Abstract
The extraradical mycelium (ERM) produced by arbuscular mycorrhizal fungi is fundamental for the maintenance of biological fertility in agricultural soils, representing an important inoculum source, together with spores and mycorrhizal root fragments. Its viability and structural traits, such as density, extent and interconnectedness, which are positively correlated with the growth and nutrition of host plants, may be affected by different agronomic practices, including the use of pesticides and by different mycorrhizospheric communities. This work, carried out using a whole-plant experimental model system, showed that structural traits of ERM, such as length and density, were strongly decreased by the herbicides dicamba and glufosinolate and the fungicides benomyl and fenhexamid, while anastomosis frequency and hyphal branching were differentially modulated by singly inoculated mycorrhizospheric bacteria, depending on their identity.
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References
Aspray TJ, Jones EE, Davies MW, Shipman M, Bending GD (2013) Increased hyphal branching and growth of ectomycorrhizal fungus Lactarius rufus by the helper bacterium Paenibacillus sp. Mycorrhiza 2:403–410. https://doi.org/10.1007/s00572-013-0483-1
Avio L, Pellegrino E, Bonari E, Giovannetti M (2006) Functional diversity of arbuscular mycorrhizal fungal isolates in relation to extraradical mycelial networks. New Phytol 172:347–357. https://doi.org/10.1111/j.1469-8137.2006.01839.x
Avio L, Turrini A, Giovannetti M, Sbrana C (2018) Designing the ideotype mycorrhizal symbionts for the production of healthy food. Front Plant Sci 9:1089. https://doi.org/10.3389/fpls.2018.01089
Battini F, Cristani C, Giovannetti M, Agnolucci M (2016) Multifunctionality and diversity of culturable bacterial communities strictly associated with spores of the plant beneficial symbiont Rhizophagus intraradices. Microbiol Res 183:68–79. https://doi.org/10.1016/j.micres.2015.11.012
Battini F, Grønlund M, Agnolucci M, Giovannetti M, Jakobsen I (2017) Facilitation of phosphorus uptake in maize plants by mycorrhizosphere bacteria. Sci Rep 7:4686. https://doi.org/10.1038/s41598-017-04959-0
Bidondo LF, Colombo R, Bompadre J, Benavides M, Scorza V, Silvani V, Pérgola M, Godeas A (2016) Cultivable bacteria associated with infective propagules of arbuscular mycorrhizal fungi. Implications for mycorrhizal activity. Appl Soil Ecol 105:86–90. https://doi.org/10.1016/j.apsoil.2016.04.013
Brito I, Goss MJ, de Carvalho M, Chatagnier O, van Tuinen D (2012) Impact of tillage system on arbuscular mycorrhizal fungal communities in the soil under Mediterranean conditions. Soil Till Res 121:63–67. https://doi.org/10.1016/j.still.2012.01.012
Calonne M, Fontaine J, Debiane D, Laruelle F, Grandmougin-Ferjani A, Lounès-Hadj Sahraoui A (2010) Propiconazole toxicity on the non-target organism, the arbuscular mycorrhizal fungus, Glomus irregulare. In: Fungicides. InTechOpen, Rijeka, pp 325–346
Campagnac E, Fontaine J, Sahraoui AL, Laruelle F, Durand R, Grandmougin-Ferjani A (2008) Differential effects of fenpropimorph and fenhexamid, two sterol biosynthesis inhibitor fungicides, on arbuscular mycorrhizal development and sterol metabolism in carrot roots. Phytochemistry 69:2912–2919. https://doi.org/10.1016/j.phytochem.2008.09.009
Campagnac E, Fontaine J, Lounès-Hadj Sahraoui A, Laruelle F, Durand R, Grandmougin-Ferjani A (2009) Fenpropimorph slows down the sterol pathway and the development of the arbuscular mycorrhizal fungus Glomus intraradices. Mycorrhiza 19:365–374. https://doi.org/10.1007/s00572-009-0238-1
Cardenas-Flores A, Cranenbrouck S, Draye X, Guillet A, Govaerts B, Declerck S (2011) The sterol biosynthesis inhibitor molecule fenhexamid impacts the vegetative compatibility of Glomus clarum. Mycorrhiza 21:443–449. https://doi.org/10.1007/s00572-011-0385-z
Casieri L, Ait Lahmidi N, Doidy J, Veneault-Fourrey C, Migeon A, Bonneau L, Courty PE, Garcia K, Charbonnier M, Delteil A, Brun A, Zimmermann S, Plassard C, Wipf D (2013) Biotrophic transportome in mutualistic plant–fungal interactions. Mycorrhiza 23:597–625. https://doi.org/10.1007/s00572-013-0496-9
Chiocchio V, Venedikian N, Martinez AE, Ana Menendez AM, Ocampo JA, Godeas A (2000) Effect of the fungicide benomyl on spore germination and hyphal length of the arbuscular mycorrhizal fungus Glomus mosseae. Internat Microbiol 3:173–175. Accessed 11 Nov 2017
Dodd JC, Jeffries P (1989) Effect of fungicides on three vesicular-arbuscular mycorrhizal fungi associated with winter wheat (Triticum aestivum L.). Biol Fertil Soils 7:120–128. https://doi.org/10.1007/BF00292569
Druille M, Cabello MN, Omacini M, Golluscio RA (2013) Glyphosate reduces spore viability and root colonization of arbuscular mycorrhizal fungi. App Soil Ecol 64:99–103. https://doi.org/10.1016/j.apsoil.2012.10.007
Fitter AH (1986) Effect of benomyl on leaf phosphorus concentration in alpine grasslands: a test of mycorrhizal benefit. New Phytol 103:767–776
Fitter AH, Nichols R (1988) The use of benomyl to control infection by vesicular–arbuscular mycorrhizal fungi. New Phytol 110:201–206
Giovannetti M, Fortuna P, Citernesi AS, Morini S, Nuti MP (2001) The occurrence of anastomosis formation and nuclear exchange in intact arbuscular mycorrhizal networks. New Phytol 151:717–724. https://doi.org/10.1046/j.0028-646x.2001.00216.x
Giovannetti M, Avio L, Sbrana C (2015) Functional significance of anastomosis in arbuscular mycorrhizal networks. In: Horton TR (ed) Mycorrhizal networks. Springer, Dordrecht, pp 41–67
Hage-Ahmed K, Rosner K, Steinkellner S (2019) Arbuscular mycorrhizal fungi and their response to pesticides. Pest Manag Sci 75:583–590. https://doi.org/10.1002/ps.5220
Hale KA, Sanders FE (1982) Effects of benomyl on vesicular arbuscular mycorrhizal infection of red clover (Trifolium pratense L.) and consequences for phosphorus inflow. J Plant Nutr 5:1355–1367. https://doi.org/10.1080/01904168209363069
Hamel C, Fyles H, Smith DL (1990) Measurement of development of endomycorrhizal mycelium using three different vital stains. New Phytol 115:297–302. https://doi.org/10.1111/j.1469-8137.1990.tb00455.x
Helander M, Saloniemi I, Omacini M, Druille M, Salminen JP, Saikkonen K (2018) Glyphosate decreases mycorrhizal colonization and affects plant-soil feedback. Sci Total Environ 642:285–291. https://doi.org/10.1016/j.scitotenv.2018.05.377
Jansa J, Mozafar A, Kuhn G, Anken T, Ruh R, Sanders IR, Frossard E (2003) Soil tillage affects the community structures of mycorrhizal fungi in maize roots. Ecol Appl 13:1164–1176. https://doi.org/10.1890/1051-0761(2003)13[1164:STATCS]2.0.CO;2
Jones MD, Durall DM, Tinker PB (1998) A comparison of arbuscular and ectomycorrhizal Eucalyptus coccifera: growth response, phosphorus uptake efficiency and external hyphal production. New Phytol 140:125–134
Kim KY, Jordan D, McDonald GA (1998) Effect of phosphate-solubilizing bacteria and vesicular-arbuscular mycorrhizae on tomato growth and soil microbial activity. Biol Fert Soils 26:79–87. https://doi.org/10.1007/s003740050347
Kjøller R, Rosendahl S (2000) Effects of fungicides on arbuscular mycorrhizal fungi: differential responses in alkaline phosphatase activity of external and internal hyphae. Biol Fert Soils 31:361–365. https://doi.org/10.1007/s003749900180
Kling M, Jakobsen I (1997) Direct application of carbendazim and propiconazole at field rates to the external mycelium of three arbuscular mycorrhizal fungi species: effect on 32P transport and succinate dehydrogenase activity. Mycorrhiza 7:33–37. https://doi.org/10.1007/s005720050160
Koide RT, Huenneke LF, Hamburg SP, Mooney HA (1988) Effects of applications of fungicide, phosphorus and nitrogen on the structure and productivity of an annual serpentine plant community. Funct Ecol 2:335–344. https://doi.org/10.2307/2389406 https://www.jstor.org/stable/2389406
Krause K, Henke C, Asiimwe T, Ulbricht A, Klemmer S, Schachtschabel D, Boland W, Kothe E (2015) Biosynthesis and secretion of indole-3-acetic acid and its morphological effects on Tricholoma vaccinum-spruce ectomycorrhiza. Appl Environ Microbiol 81:7003–7011. https://doi.org/10.1128/AEM.01991-15
Leinhos GME, Gold RE, Düggelin M, Guggenheim R (1997) Development and morphology of Uncinula necator following treatment with the fungicides kresoxim-methyl and penconazole. Mycol Res 101:1033–1046. https://doi.org/10.1017/S0953756297003651
Majumdar S, Chakraborty U (2015) Phosphate solubilizing rhizospheric Pantoea agglomerans Acti-3 promotes growth in jute plants. World J Agric Sci 11:401–410. https://doi.org/10.5829/idosi.wjas.2015.11.6.1893
Marulanda-Aguirre A, Azcon R, Ruiz-Lozano JM, Aroca R (2008) Differential effects of a Bacillus megaterium strain on Lactuca sativa plant growth depending on the origin of the arbuscular mycorrhizal fungus coinoculated: physiologic and biochemical traits. J Plant Growth Regul 27:10–18. https://doi.org/10.1007/s00344-007-9024-5
Mayo K, Davis RE, Motta J (1986) Stimulation of germination of spores of Glomus versiforme by spore-associated bacteria. Mycologia 78:426–431. https://doi.org/10.2307/3793046
Merryweather J, Fitter A (1996) Phosphorus nutrition of an obligately mycorrhizal plant treated with the fungicide benomyl in the field. New Phytol 132:307–311
Mikkelsen BL, Rosendahl S, Jakobsen I (2008) Underground resource allocation between individual networks of mycorrhizal fungi. New Phytol 180:890–898. New Phytologist (2008). https://doi.org/10.1111/j.1469-8137.2008.02623.x
Njeru EM, Avio L, Sbrana C, Turrini A, Bocci G, Bàrberi P, Giovannetti M (2014) First evidence for a major cover crop effect on arbuscular mycorrhizal fungi and organic maize growth. Agron Sustain Dev 34:841–848. https://doi.org/10.1007/s13593-013-0197-y
Oehl F, Sieverding E, Ineichen K, Mäder P, Dubois D, Boller T, Wiemken A (2004) Impact of long-term conventional and organic farming on the diversity of arbuscular mycorrhizal fungi. Oecologia 138:574–583. https://doi.org/10.1007/s00442-003-1458-2
Pepe A, Giovannetti M, Sbrana C (2016) Different levels of hyphal self-incompatibility modulate interconnectedness of mycorrhizal networks in three arbuscular mycorrhizal fungi within the Glomeraceae. Mycorrhiza 26:325–332. https://doi.org/10.1007/s00572-015-0671-2
Pepe A, Sbrana C, Ferrol N, Giovannetti M (2017) An in vivo whole-plant experimental system for the analysis of gene expression in extraradical mycorrhizal mycelium. Mycorrhiza 27:659–668. https://doi.org/10.1007/s00572-017-0779-7
Pepe A, Giovannetti M, Sbrana C (2018) Lifespan and functionality of mycorrhizal fungal mycelium are uncoupled from host plant lifespan. Sci Rep 8:10235. https://doi.org/10.1038/s41598-018-28354-5
Pivato B, Offre P, Marchelli S, Barbonaglia B, Mougel C, Lemanceau P, Berta G (2009) Bacterial effects on arbuscular mycorrhizal fungi and mycorrhiza development as influenced by the bacteria, fungi, and host plant. Mycorrhiza 19:81–90. https://doi.org/10.1007/s00572-008-0205-2
Sbrana C, Avio L, Giovannetti M (2014) Beneficial mycorrhizal symbionts affecting the production of health-promoting phytochemicals. Electrophoresis 35:1535–1546. https://doi.org/10.1002/elps.201300568
Schreiner RP, Bethlenfalvay GJ (1996) Mycorrhizae, biocides, and biocontrol. 4. Response of a mixed culture of arbuscular mycorrhizal fungi and host plant to three fungicides. Biol Fert Soils 23:189–195. https://doi.org/10.1016/0929-1393(96)00093-5
Schreiner RP, Bethlenfalvay GJ (1997) Mycorrhizae, biocides, and biocontrol 3. Effects of three different fungicides on developmental stages of three AM fungi. Biol Fert Soils 24:18–26. https://doi.org/10.1007/BF01420215
Schubert A, Marzachi C, Mazzitelli M, Cravero MC, Bonfante-Fasolo P (1987) Development of total and viable extraradical mycelium in the vesicular–arbuscular mycorrhizal fungus Glomus clarum Nicol. & Schenck. New Phytol 107:183–190. https://doi.org/10.1111/j.1469-8137.1987.tb04892.x
Smith SE, Gianinazzi-Pearson V (1990) Phosphate uptake and arbuscular activity in mycorrhizal Allium cepa L.: effects of photon irradiance and phosphate nutrition. Aust J Plant Physiol 17:177–188. https://doi.org/10.1071/PP9900177
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic Press, San Diego
Sukarno N, Smith SE, Scott ES (1993) The effect of fungicides on vesicular–arbuscular mycorrhizal symbiosis. New Phytol 125:139–147
Sukarno N, Smith FA, Smith SE, Scott ES (1996) The effect of fungicides on VAM symbiosis. II. The effect on area of interface and efficiency of P uptake and transfer to plant. New Phytol 132:583–592. https://doi.org/10.1111/j.1469-8137.1996.tb01877.x
Turrini A, Sbrana C, Avio L, Njeru EM, Bocci G, Bàrberi P, Giovannetti M (2016) Changes in the composition of native root arbuscular mycorrhizal fungal communities during a short-term cover crop-maize succession. Biol Fertil Soils 52:642–653. https://doi.org/10.1007/s00374-0161106-8
Twanabasu BR, Stevens KJ, Venables BJ (2013) The effects of triclosan on spore germination and hyphal growth of the arbuscular mycorrhizal fungus Glomus intraradices. Sci Total Environ 454:51–60. https://doi.org/10.1016/j.scitotenv.2013.02.036
Wan MT, Rahe JE, Watts RG (1998) A new technique for determining the sublethal toxicity of pesticides to the vesicular-arbuscular mycorrhizal fungus Glomus intraradices. Environ Toxicol Chem 17:1421–1428
Zocco D, Fontaine J, Lozanova E, Renard L, Bivort C, Durand R, Grandmougin-Ferjani A, Declerck S (2008) Effects of two sterol biosynthesis inhibitor fungicides (fenpropimorph and fenhexamid) on the development of an arbuscular mycorrhizal fungus. Mycol Res 112:592–601. https://doi.org/10.1016/j.mycres.2007.11.010
Zocco D, van Aarle IM, Oger E, Lanfranco L, Declerck S (2011) Fenpropimorph and fenhexamid impact phosphorus translocation by arbuscular mycorrhizal fungi. Mycorrhiza 21:363–374. https://doi.org/10.1007/s00572-010-0344-0
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This work was supported by the University of Pisa (Fondi di Ateneo) and by CNR. CBdN was supported by a post-doctoral scholarship from CAPES (Coordination for the Improvement of Higher Level Personnel).
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de Novais, C.B., Giovannetti, M., de Faria, S.M. et al. Two herbicides, two fungicides and spore-associated bacteria affect Funneliformis mosseae extraradical mycelium structural traits and viability. Mycorrhiza 29, 341–349 (2019). https://doi.org/10.1007/s00572-019-00901-6
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DOI: https://doi.org/10.1007/s00572-019-00901-6