[en] Phosphorus deficiency induces biochemical and morphological changes which affect crop yield and production. Prompt fluorescence signal characterizes the PSII activity and electron transport from PSII to PSI, while the modulated light reflection at 820 (MR 820) nm investigates the redox state of photosystem I (PSI) and plastocyanin (PC). Therefore, combining information from modulated reflection at 820 nm with chlorophyll a fluorescence can potentially provide a more complete understanding of the photosynthetic process and integrating other plant physiological measurements may help to increase the accuracy of detecting the phosphorus deficiency in wheat leaves. In our study, we combined the chlorophyll a fluorescence and MR 820 signals to study the response of wheat plants to phosphorus deficiency as indirect tools for phosphorus plant status characterization. In addition, we studied the changes in chlorophyll content index, stomatal conductance (gs), root morphology, and biomass of wheat plants. The results showed an alteration in the electron transport chain as a specific response to P deficiency in the I-P phase during the reduction of the acceptor side of PSI. Furthermore, P deficiency increased parameters related to the energy fluxes per reaction centers, namely ETo/RC, REo/RC, ABS/RC, and DIo/RC. P deficiency increased the values of MRmin and MRmax and decreased νred, which implies that the reduction of PSI and PC became slower as the phosphorus decreased. The principal component analysis of the modulated reflection and chlorophyll a fluorescence parameters, with the integration of the growth parameters as supplementary variables, accounted for over 71% of the total variance in our phosphorus data using two components and provided a reliable information on PSII and PSI photochemistry under P deficiency.
El-Mejjaouy, Yousra ; Université de Liège - ULiège > TERRA Research Centre ; AgoBioSciences, Plant Stress Physiology Laboratory, University Mohammed VI Polytechnic (UM6P), Benguerir, Morocco
Belmrhar, Laila; AgoBioSciences, Plant Stress Physiology Laboratory, University Mohammed VI Polytechnic (UM6P), Benguerir, Morocco
Zeroual, Youssef; AgoBioSciences, Plant Stress Physiology Laboratory, University Mohammed VI Polytechnic (UM6P), Benguerir, Morocco
Dumont, Benjamin ; Université de Liège - ULiège > TERRA Research Centre > Plant Sciences
Mercatoris, Benoît ; Université de Liège - ULiège > TERRA Research Centre > Biosystems Dynamics and Exchanges (BIODYNE)
Oukarroum, Abdallah ; AgoBioSciences, Plant Stress Physiology Laboratory, University Mohammed VI Polytechnic (UM6P), Benguerir, Morocco ; High Throughput Multidisciplinary Research Laboratory, University Mohammed VI Polytechnic (UM6P), Benguerir, Morocco
Language :
English
Title :
PCA-based detection of phosphorous deficiency in wheat plants using prompt fluorescence and 820 nm modulated reflection signals.
OCP - OCP Group SA [MA] Prayon [BE] UM6P [MA] ULiège - Université de Liège [BE]
Funding text :
This work was supported by the Funders of the SoilPhorLife Program, OCP Group (https:// www.ocpgroup.ma/) and Prayon (https://www. prayon.com/en/company/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. For the chemical analysis of soil and plant samples, the authors acknowledge the assistance of Mr Aziz Soulaimani and Mrs Sabah Fathallah.
Hammond JP, White PJ. Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot. 2008; 59: 93–109. https://doi.org/10.1093/jxb/erm221 PMID: 18212031
Asomaning SK. Processes and Factors Affecting Phosphorus Sorption in Soils. Sorption in 2020s. 2020; 45: 1–16. https://doi.org/10.5772/INTECHOPEN.90719
Shen J, Yuan L, Zhang J, Li H, Bai Z, Chen X, et al. Phosphorus dynamics: From soil to plant. Plant Physiol. 2011; 156: 997–1005. https://doi.org/10.1104/pp.111.175232 PMID: 21571668
Bindraban PS, Dimkpa CO, Pandey R. Exploring phosphorus fertilizers and fertilization strategies for improved human and environmental health. Biology and Fertility of Soils. Springer; 2020. pp. 299–317. https://doi.org/10.1007/s00374-019-01430-2
Torres-Dorante LO, Claassen N, Steingrobe B, Olfs H-W. Fertilizer-use efficiency of different inorganic polyphosphate sources: effects on soil P availability and plant P acquisition during early growth of corn. J Plant Nutr Soil Sci. 2006; 169: 509–515. https://doi.org/10.1002/JPLN.200520584
Sobczak A, Kowalczyk K, Gajc-Wolska J, Kowalczyk W, Niedzinska M. Growth, yield and quality of sweet pepper fruits fertilized with polyphosphates in hydroponic cultivation with led lighting. Agronomy. 2020; 10. https://doi.org/10.3390/agronomy10101560
Vance CP. Symbiotic nitrogen fixation and phosphorus acquisition. Plant nutrition in a world of declining renewable resources. Plant Physiology. Plant Physiol; 2001. pp. 390–397. https://doi.org/10.1104/pp. 010331 PMID: 11598215
VANCE CP. Energy requirement for symbiotic nitrogen fixation. Plant Physiol. 2011; 127: 390–397. https://doi.org/10.1038/267149A0
Sitko K, Gieroń Ż, Szopiński M, Zieleźnik-Rusinowska P, Rusinowski S, Pogrzeba M, et al. Influence of short-term macronutrient deprivation in maize on photosynthetic characteristics, transpiration and pigment content. Sci Reports 2019 91. 2019; 9: 1–12. https://doi.org/10.1038/s41598-019-50579-1 PMID: 31578358
Veronica N, Subrahmanyam D, Vishnu Kiran T, Yugandhar P, Bhadana VP, Padma V, et al. Influence of low phosphorus concentration on leaf photosynthetic characteristics and antioxidant response of rice genotypes. Photosynth 2017 552. 2016; 55: 285–293. https://doi.org/10.1007/S11099-016-0640-4
Hodges D., Nozzolillo C. Anthocyanin and Anthocyanoplast Content of Cruciferous Seedlings Subjected to Mineral Nutrient Deficiencies. J Plant Physiol. 1996; 147: 749–754. https://doi.org/10.1016/ S0176-1617(11)81488-4
Neuner G, Larcher W. Determination of Differences in Chilling Susceptibility of Two Soybean Varieties by Means of in vivo Chlorophyll Fluorescence Measurements. J Agron Crop Sci. 1990; 164: 73–80. https://doi.org/10.1111/J.1439-037X.1990.TB00788.X
Kalaji HM, Schansker G, Brestic M, Bussotti Filippo, Calatayud A, Lorenzo Ferroni, et al. Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynth Res. 2017; 132: 13–66. https://doi.org/10.1007/s11120-016-0318-y PMID: 27815801
Kalaji HM, Oukarroum A, Alexandrov V, Kouzmanova M, Brestic M, Zivcak M, et al. Identification of nutrient deficiency in maize and tomato plants by invivo chlorophyll a fluorescence measurements. Plant Physiol Biochem. 2014; 81: 16–25. https://doi.org/10.1016/j.plaphy.2014.03.029 PMID: 24811616
Frydenvang J, van Maarschalkerweerd M, Carstensen A, Mundus S, Schmidt SB, Pedas PR, et al. Sensitive detection of phosphorus deficiency in plants using chlorophyll a fluorescence. Plant Physiol. 2015; 169: 353–361. https://doi.org/10.1104/pp.15.00823 PMID: 26162430
Salvatori E, Fusaro L, Gottardini E, Pollastrini M, Goltsev V, Strasser RJ, et al. Plant stress analysis: Application of prompt, delayed chlorophyll fluorescence and 820 nm modulated reflectance. Insights from independent experiments. Plant Physiol Biochem. 2014; 85: 105–113. https://doi.org/10.1016/j.plaphy.2014.11.002 PMID: 25463266
Goltsev V, Zaharieva I, Chernev P, Kouzmanova M, Kalaji HM, Yordanov I, et al. Drought-induced modifications of photosynthetic electron transport in intact leaves: Analysis and use of neural networks as a tool for a rapid non-invasive estimation. Biochim Biophys Acta—Bioenerg. 2012; 1817: 1490–1498. https://doi.org/10.1016/j.bbabio.2012.04.018 PMID: 22609146
Kalaji HM, Goltsev V, Bosa K, Allakhverdiev Suleyman I, Reto, et al. Experimental in vivo measurements of light emission in plants: a perspective dedicated to David Walker. Photosynth Res 2012 1142. 2012; 114: 69–96. https://doi.org/10.1007/s11120-012-9780-3 PMID: 23065335
Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska IA, et al. Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiol Plant 2016 384. 2016; 38: 1–11. https://doi.org/10.1007/S11738-016-2113-Y
Stirbet A, Lazár D, Kromdijk J, Govindjee. Chlorophyll a fluorescence induction: Can just a one-second measurement be used to quantify abiotic stress responses? Photosynth 2018 561. 2018; 56: 86–104. https://doi.org/10.1007/S11099-018-0770-3
El-Mejjaouy Y, Lahrir M, Naciri R, Zeroual Y, Mercatoris B, Dumont B, et al. How far can chlorophyll a fluorescence detect phosphorus status in wheat leaves (Triticum durum L.). Environ Exp Bot. 2022; 194: 104762. https://doi.org/10.1016/J.ENVEXPBOT.2021.104762
Horaczek T, Dąbrowski P, Kalaji HM, Baczewska-Dąbrowska AH, Pietkiewicz S, Stępień W, et al. JIP-test as a tool for early detection of the macronutrients deficiencin miscanthus plants. Photosynthetica. 2020; 58: 507–517. https://doi.org/10.32615/ps.2019.177
Kusaka M, Kalaji HM, Mastalerczuk G, Dąbrowski P, Kowalczyk K. Potassium deficiency impact on the photosynthetic apparatus efficieof radish. Photosynthetica. 2021; 59: 127–136. https://doi.org/10.32615/ps.2020.077
Feng X, An Y, Gao J, Wang L. Photosynthetic Responses of Canola to Exogenous Application or Endogenous Overproduction of 5-Aminolevulinic Acid (ALA) under Various Nitrogen Levels. Plants (Basel, Switzerland). 2020; 9: 1–14. https://doi.org/10.3390/plants9111419 PMID: 33114095
Dąbrowski P, Baczewska-Dąbrowska AH, Bussotti F, Pollastrini M, Piekut K, Kowalik W, et al. Photosynthetic efficiency of Microcystis ssp. under salt stress. Environ Exp Bot. 2021; 186. https://doi.org/10.1016/J.ENVEXPBOT.2021.104459
Schansker G, Ohnishi M, Furutani R, Miyake C. Identification of Twelve Different Mineral Deficiencies in Hydroponically Grown Sunflower Plants on the Basis of Short Measurements of the Fluorescence and P700 Oxidation/Reduction Kinetics. Front Plant Sci. 2022; 13: 894607. https://doi.org/10.3389/fpls.2022.894607 PMID: 35720579
Strasser RJ, Tsimilli-Michael M, Qiang S, Goltsev V. Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensis. Biochim Biophys Acta—Bioenerg. 2010; 1797: 1313–1326. https://doi.org/10.1016/j.bbabio.2010.03.008 PMID: 20226756
Oukarroum A, Goltsev V, Strasser RJ. Temperature Effects on Pea Plants Probed by Simultaneous Measurements of the Kinetics of Prompt Fluorescence, Delayed Fluorescence and Modulated 820 nm Reflection. PLoS One. 2013; 8: e59433. https://doi.org/10.1371/journal.pone.0059433 PMID: 23527194
Delosme R. Étude de l’induction de fluorescence des algues vertes et des chloroplastes au début d’une illumination intense. Biochim Biophys Acta—Bioenerg. 1967; 143: 108–128. https://doi.org/10.1016/ 0005-2728(67)90115-6
Lazár D, Sušila P, Nauš J. Early detection of plant stress from changes in distributions of chlorophyll a fluorescence parameters measured with fluorescence imaging. Journal of Fluorescence. J Fluoresc; 2006. pp. 173–176. https://doi.org/10.1007/s10895-005-0032-1 PMID: 16575551
Schreiber U, Neubauer C. The Polyphasic Rise of Chlorophyll Fluorescence upon Onset of Strong Continuous Illumination: II. Partial Control by the Photosystem II Donor Side and Possible Ways of Interpretation. Zeitschrift für Naturforsch C. 1987; 42: 1255–1264. https://doi.org/10.1515/ZNC-1987-11-1218
Strasser RJ, Tsimilli-Michael M, Srivastava A. Analysis of the Chlorophyll a Fluorescence Transient. Advances in Photosynthesis and Respiration. Springer, Dordrecht; 2004. pp. 321–362.
Schansker G, Srivastava A, Strasser RJ. Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Funct Plant Biol. 2003; 30: 785–796. https://doi.org/10.1071/FP03032 PMID: 32689062
Schreiber U, Neubauer C, Klughammer C. Devices and methods for room-temperature fluorescence analysis. Philos Trans R Soc London B, Biol Sci. 1989; 323: 241–251. https://doi.org/10.1098/RSTB.1989.0007
Chen S, Yang J, Zhang M, Strasser RJ, Qiang S. Classification and characteristics of heat tolerance in Ageratina adenophora populations using fast chlorophyll a fluorescence rise O-J-I-P. Environ Exp Bot. 2016; 122: 126–140. https://doi.org/10.1016/J.ENVEXPBOT.2015.09.011
Lyu Y, Tang H, Li H, Zhang F, Rengel Z, Whalley WR, et al. Major Crop Species Show Differential Balance between Root Morphological and Physiological Responses to Variable Phosphorus Supply. Front Plant Sci. 2016; 7: 1939. https://doi.org/10.3389/fpls.2016.01939 PMID: 28066491
Meng X, Chen W-W, Wang Y-Y, Huang Z-R, Ye X, Chen L-S, et al. Effects of phosphorus deficiency on the absorption of mineral nutrients, photosynthetic system performance and antioxidant metabolism in Citrus grandis. PLoS One. 2021; 16: e0246944. https://doi.org/10.1371/journal.pone.0246944 PMID: 33596244
Péret B, Clément M, Nussaume N, Desnos T. Root developmental adaptation to phosphate starvation: better safe than sorry. Trends Plant Sci. 2011; 16: 442–450. https://doi.org/10.1016/j.tplants.2011.05. 006 PMID: 21684794
Vance CP, Uhde-Stone C, Allan DL. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource. New Phytol. 2003; 157: 423–447. https://doi.org/10.1046/j.14698137.2003.00695.x PMID: 33873400
Wissuwa M, Gamat G, Ismail AM. Is root growth under phosphorus deficiency affected by source or sink limitations? J Exp Bot. 2005; 56: 1943–1950. https://doi.org/10.1093/jxb/eri189 PMID: 15911558
Chtouki M, Naciri R, Garré S, Nguyen F, Oukarroum A. Chickpea plant responses to polyphosphate fertiliser forms and drip fertigation frequencies: effect on photosynthetic performance and phenotypic traits. Funct Plant Biol. 2021 [cited 14 Jul 2021]. https://doi.org/10.1071/fp21035 PMID: 34147138
Bessa LA, Moreira MA, Silva FG, Mota CS, Vitorino LC. Growth, nutrient concentration and principal component analysis of Cagaita (Eugenia dysenterica DC.) seedlings grown in nutrient solution. Aust J Crop Sci. 2016; 10: 425–433. https://doi.org/10.21475/ajcs.2016.10.03.p7477
Ticconi CA, Abel S. Short on phosphate: plant surveillance and countermeasures. Trends Plant Sci. 2004; 9: 548–555. https://doi.org/10.1016/j.tplants.2004.09.003 PMID: 15501180
Balemi T, Negisho K. Management of soil phosphorus and plant adaptation mechanisms to phosphorus stress for sustainable crop production: a review. J soil Sci plant Nutr. 2012; 12: 547–562. https://doi.org/10.4067/S0718-95162012005000015
Reddy VRP, Aski MS, Mishra GP, Dikshit HK, Singh A, Pandey R, et al. Genetic variation for root architectural traits in response to phosphorus deficiency in mungbean at the seedling stage. PLoS One. 2020; 15: e0221008. https://doi.org/10.1371/journal.pone.0221008 PMID: 32525951
Daszkowska-Golec A, Szarejko I. Open or Close the Gate—Stomata Action Under the Control of Phytohormones in Drought Stress Conditions. Front Plant Sci. 2013; 4: 138. https://doi.org/10.3389/fpls.2013.00138 PMID: 23717320
Schansker G, Tóth SZ, Strasser RJ. Methylviologen and dibromothymoquinone treatments of pea leaves reveal the role of photosystem I in the Chl a fluorescence rise OJIP. Biochim Biophys Acta—Bioenerg. 2005; 1706: 250–261. https://doi.org/10.1016/j.bbabio.2004.11.006 PMID: 15694353
Soudek P, Hrdinová A, Rodriguez Valseca IM, Lhotáková Z, Mihaljevič M, Petrová, et al. Thorium as an environment stressor for growth of Nicotiana glutinosa plants. Environ Exp Bot. 2019; 164: 84–100. https://doi.org/10.1016/J.ENVEXPBOT.2019.03.027
Cetner MD, Kalaji HM, Borucki W, Kowalczyk K. Phosphorus deficiency affects the i-step of chlorophyll a fluorescence induction curve of radish. Photosynthetica. 2020; 58: 671–681. https://doi.org/10.32615/ps.2020.015
Bussotti F, Gerosa G, Digrado A, Pollastrini M. Selection of chlorophyll fluorescence parameters as indicators of photosynthetic efficiency in large scale plant ecological studies. Ecol Indic. 2020; 108. https://doi.org/10.1016/j.ecolind.2019.105686
Zivcak M, Brestic M, Kunderlikova K, Olsovska K, Allakhverdiev SI. Effect of photosystem I inactivation on chlorophyll a fluorescence induction in wheat leaves: Does activity of photosystem I play any role in OJIP rise? J Photochem Photobiol B Biol. 2015; 152: 318–324. https://doi.org/10.1016/j.jphotobiol.2015.08.024 PMID: 26388470
Carstensen A, Herdean A, Schmidt SB, Sharma A, Spetea C, Pribil M, et al. The Impacts of Phosphorus Deficiency on the Photosynthetic Electron Transport Chain. Plant Physiol. 2018; 177: 184. https://doi.org/10.1104/pp.17.01624 PMID: 29540590
Tsimilli-Michael M, Strasser RJ. In vivo assessment of stress impact on plant’s vitality: Applications in detecting and evaluating the beneficial role of mycorrhization on host plants. Mycorrhiza State Art, Genet Mol Biol Eco-Function, Biotechnol Eco-Physiology, Struct Syst (Third Ed. 2008; 679–703.
Carstensen A, Szameitat AE, Frydenvang J, Husted S. Chlorophyll a fluorescence analysis can detect phosphorus deficiency under field conditions and is an effective tool to prevent grain yield reductions in spring barley (Hordeum vulgare L.). Plant Soil. 2019; 434: 79–91. https://doi.org/10.1007/s11104-018-3783-6
He L, Yu L, Li B, Du N, Guo S. The effect of exogenous calcium on cucumber fruit quality, photosynthesis, chlorophyll fluorescence, and fast chlorophyll fluorescence during the fruiting period under hypoxic stress. BMC Plant Biol. 2018; 18. https://doi.org/10.1186/s12870-018-1393-3 PMID: 30180797
Ceppi MG, Oukarroum A, Çiçek N, Strasser RJ, Schansker G. The IP amplitude of the fluorescence rise OJIP is sensitive to changes in the photosystem I content of leaves: a study on plants exposed to magnesium and sulfate deficiencies, drought stress and salt stress. Physiol Plant. 2012; 144: 277–288. https://doi.org/10.1111/j.1399-3054.2011.01549.x PMID: 22121914
Oukarroum A, Madidi SEL, Strasser RJ. Drought stress induced in barley cultivars (Hordeum vulgare L.) by polyethylene glycol, probed by germination, root length and chlorophyll a fluorescence rise (OJIP). 2006; 59: 65–74.
Stirbet A, Govindjee. On the relation between the Kautsky effect (chlorophyll a fluorescence induction) and Photosystem II: basics and applications of the OJIP fluorescence transient. J Photochem Photobiol B. 2011; 104: 236–257. https://doi.org/10.1016/j.jphotobiol.2010.12.010 PMID: 21295993
Lazár D. Simulations show that a small part of variable chlorophyll a fluorescence originates in photosystem I and contributes to overall fluorescence rise. J Theor Biol. 2013; 335: 249–264. https://doi.org/10.1016/j.jtbi.2013.06.028 PMID: 23820035
Gomes MTG, da Luz AC, dos Santos MR, do Carmo Pimentel Batitucci M, Silva DM, Falqueto AR. Drought tolerance of passion fruit plants assessed by the OJIP chlorophyll a fluorescence transient. Sci Hortic (Amsterdam). 2012; 142: 49–56. https://doi.org/10.1016/J.SCIENTA.2012.04.026
Dimitrova S, Paunov M, Pavlova B, Dankov K, Kouzmanova M, Velikova V, et al. Photosynthetic efficiency of two platanus orientalis l. Ecotypes exposed to moderately high temperature—jip-test analysis. Photosynthetica. 2020; 58: 657–670. https://doi.org/10.32615/ps.2020.012
Kumar D, Singh H, Raj S, Soni V. Chlorophyll a fluorescence kinetics of mung bean (Vigna radiata L.) grown under artificial continuous light. Biochem Biophys Reports. 2020; 24: 100813. https://doi.org/10.1016/j.bbrep.2020.100813 PMID: 32984559
Ivorra N, Barranguet C, Jonker M, Kraak MHS, Admiraal W. Metal-induced tolerance in the freshwater microbenthic diatom Gomphonema parvulum. Environ Pollut. 2002; 116: 147–157. https://doi.org/10.1016/s0269-7491(01)00152-x PMID: 11817361
Zhao L-S, Li K, Wang Q-M, Song X-Y, Su H-N, Xie B-B, et al. Nitrogen Starvation Impacts the Photosynthetic Performance of Porphyridium cruentum as Revealed by Chlorophyll a Fluorescence. Sci Reports 2017 71. 2017; 7: 1–11. https://doi.org/10.1038/s41598-017-08428-6 PMID: 28819147
Singh SK, Reddy VR, Fleisher DH, Timlin DJ. Relationship between photosynthetic pigments and chlorophyll fluorescence in soybean under varying phosphorus nutrition at ambient and elevated CO2. Photosynthetica. 2017; 55: 421–433. https://doi.org/10.1007/S11099-016-0657-0
Gao J, Li P, Ma F, Goltsev V. Photosynthetic performance during leaf expansion in Malus micromalus probed by chlorophyll a fluorescence and modulated 820 nm reflection. J Photochem Photobiol B Biol. 2014; 137: 144–150. https://doi.org/10.1016/J.JPHOTOBIOL.2013.12.005 PMID: 24373888
Dąbrowski P, Baczewska-Dąbrowska AH, Kalaji HM, Goltsev V, Paunov M, Rapacz M, et al. Exploration of Chlorophyll a Fluorescence and Plant Gas Exchange Parameters as Indicators of Drought Tolerance in Perennial Ryegrass. Sensors 2019, Vol 19, Page 2736. 2019; 19: 2736. https://doi.org/10.3390/ s19122736 PMID: 31216685
