In the world-wide leaf economics spectrum (Wright et al. 2004, Nature) variability of three key traits: photosynthesis rate, leaf nitrogen content, and leaf dry mass per area of 2500 species (from study sites with highly variable mean annual humidity and temperature) fall along the single axis of this three-trait space. However, the striking question has been what actually is the parameter that drives LES relationships.

Meta-analysis (lead by Dr. Yusuke Onoda from Kyoto University) confirms the speculations that this variation is caused by variable mesophyll conductance (e.g. CO₂ diffusion efficiency from sub-stomatal cavities to chloroplasts) and different life strategies in terms of nitrogen investment into structural cell wall material rather than photosynthetic biochemistry (see the figure below).

Illustration of structure-function relationships of two species with contrasting life strategies. Left: temperate decidous pioneer species Populus tremula and right side: evergreen Cycas taitungensis. Mesophyll tissue, epidermis, scleroids and cuticle are shown. Populus tremula leaf is positioned to fast return end of LES.  Populus invests  proportionally less resources into protective cells (scleroids, cuticle, thick mesophyll  cell walls) rather it invests into building 2 layers of thick physiologically active palisade tissue this in turn brings to high photosynthesis and fast growth rate while Cycads have proportionally more C and N invested into protective structural cells and therefore lower photosynthesis and slower growth rate. However, in longer perspective Cycas has longer leaf life span and slower energy return. That is, more nitrogen invested into cell walls means more durable and tougher leaves. On the other hand thick mesophyll cell walls represent longer liquid phase distance through cell walls (low mesophyll conductance) into the chloroplasts and therefore less efficient photosynthesis

Citation: Onoda, Y., Wright, I. J., Evans, J. R., Hikosaka, K., Kitajima, K., Niinemets, Ü., Poorter, H., Tosens, T. & Westoby, M. (2017). Physiological and structural tradeoffs underlying the leaf economics spectrum. New Phytologist, 214(4), 1447-1463. (link to full text)

Check also out a commentary titled “Peeking beneath the hood of the leaf economics spectrum” by by Reich and Flores-Moreno (link to full text) who emphasize the significance of this study: “What is most novel about their study is the bringing together of considerable data on rarely measured leaf traits, assessing both chemical (e.g. nitrogen (N) allocation) and diffusive (mesophyll conductance) constraints at the same time, and identifying a key role for cell-wall thickness in both of these.“

Abstract:

• The leaf economics spectrum (LES) represents a suite of intercorrelated leaf traits concerning construction costs per unit leaf area, nutrient concentrations, and rates of carbon fixation and tissue turnover. Although broad trade-offs among leaf structural and physiological traits have been demonstrated, we still do not have a comprehensive view of the fundamental constraints underlying the LES trade-offs.
• Here, we investigated physiological and structural mechanisms underpinning the LES by analysing a novel data compilation incorporating rarely considered traits such as the dry mass fraction in cell walls, nitrogen allocation, mesophyll CO₂ diffusion and associated anatomical traits for hundreds of species covering major growth forms.
• The analysis demonstrates that cell wall constituents are major components of leaf dry mass (18–70%), especially in leaves with high leaf mass per unit area (LMA) and long lifespan. A greater fraction of leaf mass in cell walls is typically associated with a lower fraction of leaf nitrogen (N) invested in photosynthetic proteins; and lower within-leaf CO₂ diffusion rates, as a result of thicker mesophyll cell walls.
• The costs associated with greater investments in cell walls underpin the LES: long leaf lifespans are achieved via higher LMA and in turn by higher cell wall mass fraction, but this inevitably reduces the efficiency of photosynthesis.