Updating the dual C and O isotope—Gas‐exchange model: A concept to understand plant responses to the environment and its implications for tree rings

Abstract

The combined study of carbon (C) and oxygen (O) isotopes in plant organic matter has emerged as a powerful tool for understanding plant functional responses to environmental change. The approach relies on established relationships between leaf gas exchange and isotopic fractionation to derive a series of model scenarios that can be used to infer changes in photosynthetic assimilation and stomatal conductance driven by changes in environmental parameters (CO2, water availability, air humidity, temperature, nutrients). We review the mechanistic basis for a conceptual model, in light of recently published research, and discuss where isotopic observations do not match our current understanding of plant physiological response to the environment. We demonstrate that (1) the model was applied successfully in many, but not all studies; (2) although originally conceived for leaf isotopes, the model has been applied extensively to tree‐ring isotopes in the context of tree physiology and dendrochronology. Where isotopic observations deviate from physiologically plausible conclusions, this mismatch between gas exchange and isotope response provides valuable insights into underlying physiological processes. Overall, we found that isotope responses can be grouped into situations of increasing resource limitation versus higher resource availability. The dual‐isotope model helps to interpret plant responses to a multitude of environmental factors.

Quantifying isotope parameters associated with carbonyl‐water oxygen exchange during sucrose translocation in tree phloem

“…Such investigations should also expand beyond our current focus on the leaf‐to‐petiole route to encompass sucrose translocation along tree stems, so as to ensure a thorough characterization of the fractionation processes at the phloem level. Undoubtedly, this new knowledge will be instrumental in strengthening the existing tree‐ring isotope model, the mechanistic robustness of which, – as highlighted in several recent studies, – underpins a variety of important applications ranging from interpretation and prediction of inter‐ and intra‐annual δ 18 O cel dynamics in various contexts (Zeng et al ., 2017; Belmecheri et al ., 2018; Xu et al ., 2022; Martínez‐Sancho et al ., 2023), to δ 18 O cel ‐based reconstructions of leaf‐level ecophysiological variables such as stomatal conductance (Lin et al ., 2022; Siegwolf et al ., 2023) and leaf temperature (Gessler et al ., 2014; Song et al ., 2022).…”

“…The stable oxygen isotope composition of tree ring α‐cellulose (δ 18 O cel ) has become a popular tool for reconstructing environmental (Miller et al ., 2006; Brienen et al ., 2012; Voelker et al ., 2014; Belmecheri et al ., 2018; Xu et al ., 2019; Goodwin et al ., 2022) and ecophysiological (Helliker & Richter, 2008; Song et al ., 2011; Guerrieri et al ., 2019; Ulrich et al ., 2019; Siegwolf et al ., 2023) conditions during tree growth. As widely appreciated, interpreting δ 18 O cel variations in many contexts requires a solid, mechanistic understanding of the physiological and biochemical processes underpinning δ 18 O cel (Sternberg, 2009; Lin et al ., 2022).…”

Half of the 18O enrichment of leaf sucrose is conserved in leaf cellulose of a C3 grass across atmospheric humidity and CO2 levels

“…Here defined as the δ 18 O of nutrient solution (-9.7 ± 0.2‰ SD), which was slightly depleted relative to the δ 18 O of water extracted from the leaf growth-and-differentiation zone (see The average biochemical fractionation between carbonyl oxygen and water 26.7‰, according to the temperature dependence of ε bio for cellulose synthesis in aquatic plants as reported by Sternberg & Ellsworth (2011), taken as constant for all treatments and closely similar to the constant ε bio = 27‰ used in most studies (Barbour, 2007) conductance among plant species and genotypes in the same environment (e.g., Baca Cabrera et al, 2021;Barbour et al, 2000a;Lin et al, 2022;Scheidegger et al, 2000;Siegwolf et al, 2023). These relationships are grounded in the fact that virtually all of the oxygen in cellulose originates from water (DeNiro & Epstein, 1979;Liu et al, 2016) and evaporative conditions lead to an 18 O enrichment of leaf water above source water (Δ 18 O LW , Table 1) (Cernusak et al, 2016(Cernusak et al, , 2022Dongmann et al, 1974;Farquhar et al, 2007;Flanagan et al, 1991;Roden & Ehleringer, 1999).…”

Seasonal and Species‐Level Water‐Use Strategies and Groundwater Dependence in Dryland Riparian Woodlands During Extreme Drought

“…The less coordinated response of earlywood δ 18 O and Δ 13 C res to changes in atmospheric demand (Figure 3) could also be the result of post-photosynthetic processes or seasonal differences in source water. In a recent review, Siegwolf et al (2023) note the potential for reallocation of stored carbohydrates to contribute to a dampening effect on 13 C that could obscure dual isotope (δ 18 O and Δ 13 C) interpretations in earlywood. In addition, the early season use of shallow soil moisture, which is more isotopically variable, may have overshadowed the influence of leaf water enrichment and resulted in a partial decoupling of tree-ring δ 18 O and stomatal conductance.…”