Cost–benefit analysis of mesophyll conductance: diversities of anatomical, biochemical and environmental determinants

Abstract

Background Plants invest photosynthates in construction and maintenance of their structures and functions. Such investments are considered costs. These costs are recovered by CO2 assimilation rate (A) in the leaves and thus A is regarded as the immediate, short-term benefit. In photosynthesising leaves, CO2 diffusion from the air to the carboxylation site is hindered by several structural and biochemical barriers. CO2 diffusion from the intercellular air space to the chloroplast stroma is obstructed by the mesophyll resistance. The inverses is the mesophyll conductance (gm). Whether various plants realize an optimal gm, and how much investments are needed for relevant gm, remain unsolved. Scope This review examines relationships among leaf construction costs (CC), leaf maintenance costs (MC) and gm in various plants under diverse growth conditions. Through a literature survey, we demonstrate a strong linear relationship between leaf mass per area (LMA) and leaf CC. The overall correlation of CC versus gm across plant phylogenetic groups is weak, but significant trends are evident within specific groups and/or environments. Investment in CC is necessary for increase in LMA and mesophyll cell surface area (Smes). This allows the leaf to accommodate more chloroplasts, thus increasing A. However, increases in LMA and/or Smes often accompany other changes, such as cell wall thickening, which diminishes gm. Such factors that make the correlations of CC-gm elusive are identified. Conclusions For evaluation of contribution of gm to recover CC, leaf life-span is the key factor. The estimation of MC in relation to gm, especially in terms of costs required to regulate aquaporins, could be essential for efficient control of gm over the short-term. Over the long-term, costs are mainly reflected in CC, while benefits also include ultimate fitness attributes in terms of integrated carbon gain over the life of a leaf, plant survival and reproductive output.

Leaf anatomy does not explain the large variability of mesophyll conductance across C3 crop species

“…Further bicorrelation analysis between g m_ fluo and leaf anatomical traits showed that no leaf anatomical traits were correlated with g m across species except chloroplast thickness (Figure 4). Although several studies claimed that CO 2 diffusion resistance in stroma could be low because its high pH and Rubisco concentrations could facilitate CO 2 diffusion (Mizokami et al, 2022;Terashima et al, 2011), here I observed that g m was negatively correlated with stroma thickness, similar to other studies (Liu et al, 2021;Tosens, Niinemets, Vislap, et al, 2012;Veromann-J ürgenson et al, 2020).…”

“…As discussed in many recent studies (Evans, 2021; Evans et al., 2009; Mizokami et al., 2022), the CO 2 diffusion conductance can be potentially enhanced by many other factors, such as specific protein channels in membranes, fast conversion of CO 2 to bicarbonate catalyzed by CAs in the cytosol and stroma, and concentrated Rubisco in the stroma. Therefore, the term that accounts for the effect of facilitation of CO 2 transport in each component can be expressed as follows:where ε i is defined as the enhancement due to facilitation processes in that component (Evans et al., 2009); ε was rarely considered in previous studies because of difficulties in the estimation of those values.…”

CO2‐induced chloroplast movement in one cell‐layer moss leaves

“…Although it is difficult to directly measure CO 2 concentrations at the cellular level, microscopic measurements of chlorophyll fluorescence can inform us on the extent of CO 2 heterogeneity in plant cells. An evaluation of the costs and benefits of CO 2 ‐relocation will require analyses of factors such as cytoskeletal energetics (Hill & Kirschner, 1982; Leighton & Sivak, 2022; Okamoto & Lightfoot, 1992) and the cellular CO 2 conductance (Mizokami et al, 2022).…”

CO 2 -induced chloroplast movement in one cell-layer moss leaves

“…This situation would result in the conditional CO 2 heterogeneity, and chloroplasts would show the CO 2 -tactic movements towards the water-free surfaces, which would be effective not only in increasing the CO 2 supply to the chloroplasts but also in avoiding photoinhibition of the chloroplasts. The cost-benefit analysis of CO 2 -relocation will require the discussion in context of the cytoskeletal energetics (Hill & Kirschner, 1982;Okamoto & Lightfoot, 1992;Leighton & Sivak, 2022) and evaluation of the cellular CO 2 conductance (Mizokami, et al, 2022).…”