Hydrogen isotope fractionation in carbohydrates of leaves and xylem tissues follows distinct phylogenetic patterns: a common garden experiment with 73 tree and shrub species

Abstract

Recent methodological advancements in determining the nonexchangeable hydrogen isotopic composition (δ 2 H ne ) of plant carbohydrates make it possible to disentangle the drivers of hydrogen isotope ( 2 H) fractionation processes in plants.Here, we investigated the influence of phylogeny on the δ 2 H ne of twig xylem cellulose and xylem water, as well as leaf sugars and leaf water, across 73 Northern Hemisphere tree and shrub species growing in a common garden.2 H fractionation in plant carbohydrates followed distinct phylogenetic patterns, with phylogeny reflected more in the δ 2 H ne of leaf sugars than in that of twig xylem cellulose. Phylogeny had no detectable influence on the δ 2 H ne of twig or leaf water, showing that biochemistry, not isotopic differences in plant water, caused the observed phylogenetic pattern in carbohydrates. Angiosperms were more 2 H-enriched than gymnosperms, but substantial δ 2 H ne variations also occurred at the order, family, and species levels within both clades. Differences in the strength of the phylogenetic signals in δ 2 H ne of leaf sugars and twig xylem cellulose suggest that the original phylogenetic signal of autotrophic processes was altered by subsequent species-specific metabolism.Our results will help improve 2 H fractionation models for plant carbohydrates and have important consequences for dendrochronological and ecophysiological studies.

Different responses of oxygen and hydrogen isotopes in leaf and tree-ring organic matter to lethal soil drought

“…The drought-induced variation in the 2 H-enrichment in OM among individual tree species might be partially explained by differences in growth strategies and physiological responses between angiosperm and gymnosperm species ( Schuler et al. 2023 ).…”

Biochemical and biophysical drivers of the hydrogen isotopic composition of carbohydrates and acetogenic lipids

“…It should also be considered that we only worked with tobacco plants in this study. Yet, a recent study demonstrated that δ 2 H values of carbohydrates across a large set of tree and shrub species show distinct phylogenetic differences ( 40 ). Consequently, cellulose isotope models may include order-, family-, or genera-specific 2 H-fractionation factors if comparisons are made across different species.…”

“…In the chloroplast, NADPH can be produced during the photosynthetic photolysis reaction of water by the enzyme (ferredoxin-NADP + reductase, EC 1.18.1.2). The hydride transferred to NADPH is 2 H-depleted and considered responsible for the large 2 H-fractionation observed during autotrophic biosynthesis of plant organic matter ( 7 , 14 , 32 , 39 , 40 ). NADPH can also be produced by the tricarboxylic acid cycle (cytosolic NADP-dependent isocitrate dehydrogenase involved in ammonia assimilation, EC 1.1.1.42), the malate valve [responsible for redox homeostasis, oxalacetate as precursor of aspartate and other amino acids (AA)], and the oxidative pentose phosphate pathway [glucose-6-phosphate dehydrogenase (EC 1.1.1.49) and 6-phosphogluconate dehydrogenase (EC 1.1.1.44)].…”

“…Because of the complexity of all the processes causing 2 H-fractionation in plants, we compartmentalize them into two apparent isotope fractionation factors following previous publications on the topic ( 6 , 14 , 15 , 17 , 40 , 50 ):…”