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Functional characterisation of plant leaf airspaces in 3D

Functional characterisation of plant leaf airspaces in 3D

Guillaume Théroux-Rancourt (ORCID: 0000-0002-2591-0524)
  • Grant DOI 10.55776/M2245
  • Funding program Lise Meitner
  • Status ended
  • Start January 15, 2018
  • End February 14, 2020
  • Funding amount € 162,180
  • Project website

Disciplines

Biology (100%)

Keywords

    Plant anatomy, Plant evolution, CO2 diffusion, Leaf intercellular airspace, High resolution computed tomography, Finite element method

Abstract Final report

Plant leaves are key components to the global carbon and water cycle, as virtually all terrestrial carbon going from the atmosphere to terrestrial ecosystems and ~70% of all terrestrial transpired water passes through them. Research on carbon and water fluxes at the leaf has primarily focused on how the pores on the surface of the leaf (stomata) and the cells where photosynthesis occurs (mesophyll cells) respond to changes in their environmental conditions. However, there is a space within the leaf that has often been overlooked or ignored when studying photosynthesis as this air-filled cavity barely limits the movement of CO2 in crop plants, which have most often been studied. However, this airspace was shown to limit the movement of CO 2 for certain leaf types found over a wide range of environments around the globe. Further, leaves of the flowering plants (angiosperms), the most diversified and recent plant group in terms of evolution, have improved stomatal control and water transport properties compared to their ancestors like ferns and gymnosperms such as conifers. Little is known on the diversity of the leaf airspace properties and whether or not the angiosperms have evolved improved traits similar to those related to water transport. The proposed project Functional characterisation of plant leaf airspaces in 3D will try to answer that question. The research, building from state-of-the-art three-dimensional leaf imaging through high resolution X-ray computed tomography, will allow to present the leaf airspace properties in their true volumetric nature. In combination with an in-depth analysis of photosynthesis and transpiration, the 3D representation of the leaf will make it possible to accurately describe the importance of the air space in carbon and water transport processes within the leaf, as well as the coordination of airspace properties with other related leaf traits. For this functional characterization, modelling at a small scale will be done using finite element analysis, a tool mostly used in engineering, that will accurately represent the physical processes within the diverse 3D leaf anatomies acquired. This modelling will be then used to build a leaf model that treats a canopy as a single big leaf in order to quantify the role of the leaf airspace in the plant carbon and water relations. This new knowledge is key to fully understand how leaves evolved, adapted, and optimized carbon acquisition and water loss in response to a changing environment, providing important information to reconstruct fossil leaf properties as well as to improve the prediction of plants responses to future climate.

Plant leaves are key components to the global carbon and water cycle, as virtually all terrestrial carbon going from the atmosphere to terrestrial ecosystems and ~70% of all terrestrial transpired water passes through them. Research on carbon and water fluxes at the leaf has primarily focused on how the pores on the surface of the leaf (stomata) and the cells where photosynthesis occurs (mesophyll cells) respond to changes in their environmental conditions. However, there is a space within the leaf that has often been overlooked or ignored when studying photosynthesis as this air-filled cavity barely limits the movement of CO2 in crop plants, which have most often been studied. This airspace was shown to limit the movement of CO2 for certain leaf types found over a wide range of environments around the globe. Further, leaves of the flowering plants (angiosperms), the most diversified and recent plant group in terms of evolution, have improved stomatal control and water transport properties compared to their ancestors like ferns and gymnosperms such as conifers. Little is known on the diversity of the leaf airspace properties and whether or not the angiosperms have evolved improved traits similar to those related to water transport. The project "Functional characterisation of plant leaf airspaces in 3D" answered those questions and showed that angiosperms, through smaller photosynthesising cells, were able to increase the surface area available for CO2 to diffuse and reach the photosynthesising chloroplasts. Hence, angiosperms were able to take full advantage of the increased number of pores at the leaf surface that provide more CO2 for photosynthesis by having more cell surface through which CO2 can diffuse and having an airspace that facilitates CO2 movement up to the photosynthesising cells. This restructuring of the whole leaf anatomy enabled angiosperms to dominate over the majority of the globe's biomes despite declining CO2 concentrations since the end of the Cretaceous. This research used state-of-the-art three-dimensional leaf imaging through high resolution X-ray computed tomography to present the leaf airspace properties in their true volumetric nature. This research combined an in-depth analysis of photosynthesis and transpiration with the 3D representation of the leaf to accurately describe the importance of the airspace in carbon and water transport processes within the leaf, as well as the coordination of airspace properties with other related leaf traits. This new knowledge is key to fully understand how leaves evolved, adapted, and optimized carbon acquisition and water loss in response to a changing environment, providing important information on how leaves are built, adapt to changing environmental conditions, and how they will respond to future climate.

Research institution(s)
  • Universität für Bodenkultur Wien - 100%
International project participants
  • Stefano Manzoni, University of Stockholm - Sweden

Research Output

  • 389 Citations
  • 19 Publications
  • 7 Datasets & models
  • 1 Software
  • 1 Disseminations
  • 1 Scientific Awards
  • 1 Fundings
Publications
  • 2021
    Title The three-dimensional construction of leaves is coordinated with water use efficiency in conifers
    DOI 10.1111/nph.17772
    Type Journal Article
    Author Trueba S
    Journal New Phytologist
    Pages 851-861
    Link Publication
  • 2021
    Title Maximum CO2 diffusion inside leaves is limited by the scaling of cell size and genome size
    DOI 10.1098/rspb.2020.3145
    Type Journal Article
    Author Théroux-Rancourt G
    Journal Proceedings of the Royal Society B
    Pages 20203145
    Link Publication
  • 2021
    Title The 3D construction of leaves is coordinated with water use efficiency in conifers
    DOI 10.1101/2021.04.23.441113
    Type Preprint
    Author Trueba S
    Pages 2021.04.23.441113
    Link Publication
  • 2022
    Title Desiccation of the leaf mesophyll and its implications for CO2 diffusion and light processing
    DOI 10.1111/pce.14287
    Type Journal Article
    Author Momayyezi M
    Journal Plant, Cell & Environment
    Pages 1362-1381
    Link Publication
  • 2022
    Title Structural organization of the spongy mesophyll
    DOI 10.1111/nph.17971
    Type Journal Article
    Author Borsuk A
    Journal New Phytologist
    Pages 946-960
    Link Publication
  • 2020
    Title Maximum CO2 diffusion inside leaves is limited by the scaling of cell size and genome size
    DOI 10.1101/2020.01.16.904458
    Type Preprint
    Author Théroux-Rancourt G
    Pages 2020.01.16.904458
    Link Publication
  • 2021
    Title Supplementary Information from Maximum CO2 diffusion inside leaves is limited by the scaling of cell size and genome size
    DOI 10.6084/m9.figshare.13889506.v1
    Type Other
    Author Roddy A
    Link Publication
  • 2021
    Title Supplementary Information from Maximum CO2 diffusion inside leaves is limited by the scaling of cell size and genome size
    DOI 10.6084/m9.figshare.13889506
    Type Other
    Author Roddy A
    Link Publication
  • 2023
    Title Analyzing anatomy over three dimensions unpacks the differences in mesophyll diffusive area between sun and shade Vitis vinifera leaves.
    DOI 10.1093/aobpla/plad001
    Type Journal Article
    Author Herrera Jc
    Journal AoB PLANTS
  • 2023
    Title An unsupervised, shape-based 3d cell instance segmentation method for plant tissues
    DOI 10.3217/978-3-85125-954-4-08
    Type Other
    Author Palmrich
    Link Publication
  • 2023
    Title Redundant 1-cells in Multi-labeled 2-Gmap Irregular Pyramids
    DOI 10.3217/978-3-85125-954-4-01
    Type Other
    Author Banaeyan
    Link Publication
  • 2023
    Title Towards Uncertainty Detection in Automated Leaf Tissue Segmentation
    DOI 10.3217/978-3-85125-954-4-07
    Type Other
    Author Grexova
    Link Publication
  • 2019
    Title Digitally Deconstructing Leaves in 3D Using X-ray Microcomputed Tomography and Machine Learning
    DOI 10.1101/814954
    Type Preprint
    Author Théroux-Rancourt G
    Pages 814954
    Link Publication
  • 2022
    Title Localized growth and remodelling drives spongy mesophyll morphogenesis
    DOI 10.1098/rsif.2022.0602
    Type Journal Article
    Author Treado J
    Journal Journal of the Royal Society Interface
    Pages 20220602
    Link Publication
  • 2019
    Title Emergent honeycomb topology of the leaf spongy mesophyll
    DOI 10.1101/852459
    Type Preprint
    Author Borsuk A
    Pages 852459
    Link Publication
  • 2019
    Title Shape matters: the pitfalls of analyzing mesophyll anatomy
    DOI 10.1111/nph.16360
    Type Journal Article
    Author Théroux-Rancourt G
    Journal New Phytologist
    Pages 2239-2242
    Link Publication
  • 2020
    Title The Scaling of Genome Size and Cell Size Limits Maximum Rates of Photosynthesis with Implications for Ecological Strategies
    DOI 10.1086/706186
    Type Journal Article
    Author Roddy A
    Journal International Journal of Plant Sciences
    Pages 75-87
    Link Publication
  • 2020
    Title Assessing adaptive and plastic responses in growth and functional traits in a 10-year-old common garden experiment with pedunculate oak (Quercus robur L.) suggests that directional selection can drive climatic adaptation
    DOI 10.1111/eva.13034
    Type Journal Article
    Author George J
    Journal Evolutionary Applications
    Pages 2422-2438
    Link Publication
  • 2020
    Title Digitally deconstructing leaves in 3D using X-ray microcomputed tomography and machine learning
    DOI 10.1002/aps3.11380
    Type Journal Article
    Author Théroux-Rancourt G
    Journal Applications in Plant Sciences
    Link Publication
Datasets & models
  • 2021 Link
    Title R script used to generate the theoretical conductance values based on cell size and leaf porosity. from Maximum CO2 diffusion inside leaves is limited by the scaling of cell size and genome size
    DOI 10.6084/m9.figshare.13889500
    Type Database/Collection of data
    Public Access
    Link Link
  • 2021 Link
    Title R script used to generate the theoretical conductance values based on cell size and leaf porosity. from Maximum CO2 diffusion inside leaves is limited by the scaling of cell size and genome size
    DOI 10.6084/m9.figshare.13889500.v1
    Type Database/Collection of data
    Public Access
    Link Link
  • 2021 Link
    Title R script used to generate the theoretical conductance values based on cell size and leaf porosity. from Maximum CO2 diffusion inside leaves is limited by the scaling of cell size and genome size
    DOI 10.6084/m9.figshare.13889500.v2
    Type Database/Collection of data
    Public Access
    Link Link
  • 2021 Link
    Title Supplementary Tables from Maximum CO2 diffusion inside leaves is limited by the scaling of cell size and genome size
    DOI 10.6084/m9.figshare.13889503
    Type Database/Collection of data
    Public Access
    Link Link
  • 2021 Link
    Title Supplementary Tables from Maximum CO2 diffusion inside leaves is limited by the scaling of cell size and genome size
    DOI 10.6084/m9.figshare.13889503.v1
    Type Database/Collection of data
    Public Access
    Link Link
  • 2020 Link
    Title Image Dataset for 'Digitally deconstructingleaves in 3D using X-ray microcomputed tomography and machine learning'
    DOI 10.5281/zenodo.3694972
    Type Database/Collection of data
    Public Access
    Link Link
  • 2020 Link
    Title Image Dataset for 'Digitally deconstructingleaves in 3D using X-ray microcomputed tomography and machine learning'
    DOI 10.5281/zenodo.3694973
    Type Database/Collection of data
    Public Access
    Link Link
Software
  • 2019 Link
    Title Software for the automated segmentation of microCT scans of plant leaves
    Link Link
Disseminations
  • 2020
    Title Publication in an industry magazine
    Type A magazine, newsletter or online publication
Scientific Awards
  • 2019
    Title Plant anatomy symposium in Moscow
    Type Personally asked as a key note speaker to a conference
    Level of Recognition Continental/International
Fundings
  • 2020
    Title Water's gateway to heaven: 3D imaging and modeling of transient stomatal responses in plant leaves under dynamic environments
    Type Research grant (including intramural programme)
    Start of Funding 2020
    Funder Vienna Science and Technology Fund

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