Plant Methanol Emission at the Interface of the Photosynthetic C1 Pathway, Leaf Water Status, and Growth
Suman Som1, Luiza Gallo1,3, Tomas Domigues2, Edward Baidoo3, Aymerick Eudes,4 and Kolby J. Jardine1* (firstname.lastname@example.org)
1Lawrence Berkeley National Laboratory; 2 Joint BioEnergy Institute; and 3University of São Paulo
The Poplar Esterified Cell Wall Transformations and metabolic INtegration (PECTIN) project aims to study the metabolism of cell wall ester modifications and volatile intermediates, and their role in central physiological processes in the emerging biofuel species California poplar (Populus trichocarpa). A key goal of this research is to evaluate abiotic stress responses in plants with modified expression patterns of key genes involved in cell wall metabolism with altered amounts of methyl and acetyl groups present on cell walls. These genetic modifications will be evaluated for potential impacts on plant hydraulics, physiology, and stress responses. Understanding and manipulating the metabolism of cell wall modifications will not only provide important knowledge on the physiology and ecology of plants but will also allow the generation of engineered bioenergy crops such as poplar for sustainable production of biofuels and bioproducts, addressing BER’s goal of developing renewable bioenergy resources.
While previously considered a byproduct of growth, the release of methanol from methylated pectin in primary cell walls of plants dramatically alters their elasticity, a critical parameter controlling initiation and propagation of tissue morphogenesis and growth. Given the large reservoir of methylated pectin in leaves and other plant tissues associated with the primary cell wall, leaf methanol emissions are assumed to derive from this large, stored carbon reserve with no apparent direct connection to photosynthesis. Plant methanol emissions are assumed to derive from light-independent temperature-driven growth process, and therefore assumed to have no direct metabolic connection with photosynthesis. In this study, researchers use 13CO2-labeling to demonstrate that methyl esters on primary cell walls of leaves of C3 plants are directly produced from photosynthetically linked C1 metabolism, not related to photorespiration within minutes of light exposure through a proposed series of intracellular and extracellular connected pathways. This occurs in parallel with methanol release from the primary cell wall during temperature-stimulated growth processes, which are constrained by midday leaf water stress. Upon illumination of individual leaves and branches, 13C/12C-methanol emission ratios continuously increased during photosynthesis under an elevated 13CO2 atmosphere (500-1000 ppm). Dynamic branch 13CO2 labeling of photosynthesis lasting 2.5 days showed daily increases of 13C/12C-methanol emission ratios peaking at the end of the light period with 13C-methanol emissions gradually increasing at the expense of 12C-methanol, reaching 13C/12C-methanol up to 50%. In the dark, branch 13C/12C-methanol emission ratios remained constant despite strong night-time 13C-methanol emission dynamics that mimicked 12C-methanol emissions. At midnight, when the leaf water potential recovered (-0.2 +/- 0.1 MPa) from midday values (-1.0 +/- 0.1 MPa), branch emissions of both 12C-methanol and 13C-methanol increased steadily throughout the night, despite leaf temperature and transpiration slowly decreasing. The results are consistent with a distinction between biosynthesis and incorporation of photosynthetically derived C1 carbon into leaf primary cell walls and methanol production during growth. An accelerated growth phase occurs between midnight and midday, where growth and methanol increased positively with temperature, and a decelerated growth phase between midday and midnight, where growth and methanol emissions decreased with temperature, constrained by leaf water stress. The results provide evidence for a rapid and direct connection between photosynthesis and photorespiration-independent C1 metabolism; a temperature independent hydraulic control over methanol emissions and growth rates at night; and a temperature stimulated (morning), followed by inhibited (afternoon) methanol emission and growth during the day.
The observations are consistent with a biochemical model integrating CO2 fixation by the Calvin cycle with the C1 pathway involving: 1) Photosynthesis, 2) The phosphorylated serine pathway, which synthesizes the donor methyl group of methionine in the chloroplast 3) Export of methionine to the cytosol followed by activation to S-adenosylmethionine (AdoMet), which is imported into many organelles and used to transfer methyl groups to polysaccharides, nucleic acids, proteins, lipids, and secondary metabolites, 4) Methyl esterification of new pectin monomers in the Golgi with AdoMet, 5) Transport, export, and incorporation of the newly synthesized highly methyl esterified pectin into the growing primary cell wall, and 6) Methanol production during growth associated with pectin demethylation during the day and night. These observations are consistent with the emerging view of methanol emissions as a chemical signal of leaf growth primarily occurring at night and early morning, due to reduced leaf water stress. The results are also consistent with a critical role of methanol production linked to diurnal changes in primary cell wall elasticity associated with pectin demethylation and growth. Although the rise in atmospheric CO2 inhibits major metabolic pathways like photorespiration and the isoprenoid pathway, the photorespiration-independent photosynthetic C1 pathway may accelerate. Thus, photosynthetic production of AdoMet may play a critical, yet poorly understood role in enhancing growth rates of plants and net primary productivity of ecosystems during terrestrial CO2 fertilization.
Jardine, K. J., et al. 2022. “Cell Wall Ester Modifications and Volatile Emission Signatures of Plant Response to Abiotic Stress.” Plant, Cell & Environment 45(12), 3429–44.
Dewhirst, R., J. Mortimer, K. Jardine. 2020. “Do Cell Wall Esters Facilitate Forest Response to Climate?” Trends in Plant Science 25(8), 729–32. DOI: https:/doi.org/10.1016/j.tplants.2020.05.01.1.
Jardine et al. In preparation. “Plant Methanol Emission at the Interface of the Photosynthetic C1 Pathway and Diurnal Patterns in Leaf Water Status and Growth.”
This research was supported by the DOE Office of Science, Office of Biological and Environmental Research (BER), Early Career Research Project (ECRP) grant no. FP00007421 and the DOE Joint BioEnergy Institute (http://www.jbei.org) supported by contract DE-AC02-05CH11231