Abstract
Photosynthesis and stomata dynamically respond to transient changes in light intensity; however, information regarding their long-term responses to the light intensity is limited. In the current study, biophysical properties of photosynthetic apparatus and stomatal characteristics of lettuce plants were investigated in response to long-term exposure to different photosynthetic photon flux densities (PPFDs) [75, 150, 300, and 600 µmol m−2 s−1]. Contrary to leaf growth, SLA decreased with increasing light intensity (i.e., thicker leaves under higher light intensity). Improving effect of higher light intensity on leaf fresh and dry weights was time dependent, in a way that the largest difference in biomass gain was observed following 40 days of exposure to the light treatments. Depending on the leaf developmental stages, exposure to higher light intensities caused faster development of photosynthesis system [in terms of improvement in the maximum quantum efficiency of photosystem II (PSII) and non-photochemical quenching (NPQ)] compared to lower light intensities. PSII performance index on an absorption basis was the highest under 600 PPFD. Small-sized stomata with narrow pore apertures were observed in plants grown under 75 PPFD; however, due to improvement in photosynthetic capacity and also the growth of the plants, water use efficiency (WUE) increased in a light intensity-dependent manner and the highest WUE was detected in 600 PPFD-exposed plants. In conclusion, exposing lettuce plants to higher light intensities (non-stress threshold levels) results in higher accumulation of biomass, faster development of photosynthetic system, and improved WUE.
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Aliniaeifard S, van Meeteren U (2013) Can prolonged exposure to low VPD disturb the ABA signalling in stomatal guard cells? J Exp Bot 64:3551–3566
Aliniaeifard S, van Meeteren U (2014) Natural variation in stomatal response to closing stimuli among Arabidopsis thaliana accessions after exposure to low VPD as a tool to recognize the mechanism of disturbed stomatal functioning. J Exp Bot 65:6529–6542
Aliniaeifard S, van Meeteren U (2016) Stomatal characteristics and desiccation response of leaves of cut chrysanthemum (Chrysanthemum morifolium) flowers grown at high air humidity. Sci Hort 205:84–89
Aliniaeifard S, Malcolm Matamoros P, van Meeteren U (2014) Stomatal malfunctioning under low vapor pressure deficit (VPD) conditions: induced by alterations in stomatal morphology and leaf anatomy or in the ABA signaling? Physiol Plant 152:688–699
Appenroth KJ, Keresztes A, Sarvari E, Jaglarz A, Fischer W (2003) Multiple effects of chromate on Spirodela polyrhiza: electron microscopy and biochemical investigations. Plant Biol 5:315–323
Asayesh ZM, Vahdati K, Aliniaeifard S (2017) Investigation of physiological components involved in low water conservation capacity of in vitro walnut plants. Sci Hort 224:1–7
Baker NR (2008) Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annu Rev Plant Biol 59:89–113
Bertolino LT, Caine RS, Gray JE (2019) Impact of stomatal density and morphology on water-use efficiency in a changing world. Front Plant Sci 10:225. https://doi.org/10.3389/fpls.2019.00225
Beerling DJ, Royer DL (2002) Reading a CO2 signal from fossil stomata. New Phytol 153:387–397
Carvalho FE, Ware MA, Ruban AV (2015) Quantifying the dynamics of light tolerance in A rabidopsis plants during ontogenesis. Plant Cell Environ 38:2603–2617
Demarsy E, Goldschmidt-Clermont M, Ulm R (2018) Coping with ‘dark sides of the sun’ through photoreceptor signaling. Trends Plant Sci 23:260–271
Dow GJ, Bergmann DC (2014) Patterning and processes: how stomatal development defines physiological potential. Curr Opin Plant Biol 21:67–74
Fan XX, Xu ZG, Liu XY, Tang CM, Wang LW, Xl Han (2013) Effects of light intensity on the growth and leaf development of young tomato plants grown under a combination of red and blue light. Sci Hort 153:50–55
Fanourakis D, Hyldgaard B, Giday H, Aulik I, Bouranis D, Körner O, Ottosen C-O (2019) Stomatal anatomy and closing ability is affected by supplementary light intensity in rose (Rosa hybrida L.). Hort Sci 46:81–89
Fanourakis D, Aliniaeifard S, Sellin A, Giday H, Körner O, Rezaei Nejad A, Delis C, Bouranis D, Koubouris G, Kambourakis E, Nikoloudakis N, Tsaniklidis G (2020) Stomatal behavior following mid- or long-term exposure to high relative air humidity: a review. Plant Physiol Biochem 153:92–105
Franklin KA, Larner VS, Whitelam GC (2004) The signal transducing photoreceptors of plants. Int J Dev Biol 49:653–664
Franks PJ, Beerling DJ (2009) Maximum leaf conductance driven by CO2 effects on stomatal size and density over geologic time. PNAS 106:10343–10347
Franks PJ, Leitch IJ, Ruszala EM, Hetherington AM, Beerling DJ (2012) Physiological framework for adaptation of stomata to CO2 from glacial to future concentrations. Philos Trans R Soc Lond Ser B Biol Sci 367:537–546
Franks PJ, Doheny-Adams TW, Britton-Harper ZJ, Gray JE (2015) Increasing water-use efficiency directly through genetic manipulation of stomatal density. New Phytol 207:188–195
Fu W, Li P, Wu Y (2012) Effects of different light intensities on chlorophyll fluorescence characteristics and yield in lettuce. Sci Hort 135:45–51
Fukuda N, Fujita M, Ohta Y, Sase S, Nishimura S, Ezura H (2008) Directional blue light irradiation triggers epidermal cell elongation of abaxial side resulting in inhibition of leaf epinasty in geranium under red light condition. Sci Hort 115:176–182
Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta 990:87–92
Givnish TJ, Montgomery RA, Goldstein G (2004) Adaptive radiation of photosynthetic physiology in the Hawaiian lobeliads: light regimes, static light responses, and whole-plant compensation points. Am J Bot 91:228–246
Gorton HL, Williams WE, Assmann SM (1993) Circadian rhythms in stomatal responsiveness to red and blue light. Plant Physiol 103:399–406
Hattori T, Sonobe K, Inanaga S, An P, Tsuji W, Araki H, Eneji AE, Morita S (2007) Short term stomatal responses to light intensity changes and osmotic stress in sorghum seedlings raised with and without silicon. Environ Exper Bot 60:177–182
Haworth M, Elliott-Kingston C, McElwain JC (2011) The stomatal CO2 proxy does not saturate at high atmospheric CO2 concentrations: evidence from stomatal index responses of Araucariaceae conifers. Oecologia 167:11–19
Hazrati S, Tahmasebi-Sarvestani Z, Modarres-Sanavy SAM, Mokhtassi-Bidgoli A, Nicola S (2016) Effects of water stress and light intensity on chlorophyll fluorescence parameters and pigments of Aloe vera L. Plant Physiol Biochem 106:141–148
Hoenecke M, Bula R, Tibbitts T (1992) Importance of blue’ photon levels for lettuce seedlings grown under red-light-emitting diodes. HortScience 27:427–430
Jahns P, Holzwarth AR (2012) The role of the xanthophyll cycle and of lutein in photoprotection of photosystem II. Biochim Biophys Acta 1817:182–193
Kalaji HM, Bosa K, Kościelniak J, Żuk-Gołaszewska K (2011) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environ Exp Bot 73:64–72
Kalaji HM, Carpentier R, Allakhverdiev SI, Bosa K (2012) Fluorescence parameters as early indicators of light stress in barley. J Photochem Photobiol B Biol 112:1–6
Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, Cetner MD, Łukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 38:102
Kalaji MH, Goltsev VN, Zivcak M, Brestic M (2017) Chlorophyll fluorescence: understanding crop performance: basics and applications. CRC Press, Boca Raton
Kalhor M, Aliniaeifard S, Seif M, Asayesh E, Bernard F, Hassani B, Li T (2018) Enhanced salt tolerance and photosynthetic performance: implication of ɤ-amino butyric acid application in salt-exposed lettuce (Lactuca sativa L.) plants. Plant Physiol Biochem 130:157–172
Karam F, Lahoud R, Masaad R, Kabalan R, Breidi J, Chalita C, Rouphael Y (2007) Evapotranspiration, seed yield and water use efficiency of drip irrigated sunflower under full and deficit irrigation conditions. Agric Water Manag 90:213–223
Kim HH, Goins GD, Wheeler RM, Sager JC (2004) Green-light supplementation for enhanced lettuce growth under red-and blue-light-emitting diodes. HortScience 39:1617–1622
Kromdijk J, Głowacka K, Leonelli L, Gabilly ST, Iwai M, Niyogi KK, Long SP (2016) Improving photosynthesis and crop productivity by accelerating recovery from photoprotection. Science 354:857–861
Külheim C, Ågren J, Jansson S (2002) Rapid regulation of light harvesting and plant fitness in the field. Science 297:91–93
Lake JA, Quick WP, Beerling DJ, Woodward FI (2001) Signals from mature to new leaves. Nature 411:154
Lawson T, von Caemmerer S, Baroli I (2010) Photosynthesis and stomatal behaviour, Progress in botany 72. Springer, Berlin, pp 265–304
Lee SH, Tewari RK, Hahn EJ, Paek KY (2007) Photon flux density and light quality induce changes in growth, stomatal development, photosynthesis and transpiration of Withania somnifera (L.) Dunal. plantlets. Plant Cell Tissue Organ Cult 90:141–151
Lee T, Woo S, Kwak M, Inkyin K, Lee K, Jang J, Kim I (2016) Photosynthesis and chlorophyll fluorescence responses of Populus sibirica to water deficit in a desertification area in Mongolia. Photosynthetica 54:317–320
Li Y, Li H, Li Y, Zhang S (2017) Improving water-use efficiency by decreasing stomatal conductance and transpiration rate to maintain higher ear photosynthetic rate in drought-resistant wheat. Crop J 5:231–239
Lichtenthaler H, Langsdorf G, Lenk S, Buschmann C (2005) Chlorophyll fluorescence imaging of photosynthetic activity with the flash-lamp fluorescence imaging system. Photosynthetica 43:355–369
Lichtenthaler HK, Ač A, Marek MV, Kalina J, Urban O (2007) Differences in pigment composition, photosynthetic rates and chlorophyll fluorescence images of sun and shade leaves of four tree species. Plant Physiol Biochem 45:577–588
Long SP, Humphries S, Falkowski PG (1994) Photoinhibition of photosynthesis in nature. Annu Rev Plant Physiol Plant Mol Biol 45:633–662
MacIntyre HL, Kana TM, Anning T, Geider RJ (2002) Photoacclimation of photosynthesis irradiance response curves and photosynthetic pigments in microalgae and cyanobacteria 1. J Phycol 38:17–38
Martins JPR, Schimildt ER, Alexandre RS, Falqueto AR, Otoni WC (2015) Chlorophyll a fluorescence and growth of Neoregelia concentrica (Bromeliaceae) during acclimatization in response to light levels. In Vitro Cell Dev Biol Plant 51:471–481
Matos FS, Wolfgramm R, Gonçalves FV, Cavatte PC, Ventrella MC, DaMatta FM (2009) Phenotypic plasticity in response to light in the coffee tree. Environ Exp Bot 67:421–427
Meng LL, Song JF, Wen J, Zhang J, Wei, JHJP (2016) Effects of drought stress on fluorescence characteristics of photosystem II in leaves of Plectranthus scutellarioides. Photosynthetica 54: 414–421
Morais H, Medri ME, Marur CJ, Caramori PH, Ribeiro AMDA, Gomes JC (2004) Modifications on leaf anatomy of Coffea arabica caused by shade of pigeonpea (Cajanus cajan). Braz Arch Biol Technol 47:863–871
Müller P, Li XP, Niyogi KK (2001) Non-photochemical quenching. A response to excess light energy. Plant Physiol 125:1558–1566
Nardini A, Grego F, Trifilò P, Salleo S (2010) Changes of xylem sap ionic content and stem hydraulics in response to irradiance in Laurus nobilis. Tree Physiol 30:628–635
Neelam S, Subramanyam R (2013) Alteration of photochemistry and protein degradation of photosystem II from Chlamydomonas reinhardtii under high salt grown cells. J Photochem Photobiol B Biol 124:63–70
Oukarroum A, El Madidi S, Schansker G, Strasser RJ (2007) Probing the responses of barley cultivars (Hordeum vulgare L.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. Environ Exper Bot 60:438–446
Pennisi G, Orsini F, Blasioli S, Cellini A, Crepaldi A, Braschi I, Spinelli F, Nicola S, Fernandez JA, Stanghellini C (2019) Resource use efficiency of indoor lettuce (Lactuca sativa L.) cultivation as affected by red: blue ratio provided by LED lighting. Sci Rep 9:1–11
Prioul JL, Brangeon J, Reyss A (1980) Interaction between external and internal conditions in the development of photosynthetic features in a grass leaf: I. Regional responses along a leaf during and after low-light or high-light acclimation. Plant Physiol 66:762–769
Rapacz M, Sasal M, Kalaji HM, Kościelniak J (2015) Is the OJIP test a reliable indicator of winter hardiness and freezing tolerance of common wheat and triticale under variable winter environments? PLoS ONE 10:e0134820
Roach T, Krieger-Liszkay AK (2014) Regulation of photosynthetic electron transport and photoinhibition. Curr Protein Pept Sci 15:351–362
Royer DL (2003) Estimating latest Cretaceous and Tertiary atmospheric CO2 from stomatal indices.
Sack L, Tyree MT, Holbrook NM (2005) Leaf hydraulic architecture correlates with regeneration irradiance in tropical rainforest trees. New Phytol 167:403–413
Salvatore RN, Yoon CH, Jung KW (2001) Synthesis of secondary amines. Tetrahedron 57:7785–7811
Savvides A, Fanourakis D, van Ieperen W (2011) Co-ordination of hydraulic and stomatal conductances across light qualities in cucumber leaves. J Exp Bot 63:1135–1143
Savvides A, Fanourakis D, van Ieperen W (2012) Co-ordination of hydraulic and stomatal conductances across light qualities in cucumber leaves. J Exp Bot 63:1135–1143
Schoch PG, Zinsou C, Sibi M (1980) Dependence of the stomatal index on environmental factors during stomatal differentiation in leaves of Vigna sinensis L. J Exp Bot 31:1211–1216
Smith RY, Greenwood DR, Basinger JF (2010) Estimating paleoatmospheric pCO2 during the early Eocene climatic optimum from stomatal frequency of ginkgo, Okanagan highlands, British Columbia, Canada 293:120–131
Souza R, Machado E, Silva J, Lagôa A, Silveira J (2004) Photosynthetic gas exchange, chlorophyll fluorescence and some associated metabolic changes in cowpea (Vigna unguiculata) during water stress and recovery. Environ Exper Bot 51:45–56
Steinger T, Roy B, Stanton M (2003) Evolution in stressful environments II: adaptive value and costs of plasticity in response to low light in Sinapis arvensis. J Evol Biol 16:313–323
Strasser RJ, Srivastava A, Tsimilli-Michael M (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. Probing photosynthesis: mechanisms, regulation and adaptation. 445–483.
Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. Chlorophyll a fluorescence. Springer, Dordrecht, pp 321–362
Suggett DJ, Prášil O, Borowitzka MA (2010) Chlorophyll a fluorescence in aquatic sciences: methods and applications (Vol. 4). Dordrecht: Springer
Thomas PW, Woodward FI, Quick WP (2004) Systemic irradiance signalling in tobacco. New phytol 161:193–198
Urban J, Ingwers MW, McGuire MA, Teskey RO (2017) Increase in leaf temperature opens stomata and decouples net photosynthesis from stomatal conductance in Pinus taeda and Populus deltoides x nigra. J Exp Bot 68:1757–1767
van Meeteren U, Aliniaeifard S (2016) Stomata and postharvest physiology. Postharvest ripening physiology of crops 157–216.
Vass I (2012) Molecular mechanisms of photodamage in the Photosystem II complex. Biochim Biophys Acta 1817:209–217
Wang WH, Chen J, Liu TW, Han AD, Simon M, Dong XJ, He JX, Zheng HL (2014) Regulation of the calcium-sensing receptor in both stomatal movement and photosynthetic electron transport is crucial for water use efficiency and drought tolerance in Arabidopsis. J Exp Bot 65:223–234
Yu L, Chen X, Wang Z, Wang S, Wang Y, Zhu Q, Li S, Xiang C (2013) Arabidopsis enhanced drought tolerance1/HOMEODOMAIN GLABROUS11 confers drought tolerance in transgenic rice without yield Penalty. Plant Physiol 162:1378–1391
Zavala J, Ravetta D (2001) Allocation of photoassimilates to biomass, resin and carbohydrates in Grindelia chiloensis as affected by light intensity. Field Crops Res 69:143–149
Zhang S, Ma K, Chen L (2003) Response of photosynthetic plasticity of Paeonia suffruticosa to changed light environments. Environ Exper Bot 49:121–133
Zhang G, Liu Y, Ni Y, Meng Z, Lu T, Li T (2014) Exogenous calcium alleviates low night temperature stress on the photosynthetic apparatus of tomato leaves. PLoS ONE 9:97322
Acknowledgements
We would like to thank Iran National Science Foundation (INSF) (Grant Number 96006991) and University of Tehran for their supports.
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PG, SA, MM, and ME designed the experimental setup; PG, ME, and MS performed the experiments. PG, MS, BA, and ME carried out data analysis and wrote the initial draft of the manuscript. SA critically revised the manuscript and edited it to present form. All authors read and approved it for submission.
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Ghorbanzadeh, P., Aliniaeifard, S., Esmaeili, M. et al. Dependency of Growth, Water Use Efficiency, Chlorophyll Fluorescence, and Stomatal Characteristics of Lettuce Plants to Light Intensity. J Plant Growth Regul 40, 2191–2207 (2021). https://doi.org/10.1007/s00344-020-10269-z
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DOI: https://doi.org/10.1007/s00344-020-10269-z