Intramolecular carbon isotope signals reflect metabolite allocation in plants

Wieloch, Thomas; Sharkey, Thomas David; Werner, Roland Anton; Schleucher, Jürgen; Rogers, ed., Alistair

doi:10.1093/jxb/erac028

Intramolecular carbon isotope signals reflect metabolite allocation in plants

Journal Article · Thu Jan 27 00:00:00 EST 2022 · Journal of Experimental Botany

DOI:https://doi.org/10.1093/jxb/erac028· OSTI ID:1863466

^[1]; ^[2]; Werner, Roland Anton ^[3]; Schleucher, Jürgen ^[1]; Rogers, ed., Alistair ^[4]

Department of Medical Biochemistry and Biophysics, Umeå University, 901 87 Umeå, Sweden
MSU-DOE Plant Research Laboratory, Plant Resilience Institute, and Department of Biochemistry and Molecular Biology, Michigan State University, East Lansing, MI 48824, USA
Department of Environmental Systems Science, ETH Zürich, Universitätstrasse 2, 8092 Zürich, Switzerland
Brookhaven National Laboratory, USA

Abstract

Stable isotopes at natural abundance are key tools to study physiological processes occurring outside the temporal scope of manipulation and monitoring experiments. Whole-molecule carbon isotope ratios (13C/12C) enable assessments of plant carbon uptake yet conceal information about carbon allocation. Here, we identify an intramolecular 13C/12C signal at tree-ring glucose C-5 and C-6 and develop experimentally testable theories on its origin. More specifically, we assess the potential of processes within C3 metabolism for signal introduction based (inter alia) on constraints on signal propagation posed by metabolic networks. We propose that the intramolecular signal reports carbon allocation into major metabolic pathways in actively photosynthesizing leaf cells including the anaplerotic, shikimate, and non-mevalonate pathway. We support our theoretical framework by linking it to previously reported whole-molecule 13C/12C increases in cellulose of ozone-treated Betula pendula and a highly significant relationship between the intramolecular signal and tropospheric ozone concentration. Our theory postulates a pronounced preference for leaf cytosolic triose-phosphate isomerase to catalyse the forward reaction in vivo (dihydroxyacetone phosphate to glyceraldehyde 3-phosphate). In conclusion, intramolecular 13C/12C analysis resolves information about carbon uptake and allocation enabling more comprehensive assessments of carbon metabolism than whole-molecule 13C/12C analysis.

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Research Organization:: Michigan State University, East Lansing, MI (United States)

Sponsoring Organization:: Kempe Foundations; Knut and Alice Wallenberg Foundation; Michigan AgBioResearch; Swedish Research Council; USDOE; USDOE Office of Science (SC)

Grant/Contract Number:: FG02-91ER20021

OSTI ID:: 1863466

Alternate ID(s):: OSTI ID: 1854034
OSTI ID: 1979502

Journal Information:: Journal of Experimental Botany, Journal Name: Journal of Experimental Botany Journal Issue: 8 Vol. 73; ISSN 0022-0957

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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54 ENVIRONMENTAL SCIENCES
58 GEOSCIENCES
59 BASIC BIOLOGICAL SCIENCES
carbon allocation
carbon stable isotopes
intramolecular isotope analysis
long time scales
ozone stress
primary carbon metabolism
triose-phosphate isomerase

Intramolecular carbon isotope signals reflect metabolite allocation in plants

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