Abstract
Sixty-four native bacterial colonies were isolated from mycorrhizal roots of Helianthemum almeriense colonized by Terfezia claveryi, mycorrhizosphere soil, and peridium of T. claveryi to evaluate their effect on mycorrhizal plant production. Based on the phylogenetic analysis of the 16S rDNA partial sequence, 45 different strains from 17 genera were gathered. The largest genera were Pseudomonas (40.8 % of the isolated strains), Bacillus (12.2 % of isolated strains), and Varivorax (8.2 % of isolated strains). All the bacteria were characterized phenotypically and by their plant growth-promoting rhizobacteria (PGPR) traits (auxin and siderophore production, phosphate solubilization, and ACC deaminase activity). Only bacterial combinations with several PGPR traits or Pseudomonas sp. strain 5, which presents three different PGPR traits, had a positive effect on plant survival and growth. Particularly relevant were the bacterial treatments involving auxin release, which significantly increased the root-shoot ratio and mycorrhizal colonization. Moreover, Pseudomonas mandelii strain 29 was able to considerably increase mycorrhizal colonization but not plant growth, and could be considered as mycorrhiza-helper bacteria. Therefore, the mycorrhizal roots, mycorrhizosphere soil, and peridium of desert truffles are environments enriched in bacteria which may be used to increase the survival and mycorrhization in the desert truffle plant production system at a semi-industrial scale.
Similar content being viewed by others
References
Ahmad F, Ahmad I, Khan MS (2005) Indole acetic acid production by the indigenous isolates of Azotobacter and fluorescent Pseudomonas in the presence and absence of tryptophan. Turk J Biol 29:29–34
Antony-Babu S, Deveau A, Van Nostrand JD, Zhou J, Le Tacon F, Robin C, Frey-Klett P, Uroz S (2014) Black truffle-associated bacterial communities during the development and maturation of Tuber melanosporum ascocarps and putative functional roles. Environ Microbiol 16:2831–2847. doi:10.1111/1462-2920.12294
Asghar H, Zahir Z, Arshad M, Khaliq A (2002) Relationship between in vitro production of auxins by rhizobacteria and their growth-promoting activities in Brassica juncea L. Biol Fertil Soils 35:231–237. doi:10.1007/s00374-002-0462-8
Barbieri E, Bertini L, Rossi I, Ceccaroli P, Saltarelli R, Guidi C, Zambonelli A, Stocchi V (2005) New evidence for bacterial diversity in the ascoma of the ectomycorrhizal fungus Tuber borchii Vittad. FEMS Microbiol Lett 247:23–35. doi:10.1016/j.femsle.2005.04.027
Barbieri E, Guidi C, Bertaux J, Frey-Klett P, Garbaye J, Ceccaroli P, Saltarelli R, Zambonelli A, Stocchi V (2007) Occurrence and diversity of bacterial communities in Tuber magnatum during truffle maturation. Environ Microbiol 9:2234–2246. doi:10.1111/j.1462-2920.2007.01338.x
Beneduzi A, Ambrosini A, Passaglia LM (2012) Plant growth-promoting rhizobacteria (PGPR): their potential as antagonists and biocontrol agents. Genet Mol Biol 35:1044–1051. doi:10.1590/S1415-47572012000600020
Bhattacharyya P, Jha D (2012) Plant growth-promoting rhizobacteria (PGPR): emergence in agriculture. World J Microb Biot 28:1327–1350. doi:10.1007/s11274-011-0979-9
Boddey RM, Dobereiner J (1995) Nitrogen fixation associated with grasses and cereals: recent progress and perspectives for the future. Fert Res 42:241–250. doi:10.1007/BF00750518
Couillerot O, Prigent-Combaret C, Caballero-Mellado J, Moënne-Loccoz Y (2009) Pseudomonas fluorescens and closely-related fluorescent pseudomonads as biocontrol agents of soil-borne phytopathogens. Lett Appl Microbiol 48:505–512. doi:10.1111/j.1472-765X.2009.02566.x
Dib-Bellahouel S, Fortas Z (2014) Activity of the desert truffle Terfezia boudieri Chatin, against associated soil microflora. Afr J Microbiol Res 8:3008–3016. doi:10.5897/AJMR2014.6881
Dominguez JA, Martin A, Anriquez A, Albanesi A (2012) The combined effects of Pseudomonas fluorescens and Tuber melanosporum on the quality of Pinus halepensis seedlings. Mycorrhiza 22:429–436. doi:10.1007/s00572-011-0420-0
Frankenberger W Jr, Arshad M (1995) Phytohormones in soils: microbial production and function. Marcel Dekker Inc., New York
Glick BR (1995) The enhancement of plant growth by free-living bacteria. Can J Microbiol 41:109–117. doi:10.1139/m95-015
Glick B, Jacobson C, Schwarze M, Pasternak J (1994) I-Aminocyclopropane-1-carboxylate deaminase mutants of plant growth promoting rhizobacterium Pseudomonas putida GR12–2 do not stimulate canola root elongation. Can J Microbiol 40:911–915. doi:10.1139/m94-146
Gordon SA, Weber RP (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192–195. doi:10.1104/pp.26.1.192
Goudjal Y, Zamoum M, Meklat A, Sabaou N, Mathieu F, Zitouni A (2016) Plant-growth-promoting potential of endosymbiotic actinobacteria isolated from sand truffles (Terfezia leonis Tul.) of the Algerian Sahara. Ann Microbiol 66:91–100. doi:10.1007/s13213-015-1085-2
Gryndler M, Soukupová L, Hršelová H, Gryndlerová H, Borovička J, Streiblová E, Jansa J (2013) A quest for indigenous truffle helper prokaryotes. Environ Microbiol Rep 5:346–352. doi:10.1111/1758-2229.12014
Gutiérrez A, Morte A, Honrubia M (2003) Morphological characterization of the mycorrhiza formed by Helianthemum almeriense Pau with Terfezia claveryi Chatin and Picoa lefebvrei (Pat.) Maire. Mycorrhiza 13:299–307. doi:10.1007/s00572-003-0236-7
Haas D, Defago G (2005) Biological control of soil-borne pathogens by fluorescent pseudomonads. Nat Rev Micro 3:307–319
Holt J, Krieg N, Sneath P, Staley J (1994) Bergey’s manual of determinative bacteriology, 9th edn. Williams and Wilkins, Baltimore
Jones D, Darrah P (1994) Role of root derived organic acids in the mobilization of nutrients from the rhizosphere. Plant Soil 166:247–257. doi:10.1007/bf00008338
Kamei AKD, Apou Kamei A (2014) Role of hydrogen cyanide secondary metabolite of plant growth promoting rhizobacteria as biopesticides of weeds. Global J Sci Front Res 14:109–112
Karnwal A (2009) Production of indole acetic acid by fluorescent Pseudomonas in the presence of L-tryptophan and rice root exudates. J Plant Pathol 91:61–63
Kiely PD, Haynes JM, Higgins CH, Franks A, Mark GL, Morrissey JP, O’Gara F (2006) Exploiting new systems-based strategies to elucidate plant-bacterial interactions in the rhizosphere. Microbial Ecol 51:257–266. doi:10.1007/s00248-006-9019-y
Kloepper JW, Leong J, Teintze M, Schroth MN (1980) Pseudomonas siderophores: a mechanism explaining disease-suppressive soils. Curr Microbiol 4:317–320. doi:10.1007/BF02602840
Leveau JH, Lindow SE (2005) Utilization of the plant hormone indole-3-acetic acid for growth by Pseudomonas putida strain 1290. Appl Environ Microb 71:2365–2371. doi:10.1128/AEM.71.5.2365-2371.2005
Mehta S, Nautiyal CS (2001) An efficient method for qualitative screening of phosphate-solubilizing bacteria. Curr Microbiol 43:51–56. doi:10.1007/s002840010259
Mordukhova E, Skvortsova N, Kochetkov V, Dubeikovskii A, Boronin A (1991) Synthesis of the phytohormone indole-3-acetic acid by rhizosphere bacteria of the genus Pseudomonas. Microbiology 60:345–349
Morte A, Andrino A (2014) Domestication: preparation of mycorrhizal seedlings. In: Kagan-Zur V, Roth-Bejerano N, Sitrit Y, Morte A (eds) Desert truffles, vol 38, Soil biology. Springer, Berlin Heidelberg, pp 343–365. doi:10.1007/978-3-642-40096-4_21
Morte A, Honrubia M (1995) Improvement of mycorrhizal synthesis between micropropagated Helianthemum almeriense plantlets with Terfezia claveryi (desert truffle). In: Elliott T (ed) Science and cultivation of edible fungi, vol 2., pp 863–868
Morte A, Cano A, Honrubia M, Torres P (1994) In vitro mycorrhization of micropropagated Helianthemum almeriense plantlets with Terfezia claveryi (desert truffle). Agr Sci Finland 3:309–314
Morte A, Lovisolo C, Schubert A (2000) Effect of drought stress on growth and water relations of the mycorrhizal association Helianthemum almeriense - Terfezia claveryi. Mycorrhiza 10:115–119. doi:10.1007/s005720000066
Morte A, Honrubia M, Gutiérrez A (2008) Biotechnology and cultivation of desert truffles. In: Varma A (ed) Mycorrhiza. Springer, Berlin Heidelberg, pp 467–483. doi:10.1007/978-3-540-78826-3_23
Morte A, Zamora M, Gutiérrez A, Honrubia M (2009) Desert truffle cultivation in semiarid Mediterranean areas. In: Azcón-Aguilar C, Barea JM, Gianinazzi S, Gianinazzi-Pearson V (eds) Mycorrhizas—functional processes and ecological impact. Springer, Berlin Heidelberg, pp 221–233. doi:10.1007/978-3-540-87978-7_15
Morte A, Navarro-Ródenas A, Nicolás E (2010) Physiological parameters of desert truffle mycorrhizal Helianthemun almeriense plants cultivated in orchards under water deficit conditions. Symbiosis 52:133–139. doi:10.1007/s13199-010-0080-4
Morte A, Andrino A, Honrubia M, Navarro-Ródenas A (2012) Terfezia cultivation in arid and semiarid soils. In: Zambonelli A, Bonito GM (eds) Edible ectomycorrhizal mushrooms, vol 34, Soil biology. Springer, Berlin Heidelberg, pp 241–263. doi:10.1007/978-3-642-33823-6_14
Murphy J, Riley JP (1962) A modified single solution method for the determination of phosphate in natural waters. Anal Chim Acta 27:31–36. doi:10.1016/S0003-2670(00)88444-5
Nautiyal CS (1999) An efficient microbiological growth medium for screening phosphate solubilizing microorganisms. FEMS Microbiol Lett 170:265–270. doi:10.1111/j.1574-6968.1999.tb13383.x
Palleroni NJ (2008) The road to the taxonomy of Pseudomonas. In: Cornellis P (ed) Pseudomonas: Genomics and molecular biology, Hethersett, UK, Caister Acad Press, pp 1--18
Penrose DM, Glick BR (2003) Methods for isolating and characterizing ACC deaminase‐containing plant growth‐promoting rhizobacteria. Physiol Plantarum 118:10–15. doi:10.1034/j.1399-3054.2003.00086.x
Pérez-García F, González-Benito ME (2006) Seed germination of five Helianthemum species: effect of temperature and presowing treatments. J Arid Environ 65:688–693. doi:10.1016/j.jaridenv.2005.10.008
Picard C, Bosco M (2005) Maize heterosis affects the structure and dynamics of indigenous rhizospheric auxins-producing Pseudomonas populations. FEMS Microbiol Ecol 53:349–357. doi:10.1016/j.femsec.2005.01.007
Prasad R, Kumar M, Varma A (2015) Role of PGPR in soil fertility and plant health. In: Plant-growth-promoting rhizobacteria (PGPR) and medicinal plants. Springer, pp 247–260. doi: 10.1007/978-3-319-13401-7_12
Radzki W, Gutiérrez Manero FJ, Algar E, Lucas Garcia JA, García-Villaraco A, Ramos Solano B (2013) Bacterial siderophores efficiently provide iron to iron-starved tomato plants in hydroponics culture. Anton Leeuw Int J G 104:321–330. doi:10.1007/s10482-013-9954-9
Roth-Bejerano N, Navarro-Ródenas A, Gutiérrez A (2014) Types of mycorrhizal association. In: Kagan-Zur V, Roth-Bejerano N, Sitrit Y, Morte A (eds) Desert truffles, vol 38, Soil biology. Springer, Berlin Heidelberg, pp 69–80. doi:10.1007/978-3-642-40096-4_5
Rougieux R (1963) Actions antibiotiques et stimulantes de la truffe du Desert (Terfezia boudieri Chatin). In: Annales de l Institut Pasteur. Masson Editeur 120 BLVD Saint-Germain, Paris, p 315
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A 74:5463–5467. doi:10.1073/pnas.74.12.5463
Sbrana C, Agnolucci M, Bedini S, Lepera A, Toffanin A, Giovannetti M, Nuti MP (2002) Diversity of culturable bacterial populations associated to Tuber borchii ectomycorrhizas and their activity on T. borchii mycelial growth. FEMS Microbiol Lett 211:195–201. doi:10.1111/j.1574-6968.2002.tb11224.x
Sugiyama A, Bakker MG, Badri DV, Manter DK, Vivanco JM (2012) Relationships between Arabidopsis genotype-specific biomass accumulation and associated soil microbial communities. Botany 91:123–126. doi:10.1139/cjb-2012-0217
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599. doi:10.1093/molbev/msm092
Turgeman T, Lubinsky O, Roth-Bejerano N, Kagan-Zur V, Kapulnik Y, Koltai H, Zaady E, Ben-Shabat S, Guy O, Lewinsohn E, Sitrit Y (2016) The role of pre-symbiotic auxin signaling in ectendomycorrhiza formation between the desert truffle Terfezia boudieri and Helianthemum sessiliflorum. Mycorrhiza 26:287–297. doi:10.1007/s00572-015-0667-y
Van der Hofstad G, Marugg JD, Verjans G, Weisbeek P (1986) Characterization and structural analysis of the siderophore produced by the PGPR Pseudomonas putida strain WCS358. In: iron, siderophores, and plant diseases. Springer, pp 71–75. doi: 10.1007/978-1-4615-9480-2_9
Acknowledgments
This work was supported by project CGL2011-29816 (MINECO-FEDER, Spain) and project 19484/PI/14 (FEDER-Programa de Apoyo a la Investigación de la Fundación Séneca-Agencia de Ciencia y Tecnología de la Región de Murcia, Spain). A. Navarro-Ródenas is grateful to MINECO for a postdoctoral Torres-Quevedo contract PTQ-12-05818. The authors thank JJ Bordallo for his help with DNA sequence identification and Dr. J. Zwiazek for his helpful comments on the manuscript.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
ESM 1
Supplementary Table 1. Phenotypic characteristics of the isolated bacterial strains. (DOCX 22 kb)
Rights and permissions
About this article
Cite this article
Navarro-Ródenas, A., Berná, L.M., Lozano-Carrillo, C. et al. Beneficial native bacteria improve survival and mycorrhization of desert truffle mycorrhizal plants in nursery conditions. Mycorrhiza 26, 769–779 (2016). https://doi.org/10.1007/s00572-016-0711-6
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00572-016-0711-6