Effect of arbuscular mycorrhizal fungi on the physiological functioning of maize under zinc-deficient soils
Language English Country Great Britain, England Media electronic
Document type Journal Article, Research Support, Non-U.S. Gov't
PubMed
34531432
PubMed Central
PMC8445980
DOI
10.1038/s41598-021-97742-1
PII: 10.1038/s41598-021-97742-1
Knihovny.cz E-resources
- MeSH
- Photosynthesis MeSH
- Zea mays metabolism microbiology MeSH
- Mycorrhizae metabolism pathogenicity MeSH
- Plant Stomata metabolism MeSH
- Soil chemistry MeSH
- Zinc analysis deficiency MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Soil MeSH
- Zinc MeSH
Zinc (Zn) deficiency can severely inhibit plant growth, yield, and enzymatic activities. Zn plays a vital role in various enzymatic activities in plants. Arbuscular mycorrhizal fungi (AMF) play a crucial role in improving the plant's Zn nutrition and mitigating Zn stress effects on plants. The current study was conducted to compare the response of inoculated and non-inoculated maize (YH 1898) in the presence of different levels of zinc under greenhouse conditions under a Zn deficient condition. There were two mycorrhizal levels (i.e., M + with mycorrhizae, M- without mycorrhizae) and five Zn levels (i.e., 0, 1.5, 3, 6, and 12 mg kg-1), with three replicates following completely randomized design. At the vegetative stage (before tillering), biochemical, physiological, and agronomic attributes were measured. The results showed that maize plants previously inoculated with AMF had higher gaseous exchange traits, i.e., a higher stomatal conductance rate, favoring an increased photosynthetic rate. Improvement in antioxidant enzyme activity was also observed in inoculated compared to non-inoculated maize plants. Moreover, AMF inoculation also played a beneficial role in nutrients availability and its uptake by plants. Higher Zn12 (12 mg Zn kg-1 soil) treatment accumulated a higher Zn concentration in soil, root, and shoot in AMF-inoculated than in non-inoculated maize plants. These results are consistent with mycorrhizal symbiosis beneficial role for maize physiological functioning in Zn deficient soil conditions. Additionally, AMF inoculation mitigated the stress conditions and assisted nutrient uptake by maize.
Department of Agronomy MNS University of Agriculture Multan Multan 60000 Pakistan
Department of Agronomy The University of Haripur Haripur 22620 Pakistan
Department of Biology University of Waterloo Waterloo ON N2L 3G1 Canada
Department of Botany Hindu College Moradabad Bareilly 244001 India
See more in PubMed
Alloway BJ. Soil factors associated with zinc deficiency in crops and humans. Environ. Geochem. Health. 2009;31:537–548. doi: 10.1007/s10653-009-9255-4. PubMed DOI
Bibi F, et al. 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. 2020;54:265–272.
Tahir FA, Ahamad N, Rasheed MK, Danish S. 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. 2018;13:159–166. doi: 10.12692/ijb/13.1.159-166. DOI
Rafique E, Rashid A, Ryan J, Bhatti AU. Zinc deficiency in rainfed wheat in Pakistan: Magnitude, spatial variability, management, and plant analysis diagnostic norms. Commun. Soil Sci. Plant Anal. 2006;37:181–197. doi: 10.1080/00103620500403176. DOI
Duc NH, 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
Cakmak, I. Tansley Review No. 111 Possible roles of zinc in protecting plant cells from damage by reactive oxygen species. New Phytol.146, 185–205 (2000). PubMed
Subramanian KS, Tenshia JSV, Jayalakshmi K, Ramachandran V. Antioxidant enzyme activities in arbuscular mycorrhizal (Glomus intraradices) fungus inoculated and non-inoculated maize plants under Zinc Deficiency. Indian J. Microbiol. 2011;51:37–43. doi: 10.1007/s12088-011-0078-5. PubMed DOI PMC
Aslanpour M, Baneh HD, Tehranifar A, Shoor M. Effect of mycorrhizal fungi on macronutrients and micronutrients in the white seedless grape roots under the drought conditions. Int. Trans. J. Eng. Manag. Appl. Sci. Technol. 2019;10:397–408.
Wahid F, et al. Sustainable management with mycorrhizae and phosphate solubilizing bacteria for enhanced phosphorus uptake in calcareous soils. Agriculture. 2020;10:334. doi: 10.3390/agriculture10080334. DOI
Smith SE, Smith FA, Jakobsen I. Mycorrhizal fungi can dominate phosphate supply to plants irrespective of growth responses. Plant Physiol. 2003;133:16–20. doi: 10.1104/pp.103.024380. PubMed DOI PMC
Latef AAHA, Chaoxing H. Arbuscular mycorrhizal influence on growth, photosynthetic pigments, osmotic adjustment and oxidative stress in tomato plants subjected to low temperature stress. Acta Physiol. Plant. 2011;33:1217–1225. doi: 10.1007/s11738-010-0650-3. DOI
Alizadeh O, Zare M, Nasr AH. Evaluation effect of mycorrhiza inoculate under drought stress condition on grain yield of sorghum (Sorghum bicolor) Adv. Environ. Biol. 2011;5:2361–2364.
Cavagnaro TR, et al. Arbuscular mycorrhizas, microbial communities, nutrient availability, and soil aggregates in organic tomato production. Plant Soil. 2006;282:209–225. doi: 10.1007/s11104-005-5847-7. DOI
Nunes, J. L. da S., de Souza, P. V. D., Marodin, G. A. B. & Fachinello, J. C. Effect of arbuscular mycorrhizal fungi and indolebutyric acid interaction on vegetative growth of ‘Aldrighi’ peach rootstock seedlings. Cienc. e Agrotecnologia34, 80–86 (2010).
Davies FT, Puryear JD, Newton RJ, Egilla JN, Saraiva Grossi JA. Mycorrhizal fungi enhance accumulation and tolerance of chromium in sunflower (Helianthus annuus) J. Plant Physiol. 2001;158:777–786. doi: 10.1078/0176-1617-00311. DOI
Kucey RMN, Janzen HH, Leggett ME. Microbially mediated increases in plant-available phosphorus. Adv. Agron. 1989;42:199–228. doi: 10.1016/S0065-2113(08)60525-8. DOI
Senovilla M, et al. MtCOPT2 is a Cu+ transporter specifically expressed in Medicago truncatula mycorrhizal roots. Mycorrhiza. 2020;30:781–788. doi: 10.1007/s00572-020-00987-3. PubMed DOI
Coccina, A. et al. The mycorrhizal pathway of zinc uptake contributes to zinc accumulation in barley and wheat grain. BMC Plant Biol.19, (2019). PubMed PMC
Tu JL, Liu XM, Xiao JX. Effects of arbuscular mycorrhizal inoculation on osmoregulation and antioxidant responses of blueberry plants. Bangladesh J. Bot. 2019;48:641–647. doi: 10.3329/bjb.v48i3.47942. DOI
Sato T, et al. Secretion of acid phosphatase from extraradical hyphae of the arbuscular mycorrhizal fungus Rhizophagus clarus is regulated in response to phosphate availability. Mycorrhiza. 2019;29:599–605. doi: 10.1007/s00572-019-00923-0. PubMed DOI
Subramanian KS, Bharathi C, Jegan A. Response of maize to mycorrhizal colonization at varying levels of zinc and phosphorus. Biol. Fertil. Soils. 2008;45:133–144. doi: 10.1007/s00374-008-0317-z. DOI
Walkley A, Black IA. An examination of the degtjareff method for determining soil organic matter, and a proposed modification of the chromic acid titration method. Soil Sci. 1934;37:29–38. doi: 10.1097/00010694-193401000-00003. DOI
Olsen, S., Cole, C., Watanabe, F. & Dean, L. Estimation of available phosphorus in soils by extraction with sodium bicarbonate. (United States Department of Agriculture, 1954).
Pratt, P. F. Potassium. in Methods of Soil Analysis: Part 2 Chemical and Microbiological Properties, 9.2 (ed. Norman, A. G.) 1022–1030 (John Wiley & Sons, Ltd, 1965). 10.2134/agronmonogr9.2.c20.
Lindsay WL, Norvell WA. A DTPA soil test for zinc, iron, manganese and copper. Soil Sci. Soc. Am. J. 1978;42:421–428. doi: 10.2136/sssaj1978.03615995004200030009x. DOI
Martin F, Winspear MJ, MacFarlane JD, Oaks A. Effect of methionine sulfoximine on the accumulation of ammonia in C3 and C4 leaves. Plant Physiol. 1983;71:177–181. doi: 10.1104/pp.71.1.177. PubMed DOI PMC
Ohno T, Zibilske LM. Determination of low concentrations of phosphorus in soil extracts using malachite green. Soil Sci. Soc. Am. J. 1991;55:892–895. doi: 10.2136/sssaj1991.03615995005500030046x. DOI
Ryan MH, McInerney JK, Record IR, Angus JF. Zinc bioavailability in wheat grain in relation to phosphorus fertiliser, crop sequence and mycorrhizal fungi. J. Sci. Food Agric. 2008;88:1208–1216. doi: 10.1002/jsfa.3200. DOI
Thomas, G. W. Soil pH and soil acidity. In Methods of Soil Analysis, Part 3: Chemical Methods vol. 5 475–490 (John Wiley & Sons, 1996).
Rhoades, J. D. Salinity: Electrical Conductivity and Total Dissolved Solids. in Methods of Soil Analysis, Part 3, Chemical Methods (eds. D.L. Sparks et al.) vol. 5 417–435 (Soil Science Society of America, 1996).
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
Arnon DI. Copper enzymes in isolated chloroplasts Polyphenoloxidase in Beta vulgaris. Plant Physiol. 1949;24:1–15. doi: 10.1104/pp.24.1.1. PubMed DOI PMC
Giannopolitis CN, Ries SK. Superoxide dismutases: I Occurrence in higher plants. Plant Physiol. 1977;59:309–314. doi: 10.1104/pp.59.2.309. PubMed DOI PMC
Chance B, Maehly AC. Assay of catalases and peroxidases. Methods Enzymol. 1955;2:764–775. doi: 10.1016/S0076-6879(55)02300-8. PubMed DOI
Sambrook J, Russell DW. In vitro mutagenesis using double-stranded DNA templates: selection of mutants with DpnI. Cold Spring Harb. Protoc. 2006;2:13–19. PubMed
Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein using the principle of protein dye binding. Anal. Biochem. 1976;72:248–254. doi: 10.1016/0003-2697(76)90527-3. PubMed DOI
Phillips, J. M. & Hayman, D. S. Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans. Br. Mycol. Soc.55, 158–IN18 (1970).
Vierheilig H, Coughlan AP, Wyss U, Piché Y. Ink and vinegar, a simple staining technique for arbuscular-mycorrhizal fungi. Appl. Environ. Microbiol. 1998;64:5004–5007. doi: 10.1128/AEM.64.12.5004-5007.1998. PubMed DOI PMC
Steel, R. G., Torrie, J. H. & Dickey, D. A. Principles and Procedures of Statistics: A Biometrical Approach. (McGraw Hill Book International Co., 1997).
Shahzad S, Khan MY, Zahir ZA, Asghar HN, Chaudhry UK. Comparative effectiveness of different carriers to improve the efficacy. Pakistan J. Bot. 2017;49:1523–1530.
Lawson T. Guard cell photosynthesis and stomatal function. New Phytol. 2009;181:13–34. doi: 10.1111/j.1469-8137.2008.02685.x. PubMed DOI
Goicoechea N, Antolín MC, Sánchez-Díaz M. Gas exchange is related to the hormone balance in mycorrhizal or nitrogen-fixing alfalfa subjected to drought. Physiol. Plant. 1997;100:989–997. doi: 10.1111/j.1399-3054.1997.tb00027.x. DOI
Mathur N, Vyas A. Biochemical changes in Ziziphus xylopyrus by VA mycorrhizae. Bot. Bull. Acad. Sin. 1996;37:209–212.
Sannazzaro AI, Ruiz OA, Albertó EO, Menéndez AB. Alleviation of salt stress in Lotus glaber by Glomus intraradices. Plant Soil. 2006;285:279–287. doi: 10.1007/s11104-006-9015-5. DOI
Colla G, et al. Alleviation of salt stress by arbuscular mycorrhizal in zucchini plants grown at low and high phosphorus concentration. Biol. Fertil. Soils. 2008;44:501–509. doi: 10.1007/s00374-007-0232-8. DOI
Yang Y, et al. The combined effects of arbuscular mycorrhizal fungi (AMF) and lead (Pb) stress on Pb accumulation, plant growth parameters, photosynthesis, and antioxidant enzymes in Robinia pseudoacacia L. PLoS One. 2015;10:e0145726. doi: 10.1371/journal.pone.0145726. PubMed DOI PMC
Lu C, Vonshak A. Effects of salinity stress on photosystem II function in cyanobacterial Spirulina platensis cells. Physiol. Plant. 2002;114:405–413. doi: 10.1034/j.1399-3054.2002.1140310.x. PubMed DOI
Chaves MM, Flexas J, Pinheiro C. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann. Bot. 2009;103:551–560. doi: 10.1093/aob/mcn125. PubMed DOI PMC
Toler HD, Morton JB, Cumming JR. Growth and metal accumulation of mycorrhizal sorghum exposed to elevated copper and zinc. Water. Air. Soil Pollut. 2005;164:155–172. doi: 10.1007/s11270-005-2718-z. DOI
Marschner H, Cakmak I. High Light Intensity Enhances Chlorosis and Necrosis in Leaves of Zinc, Potassium, and Magnesium Deficient Bean (Phaseolus vulgaris) Plants. J. Plant Physiol. 1989;134:308–315. doi: 10.1016/S0176-1617(89)80248-2. DOI
Arines J, Palma JM, Viarino A. Comparison of protein patterns in non-mycorrhizal and vesicular–arbuscular mycorrhizal roots of red clover. New Phytol. 1993;123:763–768. doi: 10.1111/j.1469-8137.1993.tb03787.x. DOI
Marques APGC, Oliveira RS, Rangel AOSS, Castro PML. Application of manure and compost to contaminated soils and its effect on zinc accumulation by Solanum nigrum inoculated with arbuscular mycorrhizal fungi. Environ. Pollut. 2008;151:608–620. doi: 10.1016/j.envpol.2007.03.015. PubMed DOI
Zhang W, et al. Zinc uptake by roots and accumulation in maize plants as affected by phosphorus application and arbuscular mycorrhizal colonization. Plant Soil. 2017;413:59–71. doi: 10.1007/s11104-017-3213-1. DOI
Cavagnaro TR. The role of arbuscular mycorrhizas in improving plant zinc nutrition under low soil zinc concentrations: a review. Plant Soil. 2008;304:315–325. doi: 10.1007/s11104-008-9559-7. DOI