Skip to main content
SpringerLink
Log in

Maize development and grain quality are differentially affected by mycorrhizal fungi and a growth-promoting pseudomonad in the field

  • Original Paper
  • Published:
Mycorrhiza Aims and scope Submit manuscript

Abstract

Arbuscular mycorrhizal (AM) fungi and plant growth-promoting bacteria (PGPB) can increase the growth and yield of major crops, and improve the quality of fruits and leaves. However, little is known about their impact on seed composition. Plants were inoculated with AM fungi and/or the bacterial strain Pseudomonas fluorescens Pf4 and harvested after 7 months of growth in open-field conditions. Plant growth parameters were measured (biomass, length and circumference of spikes, number of grains per cob, grain yield, and grain size) and protein, lipid, and starch content in grains were determined. Plant growth and yield were increased by inoculation with the microorganisms. Moreover, spikes and grains of inoculated plants were bigger than those produced by uninoculated plants. Regarding grain composition, the bacterial strain increased grain starch content, especially the digestible components, whereas AM fungi-enhanced protein, especially zein, content. Plant inoculation with the fluorescent pseudomonad and mycorrhizal fungi resulted in additive effects on grain composition. Overall, results showed that the bacterial strain and the AM fungi promoted maize growth cultivated in field conditions and differentially affected the grain nutritional content. Consequently, targeted plant inoculation with beneficial microorganisms can lead to commodities fulfilling consumer and industrial requirements.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

References

  • Akbari P, Ghalavand A, Modarres SA, Alikhani MA (2011) The effect of biofertilizers, nitrogen fertilizer and farmyard manure on grain yield and seed quality of sunflower (Helianthus annuus L.). J Agric Tech 7:173–184

    Google Scholar 

  • Akca Y, Sezai E (2010) Effect of plant growth promoting rhizobacteria (PGPR) inoculation on fruit quality in sweet cherry (Prunus avium L.) cv. 0900 Ziraat. J Food Agric Environ 8:769–771

    Google Scholar 

  • Alef K, Nannipieri P (1995) Methods in applied soil microbiology and biochemistry. Academic, London, pp 336–367

    Google Scholar 

  • Alkan N, Gadkar V, Yarden O, ad Kapulnik Y (2006) Analysis of quantitative interactions between two species of arbuscular mycorrhizal fungi, Glomus mosseae and G. intraradices, by real-time PCR. Appl Environ Microbiol 72:4192–4199

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Allison VJ (2002) Nutrients, arbuscular mycorrhizas and competition interact to influence seed production and germination success in Achillea millefolium. Funct Ecol 16:742–749

    Article  Google Scholar 

  • Aloui A, Recorbet G, Robert F, Schoefs B, Bertrand M, Henry C, Gianinazzi-Pearson V, Dumas-Gaudot E, Aschi-Smiti S (2011) AM symbiosis elicits shoot proteome changes that are modified during cadmium stress alleviation in Medicago truncatula. BMC Plant Biol 11:75–93

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Augé RM (2001) Water relations, drought and vesicular-arbuscular AM symbiosis. Mycorrhiza 11:3–42

    Article  Google Scholar 

  • Balakrishan N, Subramanian KS (2013) Mycorrhizal symbiosis and bioavailability of micronutrients in maize grain. Maydica 57:129–138

    Google Scholar 

  • Barea JM, Azcon-Aguilar C (1982) Production of plant growth-regulating substances by the VAM fungus Glomus mosseae. Appl Environ Microbiol 43:810–813

    CAS  PubMed Central  PubMed  Google Scholar 

  • Berta G, Sampò S, Gamalero E, Massa N, Lemanceau P (2005) Suppression of Rhizoctonia root-rot of tomato by Glomus mosseae BEG12 and Pseudomonas fluorescens A6RI is associated with their effect on the pathogen growth and on root morphogenesis. Eur J Plant Pathol 111:279–288

    Article  Google Scholar 

  • Boldt K, Pors Y, Haupt B, Bitterlich M, Kuhn 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 10:3811–3824

    Article  CAS  PubMed  Google Scholar 

  • Bonfante P, Requena N (2011) Dating in the dark: how roots respond to fungal signals to establish arbuscular mycorrhizal symbiosis. Curr Opin Plant Biol 14:451–457

    Article  CAS  PubMed  Google Scholar 

  • Bradford MA (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 76:248–254

    Article  Google Scholar 

  • 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 

  • Daei G, Ardekani MR, Rejali F, Teimuri S, Mirasari M (2009) Alleviation of salinity stress on wheat yield, yield components, and nutrient uptake using arbuscular mycorrhizal fungi under field conditions. J Plant Physiol 166:617–625

    Article  CAS  PubMed  Google Scholar 

  • Daft MJ, Hogarth BG (1983) Competitive interactions of four species of Glomus on maize and onion. Trans Br Mycol Soc 80:339–345

    Article  Google Scholar 

  • Dutta S, Podile AR (2010) Plant growth-promoting rhizobacteria (PGPR): the bugs to debug the root zone. Crit Rev Microbiol 36:232–244

    Article  PubMed  Google Scholar 

  • 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.). Agric Ecosyst Environ 59:63–68

    Article  Google Scholar 

  • Eivazi F, Tabatabai MA (1977) Phosphatases in soils. Soil Biol Biochem 9:167–172

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Forni C, Riov J, Grilli-Caiola M, Tel-Or E (1992) Indole-3-acetic acid (IAA) production by Arthrobacter species isolated from Azolla. J Gen Microbiol 138:377–381

    Article  CAS  PubMed  Google Scholar 

  • Frey-Klett P, Garbaye J, Tarkka M (2007) The mycorrhiza helper bacteria revisited. New Phytol 176:22–36

    Article  CAS  PubMed  Google Scholar 

  • Gamalero E, Fracchia L, Cavaletto M, Garbaye J, Frey-Klett P, Varese GC, Martinotti MG (2003) Characterization of functional traits of two fluorescent pseudomonads isolated from basidiomes of ectomycorrhizal fungi. Soil Biol Biochem 35:55–65

    Article  CAS  Google Scholar 

  • Gamalero E, Trotta A, Massa N, Copetta A, Martinotti MG, Berta G (2004) Impact of two fluorescent pseudomonads and an arbuscular mycorrhizal fungus on tomato plant growth, root architecture and P acquisition. Mycorrhiza 14:185–192

    Article  PubMed  Google Scholar 

  • Gamalero E, Lingua G, Tombolini R, Avidano L, Pivato B, Berta G (2005) Colonization of tomato root seedling by Pseudomonas fluorescens 92rkG5: spatio-temporal dynamics, localization, organization, viability and culturability. Micr Ecol 50:289–297

    Article  Google Scholar 

  • Gamalero E, Berta G, Massa N, Glick BR, Lingua G (2008) Synergistic interactions between the ACC deaminase-producing bacterium Pseudomonas putida UW4 and AM fungus Gigaspora rosea positively affect cucumber plant growth. FEMS Microbiol Ecol 64:459–467

    Article  CAS  PubMed  Google Scholar 

  • Gamalero E, Berta G, Massa N, Glick BR, Lingua G (2010) Interactions between Pseudomonas putida UW4 and Gigaspora rosea BEG9 and their consequences on the growth of cucumber under salt stress conditions. J Appl Microbiol 108:236–245

    Article  CAS  PubMed  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Giovannetti M, Avio L, Barale R, Ceccarelli N, Cristofani R, Iezzi A, Mignolli F, Picciarelli P, Pinto B, Reali D, Sbrana C, Scarpato R (2012) Nutraceutical value and safety of tomato fruits produced by AM plants. Br J Nutr 107:242–251

    Article  CAS  PubMed  Google Scholar 

  • Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117

    Article  CAS  Google Scholar 

  • Glick BR, Cheng Z, Czarny J, Duan J (2007) Promotion of plant growth by ACC deaminase-containing soil bacteria. Eur J Plant Pathol 119:329–339

    Article  CAS  Google Scholar 

  • Goffman FD, Bohme T (2001) Relationship between fatty acid profile and vitamin E content in maize hybrids (Zea mays L.). J Agric Food Chem 49:4990–4994

    Article  CAS  PubMed  Google Scholar 

  • Gustafson DJ, Casper BB (2006) Differential host plant performance as a function of soil arbuscular mycorrhizal fungal communities: experimentally manipulating co-occurring Glomus species. Plant Ecol 183:257–263

    Article  Google Scholar 

  • Helber N, Wippel K, Sauer N, Schaarschmidt S, Hause B, Requena N (2011) A versatile monosaccharide transporter that operates in the arbuscular mycorrhizal fungus Glomus sp. is crucial for the symbiotic relationship with plants. Plant Cell 23:3812–3823

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Heppell KB, Shumway DL, Koide RT (1998) The effect of AM infection of Abutilon theophrasti on competitiveness of offspring. Funct Ecol 12:171–175

    Article  Google Scholar 

  • Jansa J, Smith FA, Smith SE (2008) Are there benefits of simultaneous root colonization by different arbuscular mycorrhizal fungi? New Phytol 177:779–789

    Article  CAS  PubMed  Google Scholar 

  • Javed M, Arshad M, Ali K (1998) Evaluation of rhizobacteria for their growth promoting activity in maize. Pak J Soil Sci 14:36–42

    Google Scholar 

  • Kloepper JW, Lifshitz R, Zablotowitz RM (1989) Free living bacteria inocula for enhancing crop productivity. Trends Biotechnol 7:39–43

    Article  Google Scholar 

  • Koide RT (2000) Functional complementarity in the arbuscular mycorrhizal symbiosis. New Phytol 147:233–235

    Article  Google Scholar 

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

    Google Scholar 

  • Koide RT, Lu X (1995) On the cause of offspring superiority conferred by AM infection of Abutilon theophrasti. New Phytol 131:435–441

    Article  Google Scholar 

  • Kumar P, Yadava RK, Gollen B, Kumar S, Verma RK, Yadav S (2011) Nutritional content and medicinal properties of wheat: a review. Life Sci Med Res 22:1–10

    Google Scholar 

  • Lawton JW (2002) Zein: a history of processing and use. Cereal Chem 79:1–18

    Article  CAS  Google Scholar 

  • Lewis JD, Koide RT (1990) Phosphorus supply, AM infection and plant offspring vigor. Funct Ecol 4:695–702

    Article  Google Scholar 

  • Lingua G, D'Agostino G, Massa N, Antosiano M, Berta G (2002) Mycorrhiza-induced differential response to a yellows disease in tomato. Mycorrhiza 12:191–198

    Article  PubMed  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 leaf proteome of selected poplar clone: a time course analysis. PLoS ONE 7:1–25

    Article  Google Scholar 

  • Lingua G, Bona E, Manassero P, Marsano F, Todeschini V, Cantamesssa 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  CAS  PubMed Central  PubMed  Google Scholar 

  • Lu X, Koide RT (1991) Avena fatua L. seed and seedling nutrient dynamics as influenced by AM infection of the maternal generation. Plant. Cell Environ 14:931–939

    Article  CAS  Google Scholar 

  • Ludwig-Muller J (2010) Hormonal responses in host plants triggered by arbuscular mycorrhizal fungi. In: Koltai H, and Kapulnik Y (eds.) Arbuscular mycorrhizas: physiology and function. Springer, Berlin, pp. 169–190

  • Mena-Violante HG, Ocampo-Jimenez O, Dendooven L, Martinez-Soto G, Gonzalez-Castafieda J, Davies FT Jr, Olalde-Portugal V (2006) Arbuscular mycorrhizal fungi enhance fruit growth and quality of chile ancho (Capsicum annuum L. cv San Luis) plants exposed to drought. Mycorrhiza 16:261–267

    Article  PubMed  Google Scholar 

  • Momany FA, Sessa DJ, Lawton JW, Selling GW, Hamaker SAH, Willett JL (2006) Structural characterization of alpha-zein. J Agric Food Chem 54:543–547

    Article  CAS  PubMed  Google Scholar 

  • Nautiyal CS, Govindarajan R, Lavania M, Pushpangadan P (2008) Novel mechanism of modulating natural antioxidants in functional foods: involvement of plant growth-promoting rhizobacteria NRRL B-30488. J Agric Food Chem 56:4474–4481

    Article  CAS  PubMed  Google Scholar 

  • Nosheen A, Bano A, Ullah F (2011) Nutritive value of canola (Brassica napus L.) as affected by plant growth-promoting rhizobacteria. Eur J Lipid Sci Technol 113:1342–1346

    Article  CAS  Google Scholar 

  • Nzanza B, Marais D, Soundy P (2012) Effect of arbuscular mycorrhizal fungal inoculation and biochar amendment on growth and yield of tomato. Int J Agric Biol 14:965–969

    CAS  Google Scholar 

  • Ordookhani K, Khavazi K, Moezzi A, Rejali F (2010) Influence of PGPR and AMF on antioxidant activity, lycopene and potassium contents in tomato. Afr J Agricul Res 5:1108–1116

    Google Scholar 

  • Pastorello EA, Farioli L, Pravettoni V, Scibilia J, Conti A, Fortunato D, Borgonovo L, Bonomi S, Primavesi L, Ballmer-Weber B (2009) Maize food allergy: lipid-transfer proteins, endochitinases, and alpha-zein precursor are relevant maize allergens in double-blind placebo-controlled maize-challenge-positive patients. Anal Bioanal Chem 395:93–102

    Article  CAS  PubMed  Google Scholar 

  • Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase-containing plant growth-promoting rhizobacteria. Physiol Plant 118:10–15

    Article  CAS  PubMed  Google Scholar 

  • Poulton JL, Bryla D, Koide RT, Stephenson AG (2002) AM 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 

  • Salkowski E (1885) Ueber das Verhalten der Skatolcarbonsa ̈ure im Organismus. Z Physiol Chem 9:23–33

    Google Scholar 

  • Sampò S, Massa N, Cantamessa S, D'Agostino U, Bosco D, Marzachì C, Berta G (2012) Effects of two AM fungi on phytoplasma infection in the model plant Chrysanthemum carinatum. Agric Food Sci 21:39–51

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Smith SE, Read DJ (2008) Mycorrhizal symbiosis, 3rd edn. Academic, New York

    Google Scholar 

  • 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 62:227–250

    Article  CAS  PubMed  Google Scholar 

  • Song F, Kong X, Dong A, Liu X (2012) Impact of arbuscular mycorrhizal fungi on the growth and related physiological indexes of Amorpha fruticosa. J Med Plants Res 6:3648–3655

    CAS  Google Scholar 

  • Subramanian KS, Charest C, Dwyer LM, Hamilton RI (1997) Effects of arbuscular-mycorrhizas on leaf water potential, sugar and P contents during drought and recovery of maize. Can J Bot 75:1582–1591

    Article  CAS  Google Scholar 

  • Subramanian K, Bharathi C, Jegan A (2008) Response of maize to AM colonization at varying levels of zinc and phosphorus. Biol Fertil Soils 45:133–144

    Article  CAS  Google Scholar 

  • Subramanian KS, Balakrishnan N, Senthil N (2013) Mycorrhizal symbiosis to increase the grain micronutrient content in maize. Austral J Crop Sci 7:900–910

    CAS  Google Scholar 

  • Thiel J, Weier D, Sreenivasulu N, Strickert M, Weichert N, Melzer M, Czauderna T, Wobus U, Weber H, Weschke W (2008) Different hormonal regulation of cellular differentiation and function in nucellar projection and endosperm transfer cells: a microdissection-based transcriptome study of young barley grains. Plant Physiol 148:1436–1452

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tian H, Drijber RA, Zhang JL, Li XL (2013) Impact of long-term nitrogen fertilization and rotation with soybean on the diversity and phosphorus metabolism of indigenous arbuscular mycorrhizal fungi within the roots of maize (Zea mays L.). Agric Ecosys Environ 164:53–61

    Article  CAS  Google Scholar 

  • Trouvelot A, Kough JL, Gianinazzi-Pearson V (1986) Mesure du taux de mycorrhization VA d'un syst_me radiculaire. Recherche de méthodes d'estimation ayant une signification fonctionnelle. In: Gianinazzi-Pearson V, Gianinazzi S (eds) Physiological and genetical aspects of mycorrhizae. INRA, Paris, pp 217–221

    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 Hort 128:255–260

    Article  Google Scholar 

  • Venkateswarlu B, Srinivasa Rao C, Ramesh G, Venkateswarlu S, Katyal JC (2007) Effect of long-term incorporation of legume biomass on soil organic carbon, microbial biomass, nutrient build-up and grain yields of sorghum/sunflower under rainfed conditions. Soil Use Manag 23:100–107

    Article  Google Scholar 

  • Veresoglou SD, Rillig MC (2012) Suppression of fungal and nematode plant pathogens through arbuscular mycorrhizal fungi. Biol Lett 8:214–217

    Article  PubMed Central  PubMed  Google Scholar 

  • Volante A, Lingua G, Cesaro P, Cresta A, Puppo M, Ariati L, Berta G (2005) Influence of three species of arbuscular mycorrhizal fungi on the persistence of aromatic hydrocarbons in contaminated substrates. Mycorrhiza 16:43–50

    Article  CAS  PubMed  Google Scholar 

  • Weisburg WG, Barns SM, Pelletier DA, Lane DJ (1991) 16S Ribosomal DNA amplification for phylogenetic study. J Bacteriol 173(2):697–703

    Google Scholar 

  • Zahir ZA, Akram M, Arshad M, Khalid A (1998) Improving maize yield by inoculation with plant growth promoting rhizobacteria. Pak J Soil Sci 15:7–11

    Google Scholar 

Download references

Acknowledgments

The auuthors are grateful to Shimaila Rashid who performed the ACC deaminase assay and to Giorgio Lucchini for performing ICP_MS analysis. The authors also thank Mossi and Ghisolfi s.r.l. for partially funding the research.

Author information

Authors and Affiliations

  1. Dipartimento di Scienze ed Innovazione Tecnologica, Università del Piemonte Orientale Amedeo Avogadro, Viale Teresa Michel, 11, 15121, Alessandria, Italy

    Graziella Berta, Andrea Copetta, Elisa Gamalero, Elisa Bona & Patrizia Cesaro

  2. Dipartimento di Scienze per gli Alimenti, Università degli Studi di Milano, la Nutrizione e l’Ambiente Via Celoria, 2, 20133, Milano, Italy

    Alessio Scarafoni

  3. Mybasol s.r.l, via Gentilini 11, 15121, Alessandria, Italy

    Giovanni D’Agostino

Authors
  1. Graziella Berta
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Andrea Copetta
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Elisa Gamalero
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Elisa Bona
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Patrizia Cesaro
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Alessio Scarafoni
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Giovanni D’Agostino
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Graziella Berta.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Berta, G., Copetta, A., Gamalero, E. et al. Maize development and grain quality are differentially affected by mycorrhizal fungi and a growth-promoting pseudomonad in the field. Mycorrhiza 24, 161–170 (2014). https://doi.org/10.1007/s00572-013-0523-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00572-013-0523-x

Keywords

Search

Navigation