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

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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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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