Mesophyll diffusion conductance to CO2: An unappreciated central player in photosynthesis

doi:10.1016/j.plantsci.2012.05.009

Plant Science

Volumes 193–194, September 2012, Pages 70-84

https://doi.org/10.1016/j.plantsci.2012.05.009 Get rights and content

Abstract

Mesophyll diffusion conductance to CO₂ is a key photosynthetic trait that has been studied intensively in the past years. The intention of the present review is to update knowledge of g_m, and highlight the important unknown and controversial aspects that require future work. The photosynthetic limitation imposed by mesophyll conductance is large, and under certain conditions can be the most significant photosynthetic limitation. New evidence shows that anatomical traits, such as cell wall thickness and chloroplast distribution are amongst the stronger determinants of mesophyll conductance, although rapid variations in response to environmental changes might be regulated by other factors such as aquaporin conductance.

Gaps in knowledge that should be research priorities for the near future include: how different is mesophyll conductance among phylogenetically distant groups and how has it evolved? Can mesophyll conductance be uncoupled from regulation of the water path? What are the main drivers of mesophyll conductance? The need for mechanistic and phenomenological models of mesophyll conductance and its incorporation in process-based photosynthesis models is also highlighted.

Highlights

► The intention of the present review is to update the consensus knowledge on g_m. ► Gaps in knowledge and research priorities are indicated for the near future. ► In particular, how has g_m evolved among phylogenetically distant groups? ► Can g_m be uncoupled from the water path regulation? ► Mechanistic models of g_m incorpored in photosynthesis models are needed.

Introduction

Photosynthesis in plants has been considered for decades to be limited only by two factors: the velocity of diffusion of CO₂ through stomata and the capacity of photosynthetic machinery to convert light energy to biochemical energy and fix CO₂ into sugars. Diffusion is a passive physical process, but in plants can be regulated. According to Fick's law, diffusion depends on substance (e.g. CO₂) diffusivity, temperature, the nature (mainly viscosity) of the media in which diffusion occurs (e.g. water, air, etc.), and the distance of diffusion. The mesophyll pathway comprises a series of ‘physical barriers’ to CO₂ diffusion, including air, cell walls, lipid membranes and liquid cytoplasm and stroma. The ‘physical barriers’ differ in nature and size (i.e. ‘distance’) among leaves, and thus there is a large variation among leaves in diffusion conductance to CO₂ in the mesophyll (g_m).

Early studies already suggested that the diffusion of CO₂ from sub-stomatal cavities to the sites of carboxylation inside chloroplasts could limit photosynthesis (e.g., [1], [2], [3]). These early studies and most subsequent examinations of g_m are dependent on several methods for the estimation of g_m – including a method based on ¹³C-discrimination during photosynthesis[4], a method combining chlorophyll fluorescence and gas exchange measurements [5], [6] and model-based methods [6], [7], [8]. For details on methods for g_m estimation, the required precautions when using them and specific strategies of adjustment, see references [9], [10], [11]. The pioneering early studies [1], [2], [3] and a raft of subsequent studies have highlighted that g_m is the third major player in the process of photosynthesis, together with stomatal conductance and biochemical capacity.

The current understanding on g_m has been recently reviewed [12]. In addition, specific reviews on the mechanisms regulating g_m [13], and on the ecophysiological and ecological significance of g_m [14], [15], [16] have been published. These papers are recommended as the best introduction to the importance of g_m in plant physiology. As there has been rapid gain in understanding of g_m, the aims of the present paper are: (1) to update information accumulated after the recent reviews; (2) to discuss the most obscure/controversial aspects on g_m function and regulation, such as its response to CO₂, or how much it limits photosynthesis; and (3) to highlight the obvious gaps in knowledge on this subject and the future research needs.

Section snippets

How different is g_m among phylogenetically distant groups and how have mechanisms controlling g_m evolved?

The rate of diffusion conductance to CO₂ in the mesophyll (g_m) has now been estimated for more than 100 species, and it is now possible to search for phylogenetic/evolutionary patterns. The vast majority of estimates of g_m are for Spermatophytes [14] (angiosperms and gymnosperms), with only very few data for liverworts and hornworts [17]. Most surprisingly there are no measurements available for phylogenetically intermediate groups such as mosses, lycophytes, equisetophytes, or ferns. This

Changing the nature of the diffusing molecule: Carbonic anhydrases

CO₂ molecules passing from sub-stomatal cavities to chloroplasts diffuse through the gas-phase in leaf intercellular air spaces, and the liquid phase in cell walls, cytosol and chloroplast stroma and lipid phase in plasmalemma and chloroplast envelope membranes (Fig. 2). The rate of diffusion through the composite segments of the diffusion pathway depends on the effective thickness and diffusivity of each component section [16]. “Effective” denotes the circumstance that the diffusion path

Which environmental conditions affect g_m?

Mesophyll conductance to CO₂ responds to environmental factors either in the long term or rapidly, i.e. in minutes-hours [10]. Recent reviews have already highlighted the incidence of varying environmental conditions such as soil water availability, salinity, growth irradiance and temperature on g_m [12], [14]. In the recent years, the important contribution of g_m in limiting photosynthesis during drought and salinity has been emphasized, knowledge has improved for the effects of nutrient stress

Photosynthesis limitations in response to environmental variables

Once it was demonstrated and accepted by most of the scientific community that g_m is finite, and possibly dynamically regulated, it became important to quantify how much mesophyll diffusion limits photosynthesis. In the 1990s and beginning of this century, photosynthesis limitation by g_m was ignored – for simplicity and because of the difficulty to estimate g_m with methods available – despite the early warnings that g_m was finite, variable and limiting photosynthesis [3], [97]. Recently, a

Modeling and including g_m in photosynthesis models

Mesophyll diffusion of CO₂ must be taken into account in leaf gas exchange models, since considering an infinite g_m is not correct. The difficulty arises when deciding a value of g_m to be applied in each specific scenario, and as a function of how g_m varies in space and time. Currently, we are not able to incorporate g_m in models with a mechanistic basis due to the lack of sufficient knowledge on the mechanisms involved in the regulation of g_m. This being said, there have been several attempts

Co-regulation of g_m and stomatal conductance

The previous sections have demonstrated that g_m and g_s are very often co-regulated, although not under all instances. Some degree of co-regulation has been suggested between g_m and plant hydraulics. Water vapor and CO₂ share at least a part of their pathways in leaves. Both gases are exchanged with the atmosphere through stomata and cross the aerial sub-stomatal cavity. Additionally, after leaving the leaf xylem, liquid water not only moves along apoplastic pathways but also (partly mediated by

Concluding remarks and future prospects

The share of overall photosynthetic limitation by mesophyll conductance is large and can be the most significant factor limiting photosynthesis under certain conditions and certain plant functional types. This statement is backed up by ample evidence, and we argue that g_m should be included in any study analyzing limitations to photosynthesis, as well as in models for predicting rates of photosynthesis.

Significant progress has recently been made in quantitatively linking g_m to foliage

Acknowledgements

We thank Ichiro Terashima and Yusuke Mizokami for insightful suggestions on the MS and editor plus five additional anonymous reviewers for numerous useful improvements. The study was financially supported by the Estonian Ministry of Science and Education (grant SF1090065s07), the Spanish Ministry of Science and Innovation through projects BFU2008-01072 (MEFORE), AGL2009-11310/AGR, BFU2011-23294 (MECOME) and CGL2009-13079-C02-01 (PALEOISOTREE), and the European Commission through European

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ReviewMesophyll diffusion conductance to CO2: An unappreciated central player in photosynthesis

Abstract

Highlights

Introduction

Section snippets

How different is gm among phylogenetically distant groups and how have mechanisms controlling gm evolved?

Changing the nature of the diffusing molecule: Carbonic anhydrases

Which environmental conditions affect gm?

Photosynthesis limitations in response to environmental variables

Modeling and including gm in photosynthesis models

Co-regulation of gm and stomatal conductance

Concluding remarks and future prospects

Acknowledgements

Geochimica et Cosmochimica Acta

Journal of Biological Chemistry

Biophysical Journal

FEBS Letters

Journal of Biological Chemistry

Flora

Environmental and Experimental Botany

Environmental Pollution

Environmental Pollution

Internal leaf area and cellular CO2 resistance: photosynthetic implications of variations with growth conditions and plant species

Physiologia Plantarum

Biophysical Plant Physiology and Ecology

Carbon isotope discrimination measured concurrently with gas exchange to investigate CO2 diffusion in leaves of higher plants

Functional Plant Biology

Theoretical Considerations when Estimating the Mesophyll Conductance to CO2 Flux by Analysis of the Response of Photosynthesis to CO2

Plant Physiology

Gas-exchange properties of salt-stressed olive (Olea europaea L.) leaves

Plant Physiology

On the need to incorporate sensitivity to CO2 transfer conductance into the Farquhar–von Caemmerer–Berry leaf photosynthesis model

Plant, Cell and Environment

Leaf internal diffusion conductance limits photosynthesis more strongly in older leaves of Mediterranean evergreen broad-leaved species

Plant, Cell and Environment

Estimating the internal conductance to CO2 movement

Functional Plant Biology

Estimating mesophyll conductance to CO2: Methodology, potential errors, and recommendations

Journal of Experimental Botany

Theoretical reconsiderations when estimating the mesophyll conductance to CO2 diffusion in leaves of C3 plants by analysis of combined gas exchange and chlorophyll fluorescence measurements

Plant, Cell and Environment

Mesophyll conductance to CO2: Current knowledge and future prospects

Plant, Cell and Environment

Resistances along the CO2 diffusion pathway inside leaves

Journal of Experimental Botany

Role of mesophyll diffusion conductance in constraining potential photosynthetic productivity in the field

Journal of Experimental Botany

Developmental changes in mesophyll diffusion conductance and photosynthetic capacity under different light and water availabilities in Populus tremula: How structure constrains function

Plant, Cell and Environment

Leaf functional anatomy in relation to photosynthesis

Plant Physiology

To concentrate or ventilate? Carbon acquisition, isotope discrimination and physiological ecology of early land plant life forms

Philosophical Transactions of the Royal Society B: Biological Sciences

Fossil evidence for Cretaceous escalation in angiosperm leaf vein evolution

Proceedings of the National Academy of Sciences of the United States of America

CO2 and water vapor exchange across leaf cuticle (epidermis) at various water potentials

Plant Physiology

Controls on the emission of plant volatiles through stomata: A sensitivity analysis

Journal of Geophysical Research, Atmospheres

Specific reduction of chloroplast carbonic anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO2 assimilation

Planta

Photosynthetic gas exchange and discrimination against 13CO2, and C18O16O in tobacco plants modified by an antisense construct to have low chloroplastic carbonic anhydrase

Plant Physiology

Internal conductance to CO2 diffusion and C18OO discrimination in C3 leaves

Plant Physiology

Characterization and expression analysis of genes encoding α and β carbonic anhydrases in Arabidopsis

Plant, Cell and Environment

Intrinsic CO2 permeability of cell membranes and potential biological relevance of CO2 channels

ChemPhysChem

A decade of debate: Significance of CO2 permeation through membrane channels still controversial

ChemPhysChem

Effect of PCMBS on CO2 permeability of Xenopus oocytes expressing aquaporin 1 or its C189S mutant

American Journal of Physiology

Evidence that aquaporin 1 is a major pathway for CO2 transport across the human erythrocyte membrane

FASEB Journal

Effect of expressing the water channel aquaporin-1 on the CO2 permeability of Xenopus oocytes

American Journal of Physiology

The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO2 transport facilitator

Plant Journal

Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability

Review
Mesophyll diffusion conductance to CO₂: An unappreciated central player in photosynthesis

How different is g_m among phylogenetically distant groups and how have mechanisms controlling g_m evolved?

Which environmental conditions affect g_m?

Modeling and including g_m in photosynthesis models

Co-regulation of g_m and stomatal conductance

Internal leaf area and cellular CO₂ resistance: photosynthetic implications of variations with growth conditions and plant species

Carbon isotope discrimination measured concurrently with gas exchange to investigate CO₂ diffusion in leaves of higher plants

Theoretical Considerations when Estimating the Mesophyll Conductance to CO₂ Flux by Analysis of the Response of Photosynthesis to CO₂

On the need to incorporate sensitivity to CO₂ transfer conductance into the Farquhar–von Caemmerer–Berry leaf photosynthesis model

Estimating the internal conductance to CO₂ movement

Estimating mesophyll conductance to CO₂: Methodology, potential errors, and recommendations

Theoretical reconsiderations when estimating the mesophyll conductance to CO₂ diffusion in leaves of C3 plants by analysis of combined gas exchange and chlorophyll fluorescence measurements

Mesophyll conductance to CO₂: Current knowledge and future prospects

Resistances along the CO₂ diffusion pathway inside leaves

CO₂ and water vapor exchange across leaf cuticle (epidermis) at various water potentials

Specific reduction of chloroplast carbonic anhydrase activity by antisense RNA in transgenic tobacco plants has a minor effect on photosynthetic CO₂ assimilation

Photosynthetic gas exchange and discrimination against ¹³CO₂, and C₁₈O₁₆O in tobacco plants modified by an antisense construct to have low chloroplastic carbonic anhydrase

Internal conductance to CO₂ diffusion and C₁₈OO discrimination in C3 leaves

Intrinsic CO₂ permeability of cell membranes and potential biological relevance of CO₂ channels

A decade of debate: Significance of CO₂ permeation through membrane channels still controversial

Effect of PCMBS on CO₂ permeability of Xenopus oocytes expressing aquaporin 1 or its C189S mutant

Evidence that aquaporin 1 is a major pathway for CO₂ transport across the human erythrocyte membrane

Effect of expressing the water channel aquaporin-1 on the CO₂ permeability of Xenopus oocytes

The Arabidopsis thaliana aquaporin AtPIP1;2 is a physiologically relevant CO₂ transport facilitator

Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO₂ permeability

The tobacco aquaporin NtAQP1 is a membrane CO₂ pore with physiological functions

Tobacco aquaporin NtAQP1 is involved in mesophyll conductance to CO₂ in vivo

Overexpression of the barley aquaporin HvPIP2;1 increases internal CO₂ conductance and CO₂ assimilation in the leaves of transgenic rice plants

Relationship between mesophyll conductance to CO₂ diffusion and contents of aquaporin localized at plasma membrane in tobacco plants grown under drought conditions

Deactivation of aquaporins decreases internal conductance to CO₂ diffusion in tobacco leaves grown under long-term drought

Effects of HgCl₂ on CO₂ dependence of leaf photosynthesis: evidence indicating involvement of aquaporins in CO₂ diffusion across the plasma membrane

Interactive effects of nitrogen and phosphorus on the acclimation potential of foliage photosynthetic properties of cork oak, Quercus suber, to elevated atmospheric CO₂ concentrations