Durum wheat; Polyphophate; Phosphorus; Photosynthetic performance; salinity; nutrient uptake
Abstract :
[en] Salt stress impacts phosphorus (P) bioavailability, mobility, and its uptake by plants. Since P is involved in many key processes in plants, salinity and P deficiency could significantly cause serious damage to photosynthesis, the most essential physiological process for the growth and development of all green plants. Different approaches have been proposed and adopted to minimize the harmful effects of their combined effect. Optimising phosphorus nutrition seems to bring positive results to improve photosynthetic efficiency and nutrient uptake. The present work posed the question if soluble fertilizers allow wheat plants to counter the adverse effect of salt stress. A pot experiment was performed using a Moroccan cultivar of durum wheat: Karim. This study focused on different growth and physiological responses of wheat plants grown under the combined effect of salinity and P-availability. Two Orthophosphates (Ortho-A & Ortho-B) and one polyphosphate (Poly-B) were applied at different P levels (0, 30 and 45 ppm). Plant growth was analysed on some physiological parameters (stomatal conductance (SC), chlorophyll content index (CCI), chlorophyll a fluorescence, shoot and root biomass, and mineral uptake). Fertilized wheat plants showed a significant increase in photosynthetic performance and nutrient uptake. Compared to salt-stressed and unfertilized plants (C+), CCI increased by 93%, 81% and 71% at 30 ppm of P in plants fertilized by Poly-B, Ortho-B and Ortho-A, respectively. The highest significant SC was obtained at 45 ppm using Ortho-B fertilizer with an increase of 232% followed by 217% and 157% for both Poly-B and Ortho-A, respectively. The Photosynthetic performance index (PItot) was also increased by 128.5%, 90.2% and 38.8% for Ortho-B, Ortho-A and Poly B, respectively. In addition, Poly-B showed a significant enhancement in roots and shoots biomass (49.4% and 156.8%, respectively) compared to C+. Fertilized and salt-stressed plants absorbed more phosphorus. The P content significantly increased mainly at 45 ppm of P. Positive correlations were found between phosphorus uptake, biomass, and photosynthetic yield. The increased photochemical activity could be due to a significant enhancement in light energy absorbed by the enhanced Chl antenna. The positive effect of adequate P fertilization under salt stress was therefore evident in durum wheat plants.
Loudari, Aicha ; Université de Liège - ULiège > TERRA Research Centre
Mayane, Asmae
Zeroual, Youssef
Colinet, Gilles ; Université de Liège - ULiège > TERRA Research Centre > Echanges Eau - Sol - Plantes
Oukarroum, Abdallah
Language :
English
Title :
Photosynthetic performance and nutrient uptake under salt stress: Differential responses of wheat plants to contrasting phosphorus forms and rates
Alternative titles :
[fr] Performances photosynthétiques et absorption des nutriments sous stress salin : réponses différentielles des plants de blé à des formes et à des taux de phosphore contrastés
Publication date :
10 November 2022
Journal title :
Frontiers in Plant Science
eISSN :
1664-462X
Publisher :
Frontiers Media SA
Special issue title :
Chlorophyll Fluorescence Measurements and Plant Stress Responses, Volume II
Abbas G. Chen Y. Khan F. Y. Feng Y. Palta J. A. Siddique K. H. (2018). Salinity and low phosphorus differentially affect shoot and root traits in two wheat cultivars with contrasting tolerance to salt. Agronomy 8 (8), 155. doi: 10.3390/agronomy8080155
Altuntas O. Dasgan H. Y. Akhoundnejad Y. (2018). Silicon-induced salinity tolerance improves photosynthesis, leaf water status, membrane stability, and growth in pepper (Capsicum annuum l.). HortScience 53 (12), 1820–1826. doi: 10.21273/HORTSCI13411-18
Ashraf M. H. P. J. C. Harris P. J. (2013). Photosynthesis under stressful environments: an overview. Photosynthetica 51 (2), 163–190. doi: 10.1007/s11099-013-0021-6
Asrar H. Hussain T. Hadi S. M. S. Gul B. Nielsen B. L. Khan M. A. (2017). Salinity induced changes in light harvesting and carbon assimilating complexes of desmostachya bipinnata (L.) staph. Environ. Exp. Bot. 135, 86–95. doi: 10.1016/j.envexpbot.2016.12.008
Bargaz A. Nassar R. M. A. Rady M. M. Gaballah M. S. Thompson S. M. Brestic M. et al. (2016). Improved salinity tolerance by phosphorus fertilizer in two phaseolus vulgaris recombinant inbred lines contrasting in their p-efficiency. J. Agron. Crop Sci. 202 (6), 497–507. doi: 10.1111/jac.12181
Behdad A. Mohsenzadeh S. Azizi M. (2021). Growth, leaf gas exchange and physiological parameters of two glycyrrhiza glabra l. populations subjected to salt stress condition. Rhizosphere 17, 100319. doi: 10.1016/j.rhisph.2021.100319
Belouchrani A. S. Latati M. Ounane S. M. Drouiche N. Lounici H. (2020). Study of the interaction salinity: Phosphorus fertilization on sorghum. J. Plant Growth Regul. 39 (3), 1205–1210. doi: 10.1007/s00344-019-10057-4
Bouras H. Bouaziz A. Bouazzama B. Hirich A. Choukr-Allah R. (2021). How phosphorus fertilization alleviates the effect of salinity on sugar beet (Beta vulgaris l.) productivity and quality. Agronomy 11 (8), 1491. doi: 10.3390/agronomy11081491
Bouras H. Choukr-Allah R. Amouaouch Y. Bouaziz A. Devkota K. P. El Mouttaqi A. et al. (2022). How does quinoa (Chenopodium quinoa willd.) respond to phosphorus fertilization and irrigation water salinity? Plants 11 (2), 216. doi: 10.3390/plants11020216
Brestic M. Zivcak M. Kalaji H. M. Carpentier R. Allakhverdiev S. I. (2012). Photosystem II thermostability in situ: environmentally induced acclimation and genotype-specific reactions in triticum aestivum l. Plant Physiol. Biochem. 57, 93–105. doi: 10.1016/j.plaphy.2012.05.012
Broschat T. K. Klock-Moore K. A. (2000). Root and shoot growth responses to phosphate fertilization in container-grown plants. HortTechnology 10 (4), 765–767. doi: 10.21273/HORTTECH.10.4.765
Carstensen A. Herdean A. Schmidt S. B. Sharma A. Spetea C. Pribil M. et al. (2018). The impacts of phosphorus deficiency on the photosynthetic electron transport chain. Plant Physiol. 177 (1), 271–284. doi: 10.1104/pp.17.01624
Chakraborty D. Prasad R. Bhatta A. Torbert H. A. (2021). Understanding the environmental impact of phosphorus in acidic soils receiving repeated poultry litter applications. Sci. Total Environ. 779, 146267. doi: 10.1016/j.scitotenv.2021.146267
Chavarria M. R. Wherley B. Jessup R. Chandra A. (2020). Leaf anatomical responses and chemical composition of warm-season turfgrasses to increasing salinity. Curr. Plant Biol. 22, 100147. doi: 10.1016/j.cpb.2020.100147
Chaves M. M. Costa J. M. Saibo N. J. M. (2011). Recent advances in photosynthesis under drought and salinity. Adv. botanical Res. 57, 49–104. doi: 10.1016/B978-0-12-387692-8.00003-5
Chen L. Mao F. Kirumba G. C. Jiang C. Manefield M. He Y. (2015). Changes in metabolites, antioxidant system, and gene expression in microcystis aeruginosa under sodium chloride stress. Ecotoxicology Environ. Saf. 122, 126–135. doi: 10.1016/j.ecoenv.2015.07.011
Chen S. Yang J. Zhang M. Strasser R. J. Qiang S. (2016). Classification and characteristics of heat tolerance in ageratina adenophora populations using fast chlorophyll a fluorescence rise OJIP. Environ. Exp. Bot. 122, 126–140. doi: 10.1016/j.envexpbot.2015.09.011
Chen Z. Zhou M. Newman I. A. Mendham N. J. Zhang G. Shabala S. (2007). Potassium and sodium relations in salinised barley tissues as a basis of differential salt tolerance. Funct. Plant Biol. 34 (2), 150–162. doi: 10.1071/FP06237
Chtouki M. Naciri R. Garré S. Nguyen F. Zeroual Y. Oukarroum A. (2022). Phosphorus fertilizer form and application frequency affect soil p availability, chickpea yield, and p use efficiency under drip fertigation. J. Plant Nutr. Soil Sci. 185, 603–611. doi: 10.1002/jpln.202100439
Conde A. Chaves M. M. Gerós H. (2011). Membrane transport, sensing and signaling in plant adaptation to environmental stress. Plant Cell Physiol. 52 (9), 1583–1602. doi: 10.1093/pcp/pcr107
Dekker J. P. Boekema E. J. (2005). Supramolecular organization of thylakoid membrane proteins in green plants. Biochim. Biophys. Acta (BBA)-Bioenergetics 1706 (1-2), 12–39. doi: 10.1016/j.bbabio.2004.09.009
Demiral M. A. (2017). Effect of salt stress on the concentration of nitrogen and phosphorus in root and leaf of strawberry plant. Eurasian J. Soil Sci. 6 (4), 357–364. doi: 10.18393/ejss.319198
Din M. R. Ullah F. Akmal M. Shah S. Ullah N. Shafi M. et al. (2011). Effects of cadmium and salinity on growth and photosynthesis parameters. Pak J. Bot 43, 333–340.
Duarte B. Santos D. Marques J. C. Cašador I. (2013). Ecophysiological adaptations of two halophytes to salt stress: photosynthesis, PS II photochemistry and anti-oxidant feedback–implications for resilience in climate change. Plant Physiol. Biochem. 67, 178–188. doi: 10.1016/j.plaphy.2013.03.004
Eker S. Cömertpay G. Konuşkan Ö. Ülger A. C. Öztürk L. Çakmak İ. (2006). Effect of salinity stress on dry matter production and ion accumulation in hybrid maize varieties. Turkish J. Agric. forestry 30 (5), 365–373.
Elhindi K. M. El-Din A. S. Elgorban A. M. (2017). The impact of arbuscular mycorrhizal fungi in mitigating salt-induced adverse effects in sweet basil (Ocimum basilicum l.). Saudi J. Biol. Sci. 24 (1), 170–179. doi: 10.1016/j.sjbs.2016.02.010
El-Mejjaouy Y. Lahrir M. Naciri R. Zeroual Y. Mercatoris B. Dumont B. et al. (2022). How far can chlorophyll a fluorescence detect phosphorus status in wheat leaves (Triticum durum l.). Environ. Exp. Bot. 194, 104762. doi: 10.1016/j.envexpbot.2021.104762
Fahad S. Hussain S. Matloob A. Khan F. A. Khaliq A. Saud S. et al. (2015). Phytohormones and plant responses to salinity stress: a review. Plant Growth Regul. 75 (2), 391–404. doi: 10.1007/s10725-014-0013-y
Fujita K. Kai Y. Takayanagi M. El-Shemy H. Adu-Gyamfi J. J.. (2004). Genotypic variability of pigeonpea in distribution of photosynthetic carbon at low phosphorus level. Plant Science 166(3), 641–649. doi: 10.1016/j.plantsci.2003.10.032
Gao Y. Wang X. Shah J. A. Chu G. (2020). Polyphosphate fertilizers increased maize (Zea mays l.) p, fe, zn, and Mn uptake by decreasing p fixation and mobilizing microelements in calcareous soil. J. Soils Sediments 20, 1–11. doi: 10.1007/s11368-019-02375-7
García-Ortiz L. Recio-Rodríguez J. I. Rodríguez-Sánchez E. Patino-Alonso M. C. Agudo-Conde C. Rodríguez-Martín C. et al. (2012). Sodium and potassium intake present a J-shaped relationship with arterial stiffness and carotid intima-media thickness. Atherosclerosis 225 (2), 497–503. doi: 10.1016/j.atherosclerosis.2012.09.038
Grattan S. R. Grieve C. M. (1992). Mineral element acquisition and growth response of plants grown in saline environments. Agriculture Ecosyst. Environ. 38 (4), 275–300. doi: 10.1016/0167-8809(92)90151-Z
Hasanuzzaman M. Raihan M. R. H. Masud A. A. C. Rahman K. Nowroz F. Rahman M. et al. (2021). Regulation of reactive oxygen species and antioxidant defence in plants under salinity. Int. J. Mol. Sci. 22 (17), 9326. doi: 10.3390/ijms22179326
Hermans C. Hammond J. P. White P. J. Verbruggen N. (2006). How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci. 11 (12), 610–617. doi: 10.1016/j.tplants.2006.10.007
Hessini K. Issaoui K. Ferchichi S. Saif T. Abdelly C. Siddique K. H. et al. (2019). Interactive effects of salinity and nitrogen forms on plant growth, photosynthesis and osmotic adjustment in maize. Plant Physiol. Biochem. 139, 171–178. doi: 10.1016/j.plaphy.2019.03.005
Ilangumaran G. Smith D. L. (2017). Plant growth promoting rhizobacteria in amelioration of salinity stress: a systems biology perspective. Front. Plant Sci. 8, 1768. doi: 10.3389/fpls.2017.01768
Isayenkov S. V. Maathuis F. J. (2019). Plant salinity stress: many unanswered questions remain. Front. Plant Sci. 10, 80. doi: 10.3389/fpls.2019.00080
Kalaji H. M. Jajoo A. Oukarroum A. Brestic M. Zivcak M. Samborska I. A. et al. (2016). Chlorophyll a fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta physiologiae plantarum 38 (4), 1–11. doi: 10.1007/s11738-016-2113-y
Kalaji H. M. Račková L. Paganová V. Swoczyna T. Rusinowski S. Sitko K. (2018). Can chlorophyll-a fluorescence parameters be used as bio-indicators to distinguish between drought and salinity stress in tilia cordata mill? Environ. Exp. Bot. 152, 149–157. doi: 10.1016/j.envexpbot.2017.11.001
Kalaji H. M. Schansker G. Brestic M. Bussotti F. Calatayud A. Ferroni L. et al. (2017). Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynthesis Res. 132 (1), 13–66. doi: 10.1007/s11120-016-0318-y
Kaya C. Ashraf M. Dikilitas M. Tuna A. L. (2013). Alleviation of salt stress-induced adverse effects on maize plants by exogenous application of indoleacetic acid (IAA) and inorganic nutrients-a field trial. Aust. J. Crop Sci. 7 (2), 249–254. doi: 10.3316/informit.260789621744643
Keisham M. Mukherjee S. Bhatla S. C. (2018). Mechanisms of sodium transport in plants–progresses and challenges. Int. J. Mol. Sci. 19 (3), 647. doi: 10.3390/ijms19030647
Khan A. Ahmad I. Shah A. Ahmad F. Ghani A. Nawaz M. et al. (2013). Amelioration of salinity stress in wheat (Triticum aestivum l) by foliar application of phosphorus. Phyton (Buenos Aires) 82 (2), 281–287.
Khan M. Z. Islam M. A. Azom M. G. Amin M. S. (2018). Short-term influence of salinity on uptake of phosphorus by ipomoea aquatica. Int. J. Plant Soil Sci. 25 (2), 1–9. doi: 10.9734/IJPSS/2018/44822
Khorshid A. M. Moghadam F. A. Bernousi I. Khayamim S. Rajabi A. (2018). Comparison of some physiological responses to salinity and normal conditions in sugar beet. Indian J. Agric. Res. 52 (4), 362–367. doi: 10.18805/IJARe.A-320
Khourchi S. Elhaissoufi W. Loum M. Ibnyasser A. Haddine M. Ghani R. et al. (2022b). Phosphate solubilizing bacteria can significantly contribute to enhance p availability from polyphosphates and their use efficiency in wheat. Microbiological Res. 262, 127094. doi: 10.1016/j.micres.2022.127094
Khourchi S. Oukarroum A. Tika A. Delaplace P. Bargaz A. (2022a). Polyphosphate application influences morpho-physiological root traits involved in p acquisition and durum wheat growth performance. BMC Plant Biol. 22 (1), 1–15. doi: 10.1186/s12870-022-03683-w
Kim H. J. Li X. (2016). Effects of phosphorus on shoot and root growth, partitioning, and phosphorus utilization efficiency in lantana. HortScience 51 (8), 1001–1009. doi: 10.21273/HORTSCI.51.8.1001
Kim H. J. Lynch J. P. Brown K. M. (2008). Ethylene insensitivity impedes a subset of responses to phosphorus deficiency in tomato and petunia. Plant Cell Environ. 31 (12), 1744–1755. doi: 10.1111/j.1365-3040.2008.01886.x
Koyro H. W. (2006). Effect of salinity on growth, photosynthesis, water relations and solute composition of the potential cash crop halophyte plantago coronopus (L.). Environ. Exp. Bot. 56 (2), 136–146. doi: 10.1016/j.envexpbot.2005.02.001
Kohler J. Hernández J. A. Caravaca F. Roldán A. (2009). Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environmental and Experimental Botany, 65(2-3), 245–252. doi: 10.1016/j.envexpbot.2008.09.008
Kulakovskaya T. V. Vagabov V. M. Kulaev I. S. (2012). Inorganic polyphosphate in industry, agriculture and medicine: Modern state and outlook. Process Biochem. 47, 1–10. doi: 10.1016/j.procbio.2011.10.028
Kumari R. Bhatnagar S. Mehla N. Vashistha A. (2022). Potential of organic amendments (AM fungi, PGPR, vermicompost and seaweeds) in combating salt stress–a review. Plant Stress 6, 100111. doi: 10.1016/j.stress.2022.100111
Kumar V. Khare T. Sharma M. Wani S. H. (2017). “ROS-induced signaling and gene expression in crops under salinity stress,” in Reactive oxygen species and antioxidant systems in plants: role and regulation under abiotic stress (Singapore: Springer), 159–184.
Li Z. Wu N. Meng S. Wu F. Liu T. (2020). Arbuscular mycorrhizal fungi (AMF) enhance the tolerance of euonymus maackii rupr. at a moderate level of salinity. PLoS One 15 (4), e0231497. doi: 10.1371/journal.pone.0231497
Li M. Wu Y. J. Yu Z. L. Sheng G. P. Yu H. Q. (2009). Enhanced nitrogen and phosphorus removal from eutrophic lake water by ipomoea aquatica with low-energy ion implantation. Water Res. 43 (5), 1247–1256. doi: 10.1016/j.watres.2008.12.013
Lotfi R. Ghassemi-Golezani K. Pessarakli M. (2020). Salicylic acid regulates photosynthetic electron transfer and stomatal conductance of mung bean (Vigna radiata l.) under salinity stress. Biocatalysis Agric. Biotechnol. 26, 101635. doi: 10.1016/j.bcab.2020.101635
Loudari A. Benadis C. Naciri R. Soulaimani A. Zeroual Y. Gharous M. E. et al. (2020). Salt stress affects mineral nutrition in shoots and roots and chlorophyll a fluorescence of tomato plants grown in hydroponic culture. J. Plant Interact. 15 (1), 398–405. doi: 10.1080/17429145.2020.1841842
Lynch J. P. Brown K. M. (2006). “Whole plant adaptations to low phosphorus availability,” in Plant–environment interactions, 3rd edn. Ed. Huang B. (New York: Taylor and Francis).
Manaa A. Goussi R. Derbali W. Cantamessa S. Abdelly C. Barbato R. (2019). Salinity tolerance of quinoa (Chenopodium quinoa willd) as assessed by chloroplast ultrastructure and photosynthetic performance. Environ. Exp. Bot. 162, 103–114. doi: 10.1016/j.envexpbot.2019.02.012
Meng X. Chen W. W. Wang Y. Y. Huang Z. R. Ye X. Chen L. S. et al. (2021). Effects of phosphorus deficiency on the absorption of mineral nutrients, photosynthetic system performance and antioxidant metabolism in citrus grandis. PLoS One 16 (2), e0246944. doi: 10.1371/journal.pone.0246944
Mohamed H. I. El-Sayed A. A. Rady M. M. Caruso G. Sekara A. Abdelhamid M. T. (2021). Coupling effects of phosphorus fertilization source and rate on growth and ion accumulation of common bean under salinity stress. PeerJ 9, e11463. doi: 10.7717/peerj.11463
Muhammad H. M. D. Abbas A. Ahmad R. (2022). Fascinating role of silicon nanoparticles to mitigate adverse effects of salinity in fruit trees: a mechanistic approach. Silicon 14, 1–8. doi: 10.1007/s12633-021-01604-4
Muhammad I. Shalmani A. Ali M. Yang Q. H. Ahmad H. Li F. B. (2021). Mechanisms regulating the dynamics of photosynthesis under abiotic stresses. Front. Plant Sci. 11, 615942. doi: 10.3389/fpls.2020.615942
Nemeskéri E. Neményi A. Bőcs A. Pék Z. Helyes L. (2019). Physiological factors and their relationship with the productivity of processing tomato under different water supplies. Water 11 (3), 586. doi: 10.3390/agronomy9080447
Oukarroum A. Bussotti F. Goltsev V. Kalaji H. M. (2015). Correlation between reactive oxygen species production and photochemistry of photosystems I and II in lemna gibba l. plants under salt stress. Environ. Exp. Bot. 109, 80–88. doi: 10.1016/j.envexpbot.2014.08.005
Oukarroum A. El Madidi S. Schansker G. Strasser R. J. (2007). Probing the responses of barley cultivars (Hordeum vulgare l.) by chlorophyll a fluorescence OLKJIP under drought stress and re-watering. Environ. Exp. Bot. 60 (3), 438–446. doi: 10.1016/j.envexpbot.2007.01.002
Parvez S. Abbas G. Shahid M. Amjad M. Hussain M. Asad S. A et al. (2020). Effect of salinity on physiological, biochemical and photostabilizing attributes of two genotypes of quinoa (Chenopodium quinoa Willd.) exposed to arsenic stress. Ecotoxicology and environmental safety 187, 109814. doi: 10.1016/j.ecoenv.2019.109814
Pereira da Silva G. Prado R. D. M. Wadt P. G. S. Moda L. R. Caione G. (2020). Accuracy of nutritional diagnostics for phosphorus considering five standards by the method of diagnosing nutritional composition in sugarcane. J. Plant Nutr. 43 (10), 1485–1497. doi: 10.1080/01904167.2020.1730902
Pérez-López U. Robredo A. Lacuesta M. Mena-Petite A. Munoz-Rueda A. (2012). Elevated CO2 reduces stomatal and metabolic limitations on photosynthesis caused by salinity in hordeum vulgare. Photosynthesis Res. 111 (3), 269–283. doi: 10.1007/s11120-012-9721-1
Phang T. H. Shao G. Liao H. Yan X. Lam H. M. (2009). High external phosphate (Pi) increases sodium ion uptake and reduces salt tolerance of ‘Pi-tolerant’soybean. Physiologia Plantarum 135 (4), 412–425. doi: 10.1111/j.1399-3054.2008.01200.x
Pulido-Bosch A. Rigol-Sanchez J. P. Vallejos A. Andreu J. M. Ceron J. C. Molina-Sanchez L. et al. (2018). Impacts of agricultural irrigation on groundwater salinity. Environ. Earth Sci. 77 (5), 1–14. doi: 10.1007/s12665-018-7386-6
Rady M. M. El-Shewy A. A. Seif El-Yazal M. A. Abdelaal K. E. (2018). Response of salt-stressed common bean plant performances to foliar application of phosphorus (MAP). Int. Lett. Natural Sci. 72, 7–20. doi: 10.18052/www.scipress.com/ILNS.72.7
Rahimi E. Nazari F. Javadi T. Samadi S. da Silva J. A. T. (2021). Potassium-enriched clinoptilolite zeolite mitigates the adverse impacts of salinity stress in perennial ryegrass (Lolium perenne l.) by increasing silicon absorption and improving the K/Na ratio. J. Environ. Manage. 285, 112142. doi: 10.1016/j.jenvman.2021.112142
Renger G. Pieper J. Theiss C. Trostmann I. Paulsen H. Renger T. et al. (2011). Water soluble chlorophyll binding protein of higher plants: a most suitable model system for basic analyses of pigment–pigment and pigment–protein interactions in chlorophyll protein complexes. Journal of plant physiology 168(12), 1462–1472. doi: 10.1016/j.jplph.2010.12.005
Rewald B. Raveh E. Gendler T. Ephrath J. E. Rachmilevitch S. (2012). Phenotypic plasticity and water flux rates of citrus root orders under salinity. J. Exp. Bot. 63 (7), 2717–2727. doi: 10.1093/jxb/err457
Rodríguez-Martín J. A. Gutiérrez C. Torrijos M. Nanos N. (2018). Wood and bark of Pinus halepensis as archives of heavy metal pollution in the Mediterranean Region. Environmental Pollution 239, 438–447. doi: 10.1016/j.envpol.2018.04.036
Rubio L. Linares-Rueda A. García-Sánchez M. J. Fernández J. A. (2005). Physiological evidence for a sodium-dependent high-affinity phosphate and nitrate transport at the plasma membrane of leaf and root cells of zostera marina l. J. Exp. Bot. 56 (412), 613–622. doi: 10.1093/jxb/eri053
Rychter A. M. Rao I. M. Cardoso J. A. (2018). “Role of phosphorus in photosynthetic carbon assimilation and partitioning,” in Handbook of photosynthesis (CRC Press, Boca Raton), 603–625. doi: 10.1201/9781315372136
Sarkar R. K. Ray A. (2016). Submergence-tolerant rice withstands complete submergence even in saline water: Probing through chlorophyll a fluorescence induction OJIP transients. Photosynthetica 54 (2), 275–287. doi: 10.1007/s11099-016-0082-4
Schansker G. Tóth S. Z. Strasser R. J. (2006). Dark recovery of the chl a fluorescence transient (OJIP) after light adaptation: the qT-component of non-photochemical quenching is related to an activated photosystem I acceptor side. Biochim. Biophys. Acta (BBA)-Bioenergetics 1757 (7), 787–797. doi: 10.1016/j.bbabio.2006.04.019
Shabala S. Munns R. (2017). “Salinity stress: physiological constraints and adaptive mechanisms,” in Plant stress physiology (Wallingford UK: Cabi), 24–63.
Sharma A. Kumar V. Shahzad B. Ramakrishnan M. Singh Sidhu G. P. Bali A. S. et al. (2020). Photosynthetic response of plants under different abiotic stresses: a review. J. Plant Growth Regul. 39, 509–531. doi: 10.1007/s00344-019-10018-x
Shibli R. A. Sawwan J. Swaidat I. Tahat M. (2001). Increased phosphorus mitigates the adverse effects of salinity in tissue culture. Commun. Soil Sci. Plant Anal. 32 (3-4), 429–440. doi: 10.1081/CSS-100103019
Shoukat E. Abideen Z. Ahmed M. Z. Gulzar S. Nielsen B. L. (2019). Changes in growth and photosynthesis linked with intensity and duration of salinity in phragmites karka. Environ. Exp. Bot. 162, 504–514. doi: 10.1016/j.envexpbot.2019.03.024
Singh N. Singh G. Khanna V. (2016). Growth of lentil (Lens culinaris medikus) as influenced by phosphorus, rhizobium and plant growth promoting rhizobacteria. Indian J. Agric. Res. 50 (6), 567–572. doi: 10.18805/ijare.v0iOF.4573
Stirbet A. (2012). Chlorophyll a fluorescence induction: a personal perspective of the thermal phase, the J–I–P rise. Photosynthesis Res. 113 (1), 15–61. doi: 10.1007/s11120-012-9754-5
Strasser R. J. Tsimilli-Michael M. Srivastava A. (2004). “Analysis of the chlorophyll a fluorescence transient,” in Chlorophyll a fluorescence (Dordrecht: Springer), 321–362.
Tang H. Niu L. Wei J. Chen X. Chen Y. (2019). Phosphorus limitation improved salt tolerance in maize through tissue mass density increase, osmolytes accumulation, and na+ uptake inhibition. Front. Plant Sci. 10, 856. doi: 10.3389/fpls.2019.00856
Tirry N. Kouchou A. Laghmari G. Lemjereb M. Hnadi H. Amrani K. et al. (2021). Improved salinity tolerance of medicago sativa and soil enzyme activities by PGPR. Biocatalysis Agric. Biotechnol. 31, 101914. doi: 10.1016/j.bcab.2021.101914
Tsimilli-Michael M. Strasser R. J. (2008). “In vivo assessment of stress impact on plant’s vitality: applications in detecting and evaluating the beneficial role of mycorrhization on host plants,” in Mycorrhiza (Berlin, Heidelberg: Springer), 679–703.
Wahid F. Fahad S. Danish S. Adnan M. Yue Z. Saud S. et al. (2020). Sustainable management with mycorrhizae and phosphate solubilizing bacteria for enhanced phosphorus uptake in calcareous soils. Agriculture 10 (8), 334. doi: 10.3390/agriculture10080334
Wang X. Gao Y. Hu B. Chu G. (2019). Comparison of the hydrolysis characteristics of three polyphosphates and their effects on soil p and micronutrient availability. Soil Use Manag. 35, 664–674. doi: 10.1111/sum.12526
Wieneke S. Balzarolo M. Asard H. Abd Elgawad H. Peñuelas J. Rascher U. et al. (2022). Fluorescence ratio and photochemical reflectance index as a proxy for photosynthetic quantum efficiency of photosystem II along a phosphorus gradient. Agric. For. Meteorology 322, 109019. doi: 10.1016/j.agrformet.2022.109019
Wilkinson S. Davies W. J. (2002). ABA-based chemical signalling: the co-ordination of responses to stress in plants. Plant Cell Environ. 25 (2), 195–210. doi: 10.1046/j.0016-8025.2001.00824.x
Xiao L. Yuan G. Feng L. Shah G. M. Wei J. (2022). Biochar to reduce fertilizer use and soil salinity for crop production in the yellow river delta. J. Soil Sci. Plant Nutr. 22, 1–12. doi: 10.1007/s42729-021-00747-y
Xue D. Huang Y. Zhang X. Wei K. Westcott S. Li C. et al. (2009). Identification of QTLs associated with salinity tolerance at late growth stage in barley. Euphytica 169 (2), 187–196. doi: 10.1007/s10681-009-9919-2
Yang A. Akhtar S. S. Li L. Fu Q. Li Q. Naeem M. A. et al. (2020). Biochar mitigates combined effects of drought and salinity stress in quinoa. Agronomy 10 (6), 912. doi: 10.3390/agronomy10060912
Yan N. Marschner P. (2012). Response of microbial activity and biomass to increasing salinity depends on the final salinity, not the original salinity. Soil Biol. Biochem. 53, 50–55. doi: 10.1016/j.soilbio.2012.04.028
Zhao C. Zhang H. Song C. Zhu J. K. Shabala S. (2020). Mechanisms of plant responses and adaptation to soil salinity. Innovation 1 (1), 100017. doi: 10.1016/j.xinn.2020.100017
Zribi O. Abdelly C. Debez A. (2011). Interactive effects of salinity and phosphorus availability on growth, water relations, nutritional status and photosynthetic activity of barley (Hordeum vulgare L.). Plant Biology, 13(6), 872–880. doi: 10.1111/j.1438-8677.2011.00450.x
Zribi O. Mbarki S. Metoui O. Trabelsi N. Zribi F. Ksouri R. et al. (2021). Salinity and phosphorus availability differentially affect plant growth, leaf morphology, water relations, solutes accumulation and antioxidant capacity in aeluropus littoralis. Plant Biosystems-An Int. J. Dealing all Aspects Plant Biol. 155 (4), 935–943. doi: 10.1080/11263504.2020.1810808
