Coordination of photosynthetic traits across soil and climate gradients

Authors: WESTERBAND, ANDREA - Macquarie University; WRIGHT, IAN - Macquarie University; MAIRE, VINCENT - University Of Quebec; PAILLASSA, JENNIFER - University Of Quebec; PRENTICE, IAIN - Macquarie University; ATKIN, OWEN - The Australian National University; BLOOMFIELD, KEITH - Imperial College; CERNUSAK, LUCAS - James Cook University; DONG, NING - Macquarie University; Gleason, Sean; PEREIRA, CAIO - Massachusetts Institute Of Technology; LAMBERS, HANS - University Of Western Australia; LEISHMAN, MICHELLE - Macquarie University; MALHI, YADVINDER - University Of Oxford; NOLAN, RACHAEL - Western Sydney University

Submitted to: Global Change Biology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/23/2022
Publication Date: 10/24/2022
Citation: Westerband, A.C., Wright, I.J., Maire, V., Paillassa, J., Prentice, I.C., Atkin, O., Bloomfield, K.J., Cernusak, L., Dong, N., Gleason, S.M., Pereira, C.G., Lambers, H., Leishman, M.R., Malhi, Y., Nolan, R.H. 2022. Coordination of photosynthetic traits across soil and climate gradients. Global Change Biology. 29(3):856-873. https://doi.org/10.1111/gcb.16501.
DOI: https://doi.org/10.1111/gcb.16501

Interpretive Summary: Nitrogen and water are key resources involved in plant growth. It is expected that plants will invest carbon and energy in acquiring these resources relative to the availability of these resources. For example, if nitrogen is plentiful in soils but water is not (i.e., fertile soils in arid habits), we should expect plants to invest more carbon and energy towards acquiring water than nitrogen. "Least-cost" theory posits that water and nitrogen should therefore be "co-optimized" over evolutionary timescales such that investments in photosynthetic enzymes (nitrogen-rich) and water use (water evaporation through plant stomata) should be predictable from the availability of nitrogen and water in a plant's habitat. We also extend this theory to phosphorous because nitrogen and phosphorous availability are often correlated across soils and their ratio in photosynthetic enzymes are fixed. A broad survey of Australian vegetation provided strong support for these hypotheses.

Technical Abstract: • Nitrogen (photosynthetic enzymes) and water (transpiration) are key resources involved in photosynthesis. “Least-cost theory” posits that plants should co-optimise the use of these resources over ecological-evolutionary timescales. Site climate and soil properties strongly determine the cost of acquiring these resources, hence their coordination in photosynthesis. In this study we tested new predictions from least-cost theory regarding the dependency of photosynthesis on climate and soil properties. • Using the largest photosynthetic trait dataset for Australia to date (69 sites and 536 species), we tested the hypothesis that plants exhibit higher leaf nitrogen per unit area (Narea) and carboxylation capacity (Vcmax), but lower water loss (via stomatal conductance, gsw) on sites with low temperature, low precipitation, or high soil fertility (high total soil phosphorus or high pH). We further investigated variation in these traits as well as the ratio of intercellular to atmospheric CO2 (Ci:Ca) over soil and climate gradients. • Greater concentrations of total soil phosphorus (P), Australia’s key limiting nutrient, were associated with higher leaf Narea and higher Vcmax, and lower gsw and lower Ci:Ca. Similar patterns were detected on relatively arid and cold sites, supporting our hypothesis. Contrary to our expectation, soil pH, which influences fertility, exerted relatively weak control on the relationship between leaf Narea (and Vcmax) and gsw and on Ci:Ca. Despite the weak to negligible effect of pH on optimisation of gsw and leaf Narea, soil pH (along with P) strongly predicted variation in gsw, Vcmax, and leaf Narea, while Ci:Ca varied most strongly with annual precipitation. • Soils influenced the co-optimisation of photosynthetic traits as strongly as climate. Our findings highlight the importance of soil properties for photosynthesis, and the utility of least-cost theory for predicting photosynthetic performance at continental scale.