Abstract
It is well known that arbuscular mycorrhizal fungi (AMF) effects on plant growth largely depend on fungus identity. The objective of this study was to test whether three individual AMF isolates and their mixture mitigate drought stress (DS) differentially in soybean (Glycine max) genotype, predicting that under DS, the mixture of the AMF isolates would provide greater benefits to soybean plants than individual ones. In a greenhouse experiment, a drought-susceptible soybean genotype was inoculated with Septoglomus constrictum, Glomus sp., and Glomus aggregatum, known to be among the most abundant in agricultural and natural soils from central Argentina, and their mixture (Mx). Whereas under well-watered (WW) conditions, individual isolates and Mx treatment were similarly infective; under DS conditions, the Mx treatment showed lower rates of root colonization. Between WW and DS conditions, biomass was decreased in all treatments, although this effect was more marked in non-AM plants. Moreover, AMF strains improved water content and P and N concentrations. Under DS, the Mx treatment was unable to exceed the highest contents that were recorded by AMF isolates. However, under WW conditions, the Mx treatment showed a higher N content than individual isolates. Under both watering conditions, AM plants reduced oxidative damage evaluated as malondiadehyde and chlorophyll content and keep constant osmotic metabolites such as soluble sugars and proline content, without significant differences between AMF isolates and the Mx treatment. These results show that AMF play an important role in mitigating drought impacts on soybean, but that mixtures of AMF isolates did not perform as well as the best single strain inoculum, excluding complementarity effects and suggesting selection effect of AMF on DS alleviation in soybean.
Similar content being viewed by others
References
Abbaspour H, Saeidi-Sarb S, Afsharia H, Abdel-Wahhabc MA (2012) Tolerance of mycorrhiza infected Pistachio (Pistacia vera L.) seedling to drought stress under glasshouse conditions. J Plant Physiol 169:704–709
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenol oxidase in Beta vulgaris. Plant Physiol 24:1–15
Augé RM (2001) Water relations, drought and VA mycorrhizal symbiosis. Mycorrhiza 11:3–42
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Berruti A, Borriello R, Lumini E, Scariot V, Bianciotto V, Balestrini R (2013) Application of laser microdissection to identify the mycorrhizal fungi that establish arbuscules inside root cells. Front Plant Sci 4:135. doi:10.3389/fpls.2013.00135
Bressano M, Curetti M, Giachero L, Vargas Gil S, Cabello M, March G, Ducasse DA, Luna CM (2010) Mycorrhizal fungi symbiosis as strategy against oxidative stress in soybean plants. J Plant Physiol 167:1622–1626
Cruz de Carvalho MH (2008) Drought stress and reactive oxygen species: production, scavenging and signaling. Plant Signal Behav 3:156–165
Cruz C, Green JJ, Watson CA, Wilson F, Martins-Loução MA (2004) Functional aspects of root architecture and mycorrhizal inoculation with respect of nutrient uptake capacity. Mycorriza 14:177–184
Daniels BA, Skipper HD (1982) Methods for the recovery and quantitative estimation of propagules from soil. In: Schenck NC (ed) Method and principles of mycorrhizal research. American Phytopathological Soc y Press, St Paul, MN, pp 29–35
Doubková P, Kohout P, Sudová R (2013) Soil nutritional status, not inoculum identity, primarily determines the effects of arbuscular mycorrhizal fungi on the growth of Knautia arvensis plants. Mycorrhiza 23:561–572
Douds DD, Nagahashi G, Reed Hepperly P (2010) On-farm production of inoculum of indigenous arbuscular mycorrhizal fungi and assessment of diluents of compost for inoculum production. Bioresource Technol 101:2326–2330
Edathil TT, Manian S, Udaiyan K (1996) Interaction of multiple VAM fungal species on root colonization, plant growth and nutrient status of tomato seedlings (Lycopersicon esculentum Mill.). Agr Ecosyst Environ 59:63–68
Gong M, Tang M, Chen H, Zhang Q, Feng X (2013) Effects of two Glomus species on the growth and physiological performance of Sophora davidii seedlings under water stress. New For 44:399–408. doi:10.1007/s11056-012-9349-1
Grilli G, Urcelay C, Galetto L (2012) Forest fragment size and nutrient availability: complex responses of mycorrhizal fungi in native-exotic hosts. Plant Ecol 213:155–165
Gustafson DJ, Casper BB (2006) Differential host plant performance as a function of soil arbuscular fungal communities: experimentally manipulating co-occurring Glomus species. Plant Ecol 183:257–263
Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611
Hoeksema JD, Chaudhary VB, Gehring CA, Johnson NC, Karst J, Koide RT, Pringle A, Zabinski C, Bever JD, Moore JC, Wilson GWT, Klironomos JN, Umbanhowar J (2010) A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi. Ecol Letters 13:394–407
Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789
Koide RT (2000) Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytol 147:233–235
Lascano R, Antonicelli GE, Luna CM, Melchiorre M, Gomez LD, Racca RW, Trippi VS, Casano LM (2001) Antioxidant system response of different wheat cultivars under drought: field and in vitro studies. Austr J Plant Physiol 28:1095–1102
Lewandowski TJ, Dunfield KE, Antunes PM (2013) Isolate identity determines plant tolerance to pathogen attack in assembled mycorrhizal communities. PLoS ONE 8:e61329. doi:10.1371/journal.pone.0061329
Longo S, Nouhra E, Goto B, Berbara R, Urcelay C (2014) Effects of fire on arbuscular mycorrhizal fungi in the mountain Chaco forest. Forest Ecol Manag 315:86–94
Maherali H, Klironomos JL (2007) Influence of phylogeny on fungal community assembly and ecosystem functioning. Sci 316:1746–1748
McGonigle TP, Miller MH, Evans DG, Fairchild GL, Swan JA (1990) A method which gives an objective measure of colonization of roots by vesicular-arbuscular mycorrhizal fungi. New Phytol 115:495–501
Mokrasch LC (1954) Analysis of hexose phosphates and sugar mixtures with the anthrone reagent. J Biol Chem 208:55–59
Murphy J, Riley JP (1962) A modified single solution method for determination of phosphate in natural waters. Anal Chim Acta 27:31–36
Perez-Brandán C, Arzenoa JL, Huidobro J, Grümberg B, Conforto C, Hiltond S, Bending GD, Meriles JM, Vargas-Gil S (2012) Long-term effect of tillage systems on soil microbiological, chemical and physical parameters and the incidence of charcoal rot by Macrophomina phaseolina (Tassi) Goid in soybean. Crop Prot 40:73–82
Phillips JM, Hayman DS (1970) Improved procedure of clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. Trans Br Mycol Soc 55:159–161
Porcel R, Ruiz-Lozano JM (2004) Arbuscular mycorrhizal influence on leaf water potential solute accumulation and oxidative stress in soybean plants subjected to drought stress. J Exp Bot 55:1743–1750
Rapparini F, Peñuelas J (2014) Mycorrhizal fungi to alleviate drought stress on plant growth. In: Miransari M (ed) Use of microbes for the alleviation of soil stresses, vol 1. Springer, New York, pp 21–42
Ruth B, Khalvati M, Schmidhalter U (2011) Quantification of mycorrhizal water uptake via high resolution on-line water content sensors. Plant Soil 342:459–468
Saia S, Amato G, Salvatore Frenda A, Giambalvo D, Ruisi P (2014) Influence of arbuscular mycorrhizae on biomass production and nitrogen fixation of berseem clover plants subjected to water stress. PLoS ONE 9(3):e90738. doi:10.1371/journal.pone.0090738
Shukla A, Kumar A, Jha A, Salunkhe O, Vyas D (2013) Soil moisture levels affect mycorrhization during early stages of development of agroforestry plants. Biol Fertil Soils 49:545–554
Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd ed. London. Academic Press. ISBN 0123705266, 9780123705266
Smith SE, Smith FA (2011) Roles of arbuscular mycorrhizas in plant nutrition and growth: new paradigms from cellular to ecosystem scales. Annu Rev Plant Biol 63:227–250
Smith SE, Facelli E, Pope S, Smith FA (2010) Plant performance in stressful environments: interpreting new and established knowledge of the roles of arbuscular mycorrhizas. Plant Soil 326:3–20
Urcelay C, Díaz S, Gurvich DE, Chapin FS III, Cuevas E, Domínguez LS (2009) Mycorrhizal community resilience in response to experimental plant functional type removals in a woody ecosystem. J Ecol 97:1291–1301
van der Heijden MGA, Wiemken A, Sanders IR (2003) Different arbuscular mycorrhizal fungi alter coexistence and resource distribution between co-occurring plant. New Phytol 157:569–578. doi:10.1046/j.1469-8137.2003.00688.x
Varesoglou SD, Menexes G, Rillig M (2012) Do arbuscular mycorrhizal fungi affect allometric partition of host plant biomass to shoots and roots? A meta-analysis of studies from 1990 to 2010. Mycorrhiza 22:227–235
Verbruggen E, Kiers ET (2010) Evolutionary ecology of mycorrhizal functional diversity in agricultural systems. Evol Appl 3:547–560
Verbruggen E, Van der Heijden MGA, Rillig MC, Kiers ET (2013) Mycorrhizal fungal establishment in agricultural soils: factors determining inoculation success. New Phytol 197:1104–1109. doi:10.1111/j.1469-8137.2012.04348.x
Vogelsang K, Reynolds HL, Bever J (2006) Mycorrhizal fungal identity and richness determine the diversity and productivity of a tallgrass prairie system. New Phytol 172:554–562
Wagg C, Jansa J, Schmid B, Van der Heijden MGA (2011) Belowground biodiversity effects of plant symbionts support aboveground productivity. Ecol Lett 14:1001–1009
Wu QS, Xia RX, Zou YN (2006) Reactive oxygen metabolism in mycorrhizal and non-mycorrhizal citrus (Poncirus trifoliata) seedlings subjected to water stress. J Plant Physiol 163:1101–1110
Zhang Y, Zhong CL, Chen Y, Chen Z, Jiang QB, Wu C, Pinyopusarerk K (2010) Improving drought tolerance of Casuarina equisetifolia seedlings by arbuscular mycorrhizas under glasshouse conditions. New For 40:261–270
Zhu X, Song F, Liu S (2011) Arbuscular mycorrhiza impacts on drought stress of maize plants by lipid peroxidation, proline content and activity of antioxidant system. J Food Agric Environ 9:583–587
Acknowledgments
This work was funded by the National Council of Scientific and Technical Research (CONICET) through a PIP-CONICET 2010–2012 -112 200901 00157 and doctoral fellowship awarded to B.C. Grümberg, and by the National Institute of Agricultural Technology (INTA): PE PNCER 022472 and PE AERN 295582 . CU wishes to acknowledge the assistance of CONICET and the Universidad Nacional de Córdoba, both of which have provided facilities for this study. CU also acknowledges the support of Secyt and Agencia Córdoba Ciencia.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
(DOC 1.86 MB)
Rights and permissions
About this article
Cite this article
Grümberg, B.C., Urcelay, C., Shroeder, M.A. et al. The role of inoculum identity in drought stress mitigation by arbuscular mycorrhizal fungi in soybean. Biol Fertil Soils 51, 1–10 (2015). https://doi.org/10.1007/s00374-014-0942-7
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00374-014-0942-7