Microbial inoculants improve nutrients uptake and yield of durum wheat in calcareous soils under drought stress in the Mediterranean region

References

• Aguilar C, Vlamakis H, Losick R, Kolter R. 2007. Thinking about Bacillus subtilis as a multicellular organism. Curr Opin Microbiol. 10(6):638–643. doi:10.1016/j.mib.2007.09.006.
   PubMed Web of Science ®Google Scholar
• Arkhipova TN, Veselov SU, Melentiev AI, Martynenko EV, Kudoyarova GR. 2005. Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil. 272(1–2):201–209. doi:10.1007/s11104-004-5047-x.
   Web of Science ®Google Scholar
• Bohn L, Meyer AS, Rasmussen SK. 2008. Phytate: impact on environment and human nutrition. A challenge for molecular breeding. J Zhejiang Univ Sci B. 9(3):165–191. doi:10.1631/JZUS.B0710640.
   PubMed Web of Science ®Google Scholar
• Borrero C, Trillas MI, Delgado A, Avilés M. 2012. Effect of ammonium/nitrate ratio in nutrient solution on control of Fusarium wilt of tomato by Trichoderma asperellum T34. Plant Pathol. 61(1):132–139. doi:10.1111/j.1365-3059.2011.02490.x.
   Web of Science ®Google Scholar
• Cakmak I, Kutman UB. 2018. Agronomic biofortification of cereals with zinc: a review. Eur J Soil Sci. 69(1):172–180. doi:10.1111/ejss.12437.
   Web of Science ®Google Scholar
• Casida LE, Klein DA, Santoro T. 1964. Soil dehydrogenase activity. Soil Sci. 98(6):371–376. doi:10.1097/00010694-196412000-00004.
   Google Scholar
• Chen XP, Zhang YQ, Tong YP, Xue YF, Liu DY, Zhang W, Deng Y, Meng QF, Yue SC, Yan P, et al. 2017. Harvesting more grain zinc of wheat for human health. Sci Rep. 7(1):1–8. doi:10.1038/s41598-017-07484-2.
   PubMed Web of Science ®Google Scholar
• Chien SH, Prochnow LI, Cantarella H. 2009. Chapter 8 Recent developments of fertilizer production and use to improve nutrient efficiency and minimize environmental impacts. Adv Agron. 102:267–322. doi:10.1016/S0065-2113(09)01008-6
   Web of Science ®Google Scholar
• Chung YR, Hoitink HAJ. 1990. Interactions between thermophilic fungi and Trichoderma hamatum in suppression of Rhizoctonia damping-off in a bark compost-amended container medium. Phytopathology. 80(1):73–77. doi:10.1094/Phyto-80-73.
   Web of Science ®Google Scholar
• Congreves KA, Otchere O, Ferland D, Farzadfar S, Williams S and Arcand MM 2021. Nitrogen Use Efficiency Definitions of Today and Tomorrow. Front Plant Sci. 12. doi:10.3389/fpls.2021.637108.
   PubMed Web of Science ®Google Scholar
• Delgado A, Quemada M, Villalobos FJ, Mateos L. 2016. Principles of agronomy for sustainable agriculture. Cham (Switzerland): Springer. doi:10.1007/978-3-319-46116-8.
   Google Scholar
• de Santiago A, García-López AM, Quintero JM, Avilés M, Delgado A. 2013. Effect of Trichoderma asperellum strain T34 and glucose addition on iron nutrition in cucumber grown on calcareous soils. Soil Biol Biochem. 57:598–605. doi:10.1016/j.soilbio.2012.06.020
   Web of Science ®Google Scholar
• de Santiago A, Quintero JM, Avilés M, Delgado A. 2009. Effect of Trichoderma asperellum strain T34 on iron nutrition in white lupin. Soil Biol Biochem. 41(12):2453–2459. doi:10.1016/j.soilbio.2009.07.033.
   Web of Science ®Google Scholar
• de Santiago A, Quintero JM, Avilés M, Delgado A. 2011. Effect of Trichoderma asperellum strain T34 on iron, copper, manganese, and zinc uptake by wheat grown on a calcareous medium. Plant Soil. 342(1–2):97–104. doi:10.1007/s11104-010-0670-1.
   Web of Science ®Google Scholar
• Dobermann A. 2007. Nutrient use efficiency - measurement and management. In: Krauss A, Isherwood K, Heffer P, editors. Fertilizer best management practices: general principles, strategy for their adoption and voluntary initiatives versus regulations. Paris: International Fertilizer Industry Association; p. 1–28.
   Google Scholar
• Duffner A, Hoffland E, Temminghoff EJM. 2012. Bioavailability of zinc and phosphorus in calcareous soils as affected by citrate exudation. Plant Soil. 361(1–2):165–175. doi:10.1007/s11104-012-1273-9.
   Web of Science ®Google Scholar
• Eivazi F, Tabatabai MA. 1977. Phosphatases in soils. Soil Biol Biochem. 9(3):167–172. doi:10.1016/0038-0717(77)90070-0.
   Web of Science ®Google Scholar
• Eivazi F, Tabatabai MA. 1988. Glucosidases and galactosidases in soils. Soil Biol Biochem. 20(5):601–606. doi:10.1016/0038-0717(88)90141-1.
   Web of Science ®Google Scholar
• [FAO] Food and Agriculture Organization of the United Nations. 2017. World fertilizer trends and Outlook to 2020. Rome. [Internet]. [accessed 2022 Sep 20]. Available from: https://www.fao.org/3/i6895e/i6895e.pdf
   Google Scholar
• Fink JR, Inda AV, Bavaresco J, Barrón V, Torrent J, Bayer C. 2016. Phosphorus adsorption and desorption in undisturbed samples from subtropical soils under conventional tillage or no-tillage. J Plant Nutr Soil Sci. 179(2):198–205. doi:10.1002/JPLN.201500017.
   Google Scholar
• García-López AM, Avilés M, Delgado A. 2016. Effect of various microorganisms on phosphorus uptake from insoluble Ca-phosphates by cucumber plants. J Plant Nutr Soil Sci. 179(4):454–465. doi:10.1002/jpln.201500024.
   Google Scholar
• García-López AM, Delgado A. 2016. Effect of Bacillus subtilis on phosphorus uptake by cucumber as affected by iron oxides and the solubility of the phosphorus source. Agric Food Sci. 25(3):216–224. doi:10.23986/afsci.56862.
   Web of Science ®Google Scholar
• García-López AM, Recena R, Avilés M, Delgado A. 2018. Effect of Bacillus subtilis QST713 and Trichoderma asperellum T34 on P uptake by wheat and how it is modulated by soil properties. J Soils Sediments. 18(3):727–738. doi:10.1007/s11368-017-1829-7.
   Web of Science ®Google Scholar
• García-López AM, Recena R, Delgado A. 2021. The adsorbent capacity of growing media does not constrain myo-inositol hexakiphosphate hydrolysis but its use as a phosphorus source by plants. Plant Soil. 459(1–2):277–288. doi:10.1007/s11104-020-04764-1.
   Web of Science ®Google Scholar
• Gómez-Coronado F, Almeida AS, Santamaría O, Cakmak I, Poblaciones MJ. 2019. Potential of advanced breeding lines of bread-making wheat to accumulate grain minerals (Ca, Fe, Mg and Zn) and low phytates under Mediterranean conditions. J Agron Crop Sci. 205(3):341–352. doi:10.1111/jac.12325.
   Web of Science ®Google Scholar
• Gouda S, Kerry RG, Das G, Paramithiotis S, Shin HS, Patra JK. 2018. Revitalization of plant growth promoting rhizobacteria for sustainable development in agriculture. Microbiol Res. 206:131–140. doi:10.1016/j.micres.2017.08.016
   PubMed Web of Science ®Google Scholar
• Hinsinger P, Brauman A, Devau N, Gérard F, Jourdan C, Laclau JP, Le Cadre E, Jaillard B, Plassard C. 2011. Acquisition of phosphorus and other poorly mobile nutrients by roots. Where do plant nutrition models fail? Plant Soil. 348(1):29–61. doi:10.1007/S11104-011-0903-Y.
   Web of Science ®Google Scholar
• Hussain S, Hussain MB, Gulzar A, Zafar-ul-Hye M, Aon M, Qaswar M, Yaseen R. 2017. Right time of phosphorus and zinc application to maize depends on nutrient–nutrient and nutrient–inoculum interactions. Soil Sci Plant Nutr. 63(4):351–356. doi:10.1080/00380768.2017.1361784.
   Web of Science ®Google Scholar
• Jacobsen SE, Jensen CR, Liu F. 2012. Improving crop production in the arid Mediterranean climate. F Crop Res. 128:34–47. doi:10.1016/J.FCR.2011.12.001
   Web of Science ®Google Scholar
• Kazi N, Deaker R, Wilson N, Muhammad K, Trethowan R. 2016. The response of wheat genotypes to inoculation with Azospirillum brasilense in the field. F Crop Res. 196:368–378. doi:10.1016/J.FCR.2016.07.012
   Web of Science ®Google Scholar
• Keyzer M. 2010. Towards a closed phosphorus cycle. Economist . 158(4):411–425. doi:10.1007/S10645-010-9150-5.
   Web of Science ®Google Scholar
• Khande R, Sharma SK, Ramesh A, Sharma MP. 2017. Zinc solubilizing Bacillus strains that modulate growth, yield and zinc biofortification of soybean and wheat. Rhizosphere. 4:126–138. doi:10.1016/j.rhisph.2017.09.002
   Web of Science ®Google Scholar
• Khan MS, Zaidi A, Wani PA. 2007. Role of phosphate-solubilizing microorganisms in sustainable agriculture - A review. Agron Sustain Dev. 27(1):29–43. doi:10.1051/agro:2006011.
   Web of Science ®Google Scholar
• Khoshgoftarmanesh AH, Norouzi M, Afyuni M, Schulin R. 2017. Zinc biofortification of wheat through preceding crop residue incorporation into the soil. Eur J Agron. 89:131–139. doi:10.1016/j.eja.2017.05.006
   Web of Science ®Google Scholar
• Lastochkina O, Baymiev A, Shayahmetova A, Garshina D, Koryakov I, Shpirnaya I, Pusenkova L, Mardanshin I, Kasnak C, Palamutoglu R. 2020. Effects of endophytic Bacillus subtilis and salicylic acid on postharvest diseases (Phytophthora infestans, Fusarium oxysporum) development in stored potato tubers. Plants. 9(1):76. doi:10.3390/PLANTS9010076.
   Google Scholar
• López-Bellido L, López-Bellido RJ, Redondo R. 2005. Nitrogen efficiency in wheat under rainfed Mediterranean conditions as affected by split nitrogen application. F Crop Res. 94(1):86–97. doi:10.1016/j.fcr.2004.11.004.
   Web of Science ®Google Scholar
• Marschner P, Crowley D, Rengel Z. 2011. Rhizosphere interactions between microorganisms and plants govern iron and phosphorus acquisition along the root axis - model and research methods. Soil Biol Biochem. 43(5):883–894. doi:10.1016/j.soilbio.2011.01.005.
   Web of Science ®Google Scholar
• Marschner P, Solaiman Z, Rengel Z. 2006. Rhizosphere properties of Poaceae genotypes under p-limiting conditions. Plant Soil. 283(1):11–24. doi:10.1007/s11104-005-8295-5.
   Web of Science ®Google Scholar
• Masood S, Zhao XQ, Shen RF. 2020. Bacillus pumilus promotes the growth and nitrogen uptake of tomato plants under nitrogen fertilization. Sci Hortic. 272:109581. doi:10.1016/J.SCIENTA.2020.109581
   Web of Science ®Google Scholar
• Matar A, Torrent J, Ryan J. 1992. Soil and fertilizer phosphorus and crop responses in the dryland Mediterranean zone. In: Stewart BA, editor. Advances in soil science. New York (NY): Springer; p. 81–146. doi:10.1007/978-1-4612-2844-8_3
   Google Scholar
• Miljaković D, Marinković J, Balešević-Tubić S. 2020. The significance of bacillus spp. in disease suppression and growth promotion of field and vegetable crops. Microorganisms. 8(7):1–19. doi:10.3390/MICROORGANISMS8071037.
   Web of Science ®Google Scholar
• Miller LV, Krebs NF, Hambidge KM. 2007. A mathematical model of zinc absorption in humans as a function of dietary zinc and phytate. J Nutr. 137(1):135–141. doi:10.1093/jn/137.1.135.
   PubMed Web of Science ®Google Scholar
• Moreno-Lora A, Delgado A. 2020. Factors determining Zn availability and uptake by plants in soils developed under Mediterranean climate. Geoderma. 376:114509. doi:10.1016/j.geoderma.2020.114509
   Web of Science ®Google Scholar
• Moreno-Lora A, Recena R, Delgado A. 2019. Bacillus subtilis QST713 and cellulose amendment enhance phosphorus uptake while improving zinc biofortification in wheat. Appl Soil Ecol. 142:81–89. doi:10.1016/j.apsoil.2019.04.013
   Web of Science ®Google Scholar
• Murphy J, Riley JP. 1962. A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta. 27:31–36. doi:10.1016/S0003-2670(00)88444-5
   Web of Science ®Google Scholar
• Nazih N, Finlay-Moore O, Hartel PG, Fuhrmann JJ. 2001. Whole soil fatty acid methyl ester (FAME) profiles of early soybean rhizosphere as affected by temperature and matric water potential. Soil Biol Biochem. 33(4–5):693–696. doi:10.1016/S0038-0717(00)00197-8.
   Web of Science ®Google Scholar
• Nguyen ML, Glaes J, Spaepen S, Bodson B, du Jardin P, Delaplace P. 2019. Biostimulant effects of Bacillus strains on wheat from in vitro towards field conditions are modulated by nitrogen supply. J Plant Nutr Soil Sci. 182(3):325–334. doi:10.1002/jpln.201700610.
   Google Scholar
• Owen D, Williams AP, Griffith GW, Withers PJA. 2015. Use of commercial bio-inoculants to increase agricultural production through improved phosphorus acquisition. Appl Soil Ecol. 86:41–54. doi:10.1016/j.apsoil.2014.09.012
   Web of Science ®Google Scholar
• Pishchik VN, Vorobyev NI, Moiseev KG, Sviridova OV, Surin VG. 2015. Influence of Bacillus subtilis on the physiological state of wheat and the microbial community of the soil under different rates of nitrogen fertilizers. Eurasian Soil Sci. 48(1):77–84. doi:10.1134/S1064229315010135.
   Web of Science ®Google Scholar
• Prasanna R, Hossain F, Saxena G, Singh B, Kanchan A, Simranjit K, Ramakrishnan B, Ranjan K, Muthusamy V, Shivay YS. 2021. Analyses of genetic variability and genotype x cyanobacteria interactions in biofortified maize (Zea mays L.) for their responses to plant growth and physiological attributes. Eur J Agron. 130:126343. doi:10.1016/J.EJA.2021.126343
   Web of Science ®Google Scholar
• Ramesh A, Sharma SK, Sharma MP, Yadav N, Joshi OP. 2014. Inoculation of zinc solubilizing Bacillus aryabhattai strains for improved growth, mobilization and biofortification of zinc in soybean and wheat cultivated in Vertisols of central India. Appl Soil Ecol. 73:87–96. doi:10.1016/j.apsoil.2013.08.009
   Web of Science ®Google Scholar
• Recena R, Díaz I, Delgado A. 2017. Estimation of total plant available phosphorus in representative soils from Mediterranean areas. Geoderma. 297:10–18. doi:10.1016/j.geoderma.2017.02.016
   Web of Science ®Google Scholar
• Rivera-Méndez W, Obregón M, Morán-Diez ME, Hermosa R, Monte E. 2020. Trichoderma asperellum biocontrol activity and induction of systemic defenses against Sclerotium cepivorum in onion plants under tropical climate conditions. Biol Control. 141:104145. doi:10.1016/J.BIOCONTROL.2019.104145
   Web of Science ®Google Scholar
• Ryan J, Rashid A, Torrent J, Yau SK, Ibrikci H, Sommer R, Erenoglu EB 2013. Chapter one - Micronutrient constraints to crop production in the middle east-west Asia region: Significance, research, and management. Adv Agron. 122:1–84. doi:10.1016/B978-0-12-417187-9.00001-2.
   Web of Science ®Google Scholar
• Schnitkey G, Swanson K, Paulson N, Zulauf C, Coppess J, Baltz J. 2022. Nitrogen fertilizer outlook for 2023 decisions. farmdoc Dly. 12(106). https://farmdocdaily.illinois.edu/2022/07/nitrogen-fertilizer-outlook-for-2023-decisions.html
   Google Scholar
• Shaikh S, Saraf M. 2017. Biofortification of Triticum aestivum through the inoculation of zinc solubilizing plant growth promoting rhizobacteria in field experiment. Biocatal Agric Biotechnol. 9:120–126. doi:10.1016/J.BCAB.2016.12.008
   Web of Science ®Google Scholar
• Singh D, Rajawat MVS, Kaushik R, Prasanna R, Saxena AK. 2017. Beneficial role of endophytes in biofortification of Zn in wheat genotypes varying in nutrient use efficiency grown in soils sufficient and deficient in Zn. Plant Soil. 416(1–2):107–116. doi:10.1007/s11104-017-3189-x.
   Web of Science ®Google Scholar
• Soil Survey Staff. 2014. Keys to soil taxonomy. 12th. Washington (DC): USDA-Natural Resources Conservation Service.
   Google Scholar
• Sruthilaxmi CB, Babu S. 2017. Microbial bio-inoculants in Indian agriculture: ecological perspectives for a more optimized use. Agric Ecosyst Environ. 242:23–25. doi:10.1016/j.agee.2017.03.019
   Web of Science ®Google Scholar
• Tabatabai MA, Bremner JM. 1969. Use of p-nitrophenyl phosphate for assay of soil phosphatase activity. Soil Biol Biochem. 1(4):301–307. doi:10.1016/0038-0717(69)90012-1.
   Google Scholar
• Technologies S. 2013. Statgraphics Centurion XVI. Warrenton.
   Google Scholar
• Tuitert G, Szczech M, Bollen GJ. 1998. Suppression of Rhizoctonia solani in potting mixtures amended with compost made from organic household waste. Phytopathology. 88(8):764–773. doi:10.1094/PHYTO.1998.88.8.764.
   PubMed Web of Science ®Google Scholar
• Turner JT, Backman PA. 1991. Factors relating to peanut yield increases after seed treatment with Bacillus subtilis. Plant Dis. 75(4):347–353. doi:10.1094/PD-75-0347.
   Web of Science ®Google Scholar
• Ullah H, Santiago-Arenas R, Ferdous Z, Attia A, Datta A. 2019. Improving water use efficiency, nitrogen use efficiency, and radiation use efficiency in field crops under drought stress: a review. Adv Agron. 156:109–157. doi:10.1016/BS.AGRON.2019.02.002
   Web of Science ®Google Scholar
• Wang G, Xu Y, Jin J, Liu J, Zhang Q, Liu X. 2009. Effect of soil type and soybean genotype on fungal community in soybean rhizosphere during reproductive growth stages. Plant Soil. 317(1–2):135–144. doi:10.1007/s11104-008-9794-y.
   Web of Science ®Google Scholar
• Xie X, Hu W, Fan X, Chen H, Tang M. 2019. Interactions between phosphorus, zinc, and iron homeostasis in non-mycorrhizal and mycorrhizal plants. Front Plant Sci. 10:1172. doi:10.3389/FPLS.2019.01172/BIBTEX
   PubMed Web of Science ®Google Scholar
• Zadoks JC, Chang TT, Konzak CF. 1974. A decimal code for the growth stages of cereals. Weed Res. 14(6):415–421. doi:10.1111/j.1365-3180.1974.tb01084.x.
   Web of Science ®Google Scholar
• Zhang W, Liu D, Liu Y, Cui Z, Chen X, Zou C. 2016. 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. 197:74–82. doi:10.1016/j.fcr.2016.08.010
   Web of Science ®Google Scholar
• Zhao L, Liu Q, Y Qing Z, Q Yu C, Y Cun L. 2017. Effect of acid phosphatase produced by Trichoderma asperellum Q1 on growth of Arabidopsis under salt stress. J Integr Agric. 16(6):1341–1346. doi:10.1016/S2095-3119(16)61490-9.
   Web of Science ®Google Scholar