Photonic multilayer structure of Begonia chloroplasts enhances photosynthetic efficiency

Abstract

Enhanced light harvesting is an area of interest for optimizing both natural photosynthesis and artificial solar energy capture1,2. Iridescence has been shown to exist widely and in diverse forms in plants and other photosynthetic organisms and symbioses3,4, but there has yet to be any direct link demonstrated between iridescence and photosynthesis. Here we show that epidermal chloroplasts, also known as iridoplasts, in shade-dwelling species of Begonia5, notable for their brilliant blue iridescence, have a photonic crystal structure formed from a periodic arrangement of the light-absorbing thylakoid tissue itself. This structure enhances photosynthesis in two ways: by increasing light capture at the predominantly green wavelengths available in shade conditions, and by directly enhancing quantum yield by 5–10% under low-light conditions. These findings together imply that the iridoplast is a highly modified chloroplast structure adapted to make best use of the extremely low-light conditions in the tropical forest understorey in which it is found5,6. A phylogenetically diverse range of shade-dwelling plant species has been found to produce similarly structured chloroplasts79, suggesting that the ability to produce chloroplasts whose membranes are organized as a multilayer with photonic properties may be widespread. In fact, given the well-established diversity and plasticity of chloroplasts10,11, our results imply that photonic effects may be important even in plants that do not show any obvious signs of iridescence to the naked eye but where a highly ordered chloroplast structure may present a clear blue reflectance at the microscale. Chloroplasts are generally thought of as purely photochemical; we suggest that one should also think of them as a photonic structure with a complex interplay between control of light propagation, light capture and photochemistry.

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Figure 1: Blue leaf iridescence and iridoplasts in Begonia.
Figure 2: Optical properties and modelling of iridoplast structure.
Figure 3: Enhanced absorption at reflectance sideband.
Figure 4: Chlorophyll fluorescence images and quantum yield of Begonia plastids.

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Acknowledgements

We would like to thank C. Kidner, M. Hughes (Royal Botanic Gardens Edinburgh) and C. Lundquist (Royal Botanic Gardens Kew) for Begonia species identification and tissue, and A. Kelly for Begonia collection maintenance and horticultural expertise. We thank S. Casson and L. Sandbach for contributions to pilot studies. We acknowledge the Wolfson Bioimaging Facility (University of Bristol) with thanks to D. Alibhai, J. Mantell and G. Tilly for assistance with imaging and also thank S. Vialet-Chabrand (University of Essex) for assistance with fluorescence microscopy. We also thank M.J. Cryan, T. Oliver and S. Nunez from the University of Bristol for fruitful discussion on the photonic side of photosynthesis. M.J. is funded by a NERC PhD studentship. R.O and M.L.G acknowledge EPSRC grant EP/N003381/1. We are grateful for funding from ERC project number 260920 (to H.M.W.).

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M.J., M.L-G., R.O. and H.M.W. conceived the experiments, M.J., O.-P.P. and M.L.-G. carried out iridoplast optical analysis, M.J., M.L.-G. and T.L. carried out the photosynthesis experiments, M.J., O.-P.P. and M.L.-G. carried out microscopy, M.L.-G. and R.O. designed and ran optical models, and M.J., M.L.-G., R.O. and H.M.W. wrote the manuscript, which all authors commented on.

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Correspondence to Heather M. Whitney.

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The authors declare no competing financial interests.

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Supplementary Figures 1–10, Supplementary References. (PDF 4011 kb)

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Jacobs, M., Lopez-Garcia, M., Phrathep, O. et al. Photonic multilayer structure of Begonia chloroplasts enhances photosynthetic efficiency. Nature Plants 2, 16162 (2016). https://doi.org/10.1038/nplants.2016.162

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