Abstract
Molybdenum (Mo) deficiency in the farmland can limit biological nitrogen fixation (BNF) and at the same time restricts the availability and uptake of nitrogen (N) by roots. However, the impact of Mo application on N bioavailability or BNF capacity in wheat-soil systems is still unclear. Mo was applied to the soil as 0 (− Mo) and 0.15 mg kg−1 soil (+ Mo) to investigate the impacts of Mo application on δ15N natural abundance in the wheat-soil system, and the activities of soil enzymes such as nitrogenase, nitrate reductase, and microbial biomass of N, and photosynthetic variables. Mo application increased the net photosynthetic rate, intercellular CO2 concentration, nitrogenase and nitrate reductase activities, and microbial biomass of N in wheat-soil system, suggesting that Mo enhances N bioavailability and reduces nitrate (NO3−) accumulation as well as improving the efficiency of N metabolism in wheat. Hence, N uptake and N concentrations were significantly increased among wheat tissues under Mo supply, except for root N concentration. Mo application significantly increased 15N fixation and δ15N abundance in soil by 92.2% and 10.8%, while in plant it is increased by 381.6% and 13.9%, respectively as compared with − Mo treatment, indicating that Mo application is vital for nitrogenase enzyme activity which converts atmospheric N2 into bioavailable NH3 and to provide N to terrestrial ecosystems. Mo plays a vital role in increasing BNF in Mo-deficient soil (≤ 0.082 mg kg−1) and Mo-insufficient wheat. These findings suggest that Mo application may increase soil N input in wheat-soil systems under Mo deficiency conditions.
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References
Andrews M, James EK, Sprent JI, Boddey RM, Gross E, dos Reis FB (2011) Nitrogen fixation in legumes and actinorhizal plants in natural ecosystems: values obtained using 15N natural abundance. Plant Ecol Divers 4:131–140. https://doi.org/10.1080/17550874.2011.644343
Ariz I, Cruz C, Neves T, Irigoyen JJ, Garcia-Olaverri C, Nogués S, Aparicio-Tejo PM, Aranjuelo I (2015) Leaf δ15N as a physiological indicator of the responsiveness of N2-fixing alfalfa plants to elevated [CO2], temperature and low water availability. Front Plant Sci 6:574. https://doi.org/10.3389/fpls.2015.00574
Barron AR, Wurzburger N, Bellenger JP, Wright SJ, Kraepiel AMLL, Hedin LO (2009) Molybdenum limitation of asymbiotic nitrogen fixation in tropical forest soils. Nat Geosci 2:42–45. https://doi.org/10.1038/ngeo366
Bellenger JP (2017) Biological nitrogen fixation by alternative nitrogenases in boreal cyanolichens: importance of molybdenum availability and implications for current biological nitrogen fixation estimates. New Phytol 213:680–689. https://doi.org/10.1111/nph.14166
Bellenger JP, Wichard T, Kustka AB, Kraepiel AML (2008) Uptake of molybdenum and vanadium by nitrogen-fixing soil bacterium using siderophores. Nat Geosci 1:243–246. https://doi.org/10.1038/ngeo161
Bibak A, Borggaard OK (1994) Molybdenum adsorption by aluminum and iron oxides and humic acid. Soil Sci 158:323–328. https://doi.org/10.1097/00010694-199411000-00003
Bittner F (2014) Molybdenum metabolism in plants and crosstalk to iron. Front Plant Sci 5:28. https://doi.org/10.3389/fpls.2014.00028
Boddey RM, Dobereiner J (1988) Nitrogen fixation associated with grasses and cereals: recent results and perspectives for future research. Plant Soil 108:53–65. https://doi.org/10.1007/BF02370099
Boddey RM, de Oliveira OC, Urquiaga S, Reis VM, de Olivares FL, Baldani VLD, Döbereiner J (1995) Biological nitrogen fixation associated with sugar cane and rice: contributions and prospects for improvement. In management of biological nitrogen fixation for the development of more productive and sustainable agricultural systems. Springer, Dordrecht, pp 195–209. https://doi.org/10.1007/978-94-011-0055-7_9
Boddey RM, Peoples MB, Palmer B, Dart PJ (2000) Use of the 15N natural abundance technique to quantify biological nitrogen fixation by woody perennials. Nutr Cycl Agroecosystems 57:235–270. https://doi.org/10.1023/A:1009890514844
Chalk PM (2018) Can N fertilizer use efficiency be estimated using 15N natural abundance? Soil Biol Biochem 126:191–193. https://doi.org/10.1016/j.soilbio.2018.08.028
Chalk PM, Craswell ET (2018) An overview of the role and significance of 15N methodologies in quantifying biological N2 fixation (BNF) and BNF dynamics in agro-ecosystems. Symbiosis 75:1–16. https://doi.org/10.1007/s13199-017-0526-z
Chalk PM, Inácio CT, Balieiro FC, Rouws JRC (2016a) Do techniques based on 15N enrichment and 15N natural abundance give consistent estimates of the symbiotic dependence of N2-fixing plants? Plant Soil 399:415–426. https://doi.org/10.1007/s11104-015-2689-9
Chalk PM, Lam SK, Chen D (2016b) 15N methodologies for quantifying the response of N2-fixing associations to elevated [CO2]: A review. Sci Total Environ 571:624–632. https://doi.org/10.1016/j.scitotenv.2016.07.030
Darnajoux R, Zhang X, McRose DL, Miadlikowska J, Lutzoni F, Kraepiel AML, Bellenger JP (2017) Biological nitrogen fixation by alternative nitrogenases in boreal cyanolichens: importance of molybdenum availability and implications for current biological nitrogen fixation estimates. New Phytol 213:680–689. https://doi.org/10.1111/nph.14166
Demtröder L, Narberhaus F, Masepohl B (2019) Coordinated regulation of nitrogen fixation and molybdate transport by molybdenum. Mol Microbiol 111:17–30. https://doi.org/10.1111/mmi.14152
Deutschbauer AM, Arkin AP, Adams MWW (2015) Molybdenum availability is key to nitrate removal in contaminated groundwater environments. Appl Environ Microbiol 81:4976–4983. https://doi.org/10.1128/AEM.00917-15
Diatta AA, Thomason WE, Abaye O, Thompson TL, Battaglia ML, Vaughan LJ, Lo M, Filho JFDCL (2020) Assessment of nitrogen fixation by mungbean genotypes in different soil textures using 15N natural abundance method. J Soil Sci Plant Nutr 20:2230–2240. https://doi.org/10.1007/s42729-020-00290-2
Elyamine AM, Moussa MG, Ismael MA, Wei J, Zhao Y, Wu Y, Hu C (2018) Earthworms, rice straw, and plant interactions change the organic connections in soil and promote the decontamination of cadmium in soil. Int J Environ Res Public Health 15:2398. https://doi.org/10.3390/ijerph15112398
Fallik E, Chan YK, Robson RL (1991) Detection of alternative nitrogenases in aerobic gram-negative nitrogen-fixing bacteria. J Bacteriol 173:365–371. https://doi.org/10.1128/jb.173.1.365-371.1991
Ge X, Vaccaro BJ, Thorgersen MP, Poole FL, Majumder EL, Zane GM, De León KB, Lancaster WA, Moon JW, Paradis CJ, von Netzer F, Stahl DA, Adams PD, Arkin AP, Wall JD, Hazen TC, Adams MWW (2019) Iron- and aluminium-induced depletion of molybdenum in acidic environments impedes the nitrogen cycle. Environ Microbiol 21:152–163. https://doi.org/10.1111/1462-2920.14435
Glass JB, Axler RP, Chandra S, Goldman CR (2012) Molybdenum limitation of microbial nitrogen assimilation in aquatic ecosystems and pure cultures. Front Microbiol 3:1–11. https://doi.org/10.3389/fmicb.2012.00331
He ZL, Yang XE, Stoffella PJ (2005) Trace elements in agroecosystems and impacts on the environment. J Trace Elem Med Biol 19:125–140. https://doi.org/10.1016/j.jtemb.2005.02.010
Herridge DF, Marcellos H, Felton WL, Turner GL, Peoples MB (1995) Chickpea increases soil-N fertility in cereal systems through nitrate sparing and N2 fixation. Soil Biol Biochem 27:545–551. https://doi.org/10.1016/0038-0717(95)98630-7
Högberg P (1997) Tansley review no. 95 natural abundance in soil-plant systems. New Phytol 137:179–203. https://doi.org/10.1046/j.1469-8137.1997.00808.x
Houngnandan P, Yemadje RGH, Oikeh SO, Djidohokpin CF, Boeckx P, Van Cleemput O (2008) Improved estimation of biological nitrogen fixation of soybean cultivars (Glycine max L. Merril) using 15N natural abundance technique. Biol Fertil Soils 45: 175–183. https://doi.org/10.1007/s00374-008-0311-5
Hungate BA, Stiling PD, Dijkstra P, Johnson DW, Ketterer ME, Hymus GJ, Hinkle CR, Drake BG (2004) CO2 elicits long-term decline in nitrogen fixation. Science 304. https://doi.org/10.1126/science.1095549
Imran M, Hu C, Hussain S, Rana MS, Riaz M, Afzal J, Aziz O, Elyamine AM, Ismael MA, Sun X (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, Sun X, Hussain S, Hussain S, Ali U, Rana MS, Rasul F, Saleem MH, Moussa MG, Bhantana P, Afzal J, Elyamine AM, Hu C (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
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 19:2163. https://doi.org/10.3390/ijms19082163
Jean ME, Phalyvong K, Forest-Drolet J, Bellenger JP (2013) Molybdenum and phosphorus limitation of asymbiotic nitrogen fixation in forests of Eastern Canada: influence of vegetative cover and seasonal variability. Soil Biol Biochem 67:140–146. https://doi.org/10.1016/j.soilbio.2013.08.018
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
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
Larmoia T, Leppanen SM, Tuittila ES, Aarva M, Merila P, Fritze H, Tiirola M (2014) Methanotrophy induces nitrogen fixation during peatland development. Proc Natl Acad Sci U S A 111:734–739. https://doi.org/10.1073/pnas.1314284111
Lassaletta L, Billen G, Grizzetti B, Grizzetti B, Anglade J, Garnier J (2014) 50 year trends in nitrogen use efficiency of world cropping systems: the relationship between yield and nitrogen input to cropland. Environ Res Lett 9:105011. https://doi.org/10.1088/1748-9326/9/10/105011
Lo M, Filho JFDCL (2020) Assessment of nitrogen fixation by mungbean genotypes in different soil textures using 15N natural abundance method. J Soil Sci Plant Nutr 20:2230–2240. https://doi.org/10.1007/s42729-020-00290-2
Ma J, Bei Q, Wang X, Lan P, Liu G, Lin X, Liu Q, Lin Z, Liu B, Zhang Y, Jin H, Hu T, Zhu J, Xie Z (2019) Impacts of Mo application on biological nitrogen fixation and diazotrophic communities in a flooded rice-soil system. Sci Total Environ 649:686–694. https://doi.org/10.1016/j.scitotenv.2018.08.318
MacLeod KC, Holland PL (2013) Recent developments in the homogeneous reduction of dinitrogen by molybdenum and iron. Nat Chem 5:559–565. https://doi.org/10.1038/nchem.1620
Majda C, Khalid D, Aziz A, Rachid B, Badr AS, Lotfi A, Mohamed B (2019) Nutri-priming as an efficient means to improve the agronomic performance of molybdenum in common bean (Phaseolus vulgaris L.). Sci Total Environ 661:654–663. https://doi.org/10.1016/j.scitotenv.2019.01.188
Marks JA, Perakis SS, King EK, Pett-Ridge J (2015) Soil organic matter regulates molybdenum storage and mobility in forests. Biogeochemistry 125:167–183. https://doi.org/10.1007/s10533-015-0121-4
Moussa MG, Sun X, Ismael MA, Elyamine AM, Rana MS, Syaifudin M, Hu C (2021a) Molybdenum-induced effects on grain yield, macro–micro-nutrient uptake, and allocation in mo-inefficient winter wheat. J Plant Growth Regul 1–16. https://doi.org/10.1007/s00344-021-10397-0
Moussa MG, Hu C, Elyamine AM, Ismael MA, Rana MS, Imran M, Syaifudin M, Tan Q, Marty C, Sun X (2021b) Molybdenum-induced effects on nitrogen uptake efficiency and recovery in wheat (Triticum aestivum L.) using 15N-labeled nitrogen with different N forms and rates. J Plant Nutr Soil Sci 184:613–621. https://doi.org/10.1002/jpln.202100040
Peoples MB, Chalk PM, Unkovich MJ, Boddey RM (2015) Can differences in 15N natural abundance be used to quantify the transfer of nitrogen from legumes to neighbouring non-legume plant species? Soil Biol. Biochem 87:97–109. https://doi.org/10.1016/j.soilbio.2015.04.010
Pereira W, Oliveira RP, Pereira A, Sousa JS, Schultz N, Urquiaga S, Reis VM (2021) Nitrogen acquisition and 15N-fertiliser recovery efficiency of sugarcane cultivar RB92579 inoculated with five diazotrophs. Nutr Cycl Agroecosystems 119:37–50. https://doi.org/10.1007/s10705-020-10100-x
Rana MS, Hu CX, Shaaban M, Imran M, Afzal J, Moussa MG, Elyamine AM, Bhantana P, Saleem MH, Syaifudin M, Kamran M, Shah MA, Sun X (2020a) Soil phosphorus transformation characteristics in response to molybdenum supply in leguminous crops. J Environ Manag 268:110610. https://doi.org/10.1016/j.jenvman.2020.110610
Rana MS, Sun X, Imran M, Ali S, Shaaban M, Moussa MG, Khan Z, Afzal J, Binyamin R, Bhantana P, Alam M, Din IU, Younas M, Hu C (2020b) Molybdenum-induced effects on leaf ultra-structure and rhizosphere phosphorus transformation in Triticum aestivum L. Plant Physiol Biochem 153:20–29. https://doi.org/10.1016/j.plaphy.2020.05.010
Rana MS, Sun X, Imran M, Khan Z, Moussa MG, Abbas M, Bhantana P, Syaifudin M, Din IU, Younas M, Shah MA, Afzal J, Hu C (2020c) Mo-inefficient wheat response toward molybdenum supply in terms of soil phosphorus availability. J Soil Sci Plant Nutr 20:1560–1573. https://doi.org/10.1007/s42729-020-00298-8
Reed SC, Cleveland CC, Townsend AR (2013) Relationships among phosphorus, molybdenum and free-living nitrogen fixation in tropical rain forests: Results from observational and experimental analyses. Biogeochemistry 114:135–147. https://doi.org/10.1007/s10533-013-9835-3
Rice WA, Paul EA (1971) The acetylene reduction assay for measuring nitrogen fixation in waterlogged soil. Can J Microbiol 17:1049–1056. https://doi.org/10.1139/m71-166
Robinson D (2001) δ15N as an integrator of the nitrogen cycle. Trends Ecol Evol 16:153–162. https://doi.org/10.1016/S0169-5347(00)02098-X
Rousk K, Degboe J, Michelsen A, Bradley R, Bellenger JP (2017) Molybdenum and phosphorus limitation of moss-associated nitrogen fixation in boreal ecosystems. New Phytol 214:97–107. https://doi.org/10.1111/nph.14331
Shearer G, Kohl DH (1988) Natural15N abundance as a method of estimating the contribution of biologically fixed nitrogen to N2-fixing systems: potential for non-legumes. Plant Soil 110:317–327. https://doi.org/10.1007/BF02226812
Shearer G, Kohl DH (1989) Natural 15N abundance as a method of estimating the contribution of biologically fixed nitrogen to N2-fixing systems: potential for non-legumes. In: Nitrogen fixation with non-legumes. Springer, Dordrecht, pp 289–299. https://doi.org/10.1007/978-94-009-0889-5_33
Stiefel EI (2002) The biogeochemistry of molybdenum and tungsten. In: Metals ions in biological system: molybdenum and tungsten: their roles in biological processes. CRC Press 39:1–29. https://doi.org/10.1201/9780203909331
Stüeken EE, Buick R, Guy BM, Koehler MC (2015) Isotopic evidence for biological nitrogen fixation by molybdenum-nitrogenase from 3.2 Gyr. Nature 520:666–669. https://doi.org/10.1038/nature14180
Thorgersen MP, Lancaster WA, Vaccaro BJ, Poole FL, Rocha AM, Mehlhorn T, Pettenato A, Ray J, Waters RJ, Melnyk RA, Chakraborty R, Hazen TC, Deutschbauer AM, Arkin AP, Adams MWW (2015) Molybdenum availability is key to nitrate removal in contaminated groundwater environments. Appl Environ Microbiol 81:4976–4983. https://doi.org/10.1128/AEM.00917-15
Wen X, Hu C, Sun X, Zhao X, Tan Q, Liu P, Xin J, Qin S, Wang P (2018) Characterization of vegetable nitrogen uptake and soil nitrogen transformation in response to continuous molybdenum application. J Plant Nutr Soil Sci 181:516–527. https://doi.org/10.1002/jpln.201700556
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 26:2363–2374. 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
Wieder WR, Cleveland CC, Smith WK, Todd-Brown K (2015) Future productivity and carbon storage limited by terrestrial nutrient availability. Nat Geosci 8:441–444. https://doi.org/10.1038/ngeo2413
Wu S, Hu C, Tan Q, Nie Z, Sun X (2014) Effects of molybdenum on water utilization, antioxidative defense system and osmotic-adjustment ability in winter wheat (Triticum aestivum) under drought stress. Plant Physiol Biochem 83:365–374. https://doi.org/10.1016/j.plaphy.2014.08.022
Wu S, Hu C, Tan Q, Xu S, Sun X (2017) Nitric oxide mediates molybdenum-induced antioxidant defense in wheat under drought stress. Front Plant Sci 8:1085. https://doi.org/10.3389/fpls.2017.01085
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
Wurzburger N, Bellenger JP, Kraepiel AML, Hedin LO (2012) Molybdenum and phosphorus interact to constrain asymbiotic nitrogen fixation in tropical forests. PLoS ONE 7:e33710. https://doi.org/10.1371/journal.pone.0033710
Xu Y, He J, Cheng W, Xing X, Li L (2010) Natural 15N abundance in soils and plants in relation to N cycling in a rangeland in Inner Mongolia. J Plant Ecol 3:201–207. https://doi.org/10.1093/jpe/rtq023
Yoneyama T, Kouno K, Yazaki J, Kouno K, Yazaki J (1990) Variation of natural 15N abundance of crops and soils in Japan with special reference to the effect of soil conditions and fertilizer application. Soil Sci Plant Nutr 36:667–675. https://doi.org/10.1080/00380768.1990.10416804
Yun SI, Ro HM (2009) Natural 15N abundance of plant and soil inorganic-N as evidence for over-fertilization with compost. Soil Biol Biochem 41:1541–1547. https://doi.org/10.1016/j.soilbio.2009.04.014
Zhang Y, Gladyshev VN (2008) Molybdoproteomes and evolution of molybdenum utilization. J Mol Biol 379:881–899. https://doi.org/10.1016/j.jmb.2008.03.051
Zhang X, Davidson EA, Mauzerall DL, Searchinger TD, Dumas P, Shen Y (2015) Managing nitrogen for sustainable development. Nature 528:51–59. https://doi.org/10.1038/nature15743
Zou C, Gao X, Shi R, et al (2008) Micronutrient deficiencies in crop production in China. Micronutr Defic Glob Crop Prod 127–148. https://doi.org/10.1007/978-1-4020-6860-7_5
Acknowledgements
The authors thank Prof. Soliman M. Soliman., Prof. Yehia G. M. Galal., and Prof. Hussein A. Abdelaziz., from Soil & Water Research Department, Egyptian Atomic Energy Authority, for valuable suggestions to improve the early version of the manuscript. The authors would also like to thank Dr. Ibrahim A. A. Mohamed, Faculty of Agriculture, Fayoum University, for his suggestions that helped us to improve the manuscript.
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This work was supported by Hubei Province Technological Innovation Major Project (2018ABA079), the National Natural Science Foundation of China (Program No. 42077095), and Open Project for Hubei Key Laboratory of Economic Forest Germplasm Improvement and Resources Comprehensive Utilization (202020404), MGM, acknowledge CSC for his PhD scholarship (CSC No 2017GBJ001669).
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M. G. M., C. H., and X. S. conceived and designed the experiment; M. G. M., S. E., and A. M. conducted the experiment; M. H. S., M. R., Z. D., L. H., and M. A. I. handled data curation, analysis, and visualization; S. E. and X. S. provided statistical guidance; M. G. M. and M. A. I. wrote the manuscript; all authors have revised the manuscript.
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Moussa, M.G., Sun, X., El-Tohory, S. et al. Molybdenum Role in Nitrogen Bioavailability of Wheat-Soil System Using the Natural 15N Abundance Technique. J Soil Sci Plant Nutr 22, 3611–3624 (2022). https://doi.org/10.1007/s42729-022-00913-w
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DOI: https://doi.org/10.1007/s42729-022-00913-w