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Chlorophyll a fluorescence illuminates a path connecting plant molecular biology to Earth-system science

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Abstract

For decades, the dynamic nature of chlorophyll a fluorescence (ChlaF) has provided insight into the biophysics and ecophysiology of the light reactions of photosynthesis from the subcellular to leaf scales. Recent advances in remote sensing methods enable detection of ChlaF induced by sunlight across a range of larger scales, from using instruments mounted on towers above plant canopies to Earth-orbiting satellites. This signal is referred to as solar-induced fluorescence (SIF) and its application promises to overcome spatial constraints on studies of photosynthesis, opening new research directions and opportunities in ecology, ecophysiology, biogeochemistry, agriculture and forestry. However, to unleash the full potential of SIF, intensive cross-disciplinary work is required to harmonize these new advances with the rich history of biophysical and ecophysiological studies of ChlaF, fostering the development of next-generation plant physiological and Earth-system models. Here, we introduce the scale-dependent link between SIF and photosynthesis, with an emphasis on seven remaining scientific challenges, and present a roadmap to facilitate future collaborative research towards new applications of SIF.

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Fig. 1: From incoming radiation to observed SIF and photosynthesis: mechanistic challenges.
Fig. 2: The relationship between SIF and GPP across space and time.
Fig. 3: State-of-the-art SIF imaging methods allow for the observation of SIF across a continuum of scales: from the leaf-to-individual (top row) to the individual-to-landscape (bottom row).
Fig. 4: A roadmap towards the standardized interpretation of SIF.
Fig. 5: Potential and emerging SIF applications illustrated in the form of a ‘SIF city’ metro plan.

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Acknowledgements

The idea for this Perspective was conceived during the Fluorescence Across Space and Time workshop, which took place at the Hyytiälä Forestry Research Station (SMEARII, Finland) during February 2019. We thank the following participants for active discussions during the workshop: J. Bendig, K.-M. Erkkilä, N. Hibiki, L. V. Junker-Frohn, V. Kuznetsova, H. Lindqvist, P. Näthe, J. Oivukkamaki, N. Sabater, T. Solanki, T. Thum, S. Xu and C. Zhang. We also thank B. Osmond and J. Peñuelas for valuable comments on the manuscript; N. Altimir for improving graphic design of Figs. 1 and 5; and B. Siegmann for the preparation of the HyPlant image in Fig. 3. We acknowledge the Academy of Finland (project numbers 288039 and 319211) for financial support. Z.M. was supported by the Australian Research Council (FT160100477), T.M. was supported by the National Aeronautics and Space Administration (80NSSC19M0129) and S.V.W. was supported by the Generalitat Valenciana and the European Social Fund (APOSTD/2018/162). Headwall SIF images from L.P.A. and J.R.K. were supported by grants from the Institute at Brown for Environment and Society at Brown University.

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Authors and Affiliations

  1. Optics of Photosynthesis Laboratory, Institute for Atmospheric and Earth System Research (INAR)/Forest Sciences, Viikki Plant Science Center (ViPS), University of Helsinki, Helsinki, Finland

    Albert Porcar-Castell, Shari Van Wittenberghe, Jon Atherton & Paulina A. Rajewicz

  2. School of Geography, Planning, and Spatial Sciences, College of Sciences Engineering and Technology, University of Tasmania, Hobart, Tasmania, Australia

    Zbyněk Malenovský

  3. Department of Plant Sciences, University of California, Davis, Davis, CA, USA

    Troy Magney

  4. Laboratory of Earth Observation, University of Valencia, Paterna, Spain

    Shari Van Wittenberghe

  5. Department of Botany, Ecology and Plant Physiology, University of La Laguna (ULL), Tenerife, Spain

    Beatriz Fernández-Marín

  6. Laboratoire des Sciences du Climat et de l’Environnement, LSCE/IPSL, CEA-CNRS-UVSQ, Université Paris-Saclay, Gif-sur-Yvette, France

    Fabienne Maignan

  7. International Institute for Earth System Sciences, Nanjing University, Nanjing, China

    Yongguang Zhang

  8. School of Environment, Earth and Ecosystem Sciences, The Open University, Milton Keynes, UK

    Kadmiel Maseyk

  9. Institute at Brown for Environment and Society, Brown University, Providence, RI, USA

    Loren P. Albert & James R. Kellner

  10. Biology Department, West Virginia University, Morgantown, WV, USA

    Loren P. Albert

  11. Organismal and Evolutionary Biology, Viikki Plant Science Centre (ViPS), Faculty of Biological and Environmental Science, University of Helsinki, Helsinki, Finland

    Thomas Matthew Robson

  12. School of Instrumentation Science and Opto-Electronics Engineering, Beihang University, Beijing, China

    Feng Zhao

  13. Department of Plant Biology and Ecology, University of the Basque Country (UPV/EHU), Bilbao, Spain

    Jose-Ignacio Garcia-Plazaola

  14. Department of Biology, Graduate Programs in Cell & Systems Biology and Ecology & Evolutionary Biology, University of Toronto, Mississauga, Ontario, Canada

    Ingo Ensminger

  15. Molecular Plant Biology, University of Turku, Turku, Finland

    Steffen Grebe & Mikko Tikkanen

  16. Department of Ecology and Evolutionary Biology, Brown University, Providence, RI, USA

    James R. Kellner

  17. Nanoscience Center, Department of Biological and Environmental Science, University of Jyväskylä, Jyväskylä, Finland

    Janne A. Ihalainen

  18. Institute of Bio- and Geosciences, Forschungszentrum Jülich GmbH, Jülich, Germany

    Uwe Rascher

  19. Biology Department, Bowdoin College, Brunswick, ME, USA

    Barry Logan

Authors
  1. Albert Porcar-Castell
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  2. Zbyněk Malenovský
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  21. Barry Logan
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Contributions

A.P.-C. conceived the original idea and wrote the manuscript with Z.M., T.M., B.L., S.V.W., B.F.-M., F.M., Y.Z. and K.M., with comments and contributions from all co-authors. Further contributions: Fig. 1 (A.P.-C., Z.M. and S.V.W.), Fig. 2 (A.P.-C., B.F.-M., T.M. and S.V.W.), Fig. 3 (L.P.A., U.R. and J.R.K.), Fig. 4 (A.P.-C., Z.M., U.R. and B.F.-M.), Fig. 5 (J.-I.G.-P., J.A., Z.M. and I.E.), Box 1 (T.M. and A.P.-C.), Box 2 (Z.M. and A.P.-C.) and supplementary information (Z.M. and F.Z.).

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Correspondence to Albert Porcar-Castell.

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Peer review information Nature Plants thanks Jeannine Cavender-Bares, David Schimel and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

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Supplementary information

Supplementary Video 1

Three-dimensional discrete anisotropic radiative transfer (DART) modelling of chlorophyll a SIF emissions in a structurally complex white peppermint (Eucalyptus pulchella) forest stand. Virtual 3D representations of the eucalyptus, endemic to the Tasmanian island, were constructed from terrestrial LiDAR measurements of trees located southeast of Hobart, Australia. A highly clumped eucalyptus foliage is strongly affecting scattering and absorption of SIF photons. The video illustrates the impact of this specific canopy architecture on SIF signal emitted in a 3D vertical profile of the forest stand and on the top-of-canopy SIF in a diurnal course modelled with DART at 740 nm between 07:00 and 18:00 (local time).

Supplementary Video 2

Three-dimensional SIF emissions of a maize (Zea mays L.) crop modelled using the fluorescence model with weighted photon spread (FluorWPS). The virtually grown maize plants were simulated in a computer crop-growth model. The video demonstrates SIF emitted in a 3D vertical profile of maize canopy during the first 30 days of the crop development and a potential impact of sensor–observation geometry on remotely sensed SIF signal, modelled at 740 nm for various viewing zenith and azimuth angles with FluorWPS.

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Porcar-Castell, A., Malenovský, Z., Magney, T. et al. Chlorophyll a fluorescence illuminates a path connecting plant molecular biology to Earth-system science. Nat. Plants 7, 998–1009 (2021). https://doi.org/10.1038/s41477-021-00980-4

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