High levels of anoxygenic photosynthesis revealed by dual-frequency Fourier photoacoustics in Ailanthus altissima leaves
Vladimir Lysenko
A * and Tatyana Varduny A
+ Author Affiliations
- Author Affiliations
A Academy of Biology and Biotechnology, Southern Federal University, Botanichesky spusk 7, 344041 Rostov-on-Don, Russia.
Functional Plant Biology - https://doi.org/10.1071/FP21093
Submitted: 31 March 2021 Accepted: 2 March 2022 Published online: 13 April 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
In contrast to oxygenic photosynthesis, true anoxygenic photosynthesis is not associated with O2 evolution originated from water photolysis but still converts light energy to that of the phosphoanhydride bonds of ATP. In a narrow sense, anoxygenic photosynthesis is mainly known as to be related to the purple and green sulfur bacteria, but in a broad sense, it also occurs in the vascular plants. The portion of photosynthetic water photolysis that is compensated by the processes of O2 uptake (respiration, photorespiration, Mehler cycle, etc.) may be referred to as ‘quasi’ anoxygenic photosynthesis. Photoacoustic method allows for the separate detection of photolytic O2 at frequencies of measuring light about 20–40 Hz, whereas at 250–400 Hz, it detects the photochemical energy storage. We have developed a fast-Fourier transform photoacoustic method enabling measurements of both these signals simultaneously in one sample. This method allows to calculate oxygenic coefficients, which reflect the part of photochemically stored light energy that is used for the water photolysis. We show that the true anoxygenic photosynthesis in Ailanthus altissima Mill. leaves reached very high levels under low light, under moderate light at the beginning of the 1-h period, and at the end of the 40-min period under saturating light.
Keywords: CO2 uptake, cyclic electron transport, photobaric signal, photoinhibitory light conditions, photosystem I, photothermal signal, quantum yield, transpiration kinetics.
References
Allakhverdiev SI, Klimov VV, Carpentier R (1997) Evidence for the involvement of cyclic electron transport in the protection of photosystem II against photoinhibition: influence of a new phenolic compound. Biochemistry 36, 4149–4154.| Evidence for the involvement of cyclic electron transport in the protection of photosystem II against photoinhibition: influence of a new phenolic compound.Crossref | GoogleScholarGoogle Scholar | 9100008PubMed |
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology 59, 89–113.
| Chlorophyll fluorescence: a probe of photosynthesis in vivo.Crossref | GoogleScholarGoogle Scholar | 18444897PubMed |
Barja PR, Mansanares AM, Da Silva EC, Magalhães ACN, Alves PLCA (2001) A photosynthetic induction in Eucalyptus urograndis seedlings and cuttings measured by an open photoacoustic cell. Photosynthetica 39, 489–495.
| A photosynthetic induction in Eucalyptus urograndis seedlings and cuttings measured by an open photoacoustic cell.Crossref | GoogleScholarGoogle Scholar |
Berges JA, Charlebois DO, Mauzerall DC, Falkowski PG (1996) Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae. Plant Physiology 110, 689–696.
| Differential effects of nitrogen limitation on photosynthetic efficiency of photosystems I and II in microalgae.Crossref | GoogleScholarGoogle Scholar | 12226211PubMed |
Blankenship RE (2014) ‘Molecular mechanisms of photosynthesis.’, 2nd edn. pp. 320. (Wiley Blackwell: UK)
Boucher N, Carpentier R (1999) Hg2+, Cu2+, and Pb2+-induced changes in photosystem II photochemical yield and energy storage in isolated thylakoid membranes: a study using simultaneous fluorescence and photoacoustic measurements. Photosynthesis Research 59, 167–174.
| Hg2+, Cu2+, and Pb2+-induced changes in photosystem II photochemical yield and energy storage in isolated thylakoid membranes: a study using simultaneous fluorescence and photoacoustic measurements.Crossref | GoogleScholarGoogle Scholar |
Bukhov NG, Boucher N, Carpentier R (1996) Transformation of the photoacoustic signal after treatment of barley leaves with methylviologen or high temperatures. Photochemistry and Photobiology 63, 296–301.
| Transformation of the photoacoustic signal after treatment of barley leaves with methylviologen or high temperatures.Crossref | GoogleScholarGoogle Scholar |
Bults G, Horwitz BA, Malkin S, Cahen D (1982) Photoacoustic measurements of photosynthetic activities in whole leaves. Photochemistry and gas exchange. Biochimica et Biophysica Acta (BBA) – Bioenergetics 679, 452–465.
| Photoacoustic measurements of photosynthetic activities in whole leaves. Photochemistry and gas exchange.Crossref | GoogleScholarGoogle Scholar |
Buschmann C (1999) Thermal dissipation related to chlorophyll fluorescence and photosynthesis. Bulgarian Journal of Plant Physiology 25, 77–88.
Canaani O, Malkin S, Mauzerall D (1988) Pulsed photoacoustic detection of flash-induced oxygen evolution from intact leaves and its oscillations. Proceedings of the National Academy of Sciences of the United States of America 85, 4725–4729.
| Pulsed photoacoustic detection of flash-induced oxygen evolution from intact leaves and its oscillations.Crossref | GoogleScholarGoogle Scholar | 16593952PubMed |
Cha Y, Mauzerall DC (1992) Energy storage of linear and cyclic electron flows in photosynthesis. Plant Physiology 100, 1869–1877.
| Energy storage of linear and cyclic electron flows in photosynthesis.Crossref | GoogleScholarGoogle Scholar | 16653211PubMed |
Chikov VI, Akhtyamova GA (2019) Photorespiration and its role in the regulation of photosynthesis and plant productivity. American Journal of Plant Sciences 10, 2179–2202.
| Photorespiration and its role in the regulation of photosynthesis and plant productivity.Crossref | GoogleScholarGoogle Scholar |
Chu H-A, Chiu Y-F (2016) The roles of cytochrome b559 in assembly and photoprotection of photosystem II revealed by site-directed mutagenesis studies. Frontiers in Plant Science 6, 1261
| The roles of cytochrome b559 in assembly and photoprotection of photosystem II revealed by site-directed mutagenesis studies.Crossref | GoogleScholarGoogle Scholar | 26793230PubMed |
Chu Z, Lu Y, Chang J, Wang M, Jiang H, He J, Peng C, Ge Y (2011) Leaf respiration/photosynthesis relationship and variation: an investigation of 39 woody and herbaceous species in east subtropical China. Trees 25, 301–310.
| Leaf respiration/photosynthesis relationship and variation: an investigation of 39 woody and herbaceous species in east subtropical China.Crossref | GoogleScholarGoogle Scholar |
Clarke JE, Johnson GN (2001) In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley. Planta 212, 808–816.
| In vivo temperature dependence of cyclic and pseudocyclic electron transport in barley.Crossref | GoogleScholarGoogle Scholar | 11346955PubMed |
Curien G, Flori S, Villanova V, Magneschi L, Giustini C, Forti G, Matringe M, Petroutsos D, Kuntz M, Finazzi G (2016) The water to water cycles in microalgae. Plant and Cell Physiology 57, 1354–1363.
| The water to water cycles in microalgae.Crossref | GoogleScholarGoogle Scholar | 26955846PubMed |
Delosme R (2003) On some aspects of photosynthesis revealed by photoacoustic studies: a critical evaluation. Photosynthesis Research 76, 289–301.
| On some aspects of photosynthesis revealed by photoacoustic studies: a critical evaluation.Crossref | GoogleScholarGoogle Scholar | 16228588PubMed |
Falkowski PG, Fujita Y, Ley A, Mauzerall D (1986) Evidence for cyclic electron flow around photosystem II in Chlorella pyrenoidosa. Plant physiology 81, 310–312.
| Evidence for cyclic electron flow around photosystem II in Chlorella pyrenoidosa.Crossref | GoogleScholarGoogle Scholar | 16664797PubMed |
Frandas A, Jalink H, van der Schoor R (1997) Low frequency photoacoustics for monitoring thephotobaric component in vivo of green leaves. Photosynthesis Research 52, 65–67.
| Low frequency photoacoustics for monitoring thephotobaric component in vivo of green leaves.Crossref | GoogleScholarGoogle Scholar |
Govingee (2004) Chlorophyll a fluorescence: a bit of basic sand history. In ‘Chlorophyll a fluorescence: a signature of photosynthesis’. (Eds GC Papageorgiou, Govindje) pp. 2–32. (Springer: The Netherlands).
| Crossref |
Han T (2002) Portable dual frequency photoacoustic spectrometer. United States Patent 20020093658 A1.
Havaux М (1998) Probing electron transport through and around photosystem II in vivo by the combined use of photoacoustic spectroscopy and chlorophyll fluorometry. Israel Journal of Chemistry 38, 247–256.
| Probing electron transport through and around photosystem II in vivo by the combined use of photoacoustic spectroscopy and chlorophyll fluorometry.Crossref | GoogleScholarGoogle Scholar |
Herbert SK, Fork DC, Malkin S (1990) Photoacoustic measurements in vivo of energy storage by cyclic electron flow in algae and higher plants. Plant Physiology 94, 926–934.
| Photoacoustic measurements in vivo of energy storage by cyclic electron flow in algae and higher plants.Crossref | GoogleScholarGoogle Scholar | 16667873PubMed |
Hou HJM, Sakmar TP (2010) Methodology of pulsed photoacoustics and its application to probe photosystems and receptors. Sensors 10, 5642–5667.
| Methodology of pulsed photoacoustics and its application to probe photosystems and receptors.Crossref | GoogleScholarGoogle Scholar |
Ibaraki Y, Murakami J (2007) Distribution of chlorophyll fluorescence parameter Fv/Fm within individual plants under various stress conditions. Acta Horticulturae 761, 255–260.
| Distribution of chlorophyll fluorescence parameter Fv/Fm within individual plants under various stress conditions.Crossref | GoogleScholarGoogle Scholar |
Ivanov B, Kobayashi Y, Bukhov NG, Heber U (1998) Photosystem I-dependent cyclic electron flow in intact spinach chloroplasts: occurrence, dependence on redox conditions and electron acceptors and inhibition by antimycin A. Photosynthesis Research 57, 61–70.
| Photosystem I-dependent cyclic electron flow in intact spinach chloroplasts: occurrence, dependence on redox conditions and electron acceptors and inhibition by antimycin A.Crossref | GoogleScholarGoogle Scholar |
Joët T, Cournac L, Peltier G, Havaux M (2002) Cyclic electron flow around photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex. Plant Physiology 128, 760–769.
| Cyclic electron flow around photosystem I in C3 plants. In vivo control by the redox state of chloroplasts and involvement of the NADH-dehydrogenase complex.Crossref | GoogleScholarGoogle Scholar | 11842179PubMed |
Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1807, 384–389.
| Physiology of PSI cyclic electron transport in higher plants.Crossref | GoogleScholarGoogle Scholar |
Joliot P, Johnson GN (2011) Regulation of cyclic and linear electron flow in higher plants. Proceedings of National Academy of Sciences of the United States of America 108, 13317–13322.
| Regulation of cyclic and linear electron flow in higher plants.Crossref | GoogleScholarGoogle Scholar |
Joliot P, Joliot A, Johnson G (2006) Cyclic electron transfer around photosystem I. In ‘Photosystem I. Advances in photosynthesis and respiration’. vol. 24. (Eds H John, JH Golbeck) pp. 639–656. (Springer: Dordrecht)
Junge W (2019) Oxygenic photosynthesis: history, status and perspective. Quarterly Reviews of Biophysics 52, e1
| Oxygenic photosynthesis: history, status and perspective.Crossref | GoogleScholarGoogle Scholar | 30670110PubMed |
Kalaji HM, Schansker G, Brestic M, et al. (2017) Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynthesis Research 132, 13–66.
| Frequently asked questions about chlorophyll fluorescence, the sequel.Crossref | GoogleScholarGoogle Scholar | 27815801PubMed |
Kono M, Noguchi K, Terashima I (2014) Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana. Plant and Cell Physiology 55, 990–1004.
| Roles of the cyclic electron flow around PSI (CEF-PSI) and O2-dependent alternative pathways in regulation of the photosynthetic electron flow in short-term fluctuating light in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar | 24553846PubMed |
Kou J, Takahashi S, Oguchi R, Fan D-Y, Badger MR, Chow WS (2013) Estimation of the steady-state cyclic electron flux around PSI in spinach leaf discs in white light, CO2-enriched air and other varied conditions. Functional Plant Biology 40, 1018–1028.
| Estimation of the steady-state cyclic electron flux around PSI in spinach leaf discs in white light, CO2-enriched air and other varied conditions.Crossref | GoogleScholarGoogle Scholar | 32481170PubMed |
Kou J, Takahashi S, Fan D-Y, Badger MR, Chow WS (2015) Partially dissecting the steady-state electron fluxes in photosystem I in wild-type and pgr5 and ndh mutants of Arabidopsis. Frontiers in Plant Science 6, 758
| Partially dissecting the steady-state electron fluxes in photosystem I in wild-type and pgr5 and ndh mutants of Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 26442071PubMed |
Kramer DM, Evans JR (2011) The importance of energy balance in improving photosynthetic productivity. Plant Physiology 155, 70–78.
| The importance of energy balance in improving photosynthetic productivity.Crossref | GoogleScholarGoogle Scholar | 21078862PubMed |
Kuvykin IV, Vershubskii AV, Ptushenko VV, Tikhonov AN (2008) Oxygen as an alternative electron acceptor in the photosynthetic electron transport chain of C3 plants. Biochemistry (Moscow) 73, 1063–1075.
| Oxygen as an alternative electron acceptor in the photosynthetic electron transport chain of C3 plants.Crossref | GoogleScholarGoogle Scholar | 18991552PubMed |
Lake JV (1967) Respiration of leaves during photosynthesis. I. Estimates from an electrical analogue. Australian Journal of Biological Sciences 20, 487–493.
| Respiration of leaves during photosynthesis. I. Estimates from an electrical analogue.Crossref | GoogleScholarGoogle Scholar | 6033127PubMed |
Lavaud J, van Gorkom HJ, Etienne A-L (2002) Photosystem II electron transfer cycle and chlororespiration in planktonic diatoms. Photosynthesis Research 74, 51–59.
| Photosystem II electron transfer cycle and chlororespiration in planktonic diatoms.Crossref | GoogleScholarGoogle Scholar | 16228544PubMed |
Leupold D, Teuchner K, Ehlert J, Irrgang K-D, Renger G, Lokstein H (2002) Two-photon excited fluorescence from higher electronic states of chlorophylls in photosynthetic antenna complexes: a new approach to detect strong excitonic chlorophyll a/b coupling. Biophysical Journal 82, 1580–1585.
| Two-photon excited fluorescence from higher electronic states of chlorophylls in photosynthetic antenna complexes: a new approach to detect strong excitonic chlorophyll a/b coupling.Crossref | GoogleScholarGoogle Scholar | 11867470PubMed |
Lysenko V (2012) Fluorescence kinetic parameters and cyclic electron transport in guard cell chloroplasts of chlorophyll-deficient leaf tissues from variegated weeping fig (Ficus benjamina L.). Planta 235, 1023–1033.
| Fluorescence kinetic parameters and cyclic electron transport in guard cell chloroplasts of chlorophyll-deficient leaf tissues from variegated weeping fig (Ficus benjamina L.).Crossref | GoogleScholarGoogle Scholar | 22134781PubMed |
Lysenko V, Varduny T (2013) Anthocyanin-dependent anoxygenic photosynthesis in coloured flower petals? Scientific Reports 3, 3373
| Anthocyanin-dependent anoxygenic photosynthesis in coloured flower petals?Crossref | GoogleScholarGoogle Scholar | 24284801PubMed |
Lysenko V, Guo Y, Chugueva O (2017) Cyclic electron transport around photosystem II: mechanisms and methods of study. American Journal of Plant Physiology 12, 1–9.
| Cyclic electron transport around photosystem II: mechanisms and methods of study.Crossref | GoogleScholarGoogle Scholar |
Lysenko V, Lazár D, Varduny T (2018) A method of a bicolor fast-Fourier pulse-amplitude modulation chlorophyll fluorometry. Photosynthetica 56, 1447–1452.
| A method of a bicolor fast-Fourier pulse-amplitude modulation chlorophyll fluorometry.Crossref | GoogleScholarGoogle Scholar |
Malkin S (1996) The photoacoustic method in photosynthesis – monitoring and analysis of phenomena which lead to pressure changes following light excitation. In ‘Biophysical techniques in photosynthesis’. Chapter 12. (Eds J Amesz, AJ Hoff) pp. 191–205. (Kluwer Academic Publishers).
| Crossref |
Malkin S (1998) Attenuation of the photobaric–photoacoustic signal in leaves by oxygen-consuming processes. Israel Journal of Chemistry 38, 261–268.
| Attenuation of the photobaric–photoacoustic signal in leaves by oxygen-consuming processes.Crossref | GoogleScholarGoogle Scholar |
Malkin S, Canaani O (1994) The use and characteristics of the photoacoustic method in the study of photosynthesis. Annual Review of Plant Physiology and Plant Molecular Biology 45, 493–526.
| The use and characteristics of the photoacoustic method in the study of photosynthesis.Crossref | GoogleScholarGoogle Scholar |
Miyake C, Okamura M (2003) Cyclic electron flow within PSII protects PSII from its photoinhibition in thylakoid membranes from spinach chloroplasts. Plant and Cell Physiology 44, 457–462.
| Cyclic electron flow within PSII protects PSII from its photoinhibition in thylakoid membranes from spinach chloroplasts.Crossref | GoogleScholarGoogle Scholar | 12721388PubMed |
Miyake C, Miyata M, Shinzaki Y, Tomizawa K (2005) CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves – relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of chl fluorescence. Plant and Cell Physiology 46, 629–637.
| CO2 response of cyclic electron flow around PSI (CEF-PSI) in tobacco leaves – relative electron fluxes through PSI and PSII determine the magnitude of non-photochemical quenching (NPQ) of chl fluorescence.Crossref | GoogleScholarGoogle Scholar | 15701657PubMed |
Moss DA, Bendall DS (1984) Cyclic electron transport in chloroplasts. The Q-cycle and the site of action of antimycin. Biochimica et Biophysica Acta (BBA) – Bioenergetics 767, 389–395.
| Cyclic electron transport in chloroplasts. The Q-cycle and the site of action of antimycin.Crossref | GoogleScholarGoogle Scholar |
Munekage Y, Shikanai T (2005) Cyclic electron transport through photosystem I. Plant Biotechnology 22, 361–369.
| Cyclic electron transport through photosystem I.Crossref | GoogleScholarGoogle Scholar |
Nawrocki WJ, Tourasse NJ, Taly A, Rappaport F, Wollman F-A (2015) The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology. Annual Review of Plant Biology 66, 49–74.
| The plastid terminal oxidase: its elusive function points to multiple contributions to plastid physiology.Crossref | GoogleScholarGoogle Scholar | 25580838PubMed |
Nemeskéri E, Neményi A, Bőcs A, Zoltán Pék Z, Helyes L (2019) Physiological factors and their relationship with the productivity of processing tomato under different water supplies. Water 11, 586
| Physiological factors and their relationship with the productivity of processing tomato under different water supplies.Crossref | GoogleScholarGoogle Scholar |
Onno Feikema W, Marosvölgyi MA, Lavaud J, van Gorkom HJ (2006) Cyclic electron transfer in photosystem II in the marine diatom Phaeodactylum tricornutum. Biochimica Biophysica Acta – Bioenergetics 1757, 829–834.
| Cyclic electron transfer in photosystem II in the marine diatom Phaeodactylum tricornutum.Crossref | GoogleScholarGoogle Scholar |
Pal A, Singh S, Atta K, Gaikwad D, Monda K (2020) Cyanofix: cyanobacterial nitrogen fixation. Agriculture Observer 1, 53–56.
Pettai H, Oja V, Freiberg A, Laisk A (2005) Photosynthetic activity of far-red light in green plants. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1708, 311–321.
| Photosynthetic activity of far-red light in green plants.Crossref | GoogleScholarGoogle Scholar |
Pinchasov-Grinblat Y, Dubinsky Z (2013) Photoacoustics – a novel tool for the study of aquatic photosynthesis. In ‘Photosynthesis’. (Ed. Z Dubinsky) pp. 285–296. (InTech).
| Crossref |
Pospíšil P (2011) Enzymatic function of cytochrome b559 in photosystem II. Journal of Photochemistry and Photobiology B: Biology 104, 341–347.
| Enzymatic function of cytochrome b559 in photosystem II.Crossref | GoogleScholarGoogle Scholar |
Prasil О, Kolber Z, Berry JA, Falkowski PG (1996) Cyclic electron flow around photosystem II in vivo. Photosynthesis Researches 48, 395–410.
| Cyclic electron flow around photosystem II in vivo.Crossref | GoogleScholarGoogle Scholar |
Rochaix J-D (2011) Regulation of photosynthetic electron transport. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1807, 375–383.
| Regulation of photosynthetic electron transport.Crossref | GoogleScholarGoogle Scholar |
Schreiber U (2004) Pulse-amplitude-modulation (PAM) fluorometry and saturation pulse method: an overview. In ‘Chlorophyll a fluorescence: a signature of photosynthesis’. (Eds GC Papageorgiou, Govindje) pp. 279–319. (Springer: The Netherlands).
| Crossref |
Sinclair J, Sarai A, Garland S (1979) A backflow of electrons around photosystem II in Chlorells cells. Biochimica et Biophysica Acta (BBA) – Bioenergetics 546, 256–269.
| A backflow of electrons around photosystem II in Chlorells cells.Crossref | GoogleScholarGoogle Scholar |
Sipka G, Magyar M, Mezzetti A, Akhtar P, Zhu Q, Xiao Y, Han G, Santabarbara S, Shen J-R, Lambrev PH, Garab G (2021) Light-adapted charge-separated state of photosystem II: structural and functional dynamics of the closed reaction center. The Plant Cell 33, 1286–1302.
| Light-adapted charge-separated state of photosystem II: structural and functional dynamics of the closed reaction center.Crossref | GoogleScholarGoogle Scholar | 33793891PubMed |
Takagi D, Ifuku K, Nishimura T, Miyake C (2019) Antimycin A inhibits cytochrome b559-mediated cyclic electron flow within photosystem II. Photosynthesis Research 139, 487–498.
| Antimycin A inhibits cytochrome b559-mediated cyclic electron flow within photosystem II.Crossref | GoogleScholarGoogle Scholar | 29790043PubMed |
Thapper A, Mamedov F, Mokvist F, Hammarström L, Styring S (2009) Defining the far-red limit of photosystem II in spinach. The Plant Cell 21, 2391–2401.
| Defining the far-red limit of photosystem II in spinach.Crossref | GoogleScholarGoogle Scholar | 19700631PubMed |
Zhang M-M, Fan D-Y, Sun G-Y, Chow WS (2018) Optimising the linear electron transport rate measured by chlorophyll a fluorescence to empirically match the gross rate of oxygen evolution in white light: towards improved estimation of the cyclic electron flux around photosystem I in leaves. Functional Plant Biology 45, 1138–1148.
| Optimising the linear electron transport rate measured by chlorophyll a fluorescence to empirically match the gross rate of oxygen evolution in white light: towards improved estimation of the cyclic electron flux around photosystem I in leaves.Crossref | GoogleScholarGoogle Scholar | 32290975PubMed |
Zhen S, Bugbee B (2020) Far-red photons have equivalent efficiency to traditional photosynthetic photons: implications for redefining photosynthetically active radiation. Plant, Cell & Environment 43, 1259–1272.
| Far-red photons have equivalent efficiency to traditional photosynthetic photons: implications for redefining photosynthetically active radiation.Crossref | GoogleScholarGoogle Scholar |
