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AM fungi and PGP pseudomonads increase flowering, fruit production, and vitamin content in strawberry grown at low nitrogen and phosphorus levels

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Abstract

There is increasing interest in the quality of crops because of the implications concerning health, economic revenue, and food quality. Here we tested if inoculation with a mixture of arbuscular mycorrhizal fungi (AMF) and/or two strains of plant growth-promoting bacteria (PGPB), in conditions of reduced chemical inputs, affects the quality and yield of strawberry fruits. Fruit quality was measured by concentrations of soluble sugars, various organic acids, and two vitamins (ascorbic and folic acid). Co-inoculation with the AMF and each of the two PGPB resulted in increased flower and fruit production, larger fruit size, and higher concentrations of sugars and ascorbic and folic acid in comparison with fruits of uninoculated plants. These results provide further evidence that rhizospheric microorganisms affect fruit crop quality and show that they do so even under conditions of reduced chemical fertilization and can thus be exploited for sustainable agriculture.

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References

  • Aimo S, Gosetti F, D’Agostino G, Gamalero E, Gianotti V, Bottaro M, Gennaro MC, Berta G (2010) Use of arbuscular mycorrhizal fungi and beneficial soil bacteria to improve yield and quality of Saffron (Crocus sativus L.). ISHS Acta Horticult 850:159–162

    Google Scholar 

  • Altamura M, Biondi S, Colombo L, Guzzo F (2007) Elementi di Biologia dello sviluppo delle piante. EdiSES

  • Aseri GK, Jain N, Panwar J, Rao AV, Meghwal PR (2008) Biofertilizers improve plant growth, fruit yield, nutrition, metabolism and rhizosphere enzyme activities of pomegranate (Punica granatum L.) in Indian Thar Desert. Sci Hortic 117:130–135

    Article  Google Scholar 

  • Bailly A, Weisskopf L (2012) The modulating effect of bacterial volatiles on plant growth current knowledge and future challenges. Plant Signal Behav 7:1–7

    Article  Google Scholar 

  • Barea J, Azcón-Aguilar C (1982) Production of plant growth-regulating substances by the vesicular-arbuscular mycorrhizal fungus Glomus mosseae. Appl Environ Microbiol 43:810–813

    PubMed Central  CAS  PubMed  Google Scholar 

  • Barea J, Gryndler M, Lemanceau P, Schuepp H, Azcon R (2002) The rhizosphere of mycorrhizal plants. In: Schuepp H, Barea J, Haselwandter K, Gianinazzi S (eds) Mycorrhizal technology in agriculture. Birkhauser, Basel, pp 1–19

    Chapter  Google Scholar 

  • Baslam M, Esteban R, García-Plazaola JI, Goicoechea N (2013) Effectiveness of arbuscular mycorrhizal fungi (AMF) for inducing the accumulation of major carotenoids, chlorophylls and tocopherol in green and red leaf lettuces. Appl Microbiol Biotechnol 97:3119–3128

    Article  CAS  PubMed  Google Scholar 

  • Berta G, Copetta A, Gamalero E, Bona E, Cesaro P, Scarafoni A, D’Agostino G (2014) Maize development and grain quality are differentially affected by mycorrhizal fungi and a growth-promoting pseudomonad in the field. Mycorrhiza 24:161–170

    Article  PubMed  Google Scholar 

  • Bidlack W (1996) Interrelationships of food, nutrition, diet and health: the National Association of State Universities and Land Grant Colleges White Paper. J Am Coll Nutr 15:422–433

    Article  CAS  PubMed  Google Scholar 

  • Boldt K, Pörs Y, Haupt B, Bitterlich M, Kühn C, Grimm B, Franken P (2011) Photochemical processes, carbon assimilation and RNA accumulation of sucrose transporter genes in tomato arbuscular mycorrhiza. J Plant Physiol 168:1256–1263

    Article  CAS  PubMed  Google Scholar 

  • Bona E, Cattaneo C, Cesaro P, Marsano F, Lingua G, Cavaletto M, Berta G (2010) Proteomic analysis of Pteris vittata fronds: two arbuscular mycorrhizal fungi differentially modulate protein expression under arsenic contamination. Proteomics 10:3811–3834

    Article  CAS  PubMed  Google Scholar 

  • Bona E, Marsano F, Massa N, Cattaneo C, Cesaro P, Argese E, Sanità di Toppi L, Cavaletto M, Berta G (2011) Proteomic analysis as a tool for investigating arsenic stress in Pteris vittata roots colonized or not by arbuscular mycorrhizal symbiosis. J Proteomics 74:1338–1350

    Article  CAS  PubMed  Google Scholar 

  • Bryla D, Koide R (1998) Mycorrhizal response of two tomato genotype relates to their ability to acquire and utilization of phosphorus. Ann Bot 82:849–857

    Article  Google Scholar 

  • Burkowska B (2002) Growth and photosynthetic activity of micropropagated strawberry plants inoculated with endomycorrhizal fungi (AMF) and growing under drought stress. Acta Physiol Plant 24:365–370

    Article  Google Scholar 

  • Castellanos-Morales V, Villegas J, Wendelin S, Vierheilig H, Eder R, Cardenas-Navarro R (2010) Root colonisation by the arbuscular mycorrhizal fungus Glomus intraradices alters the quality of strawberry fruits (Fragaria × ananassa Duch.) at different nitrogen levels. J Sci Food Agric 90:1774–1782

    CAS  PubMed  Google Scholar 

  • Chakrabarti J, Chatterjee S, Ghosh S, Chatterjee NC, Dutta S (2010) Synergism of VAM and Rhizobium on production and metabolism of IAA in roots and root nodules of Vigna mungo. Curr Microbiol 61:203–209

    Article  CAS  PubMed  Google Scholar 

  • Chatterjee I (1973) Evolution and the biosynthesis and ascorbic acid. Science 182:1271–1272

    Article  CAS  PubMed  Google Scholar 

  • Cicatelli A, Lingua G, Todeschini V, Biondi S, Torrigiani P, Castiglione S (2012) Arbuscular mycorrhizal fungi modulate the leaf transcriptome of a Populus alba L. clone grown on a zinc and copper-contaminated soil. Environ Exp Bot 75:25–35

    Article  CAS  Google Scholar 

  • Copetta A, Lingua G, Berta G (2006) Effects of three AM fungi on growth, distribution of glandular hairs, and essential oil production in Ocimum basilicum L. var. Genovese. Mycorrhiza 16:485–494

    Article  CAS  PubMed  Google Scholar 

  • Copetta A, Lingua G, D’Agostino G, Berta G (2010) Arbuscular mycorrhizae affect melon fruit quality under field conditions. MycoMED 2010: “Mycorrhiza Symbiosis: Ecosystems and Environment of Mediterranean Area”. Marrakech

  • Copetta A, Bardi L, Bertolone E, Berta G (2011) Fruit production and quality of tomato plants (Solanum lycopersicum L.) are affected by green compost and arbuscular mycorrhizal fungi. Plant Biosyst 145:106–115

    Article  Google Scholar 

  • Cordenunsi B, Oliveira do Nascimento J, Genovese M, Lajolo F (2002) Influence of cultivar on quality parameters and chemical composition of strawberry fruits grown in Brazil. J Agric Food Chem 50:2581–2586

    Article  CAS  PubMed  Google Scholar 

  • Cruz-Rus E, Amaya I, Sanchez-Sevilla J, Botella MA, Valpuesta V, Sanchez-Sevilla JF (2011) Regulation of L-ascorbic acid content in strawberry fruits. J Exp Bot 62:4191–4201

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Danneberg G, Latus C, Zimmer W, Hundeshagen B, Schneider-Poetsch HJ, Bothe H (1993) Influence of vesicular-arbuscular mycorrhiza on phytohormone balances in maize (Zea mays L.). J Plant Physiol 141:33–39

    Article  CAS  Google Scholar 

  • De Brito Alvarez M, Gagné S, Antoun H (1995) Effect of compost on rhizosphere microflora of the tomato and on the incidence of plant-growth promoting rhizobacteria. Appl Environ Microbiol 61:194–199

    Google Scholar 

  • De Jong M, Wolters-Arts M, Feron R, Mariani C, Vriezen WH (2009) The Solanum lycopersicum auxin response factor 7 (SlARF7) regulates auxin signaling during tomato fruit set and development. Plant J 57:160–170

    Article  PubMed  Google Scholar 

  • Doumett S, Fibbi D, Cincinelli A, Giordani E, Nin S, Del M (2011) Comparison of nutritional and nutraceutical properties in cultivated fruits of Fragaria vesca L. produced in Italy. Food Res Int 44:1209–1216

    Article  CAS  Google Scholar 

  • El Ghachtouli N, Martin-Tanguy J, Paynot M, Gianinazzi S (1996) First report of the inhibition of arbuscular mycorrhizal infection of Pisum sativum by specific and irreversible inhibition of polyamine biosynthesis or by gibberellic acid treatment. FEBS Lett 385:189–192

    Article  PubMed  Google Scholar 

  • Erturk Y, Ercilsi S, Cakmakci R (2012) Yield and growth response of strawberry to plant growth-promoting rhizobacteria inoculation. J Plant Nutr 35:817–826

    Article  CAS  Google Scholar 

  • Esitken A, Yildiz HE, Ercisli S, Figen Donmez M, Turan M, Gunes A (2010) Effects of plant growth promoting bacteria (PGPB) on yield, growth and nutrient contents of organically grown strawberry. Sci Hortic 124:62–66

    Article  CAS  Google Scholar 

  • Faedi W (2010) Fragola nel mondo. In: ART spa (ed) La Fragola. Bologna, pp 358–361

  • Floss DS, Levy JG, Lévesque-Tremblay V, Pumplin N, Harrison MJ (2013) DELLA proteins regulate arbuscule formation in arbuscular mycorrhizal symbiosis. Proc Natl Acad Sci USA 110:E5025–E5034

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gamalero E, Glick B (2011) Mechanisms used by plant growth-promoting bacteria. In: Maheshwari D (ed) Bacteria in agrobiology. Plant nutrient managing. Springer, Berlin, pp 17–46

    Chapter  Google Scholar 

  • Gaur A, Gaur A, Adholeya A (2000) Growth and flowering in Petunia hybrida, Callistephus chinensis and Impatiens balsamina inoculated with mixed AM inocula or chemical fertilizers in a soil of low P fertility. Sci Hortic 84:151–162

    Article  CAS  Google Scholar 

  • Gianinazzi S, Gollotte A, Binet M, van Tuinen D, Redecher D, Wipf D (2010) Agroecology. The role of arbuscular mycorrhizas in ecosystem services. Mycorrhiza 20:519–530

    Article  PubMed  Google Scholar 

  • Glick B (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 143:3921–3931

    Google Scholar 

  • Goldstein A (1986) Bacterial solubilization of mineral phosphates: historical perspective and future prospect. Am J Altern Agric 1:51–57

    Google Scholar 

  • Gravel V, Antoun H, Tweddell R (2007) Growth stimulation and fruit yield improvement of greenhouse tomato plants by inoculation with Pseudomonas putida or Trichoderma atroviride: possible role of indole acetic acid (IAA). Soil Biol Biochem 39:1968–1977

    Article  CAS  Google Scholar 

  • Gryndler M, Vosatka M, Hrselova H, Catska V, Chvatalova I, Jansa J (2002) Effect of dual inoculation with arbuscular mycorrhizal fungi and bacteria on growth and mineral nutrition of strawberry. J Plant Nutr 25:1341–1358

    Article  CAS  Google Scholar 

  • Guerrieri E, Lingua G, Digilio MC, Massa N, Berta G (2004) Do interactions between plant roots and the rhizosphere affect parasitoid behaviour? Ecol Entomol 29:753–756

    Article  Google Scholar 

  • Hanson AD, Gregory JF (2011) Folate biosynthesis, turnover, and transport in plants. Annu Rev Plant Biol 62:105–125

    Article  CAS  PubMed  Google Scholar 

  • Harrier L, Watson C (2003) The role of arbuscular mycorrhizal fungi in sustainable cropping systems. Adv Agron 79:185–225

    Article  Google Scholar 

  • Hortyfiski JA, Zebrowska J, Gawrofiski J, Hulewicz T (1991) Factors influencing fruit size in the strawberry (Fragaria × ananassa Duch.). Euphytica 56:67–74

    Google Scholar 

  • Hrselova H, Grindler H, Vancura V (1989) Influence of inoculation with VA mycorrhizal fungus Glomus sp. on growth of strawberries and runner formation. In: Agriculture Ecosystems and Environment. Elsevier Science Publishers B.V., Amsterdam, pp 193–197

  • Jentschel K, Thiel D, Rehn F, Ludwig-Müller J (2007) Arbuscular mycorrhiza enhances auxin levels and alters auxin biosynthesis in Tropaeolum majus during early stages of colonization. Physiol Plant 129:320–333

    Article  CAS  Google Scholar 

  • Kallio H, Hakala M, Pelkkikangas A, Lapvetelainen A (2000) Sugars and acids of strawberry varieties. Eur Food Res Technol 212:81–85

    Article  CAS  Google Scholar 

  • Kapulnik Y, Tsror L, Zipori I, Hazanovsky M, Wininger S, Dag A (2010) Effect of AMF application on growth, productivity and susceptibility to Verticillium wilt of olives grown under desert conditions. Symbiosis 52:103–111

    Article  Google Scholar 

  • Keutgen A, Pawelzik E (2007) Food chemistry modifications of taste-relevant compounds in strawberry fruit under NaCl salinity. Food Chem 105:1487–1494

    Article  CAS  Google Scholar 

  • Koide R, Lu X (1992) Mycorrhizal infection of wild oats: maternal effects on offspring growth and reproduction. Oecologia 90:218–226

    Article  Google Scholar 

  • Lingua G, Bona E, Todeschini V, Cattaneo C, Marsano F, Berta G, Cavaletto M (2012) Effects of heavy metals and arbuscular mycorrhiza on the leaf proteome of a selected poplar clone: a time course analysis. PLoS ONE 7:e38662

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Lingua G, Bona E, Manassero P, Marsano F, Todeschini V, Cantamessa S, Copetta A, D’Agostino G, Gamalero E, Berta G (2013) Arbuscular mycorrhizal fungi and plant growth-promoting pseudomonads increases anthocyanin concentration in strawberry fruits (Fragaria × ananassa var. Selva) in conditions of reduced fertilization. Int J Mol Sci 14:16207–16225

    Article  PubMed Central  PubMed  Google Scholar 

  • Lu X, Koide RT (1994) The effects of mycorrhizal infection on components of plant growth and reproduction. New Phytol 128:211–218

    Article  CAS  Google Scholar 

  • Ludwig-Müller J, Kaldorf M, Sutter EG, Epstein E (1997) Indole-3-butyric acid (IBA) is enhanced in young maize (Zea mays L.) roots colonized with the arbuscular mycorrhizal fungus Glomus intraradices. Plant Sci 125:153–162

    Article  Google Scholar 

  • Mia M, Shamsuddin Z, Mahmood M (2010) Use of plant growth promoting bacteria in banana: a new insight for sustainable banana production. Int J Agric Biol 12:459–467

    Google Scholar 

  • Narayanan KR, Mudge KW, Poovaiah BW (1981) Demonstration of auxin binding to strawberry fruit membranes. Plant Physiol 68:1289–1293

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nzanza B, Marais D, Soundy P (2012) Yield and nutrient content of tomato (Solanum lycopersicum L.) as influenced by Trichoderma harzianum and Glomus mosseae inoculation. Sci Hortic 144:55–59

    Article  CAS  Google Scholar 

  • Ortu G, Balestrini R, Pereira PA, Becker JD, Küster H, Bonfante P (2012) Plant genes related to gibberellin biosynthesis and signaling are differentially regulated during the early stages of AM fungal interactions. Mol Plant 5:951–954

    Article  CAS  PubMed  Google Scholar 

  • Perez G, Olias R, Espada J, Olias JM, Sanz C (1997) Rapid determination of sugars, nonvolatile acids, and ascorbic acid in strawberry and other fruits. J Agric Food Chem 45:3545–3549

    Article  CAS  Google Scholar 

  • Perkins-Veazie P, Collins J (1995) Strawberry fruit quality and its maintenance in postharvest environments. Adv Strawberry Res 14:1–8

    Google Scholar 

  • Pirlak L, Kose M (2009) Effects of plant growth promoting rhizobacteria on yield and some fruit properties of strawberry. J Plant Nutr 32:1173–1184

    Article  CAS  Google Scholar 

  • Poulton JL, Bryla D, Koide RT, Stephenson AG (2002) Mycorrhizal infection and high soil phosphorus improve vegetative growth and the female and male functions in tomato. New Phytol 154:255–264

    Article  CAS  Google Scholar 

  • Rolland F, Baena-Gonzalez E, Sheen J (2006) Sugar sensing and signaling in plants: conserved and novel mechanisms. Annu Rev Plant Biol 57:675–709

    Article  CAS  PubMed  Google Scholar 

  • Salvioli A, Zouari I, Chalot M, Bonfante P (2012) The arbuscular mycorrhizal status has an impact on the transcriptome profile and amino acid composition of tomato fruit. BMC Plant Biol 12:44

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Scagel C (2004) Inoculation with vesicular-arbuscular mycorrhizal fungi and rhizobacteria alters nutrient allocation and flowering of Harlequin flower. Horticult Technol 14:39–48

    Google Scholar 

  • Schwyn B, Neilands J (1987) Universal chemical assay for the detection and determination of siderophores. Anal Biochem 160:47–56

    Article  CAS  PubMed  Google Scholar 

  • Seeram N (2006) Berries. In: Heber D, Blackburn G, Go V (eds) Nutritional oncology. Academic, London, pp 615–628

    Chapter  Google Scholar 

  • Serrani JC, Fos M, Atarés A, García-Martínez JL (2007) Effect of gibberellin and auxin on parthenocarpic fruit growth induction in the cv Micro-Tom of tomato. J Plant Growth Regul 26:211–221

    Article  CAS  Google Scholar 

  • Sharma RR, Singh R (2009) Gibberellic acid influences the production of malformed and button berries, and fruit yield and quality in strawberry (Fragaria × ananassa Duch.). Sci Hortic 19:430–433

    Article  Google Scholar 

  • Shaul-Keinan O, Gadkar V, Ginzberg I, Grünzweig JM, Chet I, Elad Y, Wininger S, Belausov E, Eshed Y, Atzmon N, Ben-Tal Y, Kapulnik Y (2002) Hormone concentrations in tobacco roots change during arbuscular mycorrhizal colonization with Glomus intraradices. New Phytol 154:501–507

    Article  CAS  Google Scholar 

  • Smith S, Read D (2008) Mycorrhizal symbiosis, 3rd edn. Academic, London

    Google Scholar 

  • Sturm K, Koron D, Stampar F (2003) The composition of fruit of different strawberry varieties depending on maturity stage. Food Chem 83:417–422

    Article  CAS  Google Scholar 

  • Torelli A, Trotta A, Acerbi L, Arcidiacono G, Berta G, Branca C (2000) IAA and ZR content in leek (Allium porrum L.) as influenced by P nutrition and arbuscular mycorrhizae, in relation to plant development. Plant Soil 226:29–35

    Article  CAS  Google Scholar 

  • Vázquez-Hernández MV, Arévalo-Galarza L, Jaen-Contreras D, Escamilla-García JL, Mora-Aguilera A, Hernández-Castro E, Cibrián-Tovar J, Téliz-Ortiz D (2011) Effect of Glomus mosseae and Entrophospora colombiana on plant growth, production, and fruit quality of “Maradol” papaya (Carica papaya L.). Sci Hortic 128:255–260

    Article  Google Scholar 

  • Wang C, Li X, Zhou J, Wang G, Dong Y (2008) Effects of arbuscular mycorrhizal fungi on growth and yield of cucumber plants. Commun Soil Sci Plant 39:499–509

    Article  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S ribosomal DNA amplification for phylogenetic study. J Bacteriol 173:697–703

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yao Q, Zhu HH, Chen JZ (2005) Growth responses and endogenous IAA and iPAs changes of litchi (Litchi chinensis Sonn.) seedlings induced by arbuscular mycorrhizal fungal inoculation. Sci Hortic 105:145–151

    Article  CAS  Google Scholar 

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Acknowledgments

This research was funded by the Regione Piemonte, within the program POR-FESR 2007-2013 - Project title: “Realizzazione di un sistema integrato innovativo di tecnologie di campo, hardware e software per l’ottimizzazione della gestione parametrizzata di nutrizione e irrigazione delle piante, sinergizzato al supporto eco-orientato delle coltivazioni con materiali biodegradabili e/o a completa metabolizzazione da parte della rizosfera” (Bi.R.S-OASIS).

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  1. Dipartimento di Scienze e Innovazione Tecnologica—DISIT, Università del Piemonte Orientale “A. Avogadro”, Viale T. Michel 11, 15121, Alessandria (AL), Italy

    Elisa Bona, Guido Lingua, Paola Manassero, Simone Cantamessa, Francesco Marsano, Valeria Todeschini, Andrea Copetta, Nadia Massa, Lorena Avidano, Elisa Gamalero & Graziella Berta

  2. Mybasol s.r.l., Via Gentilini 3, 15121, Alessandria (AL), Italy

    Simone Cantamessa, Andrea Copetta, Giovanni D’Agostino, Elisa Gamalero & Graziella Berta

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  1. Elisa Bona
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Bona, E., Lingua, G., Manassero, P. et al. AM fungi and PGP pseudomonads increase flowering, fruit production, and vitamin content in strawberry grown at low nitrogen and phosphorus levels. Mycorrhiza 25, 181–193 (2015). https://doi.org/10.1007/s00572-014-0599-y

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