Abstract
Molybdenum (Mo) is an essential element for the growth and development of higher plants. Its deficiency leads to a decrease in wheat (Triticum aestivum L.) growth and reduces nutritional quality of grain. However, little is known about macro- and micro-nutrient contents or their allocation within organs of wheat under Mo sufficient and deficient conditions. The objective of this study was to gain a better understanding of how Mo application affects mineral nutrient uptake and allocations among various organs of wheat. A pot experiment was conducted to explore these effects in wheat with Mo-deficiency (–Mo) and Mo supply (+ Mo) treatment. The results revealed that Mo application increased plant dry biomass, grain yield, allocations of macro-nutrients (nitrogen (N), phosphorus (P), and potassium (K)), and micro-nutrients (copper (Cu), iron (Fe), manganese (Mn), zinc (Zn), and molybdenum (Mo)) among different wheat organs except for Fe. Nutrient allocation to plant tissues also varied between different organs. A high allocation of N, P, and Zn was observed in grain, K and Cu higher allocation was found in the stem, while flag leaf and glumes accumulated higher content of Mn and Mo, under Mo application as compared with Mo deficiency treatment. Mo application increased the uptake of N, P, K, Cu, Fe, Mn, Zn, and Mo in wheat organs compared to –Mo treatment. The relative increase of N, P, K, Cu, Fe, Mn, Zn and Mo uptake in the wheat grains was 58.5%, 13.0%, 29.7%, 20.2%, 31.5%, 12.7%, 52.8% and 621%, while in the flag leaf was 199.1%, 198.5%, 203.4%, 713.7%, 281.0%, 179.1%, 128.6% and 431.5%, respectively. The research findings suggest the supportive role of Mo application in increasing macro- and micro-nutrient uptake among wheat organs and grain yield through improving macro–micro-nutrient allocations.
Similar content being viewed by others
References
Alejandro S, Höller S, Meier B, Peiter E (2020) Manganese in plants: from acquisition to subcellular allocation. Front Plant Sci. https://doi.org/10.3389/fpls.2020.00300
Barron AR, Wurzburger N, Bellenger JP, Wright SJ, Kraepiel AML, Hedin LO (2009) Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nat Geosci. https://doi.org/10.1038/ngeo366
Bhantana P, Rana MS, Sun X, Moussa MG et al (2021) Arbuscular mycorrhizal fungi and its major role in plant growth, zinc nutrition, phosphorous regulation and phytoremediation. Symbiosis. https://doi.org/10.1007/s13199-021-00756-6
Bittner F (2014) Molybdenum metabolism in plants and crosstalk to iron. Front Plant Sci. https://doi.org/10.3389/fpls.2014.00028
Chen C, Chen H, He Y, Xia R (2018) TBtools, a Toolkit for Biologists integrating various biological data handling tools with a user-friendly interface. bioRxiv. https://doi.org/10.1101/289660
Guha T, Mukherjee A, Kundu R (2021) Nano-scale zero valent iron (nZVI) priming enhances yield, alters mineral distribution and grain nutrient content of Oryza sativa L. cv. Gobindobhog: A Field Study. J Plant Growth Regul. https://doi.org/10.1007/s00344-021-10335-0
Han LZ, Wei X, Wan D, He W, Wang X, Xiong Y (2020) Effect of molybdenum on plant physiology and cadmium uptake and translocation in rape (Brassica napus l.) Under different levels of cadmium stress. Int J Environ Res Public Health. https://doi.org/10.3390/ijerph17072355
Hu C, Wang Y, Wei W (2002) Effect of molybdenum applications on concentrations of free amino acids in winter wheat at different growth stages. J Plant Nutr 25:1487–1499. https://doi.org/10.1081/PLN-120005404
Imran M, Sun X, Hussain S et al (2019b) Molybdenum-induced effects on nitrogen metabolism enzymes and elemental profile of winter wheat (Triticum aestivum L.) under different nitrogen sources. Int J Mol Sci 20:3009. https://doi.org/10.3390/ijms20123009
Imran M, Hu C, Hussain S et al (2019a) Molybdenum-induced effects on photosynthetic efficacy of winter wheat (Triticum aestivum L.)under different nitrogen sources are associated with nitrogen assimilation. Plant Physiol Biochem 141:154–163. https://doi.org/10.1016/j.plaphy.2019.05.024
Imran M, Hussain S, El-Esawi MA et al (2020) Molybdenum supply alleviates the cadmium toxicity in fragrant rice by modulating oxidative stress and antioxidant gene expression. Biomolecules 10:1–17. https://doi.org/10.3390/biom10111582
Imran M, Sun X, Hussain S, Rana MS, Saleem MH, Riaz M, Tang X, Khan I, Hu C (2021b) Molybdenum supply increases root system growth of winter wheat by enhancing nitric oxide accumulation and expression of NRT genes. Plant Soil. https://doi.org/10.1007/s11104-020-04765-0
Imran M, Hussain S, Rana MS et al (2021a) Molybdenum improves 2-acetyl-1-pyrroline, grain quality traits and yield attributes in fragrant rice through efficient nitrogen assimilation under cadmium toxicity. Ecotoxicol Environ Saf. https://doi.org/10.1016/j.ecoenv.2021.111911
Ismael MA, Elyamine AM, Zhao YY, Moussa MG, Rana MS, Afzal J, Imran M, Zhao XH, Hu CX (2018) Can selenium and molybdenum restrain cadmium toxicity to pollen grains in brassica napus? Int J Mol Sci. https://doi.org/10.3390/ijms19082163
Jat ML, Bijay-Singh, Gerard B (2014) Nutrient management and use Efficiency in wheat systems of south Asia. In: Advances in Agronomy. https://doi.org/10.1016/B978-0-12-800137-0.00005-4
Kaiser BN, Gridley KL, Brady JN, Phillips T, Tyerman SD (2005) The role of molybdenum in agricultural plant production. Ann Bot 96:745–754. https://doi.org/10.1093/aob/mci226
Kaur N, Kaur H, Mavi GS (2020) Assessment of nutritional and quality traits in biofortified bread wheat genotypes. Food Chem. https://doi.org/10.1016/j.foodchem.2019.125342
Kihara J, Bolo P, Kinyua M, Rurinda J, Piikki K (2020) Micronutrient deficiencies in African soils and the human nutritional nexus: opportunities with staple crops. Environ Geochem Health. https://doi.org/10.1007/s10653-019-00499-w
Kovács B, Puskás-Preszner A, Huzsvai L, Lévai L, Bódi É (2015) Effect of molybdenum treatment on molybdenum concentration and nitrate reduction in maize seedlings. Plant Physiol Biochem 96:38–44. https://doi.org/10.1016/j.plaphy.2015.07.013
Kumar A, Maurya BR, Raghuwanshi R, Meena VS, Tofazzal Islam M (2017) Co-inoculation with enterobacter and rhizobacteria on yield and nutrient uptake by wheat (Triticum aestivum L.) in the alluvial soil under indo-gangetic plain of India. J Plant Growth Regul. https://doi.org/10.1007/s00344-016-9663-5
Laskowski W, Górska-Warsewicz H, Rejman K, Czeczotko M, Zwolińska J (2019) How important are cereals and cereal products in the average polish diet? Nutrients. https://doi.org/10.3390/nu11030679
Li H, Li J, He Y, Li S, Liang Z, Peng C, Polle A, Bin LZ (2013) Changes in carbon, nutrients and stoichiometric relations under different soil depths, plant tissues and ages in black locust plantations. Acta Physiol Plant. https://doi.org/10.1007/s11738-013-1326-6
Liu H, Hu C, Sun X, Tan Q, Nie Z, Hu X (2010) Interactive effects of molybdenum and phosphorus fertilizers on photosynthetic characteristics of seedlings and grain yield of Brassica napus. Plant Soil 326:345–353. https://doi.org/10.1007/s11104-009-0014-1
Liu L, Xiao W, Li L, Li DM, Gao DS, Zhu CY, Fu XL (2017) Effect of exogenously applied molybdenum on its absorption and nitrate metabolism in strawberry seedlings. Plant Physiol Biochem. https://doi.org/10.1016/j.plaphy.2017.03.015
Lv X, Zhang Y, Hu L, Zhang Y, Zhang B, Xia H, Du W, Fan S, Kong L (2021) Low-nitrogen stress stimulates lateral root initiation and nitrogen assimilation in wheat: Roles of phytohormone signaling. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10112-5
Machado R, Serralheiro R (2017) Soil salinity: effect on vegetable crop growth. Management practices to prevent and mitigate soil salinization. Horticulturae 3:30
Makoil JHJR, Bambara S, Ndakidemii PA (2013) Rhizobium inoculation and the supply of molybdenum and lime affect the uptake of macroelements in common bean (P. vulgaris L.) plants. Aust J Crop Sci 7:784–793
Mendel RR, Schwarz G (2011) Molybdenum cofactor biosynthesis in plants and humans. Coord Chem Rev 255:1145–1158. https://doi.org/10.1016/j.ccr.2011.01.054
Modi AT (2002) Wheat seed quality in response to molybdenum and phosphorus. J Plant Nutr. https://doi.org/10.1081/PLN-120014703
Mohamed IAA, Shalby N, El-Badri AMA et al (2020) Stomata and xylem vessels traits improved by melatonin application contribute to enhancing salt tolerance and fatty acid composition of Brassica napus L. plants. Agronomy 10:1186
Nadeem F, Farooq M (2019) Application of micronutrients in rice-wheat cropping system of south Asia. Rice Sci. https://doi.org/10.1016/j.rsci.2019.02.002
Ndakidemi PA, Bambara S, Makoi JHJR (2011) Micronutrient uptake in common bean (Phaseolus vulgaris L.) as affected by Rhizobium inoculation, and the supply of molybdenum and lime. Plant Omics 4:40–52.
Nie Z, Hu C, Liu H, Tan Q, Sun X (2014) Differential expression of molybdenum transport and assimilation genes between two winter wheat cultivars (Triticum aestivum). Plant Physiol Biochem 82:27–33. https://doi.org/10.1016/j.plaphy.2014.05.002
Nie Z, Li S, Hu C, Sun X, Tan Q, Liu H (2015) Effects of molybdenum and phosphorus fertilizers on cold resistance in winter wheat. J Plant Nutr 38:808–820. https://doi.org/10.1080/01904167.2014.939289
Rana A, Joshi M, Prasanna R, Shivay YS, Nain L (2012) Biofortification of wheat through inoculation of plant growth promoting rhizobacteria and cyanobacteria. Eur J Soil Biol. https://doi.org/10.1016/j.ejsobi.2012.01.005
Rana MS, Sun X, Imran M et al (2020c) Mo-Inefficient wheat response toward molybdenum supply in terms of soil phosphorus availability. J Soil Sci Plant Nutr. https://doi.org/10.1007/s42729-020-00298-8
Rana MS, Sun X, Imran M et al (2020b) Molybdenum-induced effects on leaf ultra-structure and rhizosphere phosphorus transformation in Triticum aestivum L. Plant Physiol Biochem. https://doi.org/10.1016/j.plaphy.2020.05.010
Rana MS, Hu CX, Shaaban M et al (2020a) Soil phosphorus transformation characteristics in response to molybdenum supply in leguminous crops. J Environ Manage 268:110610. https://doi.org/10.1016/j.jenvman.2020.110610
Shi Z, Zhang J, Wang F, Li K, Yuan W, Liu J (2018) Arbuscular mycorrhizal inoculation increases molybdenum accumulation but decreases molybdenum toxicity in maize plants grown in polluted soil. RSC Adv. https://doi.org/10.1039/C8RA07725H
Shoaib Rana M, Bhantana P, Sun X, et al (2020) Molybdenum as an essential element for crops: an overview. Biomed J Sci Tech Res 24:18535–18547. https://doi.org/10.26717/BJSTR.2020.24.004104
Sun W, Selim HM (2017) Molybdenum-phosphate retention and transport in soils. Geoderma. https://doi.org/10.1016/j.geoderma.2017.08.031
Sun X, Hu C, Tan Q, Liu J, Liu H (2009) Effects of molybdenum on expression of cold-responsive genes in abscisic acid (ABA)-dependent and ABA-independent pathways in winter wheat under low-temperature stress. Ann Bot. https://doi.org/10.1093/aob/mcp133
Swarbreck SM, Wang M, Wang Y, Kindred D, Sylvester-Bradley R, Shi W, Varinderpal-Singh BAR, Griffiths H (2019) A roadmap for lowering crop nitrogen requirement. Trends Plant Sci. https://doi.org/10.1016/j.tplants.2019.06.006
Tripathi DK, Singh S, Singh S, Mishra S, Chauhan DK, Dubey NK (2015) Micronutrients and their diverse role in agricultural crops: advances and future prospective. Acta Physiol. Plant. https://doi.org/10.1007/s11738-015-1870-3
Wang F, Wang Z, Kou C, Ma Z, Zhao D (2016) Responses of wheat yield, macro- and micro-nutrients, and heavy metals in soil and wheat following the application of manure compost on the North China Plain. PLoS ONE. https://doi.org/10.1371/journal.pone.0146453
Wen X, Hu C, Sun X, Zhao X, Tan Q (2019) Research on the nitrogen transformation in rhizosphere of winter wheat (Triticum aestivum) under molybdenum addition. Environ Sci Pollut Res. https://doi.org/10.1007/s11356-018-3565-y
Wichard T, Mishra B, Myneni SCB, Bellenger JP, Kraepiel AML (2009) Storage and bioavailability of molybdenum in soils increased by organic matter complexation. Nat Geosci 2:625–630. https://doi.org/10.1038/ngeo589
Wu S, Hu C, Tan Q, Zhao X, Xu S, Xia Y, Sun X (2018) Nitric oxide acts downstream of abscisic acid in molybdenum-induced oxidative tolerance in wheat. Plant Cell Rep. https://doi.org/10.1007/s00299-018-2254-0
Wu S, Sun X, Tan Q, Hu C (2019) Molybdenum improves water uptake via extensive root morphology, aquaporin expressions and increased ionic concentrations in wheat under drought stress. Environ Exp Bot 157:241–249. https://doi.org/10.1016/j.envexpbot.2018.10.013
Yu M, Hu C, Wang Y (1999) Influences of seed molybdenum and molybdenum application on nitrate reductase activity, shoot dry matter, and grain yields of winter wheat cultivars. J Plant Nutr 22:1433–1441. https://doi.org/10.1080/01904169909365724
Yu M, Hu CX, Wang YH (2002) Molybdenum efficiency in winter wheat cultivars as related to molybdenum uptake and distribution. Plant Soil 245:287–293. https://doi.org/10.1023/A:1020497728331
Yu M, Hu CX, Sun X, Wang YH (2010) Influences of Mo on nitrate reductase, glutamine synthetase and nitrogen accumulation and utilization in Mo-efficient and Mo-inefficient winter wheat cultivars. Agric Sci China 9:355–361. https://doi.org/10.1016/S1671-2927(09)60104-8
Zahedifar M, Karimian N, Ronaghi A, Yasrebi J, Emam Y (2011) Soil-plant nutrient relationship at different growth stages of spinach as affected by phosphorus and manure applications. Commun Soil Sci Plant Anal. https://doi.org/10.1080/00103624.2011.587567
Zakikhani H, Yusop MK, Anuar AR, Radziah O, Soltangheisi A (2014) Effects of different levels of molybdenum on uptake of nutrients in rice cultivars. Asian J Crop Sci. https://doi.org/10.3923/ajcs.2014.236.244
Zhang M, Hu C, Zhao X, Tan Q, Sun X, Cao A, Cui M, Zhang Y (2012) Molybdenum improves antioxidant and osmotic-adjustment ability against salt stress in Chinese cabbage (Brassica campestris L. ssp. Pekinensis). Plant Soil. https://doi.org/10.1007/s11104-011-1109-z
Zou C, Gao X, Shi R, Fan X, Zhang F (2008) Micronutrient deficiencies in crop production in China. Micronutr Defic Glob Crop Prod. https://doi.org/10.1007/978-1-4020-6860-7_5
Acknowledgements
This work was supported by the National Natural Science Foundation of China (Program No. 41771329), the National Key R&D Program of China (2016YFD0200108) and the 948 Project from the Ministry of Agriculture of China (2016X41). MGM, acknowledge CSC for his PhD scholarship (CSC No 2017GBJ001669). MGM would like to thank Prof. Yehia G.M. Galal from Soil & Water Research Department, Egyptian Atomic Energy Authority, for improving the early version of the manuscript.
Author information
Authors and Affiliations
Contributions
M.G.M., C.H., and X.S. conceived and designed the experiment; M.G.M., and M.A.I conducted the experiment; A.M.E., M.S.R., and M.S. helped to analyze the data, investigation, and software; M.A.I., and X.S. provided statistical guidance; M.G.M. wrote the draft manuscript; All authors have revised the manuscript.
Corresponding author
Ethics declarations
Conflict of Interest
The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.
Additional information
Handling Editor: Rhonda Peavy.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Moussa, M.G., Sun, X., Ismael, M.A. et al. Molybdenum-Induced Effects on Grain Yield, Macro–micro-nutrient Uptake, and Allocation in Mo-Inefficient Winter Wheat. J Plant Growth Regul 41, 1516–1531 (2022). https://doi.org/10.1007/s00344-021-10397-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-021-10397-0