Zinc nutrition and arbuscular mycorrhizal symbiosis effects on maize (Zea mays L.) growth and productivity
Status PubMed-not-MEDLINE Jazyk angličtina Země Saúdská Arábie Médium print-electronic
Typ dokumentu časopisecké články, přehledy
PubMed
34759753
PubMed Central
PMC8568715
DOI
10.1016/j.sjbs.2021.06.096
PII: S1319-562X(21)00569-6
Knihovny.cz E-zdroje
- Klíčová slova
- Extraradical hyphae, Mycorrhizal colonization, Nutrient deficiency, Nutrient toxicity, Stunted growth, Symbiosis, Zinc,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Zinc (Zn) is an essential micronutrient required to enhance crop growth and yield. In the arid - semiarid region, Zn deficiency is expected due to alkaline calcareous soil. Contrarily, Zn toxicity is also becoming an environmental concern due to increasing anthropogenic activities (metal smelting, copper industry, etc.). Therefore, balanced Zn application is necessary to save resources and achieve optimum crop growth and yield. Most scientists suggest biological approaches to overcome the problem of Zn toxicity and deficiency. These biological approaches are mostly environment-friendly and cost-effective. In these biological approaches, the use of arbuscular mycorrhizae fungi (AMF) symbiosis is becoming popular. It can provide tolerance to the host plant against Zn-induced stress. Inoculation of AMF helps in balance uptake of Zn and enhances the growth and yield of crops. On the other hand, maize (Zea mays L.) is an important cereal crop due to its multifarious uses. As maize is an effective host for mycorrhizae symbiosis, that's why this review was written to elaborate on the beneficial role of arbuscular mycorrhizal fungi (AMF). The review aimed to glance at the recent advances in the use of AMF to enhance nutrient uptake, especially Zn. It was also aimed to discuss the mechanism of AMF to overcome the toxic effect of Zn. We have also discussed the detailed mechanism and physiological improvement in the maize plant. In conclusion, AMF can play an imperative role in improving maize growth, yield, and balance uptake of Zn by alleviating Zn stress and mitigating its toxicity.
City of Scientific Research and Technology Applications New Burg Al Arab Alexandria Egypt
Department of Agronomy The University of Haripur Haripur 22620 Pakistan
Institute of Bioproduct Development Skudai Johor Bahru Johor Malaysia
Sinarmas Forestry Corporate Research and Development Perawang 28772 Indonesia
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Abaid-Ullah M., Hassan M.N., Jamil M., Brader G., Shah M.K.N., Sessitsch A., Hafeez F.Y. Plant growth promoting rhizobacteria: An alternate way to improve yield and quality of wheat (Triticum aestivum) Int. J. Agric. Biol. 2015;17:51–60.
Abd-Elfattah A., Wada K. Adsorption of lead, copper, zinc, cobalt and cadmium by soils that differ in cation-exchange materials. J. Soil Sci. 1981;32:271–283. doi: 10.1111/j.1365-2389.1981.tb01706.x. DOI
Adnan M. Integrated effect of phosphorous and zinc on wheat quality and soil properties. Adv. Environ. Biol. 2016;10:40–45.
Akhtar, M., Yousaf, S., Sarwar, N., Hussain, S., 2019. Zinc biofortification of cereals—role of phosphorus and other impediments in alkaline calcareous soils. Environ. Geochem. Health. https://doi.org/10.1007/s10653-019-00279-6 PubMed
Alam M.Z., Hoque M.A., Ahammed G.J., Carpenter-Boggs L. Effects of arbuscular mycorrhizal fungi, biochar, selenium, silica gel, and sulfur on arsenic uptake and biomass growth in Pisum sativum L. Emerg. Contam. 2020;6:312–322. doi: 10.1016/j.emcon.2020.08.001. DOI
Alam M.Z., McGee R., Hoque M.A., Ahammed G.J., Carpenter-Boggs L. Effect of arbuscular mycorrhizal Fungi, Selenium and biochar on photosynthetic pigments and antioxidant enzyme activity under arsenic stress in Mung Bean (Vigna radiata) Front. Physiol. 2019;10:193. doi: 10.3389/fphys.2019.00193. PubMed DOI PMC
Ali H., Khan E., Ilahi I. Environmental chemistry and ecotoxicology of hazardous heavy metals: Environmental persistence, toxicity, and bioaccumulation. J. Chem. 2019;5:2019. doi: 10.1155/2019/6730305. DOI
Alloway B.J. Zinc in soils and crop nutrition. International Zinc Association, Brussels, International Fertilizer Industry Association, Paris. 2008 doi: 10.1016/S0065-2113(06)94003-6. DOI
Almagrabi O.A., Abdelmoneim T.S. Using of arbuscular mycorrhizal fungi to reduce the deficiency effect of phosphorous fertilization on maize plants (Zea mays L.) Life Sci. J. 2012;9:1648–1654.
Alqarawi A.A., Abd Allah E.F., Hashem A. Alleviation of salt-induced adverse impact via Mycorrhizal fungi in Ephedra Aphylla Forssk. J. Plant Interact. 2014;9:802–810. doi: 10.1080/17429145.2014.949886. DOI
Amiri A., Baninasab B., Ghobadi C., Khoshgoftarmanesh A.H. Zinc soil application enhances photosynthetic capacity and antioxidant enzyme activities in almond seedlings affected by salinity stress. Photosynthetica. 2016;54:267–274. doi: 10.1007/s11099-016-0078-0. DOI
Anamikaagarwal J., Singh A.P. Arbuscular mycorrhizal fungi and its role in sequestration of heavy metals. Trends Biosci. 2017;10:2017–2110.
Ansori A., Gholami A. Improved nutrient uptake and growth of maize in response to inoculation with thiobacillus and mycorrhiza on an alkaline Soil. Commun. Soil Sci. Plant Anal. 2015;46:2111–2126. doi: 10.1080/00103624.2015.1048251. DOI
Arain M.Y., Memon K.S., Akhtar M.S., Memon M. Soil and plant nutrient status and spatial variability for sugarcane in lower Sindh (Pakistan) Pakistan J. Bot. 2017;49:531–540.
Arnold J.M., Bauman L.F. Inheritance of and interrelationships among maize kernel traits and elemental contents 1. Crop Sci. 1976;16:439–440. doi: 10.2135/cropsci1976.0011183x001600030034x. DOI
Arshad, M., Adnan M., Ali A., Khan A.K., Khan F., Khan A., Kamal M.A., Alam M., Ullah H., Saleem A., Hussain A., Shahwar D. Integrated effect of phosphorous and zinc on wheat quality and soil properties. Advances in Environmental Biology. 2016;10(2):40–45.
Audet P., Charest C. Effects of AM colonization on “wild tobacco” plants grown in zinc-contaminated soil. Mycorrhiza. 2006;16:277–283. doi: 10.1007/s00572-006-0045-x. PubMed DOI
Auld D.S. The ins and outs of biological zinc sites. Biometals. 2009:141–148. doi: 10.1007/s10534-008-9184-1. PubMed DOI
Baghaie A.H., Aghili F., Jafarinia R. Soil-indigenous arbuscular mycorrhizal fungi and zeolite addition to soil synergistically increase grain yield and reduce cadmium uptake of bread wheat (through improved nitrogen and phosphorus nutrition and immobilization of Cd in roots) Environ. Sci. Pollut. Res. 2019;26:30794–30807. doi: 10.1007/s11356-019-06237-0. PubMed DOI
Bapiri A., Asgharzadeh A., Mujallali H., Khavazi K., Pazira E. Evaluation of Zinc solubilization potential by different strains of Fluorescent Pseudomonads. J. Appl. Sci. Environ. Manag. 2012;16:295–298.
Basu A., Prasad P., Das S.N., Kalam S., Sayyed R.Z., Reddy M.S., El Enshasy H. Plant growth promoting rhizobacteria (PGPR) as green bioinoculants: recent developments, constraints, and prospects. Sustainability. 2021;13:1140.
Battini F., Grønlund M., Agnolucci M., Giovannetti M., Jakobsen I. Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria article. Sci. Rep. 2017;7:1–11. doi: 10.1038/s41598-017-04959-0. PubMed DOI PMC
Bauddh K., Singh R.P. Growth, tolerance efficiency and phytoremediation potential of Ricinus communis (L.) and Brassica juncea (L.) in salinity and drought affected cadmium contaminated soil. Ecotoxicol. Environ. Saf. 2012;85:13–22. doi: 10.1016/j.ecoenv.2012.08.019. PubMed DOI
Bi Y.L., Li X.L., Christie P. Influence of early stages of arbuscular mycorrhiza on uptake of zinc and phosphorus by red clover from a low-phosphorus soil amended with zinc and phosphorus. Chemosphere. 2003;50:831–837. doi: 10.1016/S0045-6535(02)00227-8. PubMed DOI
Bibi, F., Saleem, I., Ehsan, S., Jamil, S., Ullah, H., Mubashir, M., Kiran, S., Ahmad, I., Irshad, I., Saleem, M., Rahi, A.A., Khurshid, M.R., Danish, S., 2020. Effect of various application rates of phosphorus combined with different zinc rates and time of zinc application on phytic acid concentration and zinc bioavailability in wheat. Agric. Nat. Resour. 54, 265–272. https://doi.org/10.34044/j.anres.2020.54.3.05
Cakmak I. Tansley Review No. 111 Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol. 2000;146:185–205. PubMed
Castillo-González J., Ojeda-Barrios D., Hernández-Rodríguez A., González-Franco A.C., Robles-Hernández L., López-Ochoa G.R. Zinc metalloenzymes in plants. Interciencia. 2018;43:242–248.
Chandrasekaran M., Chanratana M., Kim K., Seshadri S., Sa T. Impact of arbuscular mycorrhizal fungi on photosynthesis, water status, and gas exchange of plants under salt stress–a meta-analysis. Front. Plant Sci. 2019;10:457. doi: 10.3389/fpls.2019.00457. PubMed DOI PMC
Chen S., Zhao H., Zou C., Li Y., Chen Y., Wang Z., Jiang Y., Liu A., Zhao P., Wang M., Ahammed G.J. Combined inoculation with multiple arbuscular mycorrhizal fungi improves growth, nutrient uptake and photosynthesis in cucumber seedlings. Front. Microbiol. 2017;8:2516. doi: 10.3389/fmicb.2017.02516. PubMed DOI PMC
Chen Y., Shi J., Tian X., Jia Z., Wang S., Chen J., Zhu W. Impact of dissolved organic matter on Zn extractability and transfer in calcareous soil with maize straw amendment. J. Soils Sediments. 2019;19:774–784. doi: 10.1007/s11368-018-2060-x. DOI
Christie P., Li X., Chen B. Arbuscular mycorrhiza can depress translocation of zinc to shoots of host plants in soils moderately polluted with zinc. Plant Soil. 2004 doi: 10.1023/B:PLSO.0000035542.79345.1b. DOI
Ciba J., Zołotajkin M., Cebula J. Changes of chemical forms of zinc and zinc sulfide during the composting process of municipal and waste. Water. Air. Soil Pollut. 1997;93:167–173. doi: 10.1023/A:1022192126944. DOI
Coccina A., Cavagnaro T.R., Pellegrino E., Ercoli L., McLaughlin M.J., Watts-Williams S.J. The mycorrhizal pathway of zinc uptake contributes to zinc accumulation in barley and wheat grain. BMC Plant Biol. 2019;19 doi: 10.1186/s12870-019-1741-y. PubMed DOI PMC
Collins C.D., Foster B.L. Community-level consequences of mycorrhizae depend on phosphorus availability. Ecology. 2009;90:2567–2576. doi: 10.1890/08-1560.1. PubMed DOI
Csathó P., Árendás T., Szabó A., Sándor R., Ragályi P., Pokovai K., Tóth Z., Kremper R. Phosphorus-induced zinc deficiency in maize (Zea mays L.) on a calcareous chernozem soil. Agrokem. es Talajt. 2019;68:40–52. doi: 10.1556/0088.2018.00016. DOI
Dagher D.J., Pitre F.E., Hijri M. Ectomycorrhizal fungal inoculation of sphaerosporella brunnea significantly increased stem biomass of salix miyabeana and decreased lead, tin, and zinc, soil concentrations during the phytoremediation of an industrial landfill. J. Fungi. 2020;6:1–12. doi: 10.3390/jof6020087. PubMed DOI PMC
Dahar G.J., Baloch A., Bashir A., Abro A. Distribution of Micronutrients in Different Soil Series Around Tando Jam, Sindh. Pakistan. Sci. Tech. Dev. 2014;33:7–13.
Danish S., Kiran S., Fahad S., Ahmad N., Ali M.A., Tahir F.A., Rasheed M.K., Shahzad K., Li X., Wang D., Mubeen M., Abbas S., Munir T.M., Hashmi M.Z., Adnan M., Saeed B., Saud S., Khan M.N., Ullah A., Nasim W. Alleviation of chromium toxicity in maize by Fe fortification and chromium tolerant ACC deaminase producing plant growth promoting rhizobacteria. Ecotoxicol. Environ. Saf. 2019;185 doi: 10.1016/j.ecoenv.2019.109706. PubMed DOI
Danish, S., Younis, U., Akhtar, N., Ameer, A., Ijaz, M., Nasreen, S., Huma, F., Sharif, S., Ehsanullah, M., 2015. Phosphorus solubilizing bacteria and rice straw biochar consequence on maize pigments synthesis. Int. J. Biosci. 5, 31–39. https://doi.org/10.12692/ijb/5.12.31-39
Danish S., Zafar-ul-Hye M. Co-application of ACC-deaminase producing PGPR and timber-waste biochar improves pigments formation, growth and yield of wheat under drought stress. Sci. Rep. 2019;9:5999. doi: 10.1038/s41598-019-42374-9. PubMed DOI PMC
Danish S., Zafar-Ul-Hye M., Hussain S., Riaz M., Qayyum M.F. Mitigation of drought stress in maize through inoculation with drought tolerant ACC deaminase containing PGPR under axenic conditions. Pakistan J. Bot. 2020;52:49–60.
Davaran Hagh E., Mirshekari B., Ardakani M.R., Farahvash F., Rejali F. Optimizing phosphorus use in sustainable maize cropping via mycorrhizal inoculation. J. Plant Nutr. 2016;39:1348–1356. doi: 10.1080/01904167.2015.1086797. DOI
Duc N.H., Csintalan Z., Posta K. Arbuscular mycorrhizal fungi mitigate negative effects of combined drought and heat stress on tomato plants. Plant Physiol. Biochem. 2018;132:297–307. doi: 10.1016/j.plaphy.2018.09.011. PubMed DOI
Escudero-Almanza D.J., Ojeda-Barrios D.L., Hernández-Rodríguez O.A., Sánchez Chávez E., Ruíz-Anchondo T., Sida-Arreola J.P. Carbonic anhydrase and zinc in plant physiology. Chil. J. Agric. Res. 2012;72:140–146. doi: 10.4067/s0718-58392012000100022. DOI
Eshaghi, E., Nosrati, R., Owlia, P., Malboobi, M.A., Ghaseminejad, P., Ganjali, M.R., 2019. Zinc solubilization characteristics of efficient siderophore-producing soil bacteria. Iran. J. Microbiol. 11, 419–430. https://doi.org/10.18502/ijm.v11i5.1961 PubMed PMC
Fan T.T., Wang Y.J., Li C.B., He J.Z., Gao J., Zhou D.M., Friedman S.P., Sparks D.L. Effect of organic matter on sorption of Zn on soil: elucidation by wien effect measurements and EXAFS spectroscopy. Environ. Sci. Technol. 2016;50:2931–2937. doi: 10.1021/acs.est.5b05281. PubMed DOI
Farooq M., Wahid A., Kobayashi N., Fujita D., Basra S.M.A. Plant drought stress: effects, mechanisms and management. Agron. Sustain. Dev. 2009;29:185–212. doi: 10.1051/agro:2008021. DOI
Frew A. Arbuscular mycorrhizal fungal diversity increases growth and phosphorus uptake in C3 and C4 crop plants. Soil Biol. Biochem. 2019;135:248–250. doi: 10.1016/j.soilbio.2019.05.015. DOI
Hafeez B. Role of zinc in plant nutrition- a review. Am. J. Exp. Agric. 2013;3:374–391. doi: 10.9734/ajea/2013/2746. DOI
Hamid B., Zaman M., Farooq S., Fatima S., Sayyed R.Z., Baba Z.A., Sheikh T.A., Reddy M.S., El Enshasy H., Gafur A. Bacterial plant biostimulants: a sustainable way towards improving growth, productivity, and health of crops. Sustainability. 2021;13:2856.
Hao X.J., Hong J.P., Zhang T.Q., Li J.R., Gao W.J., Zheng Z.M. Effects of arbuscular mycorrhizal fungal inoculation and phosphorus (P) addition on maize P utilization and growth in reclaimed soil of a mining area. Commun. Soil Sci. Plant Anal. 2014;45:2413–2428. doi: 10.1080/00103624.2014.912295. DOI
Hashem A., Abd Allah E.F., Alqarawi A.A., Aldubise A., Egamberdieva D. Arbuscular mycorrhizal fungi enhances salinity tolerance of panicum turgidum forssk by altering photosynthetic and antioxidant pathways. J. Plant Interact. 2015;10:230–242. doi: 10.1080/17429145.2015.1052025. DOI
Hui X., Luo L., Wang S., Cao H., Huang M., Shi M., Malhi S.S., Wang Z. Critical concentration of available soil phosphorus for grain yield and zinc nutrition of winter wheat in a zinc-deficient calcareous soil. Plant Soil. 2019;444:315–330. doi: 10.1007/s11104-019-04273-w. DOI
Hussain A., Arshad M., Zahir Z.A., Asghar M. Prospects of zinc solubilizing bacteria for enhancing growth of maize. Pakistan J. Agric. Sci. 2015;52:915–922.
Imran M., Rehim A., Sarwar N., Hussain S. Zinc bioavailability in maize grains in response of phosphorous-zinc interaction. J. Plant Nutr. Soil Sci. 2016;179:60–66. doi: 10.1002/jpln.201500441. DOI
Intorne A.C., De Oliveira M.V.V., Lima M.L., Da Silva J.F., Olivares F.L., De Souza Filho G.A. Identification and characterization of Gluconacetobacter diazotrophicus mutants defective in the solubilization of phosphorus and zinc. Arch. Microbiol. 2009;191:477–483. doi: 10.1007/s00203-009-0472-0. PubMed DOI
Iqbal, M.M., Murtaza, G., Mehdi, S.M., Naz, T., Ur-Rehman, A., Farooq, O., Ali, M., Sabir, M., Ashraf, M., Sarwar, G., Du Laing, G., 2017. Evaluation of phosphorus and zinc interaction effects on wheat grown in saline-sodic soil. Pakistan J. Agric. Sci. 54, 531–537. https://doi.org/10.21162/PAKJAS/17.4983
Jansa J., Mozafar A., Frossard E. Long-distance transport of P and Zn through the hyphae of an arbuscular mycorrhizal fungus in symbiosis with maize. Agronomie. 2003;23:481–488. doi: 10.1051/agro:2003013. DOI
Jiang Q.Y., Zhuo F., Long S.H., Zhao H. Di, Yang D.J., Ye Z.H., Li S.S., Jing Y.X. Can arbuscular mycorrhizal fungi reduce Cd uptake and alleviate Cd toxicity of Lonicera japonica grown in Cd-added soils? Sci. Rep. 2016;6:1–9. doi: 10.1038/srep21805. PubMed DOI PMC
Jiang Y., Wang W., Xie Q., Liu N., Liu L., Wang D., Zhang X., Yang C., Chen X., Tang D., Wang E. Plants transfer lipids to sustain colonization by mutualistic mycorrhizal and parasitic fungi. Science (80-. 2017;). 356:1172–1173. doi: 10.1126/science.aam9970. PubMed DOI
Kabata-Pendias A. Soil-plant transfer of trace elements - An environmental issue. Geoderma. 2004;122:143–149. doi: 10.1016/j.geoderma.2004.01.004. DOI
Kabata-Pendias, A., Pendias, H., 2001. Trace elements in soils and plants, in: New York. p. 331.
Kabir, A.H., Debnath, T., Das, U., Prity, S.A., Haque, A., Rahman, M.M., Parvez, M.S., 2020. Arbuscular mycorrhizal fungi alleviate Fe-deficiency symptoms in sunflower by increasing iron uptake and its availability along with antioxidant defense. Plant Physiol. Biochem. 150, 254–262. https://doi.org/10.1016/j.plaphy.2020.03.010 PubMed
Kalam S., Basu A., Ahmad I., Sayyed R.Z., El Enshasy H.A., Dailin D.J., Suriani N. Recent understanding of soil Acidobacteria and their ecological significance: A critical review. Front. Microbiol. 2020;11:2712. PubMed PMC
Khan S., Rehman S., Zeb Khan A., Amjad Khan M., Tahir Shah M. Soil and vegetables enrichment with heavy metals from geological sources in Gilgit, northern Pakistan. Ecotoxicol. Environ. Saf. 2010;73:1820–1827. doi: 10.1016/j.ecoenv.2010.08.016. PubMed DOI
Khatun M.A., Hossain M.M., Bari M.A., Abdullahil K.M., Parvez M.S., Alam M.F., Kabir A.H. Zinc deficiency tolerance in maize is associated with the up-regulation of Zn transporter genes and antioxidant activities. Plant Biol. 2018;20:765–770. doi: 10.1111/plb.12837. PubMed DOI
Kirmani H.F., Hussain M., Ahmad F., Shahid M., Asghar A. Impact of zinc uptake on morphology, physiology and yield attributes of wheat in Pakistan. Cercet. Agron. Mold. 2018;51:29–36. doi: 10.2478/cerce-2018-0002. DOI
Kullu B., Patra D.K., Acharya S., Pradhan C., Patra H.K. AM fungi mediated bioaccumulation of hexavalent chromium in Brachiaria mutica-a mycorrhizal phytoremediation approach. Chemosphere. 2020;258 doi: 10.1016/j.chemosphere.2020.127337. PubMed DOI
Kumar, D., Dhar, S., Kumar, S., Meena, D.C., Meena, R.B., 2019. Effect of Zinc Application on Yield Attributes and Yield of Maize and Wheat in Maize-Wheat Cropping System. Int. J. Curr. Microbiol. Appl. Sci. 8, 1931–1941. https://doi.org/10.20546/ijcmas.2019.801.203
Langyan S., Dar Z.A., Chaudhary D.P., Shekhar J.C., Herlambang S., El Enshasy H., Sayyed R.Z., Rakshit S. Analysis of nutritional quality attributes and their inter-relationship in maize inbred lines for sustainable livelihood. Sustainability. 2021;13:6137.
Lehmann A., Rillig M.C. Arbuscular mycorrhizal contribution to copper, manganese and iron nutrient concentrations in crops - A meta-analysis. Soil Biol. Biochem. 2015;81:147–158. doi: 10.1016/j.soilbio.2014.11.013. DOI
Liese R., Lübbe T., Albers N.W., Meier I.C. The mycorrhizal type governs root exudation and nitrogen uptake of temperate tree species. Tree Physiol. 2018;38:83–95. doi: 10.1093/treephys/tpx131. PubMed DOI
Liu H., Gan W., Rengel Z., Zhao P. Effects of zinc fertilizer rate and application method on photosynthetic characteristics and grain yield of summer maize. J. Soil Sci. Plant Nutr. 2016;16:550–562. doi: 10.4067/S0718-95162016005000045. DOI
Mao H., Wang J., Wang Z., Zan Y., Lyons G., Zou C. Using agronomic biofortification to boost zinc, selenium, and iodine concentrations of food crops grown on the loess plateau in China. J. Soil Sci. Plant Nutr. 2014;14:459–470. doi: 10.4067/S0718-95162014005000036. DOI
Maqsood M.A., Hussain S., Aziz T., Ahmad M., Naeem M.A., Ahmad H.R., Kanwal S., Hussain M. Zinc indexing in wheat grains and associated soils of southern Punjab. Pakistan J. Agric. Sci. 2015;52:431–438.
McMullen M.D., Kresovich S., Villeda H.S., Bradbury P., Li H., Sun Q., Flint-Garcia S., Thornsberry J., Acharya C., Bottoms C., Brown P., Browne C., Eller M., Guill K., Harjes C., Kroon D., Lepak N., Mitchell S.E., Peterson B., Pressoir G., Romero S., Rosas M.O., Salvo S., Yates H., Hanson M., Jones E., Smith S., Glaubitz J.C., Goodman M., Ware D., Holland J.B., Buckler E.S. Genetic properties of the maize nested association mapping population. Science (80-. 2009;). 325:737–740. doi: 10.1126/science.1174320. PubMed DOI
Mei L., Yang X., Zhang S., Zhang T., Guo J. Arbuscular mycorrhizal fungi alleviate phosphorus limitation by reducing plant N: P ratios under warming and nitrogen addition in a temperate meadow ecosystem. Sci. Total Environ. 2019;686:1129–1139. doi: 10.1016/j.scitotenv.2019.06.035. PubMed DOI
Mendoza-Cózatl D.G., Moreno-Sánchez R. Control of glutathione and phytochelatin synthesis under cadmium stress. Pathway modeling for plants. J. Theor. Biol. 2006;238:919–936. doi: 10.1016/j.jtbi.2005.07.003. PubMed DOI
Mertens, J., Smolders, E., 2013. Zinc, in: B.J. Alloway (Ed.), Heavy Metals in Soils. Environmental Pollution. Springer, Dordrecht, Springer, Dordrecht, pp. 465–493. https://doi.org/10.1007/978-94-007-4470-7_17
Miransari M. Soil microbes and the availability of soil nutrients. Acta Physiol. Plant. 2013 doi: 10.1007/s11738-013-1338-2. DOI
Mohammad D., Hussain A., Bhatti M.B. Locational differences in forage yield and quality of maize cultivars. Pakistan J. Sci. Ind. Res. 1990;33:454–456.
Mohsin A.U., Ahmad A.U.H., Farooq M., Ullah S. Influence of zinc application through seed treatment and foliar spray on growth, productivity and grain quality of hybrid maize. J. Anim. Plant Sci. 2014;24:1494–1503.
Mumtaz M.Z., Ahmad M., Jamil M., Hussain T. Zinc solubilizing Bacillus spp. potential candidates for biofortification in maize. Microbiol. Res. 2017;202:51–60. doi: 10.1016/j.micres.2017.06.001. PubMed DOI
Nguyen T.D., Cavagnaro T.R., Watts-Williams S.J. The effects of soil phosphorus and zinc availability on plant responses to mycorrhizal fungi: a physiological and molecular assessment. Sci. Rep. 2019;9:1–13. doi: 10.1038/s41598-019-51369-5. PubMed DOI PMC
Pakistan Agriculture Research Council . Sorghum Research Program; Islamabad, Pakistan: 2020. Maize, Millet.
Pandey N., Pathak G.C., Sharma C.P. Zinc is critically required for pollen function and fertilisation in lentil. J. Trace Elem. Med. Biol. 2006;20:89–96. doi: 10.1016/j.jtemb.2005.09.006. PubMed DOI
Panezai, G.M., Kethran, R., Agha, S.A.H., Alizai, N.A., Khan, Z., 2019. Zinc status of apple orchards across apple growing regions of Balochistan. Pure Appl. Biol. 8, 920–930. https://doi.org/10.19045/bspab.2019.80034
Patel K., Kumar A., Durani S. Analysis of the structural consensus of the zinc coordination centers of metalloprotein structures. Biochim. Biophys. Acta - Proteins Proteomics. 2007;1774:1247–1253. doi: 10.1016/j.bbapap.2007.07.010. PubMed DOI
Paunov M., Koleva L., Vassilev A., Vangronsveld J., Goltsev V. Effects of different metals on photosynthesis: Cadmium and zinc affect chlorophyll fluorescence in durum wheat. Int. J. Mol. Sci. 2018;19:787. doi: 10.3390/ijms19030787. PubMed DOI PMC
Pierart A., Dumat C., Maes A.Q.M., Sejalon-Delmas N. Influence of arbuscular mycorrhizal fungi on antimony phyto-uptake and compartmentation in vegetables cultivated in urban gardens. Chemosphere. 2018;191:272–279. doi: 10.1016/j.chemosphere.2017.10.058. PubMed DOI
Plassard C., Dell B. Phosphorus nutrition of mycorrhizal trees. Tree Physiol. 2010 doi: 10.1093/treephys/tpq063. PubMed DOI
Potarzycki, J., Grzebisz, W., 2009. Effect of zinc foliar application on grain yield of maize and its yielding components. Plant, Soil Environ. 55, 519–527. https://doi.org/10.17221/95/2009-pse
Prasad N.K., Kumar S., Kumar P., Singh R.S. Components of nutrients-use efficiency as influenced by legume-wheat (Triticum aestivum) sequences. Indian J. Agric. Sci. 2000;70:503–506.
Rafiullah, Tariq, M., Khan, F., Shah, A.H., Fahad, S., Wahid, F., Ali, J., Adnan, M., Ahmad, M., Irfan, M., Zafar-ul-Hye, M., Battaglia, M.L., Zarei, T., Datta, R., Saleem, I.A., Hafeez-u-Rehman, Danish, S., 2020. Effect of micronutrients foliar supplementation on the production and eminence of plum. Qual. Assur. Saf. Crop. Foods 12, 32–40. https://doi.org/10.15586/qas.v12iSP1.793.
Rahi A.A., Anjum M.A., Iqbal Mirza J., Ahmad Ali S., Marfo T.D., Fahad S., Danish S., Datta R. Yield enhancement and better micronutrients uptake in tomato fruit through potassium humate combined with micronutrients mixture. Agriculture. 2021;11:357. doi: 10.3390/agriculture11040357. DOI
Rana A., Saharan B., Joshi M., Prasanna R., Kumar K., Nain L. Identification of multi-trait PGPR isolates and evaluating their potential as inoculants for wheat. Ann. Microbiol. 2011;61:893–900. doi: 10.1007/s13213-011-0211-z. DOI
Rashid A., Hussain F., Rashid R., Din J. Nutrient status of citrus orchards in Punjab. Pakistan J. Soil Sci. 1991;6:25–28.
Rashwan, E., El-Gohary, Y., Hafez, E., 2019. Impact of different levels of Phosphorus and seed inoculation with Arbuscular mycorrhiza (AM) on growth, yield traits and productivity of wheat. Egypt. J. Agron. 41, 11–20. https://doi.org/10.21608/agro.2019.6329.1135
Rawat N., Neelam K., Tiwari V.K., Dhaliwal H.S. Biofortification of cereals to overcome hidden hunger. Plant Breed. 2013 doi: 10.1111/pbr.12040. DOI
Redecker D., Schüßler A., Stockinger H., Stürmer S.L., Morton J.B., Walker C. An evidence-based consensus for the classification of arbuscular mycorrhizal fungi (Glomeromycota) Mycorrhiza. 2013 doi: 10.1007/s00572-013-0486-y. PubMed DOI
Rodinpuia C., Singh V., Dhananjay T. Response of maize (Zea mays L.) to foliar application of zinc and planting geometry. J. Pharmacogn. Phytochem. 2019;8:707–709.
Ruscitti M., Arango M., Beltrano J. Improvement of copper stress tolerance in pepper plants (Capsicum annuum L.) by inoculation with arbuscular mycorrhizal fungi. Theor. Exp. Plant Physiol. 2017;29:37–49. doi: 10.1007/s40626-016-0081-7. DOI
Saboor, A., Ali, M.A., Ahmed, N., Skalicky, M., Danish, S., Fahad, S., Hassan, F., Hassan, M.M., Brestic, M., EL Sabagh, A., Datta, R., 2021. Biofertilizer-Based Zinc Application Enhances Maize Growth, Gas Exchange Attributes, and Yield in Zinc-Deficient Soil. Agriculture 11, 310. https://doi.org/10.3390/agriculture11040310
Samreen, T., Humaira, Shah, H.U., Ullah, S., Javid, M., 2017. Zinc effect on growth rate, chlorophyll, protein and mineral contents of hydroponically grown mungbeans plant (Vigna radiata). Arab. J. Chem. 10, S1802–S1807. https://doi.org/10.1016/j.arabjc.2013.07.005
Saravanan V.S., Subramoniam S.R., Raj S.A. Assessing in vitro solubilization potential of different zinc solubilizing bacterial (ZSB) isolates. Brazilian J. Microbiol. 2004;35:121–125. doi: 10.1590/S1517-83822004000100020. DOI
Seregin I.V., Kozhevnikova A.D., Gracheva V.V., Bystrova E.I., Ivanov V.B. Tissue zinc distribution in maize seedling roots and its action on growth. Russ. J. Plant Physiol. 2011;58:109–117. doi: 10.1134/S1021443711010171. DOI
Seymour N.P., Edwards D.G., Thompson J.P. A dual rescaled Mitscherlich model of the simultaneous savings in phosphorus and zinc fertiliser from arbuscular mycorrhizal fungal colonisation of linseed (Linum usitatissimum L.) Plant Soil. 2019;440:97–118. doi: 10.1007/s11104-019-04065-2. DOI
Shafi M.I., Adnan M., Fahad S., Wahid F., Khan A., Yue Z., Danish S., Zafar-Ul-Hye M., Brtnicky M., Datta R. Application of single superphosphate with humic acid improves the growth, yield and phosphorus uptake of wheat (Triticum aestivum L.) in calcareous soil. Agronomy. 2020;10:1224. doi: 10.3390/agronomy10091224. DOI
Shah A.A., Bibi F., Hussain I., Yasin N.A., Akram W., Tahir M.S., Ali H.M., Salem M.Z.M., Siddiqui M.H., Danish S., Fahad S., Datta R. Synergistic effect of bacillus thuringiensis iags 199 and putrescine on alleviating cadmium-induced phytotoxicity in capsicum annum. Plants. 2020;9:151. doi: 10.3390/plants9111512. PubMed DOI PMC
Sharma S., Prasad R., Varma A., Sharma A.K. Glycoprotein Associated with Funneliformis coronatum, Gigaspora margarita and Acaulospora scrobiculata Suppress the Plant Pathogens In vitro. Asian J. Plant Pathol. 2017;11:199–202. doi: 10.3923/ajppaj.2017.199.202. DOI
Shaver T.M., Westfall D.G., Ronaghi M. Zinc Fertilizer Solubility and Its Effects on Zinc Bioailability Over Time. Journal of Plant Nutrition. 2007;30(1):123–133.
Shen H., Christie P., Li X. Uptake of zinc, cadmium and phosphorus by arbuscular mycorrhizal maize (Zea mays L.) from a low available phosphorus calcareous soil spiked with zinc and cadmium. Environ. Geochem. Health. 2006;28:111–119. doi: 10.1007/s10653-005-9020-2. PubMed DOI
Shukla, A., Kumar, A., Jha, A., Ajit, Rao, D.V.K.N., 2012. Phosphorus threshold for arbuscular mycorrhizal colonization of crops and tree seedlings. Biol. Fertil. Soils 48, 109–116. https://doi.org/10.1007/s00374-011-0576-y
Smith, S.E., Read, D.J., 2008. Mycorrhizal Symbiosis Third Edition, Soil Science Society of America Journal.
Smith, S.R., 2009. A critical review of the bioavailability and impacts of heavy metals in municipal solid waste composts compared to sewage sludge. Environ. Int. https://doi.org/10.1016/j.envint.2008.06.009 PubMed
Souza J.F., Dolder H., Cortelazzo A.L. Effect of excess cadmium and zinc ions on roots and shoots of maize seedlings. J. Plant Nutr. 2005;28:1923–1931. doi: 10.1080/01904160500310435. DOI
Spatafora J.W., Chang Y., Benny G.L., Lazarus K., Smith M.E., Berbee M.L., Bonito G., Corradi N., Grigoriev I., Gryganskyi A., James T.Y., O’Donnell K., Roberson R.W., Taylor T.N., Uehling J., Vilgalys R., White M.M., Stajich J.E. A phylum-level phylogenetic classification of zygomycete fungi based on genome-scale data. Mycologia. 2016;108:1028–1046. doi: 10.3852/16-042. PubMed DOI PMC
Stankovic, S., Kalaba, P., Stankovic, A.R., 2014. Biota as toxic metal indicators. Environ. Chem. Lett. https://doi.org/10.1007/s10311-013-0430-6
Su Z., Liang C., Sun Y., Liu X., Song C., Chen J., Sun F., Bao Y., Zhang J. The stress mechanism of zinc on the wheat. Chem. Eng. Trans. 2017;61:349–354. doi: 10.3303/CET1761056. DOI
Subramanian, K.S., Tenshia, V., Jayalakshmi, K., Ramach, V., ran, 2009. Role of arbuscular mycorrhizal fungus (Glomus intraradices) (fungus aided)in zinc nutrition of maize. J. Agric. Biotechnol. Sustain. Dev.
Taheripur, A., Kiani, S.H., Hosseinpur, A., 2016. Effect of EDTA and citric acid on phytoextraction of copper and zinc from a naturally contaminated soil by Maize (Zea mays L.) cultivars. J. Water Soil 29, 1493–1505.
Tahir, F.A., Ahamad, N., Rasheed, M.K., Danish, S., 2018. Effect of various application rate of zinc fertilizer with and without fruit waste biochar on the growth and Zn uptake in maize. Int. J. Biosci. 13, 159–166. https://doi.org/10.12692/ijb/13.1.159-166
Tariq M., Iqbal H. Maize in Pakistan - An overview. Kasetsart J. - Nat. Sci. 2010;44:757–763.
Van Nevel L., Mertens J., Staelens J., De Schrijver A., Tack F.M.G., De Neve S., Meers E., Verheyen K. Elevated Cd and Zn uptake by aspen limits the phytostabilization potential compared to five other tree species. Ecol. Eng. 2011;37:1072–1080. doi: 10.1016/j.ecoleng.2010.07.010. DOI
Ven A., Verlinden M.S., Verbruggen E., Vicca S. Experimental evidence that phosphorus fertilization and arbuscular mycorrhizal symbiosis can reduce the carbon cost of phosphorus uptake. Funct. Ecol. 2019;33:2215–2225. doi: 10.1111/1365-2435.13452. DOI
Vodnik D., Grčman H., Maček I., van Elteren J.T., Kovačevič M. The contribution of glomalin-related soil protein to Pb and Zn sequestration in polluted soil. Sci. Total Environ. 2008;392:130–136. doi: 10.1016/j.scitotenv.2007.11.016. PubMed DOI
Vodyanitskii Y.N. Zinc forms in soils (Review of publications) Eurasian Soil Sci. 2010;43:269–277.
Wada K., Abd-Elfattah A. Characterization of zinc adsorption sites in two mineral soils. Soil Sci. Plant Nutr. 1978;24:417–426. doi: 10.1080/00380768.1978.10433120. DOI
Wahid F., Fahad S., Danish S., Adnan M., Yue Z., Saud S., Siddiqui M.H., Brtnicky M., Hammerschmiedt T., Datta R. Sustainable management with mycorrhizae and phosphate solubilizing bacteria for enhanced phosphorus uptake in calcareous soils. Agriculture. 2020;10:334. doi: 10.3390/agriculture10080334. DOI
Wamberg C., Christensen S., Jakobsen I., Müller A.K., Sørensen S.J. The mycorrhizal fungus (Glomus intraradices) affects microbial activity in the rhizosphere of pea plants (Pisum sativum) Soil Biol. Biochem. 2003;35:1349–1357. doi: 10.1016/S0038-0717(03)00214-1. DOI
Wang C., White P.J., Li C. Colonization and community structure of arbuscular mycorrhizal fungi in maize roots at different depths in the soil profile respond differently to phosphorus inputs on a long-term experimental site. Mycorrhiza. 2017;27:369–381. doi: 10.1007/s00572-016-0757-5. PubMed DOI
Wang S., Li M., Liu K., Tian X., Li S., Chen Y., Jia Z. Effects of Zn, macronutrients, and their interactions through foliar applications on winter wheat grain nutritional quality. PLoS ONE. 2017;12:0181276. doi: 10.1371/journal.pone.0181276. PubMed DOI PMC
Watts-Williams S.J., Cavagnaro T.R. Arbuscular mycorrhizal fungi increase grain zinc concentration and modify the expression of root ZIP transporter genes in a modern barley (Hordeum vulgare) cultivar. Plant Sci. 2018;274:163–170. doi: 10.1016/j.plantsci.2018.05.015. PubMed DOI
Watts-Williams S.J., Tyerman S.D., Cavagnaro T.R. The dual benefit of arbuscular mycorrhizal fungi under soil zinc deficiency and toxicity: linking plant physiology and gene expression. Plant Soil. 2017;420:375–388. doi: 10.1007/s11104-017-3409-4. DOI
Welch R.M., Graham R.D. Breeding for micronutrients in staple food crops from a human nutrition perspective. J. Exp. Bot. 2004:353–364. doi: 10.1093/jxb/erh064. PubMed DOI
Weng L., Temminghoff E.J.M., Lofts S., Tipping E., Van Riemsdijk W.H. Complexation with dissolved organic matter and solubility control of heavy metals in a sandy soil. Environ. Sci. Technol. 2002;36:4804–4810. doi: 10.1021/es0200084. PubMed DOI
Xing F., Fu X.Z., Wang N.Q., Xi J.L., Huang Y., Zhou W., Ling L.L., Peng L.Z. Physiological changes and expression characteristics of ZIP family genes under zinc deficiency in navel orange (Citrus sinensis) J. Integr. Agric. 2016;15:803–811. doi: 10.1016/S2095-3119(15)61276-X. DOI
Zafar-ul-Hye M., Danish S., Abbas M., Ahmad M., Munir T.M. ACC deaminase producing PGPR Bacillus amyloliquefaciens and agrobacterium fabrum along with biochar improve wheat productivity under drought stress. Agronomy. 2019;9:343. doi: 10.3390/agronomy9070343. DOI
Zafar-Ul-Hye, M., Hussain, N.M., Danish, S., Aslam, U., Zahir, Z.A., 2019. Multi-Strain bacterial inoculation of enterobacter cloacae, serratia ficaria and burkholderia phytofirmans with fertilizers for enhancing resistance in wheat against salinity stress. Pakistan J. Bot. 51, 1839–1846. https://doi.org/10.30848/PJB2019-5(24)
Zafar-ul-Hye M., Tahzeeb-ul-Hassan M., Abid M., Fahad S., Brtnicky M., Dokulilova T., Datta R., Danish S. Potential role of compost mixed biochar with rhizobacteria in mitigating lead toxicity in spinach. Sci. Rep. 2020;10:12159. doi: 10.1038/s41598-020-69183-9. PubMed DOI PMC
Zafar-ul-Hye M., Zahra M.B., Danish S., Abbas M. Multi-strain Inoculation with PGPR Producing ACC Deaminase is More Effective Than Single-strain Inoculation to Improve Wheat (Triticum aestivum) Growth and Yield. Phyton-International J. Experimental Bot. 2020
Zare-Maivan H., Khanpour-Ardestani N., Ghanati F. Influence of mycorrhizal fungi on growth, chlorophyll content, and potassium and magnesium uptake in maize. J. Plant Nutr. 2017;40:2026–2032. doi: 10.1080/01904167.2017.1346119. DOI
Zhang T., Hu Y., Zhang K., Tian C., Guo J. Arbuscular mycorrhizal fungi improve plant growth of Ricinus communis by altering photosynthetic properties and increasing pigments under drought and salt stress. Ind. Crops Prod. 2018;117:13–19. doi: 10.1016/j.indcrop.2018.02.087. DOI
Zhang W., Liu D., Liu Y., Cui Z., Chen X., Zou C. Zinc uptake and accumulation in winter wheat relative to changes in root morphology and mycorrhizal colonization following varying phosphorus application on calcareous soil. F. Crop. Res. 2016;197:74–82. doi: 10.1016/j.fcr.2016.08.010. DOI
Zhang X., Hu W., Xie X., Wu Y., Liang F., Tang M. Arbuscular mycorrhizal fungi promote lead immobilization by increasing the polysaccharide content within pectin and inducing cell wall peroxidase activity. Chemosphere. 2021;267 doi: 10.1016/j.chemosphere.2020.128924. PubMed DOI
Zhang Y.Q., Pang L.L., Yan P., Liu D.Y., Zhang W., Yost R., Zhang F.S., Zou C.Q. Zinc fertilizer placement affects zinc content in maize plant. Plant Soil. 2013 doi: 10.1007/s11104-013-1904-9. DOI
Zhao Q., Shen Q., Ran W., Xiao T., Xu D., Xu Y. Inoculation of soil by Bacillus subtilis Y-IVI improves plant growth and colonization of the rhizosphere and interior tissues of muskmelon (Cucumis melo L.) Biol. Fertil. Soils. 2011;47:507–514. doi: 10.1007/s00374-011-0558-0. DOI
Zia M.H., Ahmad R., Khaliq I., Ahmad A., Irshad M. Micronutrients status and management in orchards soils: applied aspects. Soil Environ. 2006;25:6–16.