Silver nanoparticles protect tillering in drought-stressed wheat by improving leaf water relations and physiological functioning
Muhammad Sarwar A , Muhammad Farrukh Saleem A , Najeeb Ullah B * , Muhammad Jahanzaib Khan A , Hamza Maqsood A , Hassaan Ahmad A , Asif Tanveer C and Muhammad Shahid DA Department of Agronomy, University of Agriculture, Faisalabad, Pakistan.
B Agricultural Research Station, Office of VP for Research and Graduate Studies, Qatar University, Doha 2713, Qatar.
C Department of Agronomy, The University of Lahore, Lahore, Pakistan.
D Agronomic Research Station, Bahawalpur, Pakistan.
Functional Plant Biology 50(11) 901-914 https://doi.org/10.1071/FP23036
Submitted: 21 February 2023 Accepted: 6 July 2023 Published: 25 July 2023
Abstract
The tillering phase of wheat (Triticum aestivum) crops is extremely susceptible to drought. We explored the potential of silver nanoparticles (AgNPs) in protecting wheat genotypes from drought injury during this sensitive stage. After treating with AgNPs (60 ppm), the plants were submitted to different water levels; i.e. 100% field capacity (FC), 75% FC (mild drought), 50% FC (moderate drought) and 25% FC (severe drought) from 15 to 41 days after sowing (tillering phase). Leaf physiological data were collected at stress termination, while yield attributes were recorded at crop maturity. We found that increasing drought intensity significantly impaired leaf physiology and grain yield of both studied genotypes. Compared with control, moderately and severely drought-stressed plants produced 25% and 45% lesser grain yield per spike, respectively (averaged across genotypes and years of study). Likewise, moderate and severe drought reduced photosynthesis by 49% and 76%, respectively, compared with control. In contrast, AgNPs significantly restored leaf physiological functioning and grain yield formation at maturity. For example, under moderate and severe drought, AgNPs-treated plants produced 22% and 17% more grains per plant, respectively, than their respective water-treated plants. Our study suggests that exogenous AgNPs can protect wheat crops from drought during early development stages.
Keywords: cellular biochemistry, drought-tolerance, grain yield, osmo-protectants, senescence, silver nanoparticles, tiller formation, water relations.
References
Abid M, Tian Z, Ata-Ul-Karim ST, Cui Y, Liu Y, Zahoor R, Jiang D, Dai T (2016) Nitrogen nutrition improves the potential of wheat (Triticum aestivum L.) to alleviate the effects of drought stress during vegetative growth periods. Frontiers in Plant Science 7, 981.
| Crossref | Google Scholar |
Abid M, Ali S, Qi LK, Zahoor R, Tian Z, Jiang D, Snider JL, Dai T (2018) Physiological and biochemical changes during drought and recovery periods at tillering and jointing stages in wheat (Triticum aestivum L.). Scientific Reports 8, 4615.
| Crossref | Google Scholar |
Ahmad W, Ullah N, Xu L, El Sabagh A (2022a) Editorial: global food and nutrition security under changing climates. Frontiers in Agronomy 3, 799878.
| Crossref | Google Scholar |
Ahmad A, Aslam Z, Javed T, Hussain S, Raza A, Shabbir R, Mora-Poblete F, Saeed T, Zulfiqar F, Ali MM, Nawaz M, Rafiq M, Osman HS, Albaqami M, Ahmed MAA, Tauseef M (2022b) Screening of wheat (Triticum aestivum L.) genotypes for drought tolerance through agronomic and physiological response. Agronomy 12, 287-303.
| Crossref | Google Scholar |
Ahmed F, Javed B, Razzaq A, Mashwani Z-u-R (2021) Applications of copper and silver nanoparticles on wheat plants to induce drought tolerance and increase yield. IET Nanobiotechnology 15, 68-78.
| Crossref | Google Scholar |
Akhkha A, Boutraa T, Alhejely A (2011) The rates of photosynthesis, chlorophyll content, dark respiration, proline and abscicic acid (ABA) in wheat (Triticum durum) under water deficit conditions. International Journal of Agriculture and Biology 13, 215-221.
| Google Scholar |
Alabdallah NM, Hasan MM, Salih AM, Roushdy SS, Al-Shammari AS, Alsanie SI, El-Zaidy M (2021) Silver nanoparticles improve growth and protect against oxidative damage in eggplant seedlings under drought stress. Plant, Soil and Environment 67, 617-624.
| Crossref | Google Scholar |
Alghory A, Yazar A (2019) Evaluation of crop water stress index and leaf water potential for deficit irrigation management of sprinkler-irrigated wheat. Irrigation Science 37, 61-77.
| Crossref | Google Scholar |
Ali N, Anjum MM, Khan GR, Ali R (2022) Unraveling wheat grain quality, physiological indices, dry matter accumulation, and attenuating water stress adverse effect via foliar potassium application at different growth stages. Gesunde Pflanzen 74, 41-52.
| Crossref | Google Scholar |
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiology 24, 1-15.
| Crossref | Google Scholar |
Arzanesh MH, Alikhani HA, Khavazi K, Rahimian HA, Miransari M (2011) Wheat (Triticum aestivum L.) growth enhancement by Azospirillum sp. under drought stress. World Journal of Microbiology and Biotechnology 27, 197-205.
| Crossref | Google Scholar |
Aslam H, Ahmad MSA, Alvi AK, Rani W, Athar H-u-R, Al-Ashkar I, Almutairi KF, Ullah N, Ayman E-S (2022) He–Ne laser priming enhances drought tolerance in wheat through differential modification of photosynthetic pigments and antioxidative enzymes. Agronomy 12, 2376-2393.
| Crossref | Google Scholar |
Aurangzaib M, Ahmad Z, Jalil MI, Nawaz F, Shaheen MR, Ahmad M, Hussain A, Ejaz MK, Tabassum MA (2022) Foliar spray of silicon confers drought tolerance in wheat (Triticum aestivum L.) by enhancing morpho-physiological and antioxidant potential. Silicon 14, 4793-4807.
| Crossref | Google Scholar |
Bacher H, Sharaby Y, Walia H, Peleg Z (2022) Modifying root-to-shoot ratio improves root water influxes in wheat under drought stress. Journal of Experimental Botany 73, 1643-1654.
| Crossref | Google Scholar |
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant and Soil 39, 205-207.
| Crossref | Google Scholar |
Bayoumi TY, Eid MH, Metwali EM (2008) Application of physiological and biochemical indices as a screening technique for drought tolerance in wheat genotypes. African Journal of Biotechnology 7, 2341-2352.
| Google Scholar |
Bukhari MA, Ahmad Z, Ashraf MY, Afzal M, Nawaz F, Nafees M, Jatoi WN, Malghani NA, Shah AN, Manan A (2021) Silicon mitigates drought stress in wheat (Triticum aestivum L.) through improving photosynthetic pigments, biochemical and yield characters. Silicon 13, 4757-4772.
| Crossref | Google Scholar |
Cakmak I, Horst WJ (1991) Effect of aluminium on lipid peroxidation, superoxide dismutase, catalase, and peroxidase activities in root tips of soybean (Glycine max). Physiologia Plantarum 83, 463-468.
| Crossref | Google Scholar |
Chanu TT, Upadhyaya H (2019) Zinc oxide nanoparticle-induced responses on plants: a physiological perspective. In ‘Nanomaterials in plants, algae and microorganisms. Vol. 2’. (Eds DK Tripathi, P Ahmad, DK Chauhan, NK Dubey) pp. 43–64. (Academic Press: London, UK) doi:10.1016/B978-0-12-811488-9.00003-2
Daryanto S, Wang L, Jacinthe P-A (2016) Global synthesis of drought effects on maize and wheat production. PLoS ONE 11, e0156362.
| Crossref | Google Scholar |
Dhakal A (2021) Effect of drought stress and management in wheat – a review. Food & Agribusiness Management 2, 62-66.
| Crossref | Google Scholar |
El Sabagh A, Hossain A, Barutcular C, Islam MS, Awan SI, Galal A, Iqbal MA, Sytar O, Yildirim M, Meena RS, Fahad S, Najeeb U, Konuskan O, Habib RA, Llanes A, Hussain S, Farooq M, Hasanuzzaman M, Abdelaal KH, Hafez Y, Cig F, Saneoka H (2019) Wheat (Triticum aestivum L.) production under drought and heat stress – adverse effects, mechanisms and mitigation: a review. Applied Ecology and Environmental Research 17, 8307-8332.
| Crossref | Google Scholar |
El-Afry MM, El-Nady MF, Abdelmonteleb EB, Metwaly MMS (2012) Anatomical studies on drought-stressed wheat plants (Triticum aestivum L.) treated with some bacterial strains. Acta Biologica Szegediensis 56, 165-174.
| Google Scholar |
El-Bassiouny HMS, Mahfouze HA, Abdallah MMS, Bakry BA, El-Enany MAM (2022) Physiological and molecular response of wheat cultivars to titanium dioxide or zinc oxide nanoparticles under water stress conditions. International Journal of Agronomy 2022, 1-15.
| Google Scholar |
Figueroa-Bustos V, Palta JA, Chen Y, Siddique KHM (2019) Early season drought largely reduces grain yield in wheat cultivars with smaller root systems. Plants 8, 305-319.
| Crossref | Google Scholar |
Fleury D, Jefferies S, Kuchel H, Langridge P (2010) Genetic and genomic tools to improve drought tolerance in wheat. Journal of Experimental Botany 61, 3211-3222.
| Crossref | Google Scholar |
Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59, 309-314.
| Crossref | Google Scholar |
Grieve CM, Grattan SR (1983) Rapid assay for determination of water soluble quaternary ammonium compounds. Plant and Soil 70, 303-307.
| Crossref | Google Scholar |
Hameed A, Bibi N, Akhter J, Iqbal N (2011) Differential changes in antioxidants, proteases, and lipid peroxidation in flag leaves of wheat genotypes under different levels of water deficit conditions. Plant Physiology and Biochemistry 49, 178-185.
| Crossref | Google Scholar |
Hickey K, Wood M, Sexton T, Sahin Y, Nazarov T, Fisher J, Sanguinet KA, Cousins A, Kirchhoff H, Smertenko A (2022) Drought tolerance strategies and autophagy in resilient wheat genotypes. Cells 11, 1765-1790.
| Crossref | Google Scholar |
Hojjat SS, Ganjali A (2016) The effect of silver nanoparticle on lentil seed germination under drought stress. International Journal of Farming and Allied Sciences 5, 208-212.
| Google Scholar |
Hou Q, Ufer G, Bartels D (2016) Lipid signalling in plant responses to abiotic stress. Plant, Cell & Environment 39, 1029-1048.
| Crossref | Google Scholar |
Hussain M, Waqas-ul-Haq M, Farooq S, Jabran K, Farroq M (2016) The impact of seed priming and row spacing on the productivity of different cultivars of irrigated wheat under early season drought. Experimental Agriculture 52, 477-490.
| Crossref | Google Scholar |
Ihsan MZ, El-Nakhlawy FS, Ismail SM, Fahad S, daur I (2016) Wheat phenological development and growth studies as affected by drought and late season high temperature stress under arid environment. Frontiers in Plant Science 7, 795.
| Crossref | Google Scholar |
Iqbal M, Raja NI, Mashwani Z-U-R, Wattoo FH, Hussain M, Ejaz M, Saira H (2019) Assessment of AgNPs exposure on physiological and biochemical changes and antioxidative defence system in wheat (Triticum aestivum L) under heat stress. IET Nanobiotechnology 13, 230-236.
| Crossref | Google Scholar |
Jamshidi Goharrizi K, Baghizadeh A, Karami S, Nazari M, Afroushteh M (2022) Expression of the W36, P5CS, P5CR, MAPK3, and MAPK6 genes and proline content in bread wheat genotypes under drought stress. Cereal Research Communications 9, 1-12.
| Crossref | Google Scholar |
Jaskulska I, Jaskulski D (2020) Effects of using nanoparticles of silver (AgNPs) and copper (CuNPs) in foliar fertilizers. Przemysl Chemiczny 99, 250-253.
| Google Scholar |
Jhanzab HM, Razzaq A, Bibi Y, Yasmeen F, Yamaguchi H, Hitachi K, Tsuchida K, Komatsu S (2019) Proteomic analysis of the effect of inorganic and organic chemicals on silver nanoparticles in wheat. International Journal of Molecular Sciences 20, 825.
| Crossref | Google Scholar |
Kalal PR, Tomar RS, Jajoo A (2022) SiO2 nanopriming protects PS I and PSII complexes in wheat under drought stress. Plant Nano Biology 2, 100019.
| Crossref | Google Scholar |
Kannaujia R, Singh P, Prasad V, Pandey V (2022) Evaluating impacts of biogenic silver nanoparticles and ethylenediurea on wheat (Triticum aestivum L.) against ozone-induced damages. Environmental Research 203, 111857.
| Crossref | Google Scholar |
Lesk C, Rowhani P, Ramankutty N (2016) Influence of extreme weather disasters on global crop production. Nature 529, 84-87.
| Crossref | Google Scholar |
Liu D, Zou J, Meng Q, Zou J, Jiang W (2009) Uptake and accumulation and oxidative stress in garlic (Allium sativum L.) under lead phytotoxicity. Ecotoxicology 18, 134-143.
| Crossref | Google Scholar |
Marcińska I, Czyczyło-Mysza I, Skrzypek E, Filek M, Grzesiak S, Grzesiak MT, Janowiak F, Hura T, Dziurka M, Dziurka K, Nowakowska A, Quarrie SA (2013) Impact of osmotic stress on physiological and biochemical characteristics in drought-susceptible and drought-resistant wheat genotypes. Acta Physiologiae Plantarum 35, 451-461.
| Crossref | Google Scholar |
Maswada HF, Sunoj VSJ, Prasad PVV (2021) A comparative study on the effect of seed pre-sowing treatments with microwave radiation and salicylic acid in alleviating the drought-induced damage in wheat. Journal of Plant Growth Regulation 40, 48-66.
| Crossref | Google Scholar |
Mickky B, Aldesuquy H, Elnajar M (2019) Drought-induced change in yield capacity of ten wheat cultivars in relation to their vegetative characteristics at heading stage. Physiology and Molecular Biology of Plants 25, 1137-1148.
| Crossref | Google Scholar |
Munsif F, Farooq U, Arif M, Shah T, Jehangir M, Zaheer S, Akhtar K, Khan MS, Ahmad I, Ahmad W, Ali S, Amir R (2022) Potassium and salicylic acid function synergistically to promote the drought resilience through upregulation of antioxidant profile for enhancing potassium use efficiency and wheat yield. Annals of Applied Biology 180, 273-282.
| Crossref | Google Scholar |
Nakhforoosh A, Grausgruber H, Kaul H-P, Bodner G (2015) Dissection of drought response of modern and underutilized wheat varieties according to Passioura’s yield-water framework. Frontiers in Plant Science 6, 570.
| Crossref | Google Scholar |
Naqvi SMZA, Haq SIU, Iderawumi ARM, Anwar A, Mujtaba G, Khan NM, Islam A, Awais M, Mustafa T, Iqbal J (2022) Green synthesis of silver nanoparticles and anti-oxidant activity in plants under semiarid condition–a review. Pakistan Journal of Weed Science Research 28, 321-332.
| Crossref | Google Scholar |
Naumann G, Cammalleri C, Mentaschi L, Feyen L (2021) Increased economic drought impacts in Europe with anthropogenic warming. Nature Climate Change 11, 485-491.
| Crossref | Google Scholar |
Nawaz F, Ahmad R, Waraich EA, Naeem MS, Shabbir RN (2012) Nutrient uptake, physiological responses, and yield attributes of wheat (Triticum aestivum L.) exposed to early and late drought stress. Journal of Plant Nutrition 35, 961-974.
| Crossref | Google Scholar |
Nishida K, Khan NM, Shiozawa S (2009) Effects of salt accumulation on the leaf water potential and transpiration rate of pot-grown wheat with a controlled saline groundwater table. Soil Science and Plant Nutrition 55, 375-384.
| Crossref | Google Scholar |
Prasad P, Staggenborg S, Ristic Z (2008) Impacts of drought and/or heat stress on physiological, developmental, growth, and yield processes of crop plants. In ‘Response of crops to limited water: understanding and modeling water stress effects on plant growth processes. Vol. 1’. (Eds L Ahuja, VR Reddy, SA Saseendran, Q Yu) pp. 301–355. (American Society of Agronomy, Crop Science Society of America, Soil Science Society of America)
Rashid U, Yasmin H, Hassan MN, Naz R, Nosheen A, Sajjad M, Ilyas N, Keyani R, Jabeen Z, Mumtaz S, Alyemeni MN, Ahmad P (2022) Drought-tolerant Bacillus megaterium isolated from semi-arid conditions induces systemic tolerance of wheat under drought conditions. Plant Cell Reports 41, 549-569.
| Crossref | Google Scholar |
Razzaq A, Ammara R, Jhanzab HM, Mahmood T, Hafeez A, Hussain S (2016) A novel nanomaterial to enhance growth and yield of wheat. Journal of Nanoscience and Technology 2, 55-58.
| Google Scholar |
Saeidi M, Ardalani S, Jalali-Honarmand S, Ghobadi M-E, Abdoli M (2015) Evaluation of drought stress at vegetative growth stage on the grain yield formation and some physiological traits as well as fluorescence parameters of different bread wheat cultivars. Acta Biologica Szegediensis 59, 35-44.
| Google Scholar |
Scholander PF, Bradstreet ED, Hemmingsen EA, Hammel HT (1965) Sap pressure in vascular plants: negative hydrostatic pressure can be measured in plants. Science 148, 339-346.
| Crossref | Google Scholar |
Shah SMDM, Shabbir G, Malik SI, Raja NI, Shah ZH, Rauf M, Zahrani YA, Alghabari F, Alsamadany H, Shahzad K, Yang SH (2022) Delineation of physiological, agronomic and genetic responses of different wheat genotypes under drought condition. Agronomy 12, 1056.
| Crossref | Google Scholar |
Sheoran S, Thakur V, Narwal S, Turan R, Mamrutha HM, Singh V, Tiwari V, Sharma I (2015) Differential activity and expression profile of antioxidant enzymes and physiological changes in wheat (Triticum aestivum L.) under drought. Applied Biochemistry and Biotechnology 177, 1282-1298.
| Crossref | Google Scholar |
Silveira JAG, Araújo SAM, Lima JPMS, Viégas RA (2009) Roots and leaves display contrasting osmotic adjustment mechanisms in response to NaCl-salinity in Atriplex nummularia. Environmental and Experimental Botany 66, 1-8.
| Crossref | Google Scholar |
Soliman MH, Alnusairi GSH, Khan AA, Alnusaire TS, Fakhr MA, Abdulmajeed AM, Aldesuquy HS, Yahya M, Najeeb U (2022) Biochar and selenium nanoparticles induce water transporter genes for sustaining carbon assimilation and grain production in salt-stressed wheat. Journal of Plant Growth Regulation 42, 1-22.
| Crossref | Google Scholar |
Taran N, Storozhenko V, Svietlova N, Batsmanova L, Shvartau V, Kovalenko M (2017) Effect of zinc and copper nanoparticles on drought resistance of wheat seedlings. Nanoscale Research Letters 12, 60.
| Crossref | Google Scholar |
Tilley MS, Heiniger RW, Crozier CR (2019) Tiller initiation and its effects on yield and yield components in winter wheat. Agronomy Journal 111, 1323-1332.
| Crossref | Google Scholar |
Ullah A, Al-Busaidi WM, Al-Sadi AM, Farooq M (2022) Bread wheat genotypes accumulating free proline and phenolics can better tolerate drought stress through sustained rate of photosynthesis. Journal of Soil Science and Plant Nutrition 22, 165-176.
| Crossref | Google Scholar |
Verbeke S, Padilla-Díaz CM, Martínez-Arias C, Goossens W, Haesaert G, Steppe K (2023) Mechanistic modeling reveals the importance of turgor-driven apoplastic water transport in wheat stem parenchyma during carbohydrate mobilization. New Phytologist 237, 423-440.
| Crossref | Google Scholar |
Vijayaraghavareddy P, Lekshmy SV, Struik PC, Makarla U, Yin X, Sreeman S (2022) Production and scavenging of reactive oxygen species confer to differential sensitivity of rice and wheat to drought stress. Crop and Environment 1, 15-23.
| Crossref | Google Scholar |
Wankmüller FJP, Carminati A (2022) Stomatal regulation prevents plants from critical water potentials during drought: result of a model linking soil–plant hydraulics to abscisic acid dynamics. Ecohydrology 15, e2386.
| Crossref | Google Scholar |
Yang H, Hu W, Zhao J, Huang X, Zheng T, Fan G (2021) Genetic improvement combined with seed ethephon priming improved grain yield and drought resistance of wheat exposed to soil water deficit at tillering stage. Plant Growth Regulation 95, 399-419.
| Crossref | Google Scholar |
Yang H, Xiao Y, He P, Ai D, Zou Q, Hu J, Liu Q, Huang X, Zheng T, Fan G (2022) Straw mulch-based no-tillage improves tillering capability of dryland wheat by reducing asymmetric competition between main stem and tillers. The Crop Journal 10, 864-878.
| Crossref | Google Scholar |
Yasmeen F, Razzaq A, Iqbal MN, Jhanzab HM (2015) Effect of silver, copper and iron nanoparticles on wheat germination. International Journal of Biosciences (IJB) 6, 112-117.
| Google Scholar |
Zada A, Ali A, Shah A, Gill S, Hussain I, Ullah Z, Sher H (2020) Physiological and molecular characterization of bread wheat (Triticum aestivum L.) for drought resistance [Preprint]. Authorea 1-12.
| Crossref | Google Scholar |
Zhang J, Zhang S, Cheng M, Jiang H, Zhang X, Peng C, Lu X, Zhang M, Jin J (2018) Effect of drought on agronomic traits of rice and wheat: a meta-analysis. International Journal of Environmental Research and Public Health 15, 839-852.
| Crossref | Google Scholar |
Zhang Q, Tang W, Peng S, Li Y (2022) Limiting factors for panicle photosynthesis at the anthesis and grain filling stages in rice (Oryza sativa L.). The Plant Journal 109, 77-91.
| Crossref | Google Scholar |
Zulfiqar B, Raza MAS, Saleem MF, Aslam MU, Iqbal R, Muhammad F, Amin J, Ibrahim MA, Khan IH (2022) Biochar enhances wheat crop productivity by mitigating the effects of drought: insights into physiological and antioxidant defense mechanisms. PLoS ONE 17, e0267819.
| Crossref | Google Scholar |