Hydrogen isotopic differences between C3 and C4 land plant lipids: consequences of compartmentation in C4 photosynthetic chemistry and C3 photorespiration.

The 2 H/1 H ratio of carbon-bound H in biolipids holds potential for probing plant lipid biosynthesis and metabolism. The biochemical mechanism underlying the isotopic differences between lipids from C3 and C4 plants is still poorly understood. GC-pyrolysis-IRMS (gas chromatography-pyrolysis-isotope ratio mass spectrometry) measurement of the 2 H/1 H ratio of leaf lipids from controlled and field grown plants indicates that the biochemical isotopic fractionation (ε2 Hlipid_biochem ) differed between C3 and C4 plants in a pathway-dependent manner: ε2 HC4  > ε2 HC3 for the acetogenic pathway, ε2 HC4  < ε2 HC3 for the mevalonic acid pathway and the 1-deoxy-D-xylulose 5-phosphate pathway across all species examined. It is proposed that compartmentation of photosynthetic CO2 fixation into C4 mesophyll (M) and bundle sheath (BS) cells and suppression of photorespiration in C4 M and BS cells both result in C4 M chloroplastic pyruvate - the precursor for acetogenic pathway - being more depleted in 2 H relative to pyruvate in C3 cells. In addition, compartmentation in C4 plants also results in (i) the transferable H of NADPH being enriched in 2 H in C4 M chloroplasts compared with that in C3 chloroplasts for the 1-deoxy-D-xylulose 5-phosphate pathway pathway and (ii) pyruvate relatively 2 H-enriched being used for the mevalonic acid pathway in the cytosol of BS cells in comparison with that in C3 cells.

[1]  Z. An,et al.  Different hydrogen isotope fractionations during lipid formation in higher plants: Implications for paleohydrology reconstruction at a global scale , 2016, Scientific Reports.

[2]  M. Nilsson,et al.  Detecting long-term metabolic shifts using isotopomers: CO2-driven suppression of photorespiration in C3 plants over the 20th century , 2015, Proceedings of the National Academy of Sciences.

[3]  G. Farquhar,et al.  Allocate carbon for a reason: priorities are reflected in the ¹³C/¹²C ratios of plant lipids synthesized via three independent biosynthetic pathways. , 2015, Phytochemistry.

[4]  Y. Huang,et al.  Major Evolutionary Trends in Hydrogen Isotope Fractionation of Vascular Plant Leaf Waxes , 2014, PloS one.

[5]  S. Black,et al.  Understanding 2H/1H systematics of leaf wax n-alkanes in coastal plants at Stiffkey saltmarsh, Norfolk, UK , 2014 .

[6]  B. Hoffmann,et al.  Leaf water deuterium enrichment shapes leaf wax n-alkane δD values of angiosperm plants II: Observational evidence and global implications , 2013 .

[7]  E. Schefuß,et al.  Leaf water deuterium enrichment shapes leaf wax n-alkane δD values of angiosperm plants I: Experimental evidence and mechanistic insights , 2013 .

[8]  A. Granier,et al.  The oxygen isotope enrichment of leaf-exported assimilates – does it always reflect lamina leaf water enrichment? , 2013, The New phytologist.

[9]  Patrick L. Griffin,et al.  Tracing H isotope effects in the dynamic metabolic network using multi-nuclear (1H, 2H and 13C) solid state NMR and GC–MS , 2013 .

[10]  J. Ehleringer,et al.  Leaf-wax n-alkanes record the plant–water environment at leaf flush , 2013, Proceedings of the National Academy of Sciences.

[11]  T. Dawson,et al.  Molecular Paleohydrology: Interpreting the Hydrogen-Isotopic Composition of Lipid Biomarkers from Photosynthesizing Organisms , 2012 .

[12]  Liang Xiaoxia,et al.  Anatomical Characteristics of C4 and C 3 Photosynthetic-pathway Poaceae Plants in Hainan: Anatomical Characteristics of C4 and C 3 Photosynthetic-pathway Poaceae Plants in Hainan , 2011 .

[13]  G. Farquhar,et al.  Temperature effect on leaf water deuterium enrichment and isotopic fractionation during leaf lipid biosynthesis: results from controlled growth of C3 and C4 land plants. , 2011, Phytochemistry.

[14]  B. Helliker,et al.  Hydrogen isotope ratios of leaf wax n-alkanes in grasses are insensitive to transpiration , 2011 .

[15]  G. Gleixner,et al.  Leaf wax n-alkane δD values of field-grown barley reflect leaf water δD values at the time of leaf formation , 2010 .

[16]  G. Farquhar,et al.  Biosynthetic origin of the saw-toothed profile in delta(13)C and delta(2)H of n-alkanes and systematic isotopic differences between n-, iso- and anteiso-alkanes in leaf waxes of land plants. , 2010, Phytochemistry.

[17]  A. Sessions,et al.  Large D/H variations in bacterial lipids reflect central metabolic pathways , 2009, Proceedings of the National Academy of Sciences.

[18]  S. Le Feunteun,et al.  Investigation of Fatty Acid Elongation and Desaturation Steps in Fusarium lateritium by Quantitative Two-dimensional Deuterium NMR Spectroscopy in Chiral Oriented Media , 2009, Journal of Biological Chemistry.

[19]  A. Marchetti,et al.  Hydrogen isotope fractionation in freshwater and marine algae: II. Temperature and nitrogen limited growth rate effects , 2009 .

[20]  G. Farquhar,et al.  Biosynthetic and environmental effects on the stable carbon isotopic compositions of anteiso- (3-methyl) and iso- (2-methyl) alkanes in tobacco leaves. , 2008, Phytochemistry.

[21]  Hong Yang,et al.  Multiple controls for the variability of hydrogen isotopic compositions in higher plant n‐alkanes from modern ecosystems , 2008 .

[22]  G. Farquhar,et al.  An innovative molybdenum column liner for oxygen and hydrogen stable isotope analysis by pyrolysis. , 2008, Rapid communications in mass spectrometry : RCM.

[23]  F. Ayadi,et al.  Non-equivalence of Hydrogen Transfer from Glucose to the pro-R and pro-S Methylene Positions of Ethanol during Fermentation by Leuconostoc mesenteroides Quantified by 2H NMR at Natural Abundance* , 2008, Journal of Biological Chemistry.

[24]  J. Šantrůček,et al.  Spatial Variation of Deuterium Enrichment in Bulk Water of Snowgum Leaves1[OA] , 2006, Plant Physiology.

[25]  Graham D. Farquhar,et al.  Heavy Water Fractionation during Transpiration1 , 2006, Plant Physiology.

[26]  Hong Yang,et al.  Hydrogen isotopic compositions of n-alkanes from terrestrial plants correlate with their ecological life forms , 2006, Oecologia.

[27]  A. Sessions.  Seasonal changes in D/H fractionation accompanying lipid biosynthesis in Spartina alterniflora , 2006 .

[28]  D. G. Hildebrand.  Plant Biochemistry.An Update and Translation of the German Third Edition.ByHans‐Walter Heldtin cooperation with, Fiona Heldt.Amsterdam and Burlington (Massachusetts): Elsevier Academic Press.$79.95. xxvi + 630 p; ill.; index. ISBN: 0–12–088391–0. 2005. , 2006 .

[29]  K. Freeman,et al.  Influence of physiology and climate on δD of leaf wax n-alkanes from C3 and C4 grasses , 2006 .

[30]  W. Majeran,et al.  Functional Differentiation of Bundle Sheath and Mesophyll Maize Chloroplasts Determined by Comparative Proteomicsw⃞ , 2005, The Plant Cell Online.

[31]  R. Schneider,et al.  Climatic controls on central African hydrology during the past 20,000 years , 2005, Nature.

[32]  Tsuyoshi Endo,et al.  Cyclic electron flow around photosystem I is essential for photosynthesis , 2004, Nature.

[33]  H. Naraoka,et al.  Hydrogen and carbon isotopic fractionations of lipid biosynthesis among terrestrial (C3, C4 and CAM) and aquatic plants. , 2004, Phytochemistry.

[34]  G. Farquhar,et al.  Evaluation of models of leaf water 18O enrichment using measurements of spatial patterns of vein xylem water, leaf water and dry matter in maize leaves , 2003 .

[35]  G. Farquhar,et al.  On the progressive enrichment of the oxygen isotopic composition of water along a leaf. , 2003, Plant, cell & environment.

[36]  G. Farquhar,et al.  Diurnal variation in the stable isotope composition of water and dry matter in fruiting Lupinus angustifolius under field conditions , 2002 .

[37]  Maryvonne L. Martin,et al.  Hydrogen isotopic profile in the characterization of sugars. Influence of the metabolic pathway. , 2002, Journal of agricultural and food chemistry.

[38]  R. Robins,et al.  Natural Deuterium Distribution in Long‐Chain Fatty Acids Is Nonstatistical: A Site‐Specific Study by Quantitative 2H NMR Spectroscopy , 2001, Chembiochem : a European journal of chemical biology.

[39]  I. Møller.  PLANT MITOCHONDRIA AND OXIDATIVE STRESS: Electron Transport, NADPH Turnover, and Metabolism of Reactive Oxygen Species. , 2001, Annual review of plant physiology and plant molecular biology.

[40]  J. Ehleringer,et al.  The mean depth of soil water uptake by two temperate grassland species over time subjected to mild soil water deficit and competitive association , 2001, Plant and Soil.

[41]  W. Eisenreich,et al.  Deoxyxylulose phosphate pathway to terpenoids. , 2001, Trends in plant science.

[42]  J. Ohlrogge,et al.  Understanding in vivo carbon precursor supply for fatty acid synthesis in leaf tissue. , 2000, The Plant journal : for cell and molecular biology.

[43]  S. White,et al.  Structure and mechanism of proton‐translocating transhydrogenase , 1999, FEBS letters.

[44]  A. Schimmelmann,et al.  Fractionation of hydrogen isotopes in lipid biosynthesis , 1999 .

[45]  T. Sharkey,et al.  Intramolecular deuterium distributions reveal disequilibrium of chloroplast phosphoglucose isomerase , 1999 .

[46]  R. Grimley,et al.  The involvement of NADP(H) binding and release in energy transduction by proton-translocating nicotinamide nucleotide transhydrogenase from Escherichia coli. , 1995, Biochimica et biophysica acta.

[47]  D. Yakir.  Variations in the natural abundance of oxygen‐18 and deuterium in plant carbohydrates , 1992 .

[48]  S. Suda,et al.  Extremely Low D/H Ratios of Photoproduced Hydrogen by Cyanobacteria , 1991 .

[49]  B. N. Smith,et al.  Isotopic evidence for mesophyll reduction inZea mays, an NADP-Malic enzyme plant , 1991, Die Naturwissenschaften.

[50]  W. Cleland,et al.  Use of intermediate partitioning to calculate intrinsic isotope effects for the reaction catalyzed by malic enzyme. , 1985, Biochemistry.

[51]  K. Hanson.  Stereochemical determination of carbon partitioning between photosynthesis and photorespiration in C3 plants: use of (3R)-D-[3-3H1, 3-14C]glyceric acid. , 1984, Archives of biochemistry and biophysics.

[52]  P. Hattersley.  Characterization of C4 Type Leaf Anatomy in Grasses (Poaceae). Mesophyll: Bundle Sheath Area Ratios , 1984 .

[53]  G. Edwards,et al.  C3, C4: Mechanisms and Cellular and Environmental Regulation of Photosynthesis , 1983 .

[54]  W. Cleland,et al.  Use of multiple isotope effects to determine enzyme mechanisms and intrinsic isotope effects. Malic enzyme and glucose-6-phosphate dehydrogenase. , 1982, Biochemistry.

[55]  B. Sedgwick,et al.  The biosynthesis of long-chain fatty acids. Stereochemical differentiation in the enzymic incorporation of chiral acetates. , 1977, European journal of biochemistry.

[56]  D. Keister,et al.  Pyridine nucleotide transhydrogenase from spinach. I. Purification and properties. , 1960, The Journal of biological chemistry.

[57]  D. Keister,et al.  Pyridine nucleotide transhydrogenasè from spinach , 1959 .

[58]  G. Edwards,et al.  Chapter 4 C4 Photosynthesis: Kranz Forms and Single-Cell C4 in Terrestrial Plants , 2010 .

[59]  By W. Dansga,et al.  Stable isotopes in precipitation , 2010 .

[60]  Youping Zhou.  Carbon, oxygen and hydrogen isotope compositions of plant material : insights from controlled growth experiments and modelling , 2005 .

[61]  W. Eisenreich,et al.  Systematics of 2H patterns in natural compounds and its importance for the elucidation of biosynthetic pathways , 2004, Phytochemistry Reviews.

[62]  W. Eisenreich,et al.  Quantitative assessment of crosstalk between the two isoprenoid biosynthesis pathways in plants by NMR spectroscopy , 2004, Phytochemistry Reviews.

[63]  R. Robins,et al.  Measurement of 2H distribution in natural products by quantitative 2H NMR: An approach to understanding metabolism and enzyme mechanism? , 2004, Phytochemistry Reviews.

[64]  J. Hayes.  Fractionation of Carbon and Hydrogen Isotopes in Biosynthetic Processes , 2001 .

[65]  R. Furbank,et al.  The CO 2 Concentrating Function of C 4 Photosynthesis , 1990 .

[66]  J. Ehleringer,et al.  Carbon Isotope Discrimination and Photosynthesis , 1989 .

[67]  H. Ziegler.  Hydrogen Isotope Fractionation in Plant Tissues , 1989 .

[68]  G. B. Allison,et al.  The distribution of deuterium and 18O in dry soils: 1. Theory , 1983 .