar V.V., et al. Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature 2007, 447:735-738.
46. Amerik A.Y., Hochstrasser M. Mechanism and function of deubiquitinating enzymes. Biochim. Biophys. Acta 2004, 1695:189-207.
47. Kabeya Y., et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J. 2000, 19:5720-5728.
48. Pattingre S., et al. Bcl-2 antiapoptotic proteins inhibit Beclin 1-dependent autophagy. Cell 2005, 122:927-939.
49. Hanaoka H., et al. Leaf senescence and starvation-induced chlorosis are accelerated by the disruption of an Arabidopsis autophagy gene. Plant Physiol. 2002, 129:1181-1193.
50. Liu Y., et al. Autophagy regulates programmed cell death during the plant innate immune response. Cell 2005, 121:567-577.
51. Slavikova S., et al. An autophagy-associated Atg8 protein is involved in the responses of Arabidopsis seedlings to hormonal controls and abiotic stresses. J. Exp. Bot. 2008, 59:4029-4043.
52. Yoshimoto K., et al. Autophagy negatively regulates cell death by controlling NPR1-dependent salicylic acid signaling during senescence and the innate immune response in Arabidopsis. Plant Cell 2009, 21:2914-2927.
53. Wullschleger S., et al. TOR signaling in growth and metabolism. Cell 2006, 124:471-484.
54. Gingras A.C., et al. Regulation of translation initiation by FRAP/mTOR. Genes Dev. 2001, 15:807-826.
55. Schmelzle T., Hall M.N. TOR, a central controller of cell growth. Cell 2000, 103:253-262.
56. Hannah M.A., et al. Combined transcript and metabolite profiling of Arabidopsis grown under widely variant growth conditions facilitates the identification of novel metabolite-mediated regulation of gene expression. Plant Physiol. 2010, 152:2120-2129.
57. Lopez-Berges M.S., et al. A nitrogen response pathway regulates virulence functions in Fusarium oxysporum via the protein kinase TOR and the bZIP protein MeaB. Plant Cell 2010, 22:2459-2475.
58. Book A.J., et al. The RPN5 subunit of the 26s proteasome is essential for gametogenesis, sporophyte development, and complex assembly in Arabidopsis. Plant Cell 2009, 21:460-478.
59. Hellmann H., Estelle M. Plant development: regulation by protein degradation. Science 2002, 297:793-797.
60. Zhang Y., et al. Roles of proteolysis in plant self-incompatibility. Annu. Rev. Plant Biol. 2009, 60:21-42.
61. Lim P.O., et al. Leaf senescence. Annu. Rev. Plant Biol. 2007, 58:115-136.
62. Kinoshita T., et al. Vacuolar processing enzyme is up-regulated in the lytic vacuoles of vegetative tissues during senescence and under various stressed conditions. Plant J. 1999, 19:43-53.
63. Otegui M.S., et al. Senescence-associated vacuoles with intense proteolytic activity develop in leaves of Arabidopsis and soybean. Plant J. 2005, 41:831-844.
64. Chung T., et al. ATG8 lipidation and ATG8-mediated autophagy in Arabidopsis require ATG12 expressed from the differentially controlled ATG12A AND ATG12B loci. Plant J. 2010, 62:483-493.
65. Thompson A.R., Vierstra R.D. Autophagic recycling: lessons from yeast help define the process in plants. Curr. Opin. Plant Biol. 2005, 8:165-173.
66. Thompson A.R., et al. Autophagic nutrient recycling in Arabidopsis directed by the ATG8 and ATG12 conjugation pathways. Plant Physiol. 2005, 138:2097-2110.
67. Seay M., et al. Autophagy and plant innate immunity. Cell Microbiol. 2006, 8:899-906.
68. Hayward A.P., et al. Autophagy and plant innate immunity: defense through degradation. Semin. Cell Dev. Biol. 2009, 20:1041-1047.
69. Tzin V., Galili G. New insights into the shikimate and aromatic amino acids biosynthesis pathways in plants. Mol. Plant 2010, 3:956-972.
70. Li J., Last R.L. The Arabidopsis thaliana trp5 mutant has a feedback-resistant anthranilate synthase and elevated soluble tryptophan. Plant Physiol. 1996, 110:51-59.
71. Radwanski E.R., Last R.L. Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell 1995, 7:921-934.
72. Less H., Galili G. Principal transcriptional programs regulating plant amino acid metabolism in response to abiotic stresses. Plant Physiol. 2008, 147:316-330.
73. Angelovici R., et al. A seed high-lysine trait is negatively associated with the TCA cycle and slows down Arabidopsis seed germination. New Phytol. 2010, 189:148-159.
74. Galili G. New insights into the regulation and functional significance of lysine metabolism in plants. Annu. Rev. Plant Biol. 2002, 53:27-43.
75. Stepansky A., Galili G. Synthesis of the Arabidopsis bifunctional lysine-ketoglutarate reductase/saccharopine dehydrogenase enzyme of lysine catabolism is concertedly regulated by metabolic and stress-associated signals. Plant Physiol. 2003, 133:1407-1415.
76. Jander G., et al. Application of a high-throughput HPLC-MS/MS assay to Arabidopsis mutant screening; evidence that threonine aldolase plays a role in seed nutritional quality. Plant J. 2004, 39:465-475.
77. Jander G., et al. Ethylmethanesulfonate saturation mutagenesis in Arabidopsis to determine frequency of herbicide resistance. Plant Physiol. 2003, 131:139-146.
78. Ishizaki K., et al. The mitochondrial electron transfer flavoprotein complex is essential for survival of Arabidopsis in extended darkness. Plant J. 2006, 47:751-760.
79. Gu L.P., et al. Broad connections in the Arabidopsis seed metabolic network revealed by metabolite profiling of an amino acid catabolism mutant. Plant J. 2010, 61:579-590.
80. Engqvist M.K.M., et al. Plant D-2-hydroxyglutarate dehydrogenase participates in the catabolism of lysine especially during senescence. J. Biol. Chem. 2011, 286:11382-11390.
81. Slavikova S., et al. The autophagy-associated Atg8 gene family operates both under favourable growth conditions and under starvation stresses in Arabidopsis plants. J. Exp. Bot. 2005, 56:2839-2849.
82. Hörtensteiner S. Chlorophyll degradation during senescence. Annu. Rev. Plant Biol. 2006, 57:55-77.
83. Schelbert S., et al. Pheophytin pheophorbide hydrolase (pheophytinase) is involved in chlorophyll breakdown during leaf senescence in Arabidopsis. Plant Cell 2009, 21:767-785.
84. Araújo W.L., et al. Identification of the 2-hydroxyglutarate and isovaleryl-CoA dehydrogenases as alternative electron donors linking lysine catabolism to the electron transport chain of Arabidopsis mitochondria. Plant Cell 2010, 22:1549-1563.
85. Heazlewood J.L., et al. Experimental analysis of the Arabidopsis mitochondrial proteome highlights signaling and regulatory components, provides assessment of targeting prediction programs, and indicates plant-specific mitochondrial proteins. Plant Cell 2004, 16:241-256.
86. Buchanan-Wollaston V., et al. Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J. 2005, 42:567-585.
87. Lehmann M., et al. The metabolic response of Arabidopsis roots to oxidative stress is distinct from that of heterotrophic cells in culture and highlights a complex relationship between the levels of transcripts, metabolites, and flux. Mol. Plant 2009, 2:390-406.
88. Ruzicka F.J., Beinert H. A new iron-sulfur flavoprotein of the respiratory chain. A component of the fatty acid beta oxidation pathway. J. Biol. Chem. 1977, 252:8440-8445.
89. Beckmann J.D., Frerman F.E. Electron-transfer flavoprotein-ubiquinone oxidoreductase from pig liver- purification and molecular redox, and catalytic properties. Biochemistry 1985, 24:3913-3921.
90. Frerman F.E. Acyl-CoA dehydrogenases, electron-transfer flavoprotein and electron-transfer flavoprotein dehydrogenases. Biochem. Soc. Trans. 1988, 16:416-418.
91. Frerman F.E., Goodman S.I. Defects of electron transfer flavoprotein and electron transfer flavoprotein-ubiquinone oxidoreductase: glutaric acidemia type II. The Metabolic and Molecular Bases of Inherited Disease 2001, 2357-2365. McGraw-Hill. 8th edn. C.R. Scriver (Ed.).
92. Ghisla S., Thorpe C. Acyl-CoA dehydrogenases - a mechanistic overview. Eur. J. Biochem. 2004, 271:494-508.
93. He M., et al. A new genetic disorder in mitochondrial fatty acid beta-oxidation: ACAD9 deficiency. Am. J. Hum. Genet. 2007, 81:87-103.
94. Hoskins D.D., Mackenzie C.G. Solubilization and electron transfer flavoprotein requirement of mitochondrial sarcosine dehydrogenase and dimethylglycine dehydrogenase. J. Biol. Chem. 1961, 236:177-183.
95. Watmough N.J., Frerman F.E. The electron transfer flavoprotein: ubiquinone oxidoreductases. Biochim. Biophys. Acta 2010, 1797:1910-1916.
96. Engqvist M., et al. Two D-2-hydroxy-acid dehydrogenases in Arabidopsis thaliana with catalytic capacities to participate in the last reactions of the methylglyoxal and beta-oxidation pathways. J. Biol. Chem. 2009, 284:25026-25037.
97. Diaz C., et al. Characterization of markers to determine the extent and variability of leaf senescence in Arabidopsis. A metabolic profiling approach. Plant Physiol. 2005, 138:898-908.
98. Schippers J.H., et al. The Arabidopsis onset of leaf death5 mutation of quinolinate synthase affects nicotinamide adenine dinucleotide biosynthesis and causes early ageing. Plant Cell 2008, 20:2909-2925.
99. Weigelt K., et al. Increasing amino acid supply in pea embryos reveals specific interactions of N and C metabolism, and highlights the importance of mitochondrial metabolism. Plant J. 2008, 55:909-926.
100. Obata T., et al. Alteration of mitochondrial protein complexes in relation to metabolic regulation under short-term oxidative stress in Arabidopsis seedlings. Phytochemistry 2011, 72:1081-1091.
101. Struys E.A., et al. Mutations in the D-2-hydroxyglutarate dehydrogenase gene cause D-2-hydroxyglutaric aciduria. Am. J. Hum. Genet. 2005, 76:358-360.
102. Dang L., et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature 2009, 462:739-744.
103. O'Connor G., et al. A novel mutation as a cause of L-2-hydroxyglutaric aciduria. J. Neurol. 2009, 256:672-673.
104. Nunes-Nesi A., et al. Targeting mitochondrial metabolism and machinery as a means to enhance photosynthesis. Plant Physiol. 2011, 155:101-107.
105. Sweetlove L.J., et al. Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci. 2010, 15:462-470.
106. van der Merwe M.J., et al. Decreased mitochondrial activities of malate dehydrogenase and fumarase in tomato lead to altered root growth and architecture via diverse mechanisms. Plant Physiol. 2009, 149:653-669.
107. van der Merwe M.J., et al. Tricarboxylic acid cycle activity regulates tomato root growth via effects on secondary cell wall production. Plant Physiol. 2010, 153:611-621.
108. Sulpice R., et al. Mild reductions in cytosolic NADP-dependent isocitrate dehydrogenase activity result in lower amino acid contents and pigmentation without impacting growth. Amino Acids 2010, 39:1055-1066.
109. Studart-Guimarães C., et al. Reduced expression of succinyl-coenzyme A ligase can be compensated for by up-regulation of the gamma-aminobutyrate shunt in illuminated tomato leaves. Plant Physiol. 2007, 145:626-639.
110. Sienkiewicz-Porzucek A., et al. Mild reductions in mitochondrial NAD-dependent isocitrate dehydrogenase activity result in altered nitrate assimilation and pigmentation but do not impact growth. Mol. Plant 2010, 3:156-173.
111. Sienkiewicz-Porzucek A., et al. Mild reductions in mitochondrial citrate synthase activity result in a compromised nitrate assimilation and reduced leaf pigmentation but have no effect on photosynthetic performance or growth. Plant Physiol. 2008, 147:115-127.
112. Nunes-Nesi A., et al. Enhanced photosynthetic performance and growth as a consequence of decreasing mitochondrial malate dehydrogenase activity in transgenic tomato plants. Plant Physiol. 2005, 137:611-622.
113. Nunes-Nesi A., et al. Deficiency of mitochondrial fumarase activity in tomato plants impairs photosynthesis via an effect on stomatal function. Plant J. 2007, 50:1093-1106.
114. Araújo W.L., et al. Inhibition of 2-oxoglutarate dehydrogenase in potato tuber suggests the enzyme is limiting for respiration and confirms its importance in nitrogen assimilation. Plant Physiol. 2008, 148:1782-1796.
115. Bauwe H., et al. Photorespiration: players, partners and origin. Trends Plant Sci. 2010, 15:330-336.
116. Foyer C.H., et al. Respiration and nitrogen assimilation: targeting mitochondria-associated metabolism as a means to enhance nitrogen use efficiency. J. Exp. Bot. 2011, 62:1467-1482.
117. Reumann S., Weber A.P.M. Plant peroxisomes respire in the light: Some gaps of the photorespiratory C2 cycle have become filled--others remain. Biochim. Biophys. Acta 2006, 1763:1496-1510.
118. Bräutigam A., Weber A.P.M. Do metabolite transport processes limit photosynthesis?. Plant Physiol. 2011, 155:43-48.
119. Palmieri F., et al. Evolution, structure and function of mitochondrial carriers in plants. Plant J. 2011, 66:161-181.
120. Schwechheimer C., Schwager K. Regulated proteolysis and plant development. Plant Cell Rep. 2004, 23:353-364.
121. Schwechheimer C., Villalobos L.I.A.C. Cullin-containing E3 ubiquitin ligases in plant development. Curr. Opin. Plant Biol. 2004, 7:677-686.
122. Henriques R., et al. Regulated proteolysis in light-related signaling pathways. Curr. Opin. Plant Biol. 2009, 12:49-56.
123. Lee J.-H., et al. Characterization of Arabidopsis and rice DWD proteins and their roles as substrate receptors for CUL4-RING E3 ubiquitin ligases. Plant Cell 2008, 20:152-167.
124. Lee J.-H., et al. DWA1 and DWA2, two Arabidopsis DWD protein components of CUL4-based E3 ligases, act together as negative regulators in ABA signal transduction. Plant Cell 2010, 22:1716-1732.
125. Zhang Y., et al. Arabidopsis DDB1-CUL4 ASSOCIATED FACTOR1 forms a nuclear E3 ubiquitin ligase with DDB1 and CUL4 that is involved in multiple plant developmental processes. Plant Cell 2008, 20:1437-1455.
126. Picault N., et al. The growing family of mitochondrial carriers in Arabidopsis. Trends Plant Sci. 2004, 9:138-146.
127. Linka N., Weber A.P.M. Intracellular metabolite transporters in plants. Mol. Plant 2010, 3:21-53.
128. Saito K., et al. Decoding genes with coexpression networks and metabolomics - 'majority report by precogs'. Trends Plant Sci. 2008, 13:36-43.
129. Hirai M.Y., et al. Omics-based identification of Arabidopsis Myb transcription factors regulating aliphatic glucosinolate biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 2007, 104:6478-6483.
130. Tohge T., Fernie A.R. Combining genetic diversity, informatics and metabolomics to facilitate annotation of plant gene function. Nat. Protoc. 2010, 5:1210-1227.
131. Naoumkina M.A., et al. Genomic and coexpression analyses predict multiple genes involved in triterpene saponin biosynthesis in Medicago truncatula. Plant Cell 2010, 22:850-866.
132. Guttikonda S., et al. Whole genome co-expression analysis of soybean cytochrome P450 genes identifies nodulation-specific P450 monooxygenases. BMC Plant Biol. 2010, 10:243.
133. Obayashi T., et al. ATTED-II: a database of co-expressed genes and cis elements for identifying co-regulated gene groups in Arabidopsis. Nucleic Acids Res. 2007, 35:D863-D869.
134. Akiyama K., et al. PRIMe: a web site that assembles tools for metabolomics and transcriptomics. In Silico Biol. 2008, 8:339-345.
135. Bagatelj V., Mrvar A. Pajek - program for large network analysis. Connections 1998, 21:47-57.