Far-red photons have equivalent efficiency to traditional photosynthetic photons: Implications for redefining photosynthetically active radiation

Plant Cell and Environment

Volumn 43, Issue 5, 2020, Pages 1259-1272

  Zhen, Shuyang ^a   Bugbee, Bruce ^a  

^a UTAH STATE UNIVERSITY   (United States)

Author keywords

Chl d and f; Emerson enhancement; far red; photosynthetically active radiation; photosystems; whole plant canopy photosynthesis

Indexed keywords

LEAF AREA; PHOTOCHEMISTRY; PHOTOSYNTHESIS; PHOTOSYNTHETICALLY ACTIVE RADIATION; SOLAR RADIATION;

EMBRYOPHYTA;

EDIBLE PLANT; PHOTON; PHOTOSYNTHESIS; PLANT LEAF; RADIATION RESPONSE;

PHOTONS; PHOTOSYNTHESIS; PLANT LEAVES; PLANTS, EDIBLE;

EID: 85079394210     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/pce.13730     Document Type: Article

References (66)

1. Allen, J. F. (2003). State transitions–A question of balance. Science, 299, 1530–1532.
2. Amthor, J. S. (2010). From sunlight to phytomass: On the potential efficiency of converting solar radiation to phyto-energy. New Phytologist, 188, 939–959.
3. Barber, J., & Archer, M. D. (2001). P680, the primary electron donor of photosystem II. Journal of Photochemistry and Photobiology A: Chemistry, 142, 97–106.
4. Björn, L. O., Papageorgiou, G. C., Blankenship, R. E., & Govindjee. (2009). A viewpoint: Why chlorophyll a? Photosynthesis Research, 99, 85–98.
5. Blankenship, R. E., & Chen, M. (2013). Spectrum expansion and antenna reduction can enhance photosynthesis for energy production. Current Opinion in Chemical Biology, 17, 457–461.
6. Bugbee, B., & Monje, O. (1992). The limits of crop productivity. Bioscience, 42, 494–502.
7. Butler, W. L. (1978). Energy distribution in the photochemical apparatus of photosynthesis. Annual Review of Plant Physiology, 29, 345–378.
8. Chen, M., & Blankenship, R. E. (2011). Expanding the solar spectrum used by photosynthesis. Trends in Plant Science, 16, 427–431.
9. Chen, M., Schliep, M., Willows, R. D., Cai, Z., Neilan, B. A., & Scheer, H. (2010). A red-shifted chlorophyll. Science, 329, 1318–1319.
10. Croce, R., & van Amerongen, H. (2013). Light-harvesting in photosystem I. Photosynthesis Research, 116, 153–166.
11. Duysens, L. N. M., & Amesz, J. (1962). Function and identification of two photochemical systems in photosynthesis. Biochimica et Biophysica Acta, 64, 243–260.
12. Emerson, R., Chalmers, R., & Cederstrand, C. (1957). Some factors influencing the long-wave limit of photosynthesis. Proceeding of the National Academy of Science USA, 43, 133–143.
13. Emerson, R., & Lewis, C. M. (1943). The dependence of the quantum yield of chlorella photosynthesis on wave length of light. American Journal of Botany, 30, 165–178.
14. Emerson, R., & Rabinowitch, E. (1960). Red drop and role of auxiliary pigments in photosynthesis. Plant Physiology, 35, 477–485.
15. Evans, J. R. (1987). The dependence of quantum yield on wavelength and growth irradiance. Australian Journal of Plant Physiology, 14, 69–79.
16. Finazzi, G., & Johnson, G. N. (2016). Cyclic electron flow: Facts and hypotheses. Photosynthesis Research, 129, 227–230.
17. Gan, F., Zhang, S., Rockwell, N. C., Martin, S. S., Lagarias, J. C., & Bryant, D. A. (2014). Extensive remodeling of a cyanobacterial photosynthetic apparatus in far red light. Science, 345, 1312–1317.
18. Gifford, R. M., Thorne, J. H., Hitz, W. D., & Giaquinta, R. T. (1984). Crop productivity and photoassimilate partitioning. Science, 225, 801–808.
19. Gobets, B., & van Grondelle, R. (2001). Energy transfer and trapping in photosystem I. 2001. Biochimica et Biophysica Acta, 1507, 80–99.
20. Hanson, M. R., Lin, M. T., Carmo-silva, A. E., & Parry, M. A. J. (2016). Towards enginnering carboxysomes into C3 plants. The Plant Journal, 87, 38–50.
21. Heber, U., & Walker, D. (1992). Concerning a dual function of coupled cyclic electron transport in leaves. Plant Physiology, 100, 1621–1626.
22. Hill, R., & Bendall, F. (1960). Function of the two cytochrome components in chloroplasts: A working hypothesis. Nature, 186, 136–137.
23. Ho, M.-Y., Shen, G., Canniffe, D. P., Zhao, C., & Bryant, D. A. (2016). Light-dependent chlorophyll f synthase is a highly divergent paralog of PsbA of photosystem II. Science, 353, aaf9178.
24. Hogewoning, S. W., Wientjes, E., Douwstra, P., Trouwborst, G., van Ieperen, W., Croce, R., & Harbinson, J. (2012). Photosynthetic quantum yield dynamics: From photosystems to leaves. Plant Cell, 24, 1921–1935.
25. Holmes, M. G., Sager, J. C., & Klein, W. H. (1986). Sensitivity to far-red radiation in stomata of Phaseolus vulgaris L: Rhythmic effects on conductance and photosynthesis. Planta, 168, 516–522.
26. Holmes, M. G., & Smith, H. (1977). The function of phytochrome in the natural environment-II. The influence of vegetation canopies on the spectral energy distribution of natural daylight. Photochemistry and Photobiology, 25, 539–545.
27. Hu, Q., Miyashita, H., Iwasaki, I., Kurano, N., Miyachi, S., Iwaki, M., & Itoh, S. (1998). A photosystem I reaction center driven by chlorophyll d in oxygenic photosynthesis. Proceeding of the National Academy of Science USA, 95, 13319–13323.
28. Inada, K. (1976). Action spectra for photosynthesis in higher plants. Plant & Cell Physiology, 17, 355–365.
29. Johnson, G. N. (2011). Physiology of PSI cyclic electron transport in higher plants. Biochimica et Biophysica Acta, 1807, 384–389.
30. Kasperbauer, M. J. (1971). Spectral distribution of light in a tobacco canopy and effects of end-of-day light quality on growth and development. Plant Physiology, 47, 775–778.
31. Kirst, H., Shen, Y., Vamvaka, E., Betterle, N., Xu, D., Warek, U., … Melis, A. (2018). Downregulation of the CpSRP43 gene expression confers a truncated light-harvesting antenna (TLA) and enhances biomass and leaf-to-stem ratio in Nicotiana tabacum canopies. Planta, 248, 139–154.
32. Koehne, B., Elli, G., Jennings, R. C., Wilhelm, C., & Trissl, H. W. (1999). Spectroscopic and molecular characterization of a long wavelength absorbing antenna of Ostreobium sp. Biochimica et Biophysica Acta, 1412, 94–107.
33. Kok, B. (1961). Partial purification and determination of oxidation reduction potential of the photosynthetic chlorophyll complex absorbing at 700 mμ. Biochimica et Biophysica Acta, 48, 527–533.
34. Kono, M., Kawaguchi, H., Mizusawa, N., Yamori, W., Suzuki, Y., & Terashima, I. (2020). Far-red light accelerates photosynthesis in the low-light phases of fluctuating light. Plant & Cell Physiology, 61, 192–202. https://doi.org/10.1093/pcp/pcz191
35. Kono, M., Yamori, W., Suzuki, Y., & Terashima, I. (2017). Photoprotection of PSI by far-red light against the fluctuating light-induced photoinhibition in Arabidopsis thaliana and field-grown plants. Plant & Cell Physiology, 58, 35–45.
36. Kromdijk, J., Glowacka, K., Leonelli, L., Gabilly, S. T., Iwai, M., Niyogi, K. K., & Long, S. P. (2016). Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science, 354, 857–861.
37. Kubis, A., & Bar-Even, A. (2019). Synthetic biology approaches for improving photosynthesis. Journal of Experimental Botany, 70, 1425–1433.
38. Laisk, A., Oja, V., Eichelmann, H., & Dall'Osto, L. (2014). Action spectra of photosystems II and I and quantum yield of photosynthesis in leaves in state 1. Biochimica et Biophysica Acta, 1837, 315–325.
39. Long, S. P., Zhu, X.-G., Naidu, S. L., & Ort, D. R. (2006). Can improvement in photosynthesis increase crop yields? Plant, Cell and Environment, 29, 315–330.
40. Loughlin, P., Lin, Y., & Chen, M. (2013). Chlorophyll d and Acaryochloris marina: Current status. Photosynthesis Research, 116, 277–293.
41. McCree, K. J. (1972a). Significance of enhancement for calculation based on the action spectrum for photosynthesis. Plant Physiology, 49, 704–706.
42. McCree, K. J. (1972b). The action spectrum, absorptance and quantum yield of photosynthesis in crop plants. Agricultural Meteorology, 9, 191–216.
43. Melis, A. (2009). Solar energy conversion efficiency in photosynthesis: Minimizing the chlorophyll antennae to maximize efficiency. Plant Science, 177, 272–280.
44. Miyashita, H., Ikemoto, H., Kurano, N., Adachi, K., Chihara, M., & Miyachi, S. (1996). Chlorophyll d as a major pigment. Nature, 383, 402.
45. Murakami, K., Matsuda, R., & Fujiwara, K. (2018). A mathematical model of photosynthetic electron transport in response to the light spectrum based on excitation energy distributed to photosystems. Plant & Cell Physiology, 59, 1643–1651.
46. Myers, J. (1971). Enhancement studies in photosynthesis. Annual Review of Plant Physiology, 22, 289–312.
47. Nelson, J. A., & Bugbee, B. (2015). Analysis of environmental effects on leaf temperature under sunlight, high pressure sodium and light emitting diodes. PLoS One, 10, e0138930.
48. Nürnberg, D. J., Morton, J., Santabarbara, S., Telfer, A., Joliot, P., Antonaru, L. A., … Rutherford, A. W. (2018). Photochemistry beyond the red limit in chlorophyll f-containing photosystems. Science, 360, 1210–1213.
49. Ort, D. R., Merchant, S. S., Alric, J., Barkan, A., Blankenship, R. E., Bock, R., … Zhu, X. G. (2015). Redesigning photosynthesis to sustainably meet global food and bioenergy demand. Proceeding of the National Academy of Science USA, 112, 8529–8536.
50. Rivadossi, A., Zucchelli, G., Garlaschi, F. M., & Jennings, R. C. (1999). The importance of PS I chlorophyll red forms in light-harvesting by leaves. Photosynthesis Research, 60, 209–215.
51. Rochaix, J. D. (2011). Regulation of photosynthetic electron transport. Biochimica et Biophysica Acta, 1807, 878–886.
52. Rumeau, D., Peltier, G., & Cournac, L. (2007). Chlororespiration and cyclic electron flow around PSI during photosynthesis and plant stress response. Plant, Cell and Environment, 30, 1041–1051.
53. Sagun, J. V., Badger, M. R., Chow, W. S., & Ghannoum, O. (2019). Cyclic electron flow and light partitioning between the two photosystems in leaves of plants with different functional types. Photosynthesis Research, 142, 321–334.
54. 3 chassis in the synthetic biology age. The Plant Journal, 87, 51–65.
55. South, P. F., Cavanagh, A. P., Liu, H. W., & Ort, D. R. (2019). Synthetic glycolate metabolism pathways stimulate crop growth and productivity in the field. Science, 363, eaat9077.
56. 4 photosynthesis. Proceeding of the National Academy of Science USA, 102, 16898–16903.
57. Tomo, T., Okubo, T., Akimoto, S., Yokono, M., Miyashita, H., Tsuchiya, T., … Mimuro, M. (2007). Identification of the special pair of photosystem II in a chlorophyll d-dominated cyanobacterium. Proceeding of the National Academy of Science USA, 104, 7283–7288.
58. van Iersel, M. W., & Bugbee, B. (2000). A multiple chamber, semicontinuous, crop carbon dioxide exchange system: Design, calibration, and data interpretation. Journal of American Society for Horticultural Science, 125, 86–92.
59. Wolf, B. M., & Blankenship, R. E. (2019). Far-red acclimation in diverse oxygenic photosynthetic organisms. Photosynthesis Research, 142, 349–359. https://doi.org/10.1007/s11120-019-00653-6
60. Wong, S. C., Cowan, I. R., & Farquhar, G. D. (1979). Stomatal conductance correlates with photosynthetic capacity. Nature, 282, 424–426.
61. 2 during ontogeny. Plant Physiology, 78, 821–825.
62. Yamori, W. (2016). Photosynthetic response to fluctuating environments and photoprotective strategies under abiotic stress. Journal of Plant Research, 129, 379–395.
63. Yamori, W., & Shikanai, T. (2016). Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annual Review of Plant Biology, 67, 81–106.
64. Zhen, S., Haidekker, M., & van Iersel, M. W. (2018). Far-red light enhances photochemical efficiency in a wavelength-dependent manner. Physiologia Plantarum, 167, 21–33. https://doi.org/10.1111/ppl.12834
65. Zhen, S., & van Iersel, M. W. (2017). Far-red light is needed for efficient photochemistry and photosynthesis. Journal of Plant Physiology, 209, 115–122.
66. Zhu, X. G., Long, S. P., & Ort, D. R. (2010). Improving photosynthetic efficiency for greater yield. Annual Review of Plant Biology, 61, 235–261.