Metabolic flux analysis of plastidic isoprenoid biosynthesis in poplar leaves emitting and nonemitting isoprene

Plant Physiology

Volumn 165, Issue 1, 2014, Pages 37-51

  Ghirardo, Andrea ^a   Wright, Louwrance Peter ^b   Bi, Zhen ^a   Rosenkranz, Maaria ^a   Pulido, Pablo ^c   Rodríguez Concepción, Manuel ^c   Niinemets, Ülo ^d   Brüggemann, Nicolas ^e   Gershenzon, Jonathan ^b   Schnitzler, Jörg Peter ^a  

^a INSTITUTE OF EPIDEMIOLOGY   (Germany)

^b MAX PLANCK INSTITUTE FOR CHEMICAL ECOLOGY   (Germany)

^c CSIC   (Spain)

^d ESTONIAN UNIVERSITY OF LIFE SCIENCES   (Estonia)

^e FORSCHUNGSZENTRUM JÜLICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

1,3 BUTADIENE DERIVATIVE; 2-C-METHYLERYTHRITOL 4-PHOSPHATE; 3,3-DIMETHYLALLYL PYROPHOSPHATE; CARBON; CARBON DIOXIDE; DEOXYXYLULOSE-5-PHOSPHATE SYNTHASE; ERYTHRITOL; HEMITERPENE; ISOPRENE; ORGANOPHOSPHORUS COMPOUND; PENTANE; PIGMENT; SUGAR PHOSPHATE; TRANSFERASE;

ANALOGS AND DERIVATIVES; BIOLOGICAL MODEL; BIOSYNTHESIS; DOWN REGULATION; ENZYMOLOGY; ISOTOPE LABELING; LIGHT; METABOLIC FLUX ANALYSIS; METABOLISM; PLANT LEAF; PLASTID; POPULUS; PROCEDURES; RADIATION RESPONSE; TEMPERATURE;

BUTADIENES; CARBON; CARBON DIOXIDE; CARBON ISOTOPES; DOWN-REGULATION; ERYTHRITOL; HEMITERPENES; ISOTOPE LABELING; LIGHT; METABOLIC FLUX ANALYSIS; MODELS, BIOLOGICAL; ORGANOPHOSPHORUS COMPOUNDS; PENTANES; PIGMENTS, BIOLOGICAL; PLANT LEAVES; PLASTIDS; POPULUS; SUGAR PHOSPHATES; TEMPERATURE; TRANSFERASES;

EID: 84899823167     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.114.236018     Document Type: Article

References (95)

1. Affek HP, Yakir D (2003) Natural abundance carbon isotope composition of isoprene reflects incomplete coupling between isoprene synthesis and photosynthetic carbon flow. Plant Physiol 131: 1727-1736
2. Archibald AT, Levine JG, Abraham NL, Cooke MC, Edwards PM, Heard DE, Jenkin ME, Karunaharan A, et al (2011) Impacts of HOx regeneration and recycling in the oxidation of isoprene: consequences for the composition of past, present and future atmospheres. Geophys Res Lett 38: L05804, DOI: 10.1029/2010GL046520
3. Arneth A, Monson RK, Schurgers G, Niinemets Ü, Palmer PI (2008) Why are estimates of global terrestrial isoprene emissions so similar (and why is this not so for monoterpenes)? Atmos Chem Phys 8: 4605-4620
4. Banerjee A, Wu Y, Banerjee R, Li Y, Yan H, Sharkey TD (2013) Feedback inhibition of deoxy-D-xylulose-5-phosphate synthase regulates the methylerythritol 4-phosphate pathway. J Biol Chem 288: 16926-16936
5. Behnke K, Ehlting B, Teuber M, Bauerfeind M, Louis S, Hänsch R, Polle A, Bohlmann J, Schnitzler JP (2007) Transgenic, non-isoprene emitting poplars don't like it hot. Plant J 51: 485-499
6. Behnke K, Ghirardo A, Janz D, Kanawati B, Esperschütz J, Zimmer I, Schmitt-Kopplin P, Niinemets Ü, Polle A, Schnitzler JP, et al (2013) Isoprene function in two contrasting poplars under salt and sunflecks. Tree Physiol 33: 562-578
7. Behnke K, Grote R, Brüggemann N, Zimmer I, Zhou G, Elobeid M, Janz D, Polle A, Schnitzler JP (2012) Isoprene emission-free poplars: a chance to reduce the impact from poplar plantations on the atmosphere. New Phytol 194: 70-82
8. Behnke K, Kaiser A, Zimmer I, Brüggemann N, Janz D, Polle A, Hampp R, Hänsch R, Popko J, Schmitt-Kopplin P, et al (2010a) RNAi-mediated suppression of isoprene emission in poplar transiently impacts phenolic metabolism under high temperature and high light intensities: a transcriptomic and metabolomic analysis. Plant Mol Biol 74: 61-75
9. Behnke K, Kleist E, Uerlings R, Wildt J, Rennenberg H, Schnitzler JP (2009) RNAi-mediated suppression of isoprene biosynthesis in hybrid poplar impacts ozone tolerance. Tree Physiol 29: 725-736
10. Behnke K, LoivamäkiM, Zimmer I, Rennenberg H, Schnitzler JP, Louis S (2010b) Isoprene emission protects photosynthesis in sunfleck exposed grey poplar. Photosynth Res 104: 5-17
11. Beisel KG, Jahnke S, Hofmann D, Köppchen S, Schurr U, Matsubara S (2010) Continuous turnover of carotenes and chlorophyll a in mature leaves of Arabidopsis revealed by 14CO2 pulse-chase labeling. Plant Physiol 152: 2188-2199
12. Bick JA, Lange BM (2003) Metabolic cross talk between cytosolic and plastidial pathways of isoprenoid biosynthesis: unidirectional transport of intermediates across the chloroplast envelope membrane. Arch Biochem Biophys 415: 146-154
13. Brilli F, Barta C, Fortunati A, Lerdau M, Loreto F, Centritto M (2007) Response of isoprene emission and carbon metabolism to drought in white poplar (Populus alba) saplings. New Phytol 175: 244-254
14. Brüggemann N, Schnitzler JP (2002a) Relationship of isopentenyl diphosphate (IDP) isomerase activity to isoprene emission of oak leaves. Tree Physiol 22: 1011-1018
15. Brüggemann N, Schnitzler JP (2002b) Diurnal variation of dimethylallyl diphosphate concentrations in oak (Quercus robur) leaves. Physiol Plant 115: 190-196
16. Cazzonelli CI, Pogson BJ (2010) Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci 15: 266-274
17. Chang MCY, Keasling JD (2006) Production of isoprenoid pharmaceuticals by engineered microbes. Nat Chem Biol 2: 674-681
18. Cinege G, Louis S, Hänsch R, Schnitzler JP (2009) Regulation of isoprene synthase promoter by environmental and internal factors. Plant Mol Biol 69: 593-604
19. Coplen TB, Brand WA, Gehre M, Gröning M, Meijer HAJ, Toman B, Verkouteren RM (2006) New guidelines for δ13C measurements. Anal Chem 78: 2439-2441
20. Delwiche CF, Sharkey TD (1993) Rapid appearance of 13C in biogenic isoprene when 13CO2 is fed to intact leaves. Plant Cell Environ 650: 587-591
21. Dudareva N, Andersson S, Orlova I, Gatto N, Reichelt M, Rhodes D, Boland W, Gershenzon J (2005) The nonmevalonate pathway supports both monoterpene and sesquiterpene formation in snapdragon flowers. Proc Natl Acad Sci USA 102: 933-938
22. Dudareva N, Klempien A, Muhlemann JK, Kaplan I (2013) Biosynthesis, function and metabolic engineering of plant volatile organic compounds. New Phytol 198: 16-32
23. Ehlting B, Dluzniewska P, Dietrich H, Selle A, Teuber M, Hänsch R, Nehls U, Polle A, Schnitzler JP, Rennenberg H, et al (2007) Interaction of nitrogen nutrition and salinity in grey poplar (Populus tremula 3 alba). Plant Cell Environ 30: 796-811
24. Enfissi EM, Fraser PD, Lois LM, Boronat A, SchuchW, Bramley PM (2005) Metabolic engineering of the mevalonate and non-mevalonate isopentenyl diphosphate-forming pathways for the production of healthpromoting isoprenoids in tomato. Plant Biotechnol J 3: 17-27
25. Estévez JM, Cantero A, Reindl A, Reichler S, León P (2001) 1-Deoxy-Dxylulose-5-phosphate synthase, a limiting enzyme for plastidic isoprenoid biosynthesis in plants. J Biol Chem 276: 22901-22909
26. Fuentes J, Lerdau M, Atkinson R, Baldocchi D, BottenheimJ, Ciccioli P, Lamb B, Geron C, Gu L, Guenther A, et al (2000) Biogenic hydrocarbons in the atmospheric boundary layer: a review. Bull Am Meteorol Soc 81: 1537-1575
27. Gerber E, Hemmerlin A, Hartmann M, Heintz D, Hartmann MA, Mutterer J, Rodríguez-Concepción M, Boronat A, Van Dorsselaer A, Rohmer M, et al (2009) The plastidial 2-C-methyl-D-erythritol 4-phosphate pathway provides the isoprenyl moiety for protein geranylgeranylation in tobacco BY-2 cells. Plant Cell 21: 285-300
28. Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nat Chem Biol 3: 408-414
29. Ghirardo A, Gutknecht J, Zimmer I, Brüggemann N, Schnitzler JP (2011) Biogenic volatile organic compound and respiratory CO2 emissions after 13C-labeling: online tracing of C translocation dynamics in poplar plants. PLoS ONE 6: e17393
30. Ghirardo A, Koch K, Taipale R, Zimmer I, Schnitzler JP, Rinne J (2010a) Determination of de novo and pool emissions of terpenes from four common boreal/alpine trees by 13CO2 labelling and PTR-MS analysis. Plant Cell Environ 33: 781-792
31. Ghirardo A, Zimmer I, Brüggemann N, Schnitzler JP (2010b) Analysis of 1-deoxy-D-xylulose 5-phosphate synthase activity in grey poplar leaves using isotope ratio mass spectrometry. Phytochemistry 71: 918-922
32. Giuliano G, Tavazza R, Diretto G, Beyer P, Taylor MA (2008) Metabolic engineering of carotenoid biosynthesis in plants. Trends Biotechnol 26: 139-145
33. Guenther A (2013) Upscaling biogenic volatile compound emissions from leaves to landscapes. In Ü Niinemets, RK Monson, eds, Biology, Controls and Models of Tree Volatile Organic Compound Emissions. Springer, Berlin, pp 391-414
34. Guevara-García A, San Román C, Arroyo A, Cortés ME, de la Luz Gutiérrez-Nava M, León P, Leon P (2005) Characterization of the Arabidopsis clb6 mutant illustrates the importance of posttranscriptional regulation of the methyl-D-erythritol 4-phosphate pathway. Plant Cell 17: 628-643
35. Hemmerlin A, Hoeffler JF, Meyer O, Tritsch D, Kagan IA, Grosdemange-Billiard C, Rohmer M, Bach TJ (2003) Cross-talk between the cytosolic mevalonate and the plastidial methylerythritol phosphate pathways in tobacco bright yellow-2 cells. J Biol Chem 278: 26666-26676
36. Illarionova V, Kaiser J, Ostrozhenkova E, Bacher A, FischerM, Eisenreich W, Rohdich F (2006) Nonmevalonate terpene biosynthesis enzymes as antiinfective drug targets: substrate synthesis and high-throughput screening methods. J Org Chem 71: 8824-8834
37. Ivanova LA, Ronzhina DA, Ivanov LA, Stroukova LV, Peuke AD, Rennenberg H (2009) Chloroplast parameters differ in wild type and transgenic poplars overexpressing gsh1 in the cytosol. Plant Biol (Stuttg) 11: 625-630
38. Kaling M, Kanawati B, Ghirardo A, Albert A, Winkler JB, Heller W, Barta C, Loreto F, Schmitt-Kopplin P, Schnitzler J-P (2014) UV-SI: UV-B mediated metabolic rearrangements in poplar revealed by non-targeted metabolomics. Plant Cell Environ http://dx.doi.org/10.1111/pce.12348
39. Karl T, Fall R, Rosenstiel TN, Prazeller P, Larsen B, Seufert G, Lindinger W (2002) On-line analysis of the 13CO2 labeling of leaf isoprene suggests multiple subcellular origins of isoprene precursors. Planta 215: 894-905
40. Kasahara H, Hanada A, Kuzuyama T, Takagi M, Kamiya Y, Yamaguchi S (2002) Contribution of the mevalonate and methylerythritol phosphate pathways to the biosynthesis of gibberellins in Arabidopsis. J Biol Chem 277: 45188-45194
41. Kiendler-Scharr A, Andres S, Bachner M, Behnke K, Broch S, Hofzumahaus A, Holland F, Kleist E, et al (2012) Isoprene in poplar emissions: effects on new particle formation and OH concentrations. Atmos Chem Phys 12: 1021-1030
42. Kreuzwieser J, Graus M, Wisthaler A, Hansel A, Rennenberg H, Schnitzler JP (2002) Xylem-transported glucose as an additional carbon source for leaf isoprene formation in Quercus robur. New Phytol 156: 171-178
43. Lange BM, Wildung MR, McCaskill D, Croteau R (1998) A family of transketolases that directs isoprenoid biosynthesis via a mevalonateindependent pathway. Proc Natl Acad Sci USA 95: 2100-2104
44. Laule O, Fürholz A, Chang HS, Zhu T, Wang X, Heifetz PB, Gruissem W, Lange M (2003) Crosstalk between cytosolic and plastidial pathways of isoprenoid biosynthesis in Arabidopsis thaliana. Proc Natl Acad Sci USA 100: 6866-6871
45. Li Z, Sharkey T (2013a) Molecular and pathway controls on biogenic volatile organic compound emissions. In Ü Niinemets, RK Monson, eds, Biology, Controls and Models of Tree Volatile Organic Compound Emissions. Springer, Berlin, pp 119-151
46. Li Z, Sharkey TD (2013b) Metabolic profiling of the methylerythritol phosphate pathway reveals the source of post-illumination isoprene burst from leaves. Plant Cell Environ 36: 429-437
47. Lois LM, Rodríguez-Concepción M, Gallego F, Campos N, Boronat A (2000) Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-D-xylulose 5-phosphate synthase. Plant J 22: 503-513
48. Loivamäki M, Louis S, Cinege G, Zimmer I, Fischbach RJ, Schnitzler JP (2007) Circadian rhythms of isoprene biosynthesis in grey poplar leaves. Plant Physiol 143: 540-551
49. Loreto F, Ciccioli P, Brancaleoni E, Frattoni M, Delfine S (2000) Incomplete 13C labelling of α-pinene content of Quercus ilex leaves and appearance of unlabelled C in α-pinene emission in the dark. Plant Cell Environ 23: 229-234
50. Loreto F, Pinelli P, Brancaleoni E, Ciccioli P (2004) 13C labeling reveals chloroplastic and extrachloroplastic pools of dimethylallyl pyrophosphate and their contribution to isoprene formation. Plant Physiol 135: 1903-1907
51. Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15: 154-166
52. Loreto F, Velikova V (2001) Isoprene produced by leaves protects the photosynthetic apparatus against ozone damage, quenches ozone products, and reduces lipid peroxidation of cellular membranes. Plant Physiol 127: 1781-1787
53. Mayrhofer S, Teuber M, Zimmer I, Louis S, Fischbach RJ, Schnitzler JP (2005) Diurnal and seasonal variation of isoprene biosynthesis-related genes in grey poplar leaves. Plant Physiol 139: 474-484
54. Mongélard G, Seemann M, Boisson AM, Rohmer M, Bligny R, Rivasseau C (2011) Measurement of carbon flux through the MEP pathway for isoprenoid synthesis by 31P-NMR spectroscopy after specific inhibition of 2-C-methyl-D-erythritol 2,4-cyclodiphosphate reductase: effect of light and temperature. Plant Cell Environ 34: 1241-1247
55. Monson RK, Grote R, Niinemets Ü, Schnitzler JP (2012) Modeling the isoprene emission rate from leaves. New Phytol 195: 541-559
56. Moses T, Pollier J, Thevelein JM, Goossens A (2013) Bioengineering of plant (tri)terpenoids: from metabolic engineering of plants to synthetic biology in vivo and in vitro. New Phytol 200: 27-43
57. Muñoz-Bertomeu J, Arrillaga I, Ros R, Segura J (2006) Up-regulation of 1-deoxy-D-xylulose-5-phosphate synthase enhances production of essential oils in transgenic spike lavender. Plant Physiol 142: 890-900
58. Niinemets Ü, Monson RK (2013) State-of-the-art of BVOC research: what do we have and what have we missed? In Ü Niinemets, RK Monson, eds, Biology, Controls and Models of Tree Volatile Organic Compound Emissions. Springer, Berlin, pp 95-118
59. Niinemets U, Tenhunen JD, Harley PC, Steinbrecher R (1999) A model of isoprene emission based on energetic requirements for isoprene synthesis and leaf photosynthetic properties for Liquidambar and Quercus. Plant Cell Environ 22: 1319-1335
60. Peñuelas J, Llusià J, Asensio D, Munné-Bosch S (2005) Linking isoprene with plant thermotolerance, antioxidants and monoterpene emissions. Plant Cell Environ 28: 278-286
61. Poisson N, Kanakidou M, Crutzen PJ (2000) Impact of non-methane hydrocarbons on tropospheric chemistry and the oxidizing power of the global troposphere: 3-dimensional modelling results. J Atmos Chem 36: 157-230
62. Pulido P, Toledo-Ortiz G, Phillips MA, Wright LP, Rodríguez-Concepción M (2013) Arabidopsis J-protein J20 delivers the first enzyme of the plastidial isoprenoid pathway to protein quality control. Plant Cell 25: 4183-4194
63. Rasulov B, Bichele I, Laisk A, Niinemets Ü (2013) Competition between isoprene emission and pigments synthesis during leaf development in aspen. Plant Cell Environ 37: 724-741
64. Rasulov B, Copolovici L, Laisk A, Niinemets U (2009a) Postillumination isoprene emission: in vivo measurements of dimethylallyldiphosphate pool size and isoprene synthase kinetics in aspen leaves. Plant Physiol 149: 1609-1618
65. Rasulov B, Hüve K, Bichele I, Laisk A, Niinemets Ü (2010) Temperature response of isoprene emission in vivo reflects a combined effect of substrate limitations and isoprene synthase activity: a kinetic analysis. Plant Physiol 154: 1558-1570
66. Rasulov B, Hüve K, Välbe M, Laisk A, Niinemets U (2009b) Evidence that light, carbon dioxide, and oxygen dependencies of leaf isoprene emission are driven by energy status in hybrid aspen. Plant Physiol 151: 448-460
67. Rios-Estepa R, Lange BM (2007) Experimental and mathematical approaches to modeling plant metabolic networks. Phytochemistry 68: 2351-2374
68. Rodríguez-Concepción M (2006) Early steps in isoprenoid biosynthesis: multilevel regulation of the supply of common precursors in plant cells. Phytochem Rev 5: 1-15
69. Rosenstiel TN, Potosnak MJ, Griffin KL, Fall R, Monson RK (2003) Increased CO2 uncouples growth from isoprene emission in an agriforest ecosystem. Nature 421: 256-259
70. Ryan AC, Hewitt CN, Possell M, Vickers CE, Purnell A, Mullineaux PM, Davies WJ, Dodd IC (2014) Isoprene emission protects photosynthesis but reduces plant productivity during drought in transgenic tobacco (Nicotiana tabacum) plants. New Phytol 201: 205-216
71. Schnitzler JP, Graus M, Kreuzwieser J, Heizmann U, Rennenberg H, Wisthaler A, Hansel A (2004) Contribution of different carbon sources to isoprene biosynthesis in poplar leaves. Plant Physiol 135: 152-160
72. Schnitzler JP, Louis S, Behnke K, Loivamäki M (2010) Poplar volatiles: biosynthesis, regulation and (eco)physiology of isoprene and stressinduced isoprenoids. Plant Biol (Stuttg) 12: 302-316
73. Schnitzler JP, Zimmer I, Bachl A, Arend M, Fromm J, Fischbach RJ (2005) Biochemical properties of isoprene synthase in poplar (Populus 3 canescens). Planta 222: 777-786
74. Sharkey TD (1995) Why plants emits isoprene. Nature 374: 769
75. Sharkey TD, Wiberley AE, Donohue AR (2008) Isoprene emission from plants: why and how. Ann Bot (Lond) 101: 5-18
76. Sharkey TD, Yeh S (2001) Isoprene emission from plants. Annu Rev Plant Physiol Plant Mol Biol 52: 407-436
77. Sun Z, Hüve K, Vislap V, Niinemets U (2013a) Elevated [CO2] magnifies isoprene emissions under heat and improves thermal resistance in hybrid aspen. J Exp Bot 64: 5509-5523
78. Sun Z, Niinemets Ü, Hüve K, Noe SM, Rasulov B, Copolovici L, Vislap V (2012) Enhanced isoprene emission capacity and altered light responsiveness in aspen grown under elevated atmospheric CO2 concentration. Glob Change Biol 18: 3423-3440
79. Sun Z, Niinemets U, HüveK, Rasulov B, NoeSM (2013b) Elevated atmospheric CO2 concentration leads to increased whole-plant isoprene emission in hybrid aspen (Populus tremula 3 Populus tremuloides). New Phytol 198: 788-800
80. Thulasiram HV, Erickson HK, Poulter CD (2007) Chimeras of two isoprenoid synthases catalyze all four coupling reactions in isoprenoid biosynthesis. Science 316: 73-76
81. Trowbridge AM, Asensio D, Eller ASD, Way DA, Wilkinson MJ, Schnitzler JP, Jackson RB, Monson RK (2012) Contribution of various carbon sources toward isoprene biosynthesis in poplar leaves mediated by altered atmospheric CO2 concentrations. PLoS ONE 7: e32387
82. Velikova V, Ghirardo A, Vanzo E, Merl J, Hauck SM, Schnitzler JP (January 22, 2014) The genetic manipulation of isoprene emissions in poplar plants remodels the chloroplast proteome. J Proteome Res http://dx.doi.org/10.1021/pr401124z
83. Velikova V, Loreto F (2005) On the relationship between isoprene emission and thermotolerance in Phragmites australis leaves exposed to high temperatures and during the recovery from a heat stress. Plant Cell Environ 28: 318-327
84. Vickers CE, Gershenzon J, Lerdau MT, Loreto F (2009) A unified mechanism of action for volatile isoprenoids in plant abiotic stress. Nat Chem Biol 5: 283-291
85. Vranová E, Coman D, Gruissem W (2012) Structure and dynamics of the isoprenoid pathway network. Mol Plant 5: 318-333
86. Way DA, Ghirardo A, Kanawati B, Esperschütz J, Monson RK, Jackson RB, Schmitt-Kopplin P, Schnitzler JP (2013) Increasing atmospheric CO2 reduces metabolic and physiological differences between isopreneand non-isoprene-emitting poplars. New Phytol 200: 534-546
87. Way DA, Schnitzler JP, Monson RK, Jackson RB (2011) Enhanced isoprene-related tolerance of heat-and light-stressed photosynthesis at low, but not high, CO2 concentrations. Oecologia 166: 273-282
88. Weise SE, Li Z, Sutter AE, Corrion A, Banerjee A, Sharkey TD (2013) Measuring dimethylallyl diphosphate available for isoprene synthesis. Anal Biochem 435: 27-34
89. Werner RA, Brand WA (2001) Referencing strategies and techniques in stable isotope ratio analysis. Rapid Commun Mass Spectrom 15: 501-519
90. Wiberley AE, Donohue AR, Westphal MM, Sharkey TD (2009) Regulation of isoprene emission from poplar leaves throughout a day. Plant Cell Environ 32: 939-947
91. Wolfertz M, Sharkey TD, Boland W, Kühnemann F (2004) Rapid regulation of the methylerythritol 4-phosphate pathway during isoprene synthesis. Plant Physiol 135: 1939-1945
92. Wu S, Schalk M, Clark A, Miles RB, Coates R, Chappell J (2006) Redirection of cytosolic or plastidic isoprenoid precursors elevates terpene production in plants. Nat Biotechnol 24: 1441-1447
93. Xiao Y, Savchenko T, Baidoo EEK, Chehab WE, Hayden DM, Tolstikov V, Corwin JA, Kliebenstein DJ, Keasling JD, Dehesh K (2012) Retrograde signaling by the plastidial metabolite MEcPP regulates expression of nuclear stress-response genes. Cell 149: 1525-1535
94. Zeidler JG, Lichtenthaler HL, May HU, Lichtenthaler FW (1997) Is isoprene emitted by plants synthesized via the novel isopentenyl pyrophosphate pathway? Z Naturforsch C 53: 980-986
95. Zhou C, Li Z, Wiberley-Bradford AE, Weise SE, Sharkey TD (2013) Isopentenyl diphosphate and dimethylallyl diphosphate/isopentenyl diphosphate ratio measured with recombinant isopentenyl diphosphate isomerase and isoprene synthase. Anal Biochem 440: 130-136