Abstract
Aims
Many studies have reported beneficial effects of yeasts on the colonization and development of arbuscular mycorrhizae, thought a few studies have also shown neutral effects. All these studies have in common that the mechanism, by which yeasts and mycorrhizae interact, is little understood. Here, we explore how plant growth-promoting yeasts affect the colonization of tomato plants by beneficial mycorrhizal fungi.
Methods
We tested the influence of the soil yeasts Candida saitoana, Tausonia pullulans, and Saccharomyces eubayanus on colonization of tomato roots by the mycorrhizal fungus Rhizophagus irregularis. We analyzed mycorrhizal parameters and the expression pattern of mycorrhiza-specific genes. In plants co-inoculated with S. eubayanus and R. irregularis, we measured the root accumulation pattern of jasmonic acid, oxo-phytodienoic acid, abscisic acid and salicylic acid, and the expression of genes related to plant hormone signaling and metabolism.
Results
The three yeasts had distinct effects on mycorrhizal colonization: C. saitoana had no effect on mycorrhizal parameters, T. pullulans delayed mycorrhizal colonization at an early stage, and S. eubayanus slowed colonization down throughout the entire trial. In plants co-inoculated with S. eubayanus and R. irregularis, we observed a sustained increase in jasmonic acid and up-regulation of the JA biosynthesis related genes LOXD, OPR3, and AOS1.
Conclusion
Co-inoculation with yeast affected mycorrhizal colonization and altered the expression pattern of mycorrhizal and plant defense-related genes. In particular, the yeast S. eubayanus modified plant defense hormones such as jasmonic acid, which is linked to mycorrhizal-induced resistance in tomato plants.
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References
Amprayn K-o, Rose MT, Kecskés M, Pereg L, Nguyen HT, Kennedy IR (2012) Plant growth promoting characteristics of soil yeast (Candida tropicalis HY) and its effectiveness for promoting rice growth. Appl Soil Ecol 61:295–299
Bedini A, Mercy L, Schneider C, Franken P, Lucic-Mercy E (2018) Unraveling the initial plant hormone signaling, metabolic mechanisms and plant defense triggering the endomycorrhizal symbiosis behavior. Front Plant Sci 9:1800
Boby VU, Balakrishna AN, Bagyaraj DJ (2008) Interaction between Glomus mosseae and soil yeasts on growth and nutrition of cowpea. Microbiol Res 163:693–700
Bonfante P, Genre A (2010) Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat Commun 1:48
Chabot C, Bécard G, Piché Y (1992) Life cycle of Glomus intraradix in root organ culture. Mycologia 84:315–321
Cloete KJ, Valentine AJ, Stander MA, Blomerus LM, Botha A (2009) Evidence of symbiosis between the soil yeast Cryptococcus laurentii and a sclerophyllous medicinal shrub, Agathosma betulina (Berg.) Pillans. Microbial Ecol 57(4):624–632
de Mendiburu F (2020) agricolae tutorial (Version 1.3–3)
Etemadi M, Gutjahr C, Couzigou J-M, Zouine M, Lauressergues D, Timmers A et al (2014) Auxin perception is required for arbuscule development in arbuscular mycorrhizal symbiosis. Plant Physiol 166:281–292
Fernández Merlos M, López-Ráez JA, Martínez-Medina A, Ferrol N, Azcón C, Bonfante P et al (2014) Defense related phytohormones regulation in arbuscular. J Chem Ecol 40:791–803
Fiorilli V, Wang JY, Bonfante P, Lanfranco L, Al-Babili S (2019) Apocarotenoids: old and new mediators of the arbuscular mycorrhizal symbiosis. Front Plant Sci 10:1186
Flors V, Ton J, van Doorn R, Jakab G, García-Agustín P, Mauch-Mani B (2008) Interplay between JA, SA and ABA signalling during basal and induced resistance against Pseudomonas syringae and Alternaria brassicicola. Plant J 54:81–92
Floss DS, Levy JG, Lévesque-Tremblay V, Pumplin N, Harrison MJ (2013) DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. PNAS USA 110:5025–5034
Foo E, Ross JJ, Jones WT, Reid JB (2013) Plant hormones in arbuscular mycorrhizal symbioses: an emerging role for gibberellins. Ann Bot 111:769–779
Fracchia S, Godeas A, Scervino JM, Sampedro I, Ocampo JA, Garcıa-Romera I (2003) Interaction between the soil yeast Rhodotorula mucilaginosa and the arbuscular mycorrhizal fungi Glomus mosseae and Gigaspora rosea. Soil Biol Biochem 35:701–707
Giraudoux P, Giraudoux MP, MASS S (2018). Package ‘pgirmess’
Gollner MJ, Püschel D, Rydlová J, Vosátka M (2006) Effect of inoculation with soil yeasts on mycorrhizal symbiosis of maize. Pedobiologia 50:341–345
Hause B, Schaarschmidt S (2009) The role of jasmonates in mutualistic symbioses between plants and soil-born microorganisms. Phytochemistry 70:1589–1599
Hause B, Mrosk C, Isayenkov S, Strack D (2007) Jasmonates in arbuscular mycorrhizal interactions. Phytochemistry 68:101–110
Herrera Medina MJ, Gagnon H, Piché Y, Ocampo JA, García-Garrido JM, Vierheilig H (2003) Root colonization by arbuscular mycorrhizal fungi is affected by the salicylic acid content of the plant. Plant Sci 164:993–998
Herrera-Medina MJ, Steinkellner S, Vierheilig H, Ocampo Bote JA, García-Garrido JM (2007) Abscisic acid determines arbuscule development and functionality in the tomato arbuscular mycorrhiza. New Phytol 175:554–564
Herrera-Medina MJ, Tamayo M, Vierheilig H, Ocampo JA, García-Garrido JM (2008) The jasmonic acid signalling pathway restricts the development and functionality in the tomato arbuscular mycorrhiza. J Plant Growth Regul 175:554–564
Hewitt EJ (1966) Sand water culture methods used in the study of plant nutrition. Commonwealth Agricult Bureau, Technical communication N∘ 22
Ho-Plágaro T, Morcillo RJL, Tamayo-Navarrete MI, Huertas R, Molinero-Rosales N, López-Ráez JA et al (2021) DLK2 regulates arbuscule hyphal branching during arbuscularmycorrhizal simbiosis. New Phytol 229:548–562
Jung SC, Martinez-Medina A, Lopez-Raez JA, Pozo MJ (2012) Mycorrhiza-Induced Resistance and Priming of Plant Defenses. J Chem Ecol 38:651–664
Koo AJK, Gao X, Jones AD, Howe GA (2009) A rapid wound signal activates the systemic synthesis of bioactive jasmonates in Arabidopsis. Plant J 59:974–986
Lanfranco L, Fiorilli V, Venice F, Bonfante P (2018) Strigolactones cross the kingdoms: plants, fungi, and bacteria in the arbuscular mycorrhizal symbiosis. J Exp Bot 69:2175–2188
León Morcillo R, Martín Rodríguez JA, Vierheilig H, Ocampo JA, García Garrido JM (2012) Late activation of the 9-oxylipin pathway during Arbuscular Mycorrhiza formation in tomato and its regulation by jasmonate signalling. J Exp Bot 63:3545–3558
Liao D, Wang S, Cui M, Liu J, Chen A, Xu G (2018) Phytohormones regulate the development of arbuscular mycorrhizal symbiosis. Int J Mol Sci 19:3146
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408
López-Ráez JA, Kohlen W, Charnikhova T, Mulder P, Undas AK, Sergeant MJ et al (2010) Does abscisic acid affect strigolactone biosynthesis? New Phytol 187:343–354
Martinez-Medina A, Fernandez I, Lok GB, Pozo MJ, Pieterse CMJ, Van Wees SCM (2017) Shifting from priming of salicylic acid- to jasmonic acid-regulated defences by Trichoderma protects tomato against the root knot nematode Meloidogyne incognita. New Phytol 213:1363–1377
Martín-Rodríguez J, León-Morcillo R, Vierheilig H, Ocampo JA, Ludwig-Müller J, García-Garrido JM (2011) Ethylene-dependent/ethylene-independent ABA regulation of tomato plants colonized by arbuscular mycorrhiza fungi. New Phytol 190:193–205
Martín-Rodríguez JA, Huertas R, Ho-Plágaro T, Ocampo JA, Turecková V, Tarkowská D et al (2016) Gibberellin-abscisic acid balances during arbuscular mycorrhiza formation in tomato. Front Plant Sci 7:1273
Mestre MC, Rosa CA, Safar SVB, Libkind D, Fontenla SB (2011) Yeast communities associated with the bulk-soil, rhizosphere and ectomycorrhizosphere of a Nothofagus pumilio forest in northwestern Patagonia, Argentina. FEMS Microbiol Ecol 78:31–541
Mestre MC, Fontenla S, Rosa CA (2014) Ecology of cultivable yeasts in pristine forests in northern Patagonia (Argentina) influenced by different environmental factors. Can J Microbiol 60:371–382
Mestre MC, Fontenla S, Bruzone MC, Fernández NV, Dames J (2016) Detection of plant growth enhancing features in psychrotolerant yeasts from Patagonia (Argentina). J Basic Microbiol 56:1098–1106
Mestre MC, Pastorino MJ, Aparicio AG, Fontenla SB (2017) Natives helping foreigners?: The effect of inoculation of poplar with patagonian beneficial microorganisms. J Soil Sci Plant Nutr 17:1028–1039
Mestre MC, Severino ME, Fontenla S (2021) Evaluation and selection of culture media for the detection of auxin-like compounds and phosphate solubilization on soil yeasts. Rev Arg Microbiol 53(1):78–83
Mohamed HM (2015) Effect of Arbuscular Mycorrhizal Fungus (Glomus Mosseae) and Soil Yeasts Interaction on Root Nodulation, N-Fixation and Growth of Faba Bean (Vichia faba). Malaysian J Soil Sci 19:157–168
Nassar A, El-Tarabily K, Sivasithamparam K (2005) Promotion of plant growth by an auxin-producing isolate of the yeast Williopsis saturnus endophytic in maize (Zea mays L.) roots. Biol Fertil Soils 42:97–108
Nutaratat P, Srisuk N, Arunrattiyakorn P, Limtong S (2014) Plant growth-promoting traits of epiphytic and endophytic yeasts isolated from rice and sugar cane leaves in Thailand. Fungal Biol 118:683–694
Phillips JM, Hayman DS (1970) Improved procedures for clearing roots and staining parasitic and vesicular-arbuscular mycorrhizal fungi for rapid assessment of infection. T Brit Mycol Society 55:158–161
Pozo MJ, López-Ráez JA, Azcón-Aguilar C, García-Garrido JM (2015) Phytohormones as integrators of environmental signals in the regulation of mycorrhizal symbioses. New Phytol 205:1431–1436
Rich MK, Courty PE, Roux C, Reinhardt D (2017) Role of the GRAS transcription factor ATA/RAM1 in the transcriptional reprogramming of arbuscular mycorrhiza in Petunia hybrida. BMC Genomics 18:589
Sampedro I, Aranda E, Scervino JM, Fracchia S, Garcia-Romera I, Ocampo JA, Godeas A (2004) Improvement by soil yeasts of arbuscular mycorrhizal symbiosis of soybean (Glycine max) colonized by Glomus mosseae. Mycorrhiza 14:229–234
Sánchez-Romera B, Calvo-Polanco M, Ruiz-Lozano JM, Zamarreño ÁM, Arbona V, García-Mina JM, Gómez-Cadenas A, Aroca R (2018) Involvement of the def-1 mutation in the response of tomato plants to arbuscular mycorrhizal symbiosis under well-watered and drought conditions. Plant Cell Physiol 59:248–261
Sarabia M, Cornejo P, Azcón R, Carreón-Abud Y, Larsen J (2017) Mineral phosphorus fertilization modulates interactions between maize, rhizosphere yeasts and arbuscular mycorrhizal fungi. Rhizosphere 4:89–93
Singh CS, Kapoor A, Wange SS (1991) The enhancement of root colonisation of legumes by vesicular-arbuscular mycorrhizal (VAM) fungi through the inoculation of the legume seed with commercial yeast (Saccharomyces cerevisiae). Plant Soil 131:129–133
Smith SE, Read DJ (2008) Mycorrhizal symbiosis. Academic press, London
Thaler JS, Fidantsef AL, Bostock RM (2002) Antagonism between Jasmonate- and Salicylate-mediates induced plant resistance: effect of concentration and timing of elicitation on defence-related proteins, herbivore, and pathogen performance in tomato. J Chem Ecol 28:1131–1159
Torres-Vera RM, García J, Lopez-Raez Pozo MJ., JA, (2016) Expression of molecular markers associated to defense signalling pathways and strigolactone biosynthesis during the early interaction tomato-Phelipanche ramose. Physiol Mol Plant Pathol 94:100e107101
Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorrhization VA d’un système radiculaire. Recherche de methods d’estimation ayant une signification fonctionelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, pp 217–221
Wickham H (2016) Programming with ggplot2. In ggplot2. Springer, Cham, pp. 241–253
Xin G, Glawe D, Doty SL (2009) Characterization of three endophytic, indole-3-acetic acid-producing yeasts occurring in Populus trees. Mycol Res 113:973–980
Acknowledgements
LCMS analyses were carried out by Dr. Lourdes Sánchez-Moreno at the Scientific Instrumentation Service of the Estación Experimental del Zaidín (CSIC), Granada, Spain. This work was supported by Fondo para la Investigación Científica y Tecnológica (FONCYT) projects PICT2018-3441, Argentina. M.C.M. work at Estación Experimental del Zaidín (EEZ) was supported by a Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) partial fellowship for Assistant Researchers.
Funding
This work was supported by Fondo para la Investigación Científica y Tecnológica (FONCYT) projects PICT2018-3441, Argentina. M.C.M. work at Estación Experimental del Zaidín (EEZ) was supported by a Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) partial fellowship for Assistant Researchers.
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MCMestre and JMGarcía-Garrido contributed to the study conception and design. Material preparation and data collection was performed by MCMestre and MI Tamayo Navarrete; data analysis was performed by MCMestre and JM García-Garrido. The first draft of the manuscript was written by MCMestre and all authors commented on previous version of the manuscript. All author read and approved the final manuscript.
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Mestre, M.C., Tamayo Navarrete, M.I. & García Garrido, J.M. Exploring the yeast-mycorrhiza-plant interaction: Saccharomyces eubayanus negative effects on arbuscular mycorrhizal formation in tomato plants. Plant Soil 479, 529–542 (2022). https://doi.org/10.1007/s11104-022-05538-7
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DOI: https://doi.org/10.1007/s11104-022-05538-7