Low light often limits photosynthesis and growth and reduces plant quality and is the main limiting factor for the production of horticultural crops, such as vegetables and ornamental bedding plants, during the winter in temperate climates (Gaudreau and Chartbonneau, 1994; Lopez and Runkle, 2008; Nelson, 2012). Daily light integral [DLI (total PPF integrated over 24-h)] in greenhouses in the northern latitudes of the United States can be as low as 2.5–10 mol·m−2·d−1 from November to February (Korczynski et al., 2002). Supplemental lighting is often needed to produce high-quality crops in controlled-environment agriculture but can substantially increase production costs. For example, van Iersel and Gianino (2017) estimated that the cost of supplemental lighting provided by high-pressure sodium lamps can account for about 30% of the farm gate value for vegetable greenhouses. The high cost of supplemental lighting in controlled environments necessitates the need for more efficient use of supplemental light.
Supplemental light use efficiency can be improved by implementing energy-efficient lights, such as light-emitting diodes (LEDs) (Nelson and Bugbee, 2014). In addition to the efficiency of the lights, the overall efficiency at which the electrical energy is converted into plant biomass depends on how efficiently plants use light for photosynthesis. Not all the light absorbed by plants is used in the photochemical reactions of photosynthesis. Some of the absorbed light is dissipated as heat and a small fraction is re-emitted as chlorophyll fluorescence (Maxwell and Johnson, 2000). The quantum yield of photosystem II, the efficiency with which photosystem II (PSII) uses absorbed photons for electron transport, or the moles of electrons transported per mole of photons (typically expressed as a unitless fraction) can be easily measured using chlorophyll fluorescence (Genty et al., 1989; Maxwell and Johnson, 2000). In addition, chlorophyll fluorescence can be used to estimate the ETR, which is often closely correlated with photosynthetic rate (Beer et al., 1998; Flexas et al., 1999), and the degree of heat dissipation under various light conditions. As light intensity increases, plants use the absorbed light less efficiently for photosynthesis, while more of that absorbed light energy is dissipated as heat or through chlorophyll fluorescence (Baker, 2008; Demmig-Adams et al., 1996; van Iersel et al., 2016b). As a result, supplemental light provided at high intensities or in addition to a high ambient light intensity is expected to be used relatively inefficiently for photosynthesis (van Iersel and Gianino, 2017) and presumably growth. Clearly, it is not beneficial to provide supplemental light when plants cannot use that light efficiently for photosynthesis.
Genetic adaptation of plants to their light environment occurs over generations and at the population level and has resulted in photosynthetic differences among species. High-light-adapted species generally have greater photosynthetic capacity; i.e., a higher maximum photosynthetic rate and a higher light-saturation point than shade-adapted species (Björkman, 1981). By contrast, shade-adapted species tend to reach maximum photosynthetic capacity at much lower light intensity and are more likely to incur damage to the photosynthetic reaction centers under high light [photoinhibition (Demmig-Adams and Adams, 1992)]. Although the photosynthetic responses to PPF have been reported for many species, this information has seldom been used to examine how the supplemental light use efficiency changes with changing PPF and how supplemental lighting can be optimized for different species. van Iersel and Gianino (2017) reported that plants with different photosynthetic capacities responded differently to supplemental light. They simulated the responses of net photosynthesis (An) of two species to supplemental light provided at different ambient PPF and found that the high-light-adapted species Campanula portenschlagiana (with greater photosynthetic capacity) showed pronounced increases in An when supplemental light was provided at a relatively high ambient PPF of 250 μmol·m−2·s−1, whereas little increase in An was observed in the low-light-adapted plant Heuchera americana when supplemental light was provided at the same ambient PPF (van Iersel and Gianino, 2017).
In addition to adaptation, short-term acclimation to light, typically taking place within minutes to weeks (within the life cycle of a plant), can also induce phenotypic modifications that alter plants’ photosynthetic light use efficiency (Anderson et al., 1995; Björkman, 1981; Valladares and Niinemets, 2008). Such modifications include changes in leaf anatomical structures (Evans and Poorter, 2001; McMillen and McClendon, 1983), chlorophyll content and chlorophyll a/b ratio (Givnish, 1988; Niinemets, 2010), changes in electron transport capacity per unit chlorophyll (Anderson and Osmond, 1987), rubisco content and activity (Björkman, 1981; Seemann, 1989), xanthophyll cycle pigment pool size (involved in heat dissipation of the absorbed light) (Demmig-Adams and Adams, 1992; Logan et al., 1998), and maximum photosynthetic capacity (Oguchi et al., 2005). The importance of acclimation to different light levels for the efficiency with which plants use supplemental light for photochemistry has not been studied.
Currently, supplemental lighting in greenhouses is typically controlled by a timer or based on ambient light levels. The ability of a crop to efficiently use the supplemental light for photosynthesis is seldom considered when developing supplemental lighting strategies. Few studies have investigated the feasibility of optimizing supplemental lighting in controlled environments based on plant physiological responses to light (van Iersel et al., 2016a, 2016b) and there is a need for information on how supplemental lighting can be optimized for crops adapted and/or acclimated to different light environments. Chlorophyll fluorescence measurements are especially well-suited for this purpose because they can be used to determine how efficiently plants use the provided light in a real-time, noninvasive manner. Therefore, our objectives were the following: 1) to determine the photochemical responses of different species to a wide range of light intensities; 2) to quantify how light acclimation affects crops’ photochemistry; and 3) to examine how supplemental light use efficiency changes with changing ambient light levels, and how supplemental light can be optimized for crops adapted and/or acclimated to different light environments.
Adams, W.W. III & Demmig-Adams, B. 1992 Operation of the xanthophyll cycle in higher plants in response to diurnal changes in incident sunlight Planta 186 390 398
Anderson, J.M., Chow, W.S. & Park, Y. 1995 The grand design of photosynthesis: Acclimation of the photosynthetic apparatus to environmental cues Photosynth. Res. 46 129 139
Anderson, J.M. & Osmond, C.B. 1987 Shade - sun responses: Compromises between acclimation and photoinhibition, p. 1–36. In: D.J. Kyle, C.B. Osmond, and C.J. Arntzen (eds.). Photoinhibition. Elsevier Science, Amsterdam, The Netherlands
Aro, E., McCaffery, S. & Anderson, J.M. 1993 Photoinhibition and D1 protein degradation in peas acclimated to different growth irradiances Plant Physiol. 103 835 843
Baker, N.R., Harbinson, J. & Kramer, D.M. 2007 Determining the limitations and regulation of photosynthetic energy transduction in leaves Plant Cell Environ. 30 1107 1125
Beer, S., Vilenkin, B., Weil, A., Veste, M., Susel, L. & Eshel, A. 1998 Measuring photosynthetic rates in seagrasses by pulse amplitude modulated (PAM) fluorometry Mar. Ecol. Prog. Ser. 174 293 300
Björkman, O. 1981 Responses to different quantum flux densities, p. 57–107. In: O.L. Lange, P.S. Nobel, C.B. Osmond, and H. Ziegler (eds.). Physiological plant ecology I. Encyclopedia of plant physiology, Vol. 12A. Springer-Verlag, Berlin, Germany
Björkman, O. & Demmig, B. 1987 Photon yield of O2 evolution and chlorophyll fluorescence characteristics at 77k among vascular plants of diverse origins Planta 170 489 504
Blankenship, R.E. 2014 Molecular mechanisms of photosynthesis. 2nd ed. Wiley, Oxford, UK
Chow, W.S., Qian, L., Goodchild, D.J. & Anderson, J.M. 1988 Photosynthetic acclimation of Alocasia macrorrhiza (L.) G. Don to growth irradiance: Structure, function and composition of chloroplasts Austral. J. Plant Physiol. 15 107 122
Demmig-Adams, B. & Adams, W.W. III 1992 Photoprotection and other responses of plants to high light stress Annu. Rev. Plant Physiol. Plant Mol. Biol. 43 599 626
Demmig-Adams, B. & Adams, W.W. III 1996 The role of xanthophyll cycle carotenoids in the protection of photosynthesis Trends Plant Sci. 1 21 26
Demmig-Adams, B. & Adams, W.W. III 2006 Photoprotection in an ecological context: The remarkable complexity of thermal energy dissipation New Phytol. 172 11 21
Demmig-Adams, B., Adams, W.W. III, Barker, D.H., Logan, B.A., Bowling, D.R. & Verhoeven, A.S. 1996 Using chlorophyll fluorescence to assess the fraction of absorbed light allocated to thermal dissipation of excess excitation Physiol. Plant. 98 253 264
Demmig-Adams, B., Cohu, C.M., Muller, O. & Adams, W.W. III 2012 Modulation of photosynthetic energy conversion in nature: From seconds to seasons Photosynth. Res. 113 75 88
Evans, J.R. & Poorter, H. 2001 Photosynthetic acclimation of plants to growth irradiance: The relative importance of specific leaf area and nitrogen partitioning in maximizing carbon gain Plant Cell Environ. 24 755 767
Flexas, J., Escalona, J.M. & Medrano, H. 1999 Water stress induces different levels of photosynthesis and electron transport rate regulation in grapevines Plant Cell Environ. 22 39 48
Gaudreau, L. & Chartbonneau, J. 1994 Photoperiod and photosynthetic photon flux influence growth and quality of greenhouse-grown lettuce HortScience 29 1285 1289
Genty, B., Briantais, J. & Baker, N.R. 1989 The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence Biochim. Biophys. Acta 990 87 92
Korczynski, P.C., Logan, J. & Faust, J.E. 2002 Mapping monthly distribution of daily light integrals across the contiguous United States HortTechnology 12 12 16
Logan, B.A., Demmig-Adams, B., Adams, W.W. III & Grace, S.C. 1998 Antioxidants and xanthophyll cycle-dependent energy dissipation in Cucurbita pepo L. and Vinca major L. acclimated to four growth PPFDs in the field J. Expt. Bot. 49 1869 1879
Lopez, R.G. & Runkle, E. 2008 Photosynthetic daily light integral during propagation influences rooting and growth of cuttings and subsequent development of new guinea impatiens and petunia HortScience 43 2052 2059
Matos, F.S., Wolfgramm, R., Gonçalves, F.V., Cavatte, P.C., Ventrella, M.C. & DaMatta, F.M. 2009 Phenotypic plasticity in response to light in the coffee tree Environ. Expt. Bot. 67 421 427
McMillen, G.G. & McClendon, J.H. 1983 Dependence of photosynthetic rates on leaf density thickness in deciduous woody plants grown in sun and shade Plant Physiol. 72 674 678
Murchie, E.H. & Horton, P. 1997 Acclimation of photosynthesis to irradiance and spectral quality in British plant species: Chlorophyll content, photosynthetic capacity and habitat preference Plant Cell Environ. 20 438 448
Nelson, P.V. 2012 Greenhouse operation and management. 7th ed. Prentice Hall, Upper Saddle River, NJ
Nelson, J.A. & Bugbee, B. 2014 Economic analysis of greenhouse lighting: Light emitting diodes vs. high intensity discharge fixtures PLoS One 9 6 e99010
Nemali, K.S. & van Iersel, M.W. 2004 Acclimation of wax begonia to light intensity: Changes in photosynthesis, respiration, and chlorophyll concentration J. Amer. Soc. Hort. Sci. 129 745 751
Niinemets, Ü. 2010 A review of light interception in plant stands from leaf to canopy in different plant functional types and in species with varying shade tolerance Ecol. Res. 25 693 714
Oguchi, R., Hikosaka, K. & Hirose, T. 2005 Leaf anatomy as a constraint for photosynthetic acclimation: Differential responses in leaf anatomy to increasing growth irradiance among three deciduous trees Plant Cell Environ. 28 916 927
Seemann, J.R. 1989 Light adaptation/acclimation of photosynthesis and the regulation of ribulose-1,5-bisphosphate carboxylase activity in sun and shade plants Plant Physiol. 91 379 386
van Iersel, M.W. & Gianino, D. 2017 An adaptive control approach for LED lights can reduce the energy costs of supplemental lighting in greenhouses HortScience 52 72 77
van Iersel, M.W., Mattos, E., Weaver, G., Ferrarezi, R.S., Martin, M.T. & Haidekker, M. 2016a Using chlorophyll fluorescence to control lighting in controlled environment agriculture Acta Hort. 1134 427 433
van Iersel, M.W., Weaver, G., Martin, M.T., Ferrarezi, R.S., Mattos, E. & Haidekker, M. 2016b A chlorophyll fluorescence-based biofeedback system to control photosynthetic lighting in controlled environment agriculture J. Amer. Soc. Hort. Sci. 141 169 176
Verhoeven, A.S., Demmig-Adams, B. & Adams, W.W. III 1997 Enhanced employment of the xanthophyll cycle and thermal energy dissipation in spinach expose to high light and N stress Plant Physiol. 113 817 824