Skip to main content
SpringerLink
Log in

Survey of Plant Growth-Promoting Mechanisms in Native Portuguese Chickpea Mesorhizobium Isolates

  • Plant Microbe Interactions
  • Published:
Microbial Ecology Aims and scope Submit manuscript

Abstract

Rhizobia may possess other plant growth-promoting mechanisms besides nitrogen fixation. These mechanisms and the tolerance to different environmental factors, such as metals, may contribute to the use of rhizobia inocula to establish a successful legume-rhizobia symbiosis. Our goal was to characterize a collection of native Portuguese chickpea Mesorhizobium isolates in terms of plant growth-promoting (PGP) traits and tolerance to different metals as well as to investigate whether these characteristics are related to the biogeography of the isolates. The occurrence of six PGP mechanisms and tolerance to five metals were evaluated in 61 chickpea Mesorhizobium isolates previously obtained from distinct provinces in Portugal and assigned to different species clusters. Chickpea microsymbionts show high diversity in terms of PGP traits as well as in their ability to tolerate different metals. All isolates synthesized indoleacetic acid, 50 isolates produced siderophores, 19 isolates solubilized phosphate, 12 isolates displayed acid phosphatase activity, and 22 exhibited cytokinin activity. Most isolates tolerated Zn or Pb but not Ni, Co, or Cu. Several associations between specific PGP mechanisms and the province of origin and species clusters of the isolates were found. Our data suggests that the isolate’s tolerance to metals and ability to solubilize inorganic phosphate and to produce IAA may be responsible for the persistence and distribution of the native Portuguese chickpea Mesorhizobium species. Furthermore, this study revealed several chickpea microsymbionts with potential as PGP rhizobacteria as well as for utilization in phytoremediation strategies.

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

References

  1. Glick BR (2012) Plant growth-promoting bacteria: mechanisms and applications. Scientifica ID963401, 15 pages

  2. Zahran HH (2006) Nitrogen (N2) fixation in vegetable legumes: biotechnological perspectives. In: Ray RC, Ward OP (eds) Microbial biotechnology in horticulture, vol 1. Science, Enfield, pp 49–82

    Google Scholar 

  3. Esitken A, Ercisli S, Karlidag H et al (2005) Potential use of plant growth promoting rhizobacteria (PGPR) in organic apricot production. In: Libek A, Kaufmane E, Sasnauskas A (eds) Proceedings of the international scientific conference of environmentally friendly fruit growing, Polli, Estonia, pp. 90–97

  4. Chabot R, Antoun H, Cescas M (1996) Growth promotion of maize and lettuce by phosphate-solubilizing Rhizobium leguminosarum biovar phaseoli. Plant Soil 184:311–321. doi:10.1007/BF00010460

    Article  CAS  Google Scholar 

  5. Rodriguez H, Fraga R (1999) Phosphate solubilizing bacteria and their role in plant growth promotion. Biotechnol Adv 17:319–339. doi:10.1016/S0734-9750(99)00014-2

    Article  CAS  PubMed  Google Scholar 

  6. Rodriguez H, Fraga R, Gonzalez T et al (2006) Genetics of phosphate solubilization and its potential applications for improving plant growth-promoting bacteria. Plant Soil 287:15–21. doi:10.1007/s11104-006-9056-9

    Article  CAS  Google Scholar 

  7. Johnston AWB (2004) Mechanisms and regulation of iron uptake in the rhizobia. In: Crosa JH, Payne SM (eds) Iron transport in bacteria: molecular genetics, biochemistry, microbial pathogenesis and ecology. ASM Press, Washington, pp 469–488

    Chapter  Google Scholar 

  8. Avis TJ, Gravel V, Antoun H et al (2008) Multifaceted beneficial effects of rhizosphere microorganisms on plant health and productivity. Soil Biol Biochem 40:1733–1740. doi:10.1016/j.soilbio.2008.02.013

    Article  CAS  Google Scholar 

  9. Hayat R, Ali S, Amara U et al (2010) Soil beneficial bacteria and their role in plant growth promotion: a review. Ann Microbiol 60:579–598. doi:10.1007/s13213-010-0117-1

    Article  Google Scholar 

  10. Cooper JB, Long SR (1994) Morphogenetic rescue of Rhizobium meliloti nodulation mutants by trans-zeatin secretion. Plant Cell 6:215–225. doi:10.1105/tpc.6.2.215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Ma WB, Sebestianova SB, Sebestian J et al (2003) Prevalence of 1-aminocyclopropane-1-carboxylate deaminase in Rhizobium spp. Anton Leeuw Int J Gen Mol Microbiol 83:285–291. doi:10.1023/A:1023360919140

    Article  CAS  Google Scholar 

  12. Nascimento FX, Brígido C, Glick BR et al (2012) ACC deaminase genes are conserved among Mesorhizobium species able to nodulate the same host plant. FEMS Microbiol Lett 336:26–37. doi:10.1111/j.1574-6968.2012.02648.x

    Article  CAS  PubMed  Google Scholar 

  13. Yuhashi KI, Ichikawa N, Ezura H et al (2000) Rhizobitoxine production by Bradyrhizobium elkanii enhances nodulation and competitiveness on Macroptilium atropurpureum. Appl Environ Microbiol 66:2658–2663. doi:10.1128/AEM.66.6.2658-2663.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Boiero L, Perrig D, Masciarelli O et al (2007) Phytohormone production by three strains of Bradyrhizobium japonicum and possible physiological and technological implications. Appl Microbiol Biotechnol 74:874–880. doi:10.1007/s00253-006-0731-9

    Article  CAS  PubMed  Google Scholar 

  15. Ali B, Hayat S, Hasan SA, Ahmad A (2008) IAA and 4-Cl-IAA increases the growth and nitrogen fixation in mung bean. Commun Soil Sci Plant Anal 39:2695–2705. doi:10.1080/00103620802358839

    Article  CAS  Google Scholar 

  16. Camerini S, Senatore B, Lonardo E et al (2008) Introduction of a novel pathway for IAA biosynthesis to rhizobia alters vetch root nodule development. Arch Microbiol 190:67–77. doi:10.1007/s00203-008-0365-7

    Article  CAS  PubMed  Google Scholar 

  17. Bianco C, Defez R (2009) Medicago truncatula improves salt tolerance when nodulated by an indole-3-acetic acid-overproducing Sinorhizobium meliloti strain. J Exp Bot 60:3097–3107. doi:10.1093/jxb/erp140

    Article  CAS  PubMed  Google Scholar 

  18. Bianco C, Defez R (2010) Improvement of phosphate solubilization and Medicago plant yield by an indole-3-acetic acid-overproducing strain of Sinorhizobium meliloti. Appl Environ Microbiol 76:4626–4632. doi:10.1128/AEM.02756-09

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Podlesakova K, Fardoux J, Patrel et al (2013) Rhizobial synthesized cytokinins contribute to but are not essential for the symbiotic interaction between photosynthetic Bradyrhizobia and Aeschynomene legumes. Mol Plant Microbe Interact 26:1232–1238. doi:10.1094/MPMI-03-13-0076-R

    Article  CAS  PubMed  Google Scholar 

  20. Xu J, Li LX, Luo L (2012) Effects of engineered Sinorhizobium meliloti on cytokinin synthesis and tolerance of alfalfa to extreme drought stress. Appl Environ Microbiol 78:8056–8061. doi:10.1128/AEM.01276-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Ma WB, Guinel FC, Glick BR (2003) Rhizobium leguminosarum biovar viciae 1-aminocyclopropane-1-carboxylate deaminase promotes nodulation of pea plants. Appl Environ Microbiol 69:4396–4402. doi:10.1128/AEM.69.8.4396-4402.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Ma WB, Charles TC, Glick BR (2004) Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in Sinorhizobium meliloti increases its ability to nodulate alfalfa. Appl Environ Microbiol 70:5891–5897. doi:10.1128/AEM.70.10.5891-5897.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Nascimento F, Brígido C, Alho L et al (2012) Enhanced chickpea growth-promotion ability of a Mesorhizobium strain expressing an exogenous ACC deaminase gene. Plant Soil 353:221–230. doi:10.1007/s11104-011-1025-2

    Article  CAS  Google Scholar 

  24. Nascimento FX, Brígido C, Glick BR et al (2012) Mesorhizobium ciceri LMS-1 expressing an exogenous 1-aminocyclopropane-1-carboxylate (ACC) deaminase increases its nodulation abilities and chickpea plant resistance to soil constraints. Lett Appl Microbiol 55:15–21. doi:10.1111/j.1472-765X.2012.03251.x

    Article  CAS  PubMed  Google Scholar 

  25. Brígido C, Nascimento FX, Duan J et al (2013) Expression of an exogenous 1-aminocyclopropane-1-carboxylate deaminase gene in Mesorhizobium spp. reduces the negative effects of salt stress in chickpea. FEMS Microbiol Lett 349:46–53. doi:10.1111/1574-6968.12294

    PubMed  Google Scholar 

  26. Brígido C, Glick BR (2015) Phytoremediation using rhizobia. In: Ansari AA, Gill SS, Gill R, Lanza RG, Newman L (eds) Phytoremediation: management of environmental contaminants, vol 2. Springer, New York, pp 95–114

    Google Scholar 

  27. Zheng ZW, Fang W, Lee HY, Yang ZY (2005) Responses of Azorhizobium caulinodans to cadmium stress. FEMS Microbiol Ecol 54:455–461. doi:10.1016/j.femsec.2005.05.006

    Article  CAS  Google Scholar 

  28. Broos K, Uyttebroek M, Mertens J et al (2004) A survey of symbiotic nitrogen fixation by white clover grown on metal contaminated soils. Soil Biol Biochem 36:633–640. doi:10.1016/j.soilbio.2003.11.007

    Article  CAS  Google Scholar 

  29. Younis M (2007) Responses of Lablab purpureus-rhizobium symbiosis to heavy metals in pot and field experiments. World J Agric Sci 3:111–122, Accession # 25165156

    Google Scholar 

  30. Stephens JHG, Rask HM (2000) Inoculant production and formulation. Field Crop Res 65:249–258. doi:10.1016/S0378-4290(99)00090-8

    Article  Google Scholar 

  31. Alexandre A, Brígido C, Laranjo M, Rodrigues S, Oliveira S (2009) A survey of chickpea rhizobia diversity in Portugal reveals the predominance of species distinct from Mesorhizobium ciceri and Mesorhizobium mediterraneum. Microb Ecol 58:930–941. doi:10.1007/s00248-009-9536-6

    Article  PubMed  Google Scholar 

  32. Brígido C, Alexandre A, Oliveira S (2012) Transcriptional analysis of major chaperone genes in salt-tolerant and salt-sensitive mesorhizobia. Microbiol Res 167:623–629. doi:10.1016/j.micres.2012.01.006

    Article  PubMed  Google Scholar 

  33. Jarvis BDW, van Berkum P, Chen WX et al (1997) Transfer of Rhizobium loti, Rhizobium huakuii, Rhizobium ciceri, Rhizobium mediterraneum, and Rhizobium tianshanense to Mesorhizobium gen. nov. Int J Syst Bacteriol 47:895–898. doi:10.1099/00207713-47-3-895

    Article  Google Scholar 

  34. Alexandre A, Oliveira S (2011) Most heat-tolerant rhizobia show high induction of major chaperone genes upon stress. FEMS Microbiol Ecol 75:28–36. doi:10.1111/j.1574-6941.2010.00993.x

    Article  CAS  PubMed  Google Scholar 

  35. Brígido C, Alexandre A, Laranjo M, Oliveira S (2007) Moderately acidophilic mesorhizobia isolated from chickpea. Lett Appl Microbiol 44:168–174. doi:10.1111/j.1472-765X.2006.02061.x

    Article  PubMed  Google Scholar 

  36. Brígido C, Oliveira S (2013) Most acid-tolerant chickpea mesorhizobia show induction of major chaperone genes upon acid shock. Microb Ecol 65:145–153. doi:10.1007/s00248-012-0098-7

    Article  PubMed  Google Scholar 

  37. Schwyn R, Neilands J (1987) Universal chemical assay for detection and estimation of siderophores. Anal Biochem 160:47–56. doi:10.1016/0003-2697(87)90612-9

    Article  CAS  PubMed  Google Scholar 

  38. Alexander D, Zuberer D (1991) Use of chrome azurol-S-reagents to evaluate siderophore production by rhizosphere bacteria. Biol Fertil Soil 12:39–45. doi:10.1007/BF00369386

    Article  CAS  Google Scholar 

  39. Gupta R, Singal R, Skankar A et al (1994) A modified plate assay for screening phosphate solubilizing microorganisms. J Gen Appl Microbiol 40:255–260. doi:10.2323/jgam.40.255

    Article  CAS  Google Scholar 

  40. Glickmann E, Dessaux Y (1995) A critical examination of the specificity of the Salkowski reagent for indolic compounds produced by phytopathogenic bacteria. Appl Environ Microbiol 61:793–796

    CAS  PubMed  PubMed Central  Google Scholar 

  41. Patten CL, Glick BR (2002) The role of Pseudomonas putida indoleacetic acid in the development of the host plant system. Appl Environ Microbiol 68:3795–3801. doi:10.1128/AEM.68.8.3795-3801.2002

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. O’Gara F, Shanmugam KT (1976) Control of symbiotic nitrogen fixation in rhizobia regulation of NH4+ assimilation. Biochim Biophys Acta 451:342–352. doi:10.1016/0304-4165(76)90129-X

    Article  PubMed  Google Scholar 

  43. Gordon S, Weber R (1951) Colorimetric estimation of indoleacetic acid. Plant Physiol 26:192–195. doi:10.1104/pp.26.1.192

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. De Freitas J, Banerjee M, Germida J (1997) Phosphate-solubilizing rhizobacteria enhance the growth and yield but not phosphorus uptake of canola (Brassica napus L.). Biol Fertil Soil 24:358–364

    Article  Google Scholar 

  45. Oliveira C, Alves V, Marriel IE et al (2009) Phosphate solubilizing microorganisms isolated from rhizosphere of maize cultivated in an oxisol of the Brazilian Cerrado Biome. Soil Biol Biochem 41:1782–1787. doi:10.1016/j.soilbio.2008.01.012

    Article  CAS  Google Scholar 

  46. Charles TC, Newcomb W, Finan TM (1991) NDVF, a novel locus located on megaplasmid pRMESU47B (PEXO) of Rhizobium meliloti is required for normal nodule development. J Bacteriol 173:3981–3992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Hussain A, Hasnain S (2011) Interactions of bacterial cytokinins and IAA in the rhizosphere may alter phytostimulatory efficiency of rhizobacteria. World J Microbiol Biotechnol 27:2645–2654. doi:10.1007/s11274-011-0738-y

    Article  CAS  Google Scholar 

  48. Carson K, Meyer J, Dilworth M (2000) Hydroxamate siderophores of root nodule bacteria. Soil Biol Biochem 32:11–21. doi:10.1016/S0038-0717(99)00107-8

    Article  CAS  Google Scholar 

  49. Arora N, Kang S, Maheshwari D (2001) Isolation of siderophore-producing strains of Rhizobium meliloti and their biocontrol potential against Macrophomina phaseolina that causes charcoal rot of groundnut. Curr Sci 81:673–677

    Google Scholar 

  50. Vargas LK, Lisboa BB, Schlindwein G et al (2009) Occurrence of plant growth-promoting traits in clover-nodulating rhizobia strains isolated from different soils in Rio Grande do Sul state. Rev Bras Cienc Solo 33:1227–1235

    Article  Google Scholar 

  51. Alikhani HA, Saleh-Rastin N, Antoun H (2006) Phosphate solubilization activity of rhizobia native to Iranian soils. Plant Soil 287:35–41. doi:10.1007/s11104-006-9059-6

    Article  CAS  Google Scholar 

  52. Peix A, Rivas-Boyero AA, Mateos PF et al (2001) Growth promotion of chickpea and barley by a phosphate solubilizing strain of Mesorhizobium mediterraneum under growth chamber conditions. Soil Biol Biochem 33:103–110. doi:10.1016/S0038-0717(00)00120-6

    Article  CAS  Google Scholar 

  53. Ahmad F, Ahmad I, Khan MS (2008) Screening of free-living rhizospheric bacteria for their multiple plant growth promoting activities. Microbiol Res 163:173–181. doi:10.1016/j.micres.2006.04.001

    Article  CAS  PubMed  Google Scholar 

  54. Jida M, Assefa F (2011) Phenotypic and plant growth promoting characteristics of Rhizobium leguminosarum bv. viciae from lentil growing areas of Ethiopia. Afr J Microbiol Res 5:4133–4142

    Google Scholar 

  55. Oburger E, Jones D, Wenzel W (2011) Phosphorus saturation and pH differentially regulate the efficiency of organic acid anion-mediated P solubilization mechanisms in soil. Plant Soil 341:363–382. doi:10.1007/s11104-010-0650-5

    Article  CAS  Google Scholar 

  56. Neila A, Adnane B, Mustapha F et al (2014) Phaseolus vulgaris-rhizobia symbiosis increases the phosphorus uptake and symbiotic N2 fixation under insoluble phosphorus. J Plant Nutr 37:643–657. doi:10.1080/01904167.2013.872275

    Article  CAS  Google Scholar 

  57. Vassilev N, Vassileva M, Nikolaeva I (2006) Simultaneous P-solubilizing and biocontrol activity of microorganisms: potentials and future trends. App Microbiol Biotechnol 71:137–144. doi:10.1007/s00253-006-0380-z

    Article  CAS  Google Scholar 

  58. Caballero-Mellado J, Onofre-Lemus J, Estrada-de los Santos P, Martinez-Aguilar L (2007) The tomato rhizosphere, an environment rich in nitrogen-fixing Burkholderia species with capabilities of interest for agriculture and bioremediation. Appl Environ Microbiol 73:5308–5319. doi:10.1128/aem.00324-07

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Hamdali H, Bouizgarne B, Hafidi M et al (2008) Screening for rock phosphate solubilizing Actinomycetes from Moroccan phosphate mines. Appl Soil Ecol 38:12–19. doi:10.1016/j.apsoil.2007.08.007

    Article  Google Scholar 

  60. Hamdali H, Hafidi M, Virolle MJ, Ouhdouch Y (2008) Rock phosphate-solubilizing Actinomycetes: screening for plant growth-promoting activities. World J Microbiol Biotechnol 24:2565–2575. doi:10.1007/s11274-008-9817-0

    Article  CAS  Google Scholar 

  61. Viruel E, Lucca ME, Sineriz F (2011) Plant growth promotion traits of phosphobacteria isolated from Puna, Argentina. Arch Microbiol 193:489–496. doi:10.1007/s00203-011-0692-y

    Article  CAS  PubMed  Google Scholar 

  62. Sharma SB, Sayyed RZ, Trivedi MH, Gobi TA (2013) Phosphate solubilizing microbes: sustainable approach for managing phosphorus deficiency in agricultural soils. Springerplus 2. doi:10.1186/2193-1801-2-587

  63. Renella G, Landi L, Ascher J et al (2006) Phosphomonoesterase production and persistence and composition of bacterial communities during plant material decomposition in soils with different pH values. Soil Biol Biochem 38:795–802. doi:10.1016/j.soilbio.2005.07.005

    Article  CAS  Google Scholar 

  64. Tao G, Tian S, Cai M et al (2008) Phosphate solubilizing and mineralizing abilities of bacteria isolated from soils. Pedosphere 18:515–523. doi:10.1016/S1002-0160(08)60042-9

    Article  CAS  Google Scholar 

  65. Arkhipova T, Prinsen E, Veselov S et al (2003) Cytokinin producing bacteria enhances plant growth in drying soil. Plant Soil 292:305–315. doi:10.1007/s11104-007-9233-5

    Article  Google Scholar 

  66. Arkhipova T, Veselov S, Melentiev A et al (2005) Ability of bacterium Bacillus subtilis to produce cytokinins and to influence the growth and endogenous hormone content of lettuce plants. Plant Soil 272:201–209. doi:10.1007/s11104-004-5047-x

    Article  CAS  Google Scholar 

  67. Mehnaz S, Lazarovits G (2006) Inoculation effects of Pseudomonas putida, Gluconacetobacter azotocaptans, and Azospirillum lipoferum on corn plant growth under greenhouse conditions. Microb Ecol 51:326–335. doi:10.1007/s00248-006-9039-7

    Article  PubMed  Google Scholar 

  68. Caba J, Centeno M, Fernandez B et al (2000) Inoculation and nitrate alter phytohormone levels in soybean roots: differences between a super nodulating mutant and the wild type. Planta 211:98–104. doi:10.1007/s004250000265

    Article  CAS  PubMed  Google Scholar 

  69. Pii Y, Crimi M, Cremonese G et al (2007) Auxin and nitric oxide control indeterminate nodule formation. BMC Plant Biol 7:21. doi:10.1186/1471-2229-7-21

    Article  PubMed  PubMed Central  Google Scholar 

  70. Spaepen S, Vanderleyden J, Remans R (2007) Indole-3-acetic acid in microbial and microorganism-plant signaling. FEMS Microbiol Rev 31:425–448. doi:10.1111/j.1574-6976.2007.00072.x

    Article  CAS  PubMed  Google Scholar 

  71. Pavlova ZB, Lutova LA (2000) Nodulation as a model for studying differentiation in higher plants. Russ J Genet 36:975–988

    CAS  Google Scholar 

  72. Akimova GP, Sokolova MG (2012) Cytokinin content during early stages of legume-rhizobial symbiosis and effect of hypothermia. Russ J Plant Physiol 59:656–661. doi:10.1134/S1021443712030028

    Article  CAS  Google Scholar 

  73. Ona O, Smets I, Gysegom P et al (2003) The effect of pH on indole-3-acetic acid (IAA) biosynthesis of Azospirillum brasilense Sp7. Symbiosis 35:199–208

    CAS  Google Scholar 

  74. Ona O, Van Impe J, Prinsen E, Vanderleyden J (2005) Growth and indole-3-acetic acid biosynthesis of Azospirillum brasilense Sp245 is environmentally controlled. FEMS Microbiol Lett 246:125–132. doi:10.1016/j.femsle.2005.03.048

    Article  CAS  PubMed  Google Scholar 

  75. Brandl MT, Quinones B, Lindow SE (2001) Heterogeneous transcription of an indoleacetic acid biosynthetic gene in Erwinia herbicola on plant surfaces. Proc Natl Acad Sci U S A 98:3454–3459. doi:10.1073/pnas.061014498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Patten CL, Glick BR (2002) Regulation of indoleacetic acid production in Pseudomonas putida GR12-2 by tryptophan and the stationary-phase sigma factor RpoS. Can J Microbiol 48:635–642. doi:10.1139/W02-053

    Article  CAS  PubMed  Google Scholar 

  77. Nukui N, Minamisawa K, Ayabe S-I et al (2006) Expression of the 1-aminocyclopropane-1-carboxylic acid deaminase gene requires symbiotic nitrogen-fixing regulator gene nifA2 in Mesorhizobium loti MAFF303099. Appl Environ Microbiol 72:4964–4969. doi:10.1080/AEM.02745-05

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Pereira S, Lima A, Figueira E (2006) Screening possible mechanisms mediating cadmium resistance in Rhizobium leguminosarum bv. viciae isolated from contaminated Portuguese soils. Microb Ecol 52:176–186. doi:10.1007/s00248-006-9057-5

    Article  CAS  PubMed  Google Scholar 

  79. Nonnoi F, Chinnaswamy A, de la Torre VSG et al (2012) Metal tolerance of rhizobial strains isolated from nodules of herbaceous legumes (Medicago spp. and Trifolium spp.) growing in mercury-contaminated soils. Appl Soil Ecol 61:49–59. doi:10.1016/j.apsoil.2012.06.004

    Article  Google Scholar 

  80. Gray CW, McLaren RG, Roberts AHC, Condron LM (1998) Sorption and desorption of cadmium from some New Zealand soils: effect of pH and contact time. Aust J Soil Res 36:199–216. doi:10.1071/S97085

    Article  CAS  Google Scholar 

  81. Abou-Shanab RA, Ghozlan H, Ghanem K, Moawad H (2005) Behaviour of bacterial populations isolated from rhizosphere of Diplachne fusca dominant in industrial sites. World J Microbiol Biotechnol 21:1095–1101. doi:10.1007/s11274-004-0005-6

    Article  CAS  Google Scholar 

  82. Wani PA, Khan MS, Zaidi A (2008) Chromium-reducing and plant growth-promoting Mesorhizobium improves chickpea growth in chromium-amended soil. Biotechnol Lett 30:159–163. doi:10.1007/s10529-007-9515-2

    Article  CAS  PubMed  Google Scholar 

  83. Wani PA, Khan MS, Zaidi A (2008) Effect of metal-tolerant plant growth-promoting Rhizobium on the performance of pea grown in metal-amended soil. Arch Environ Contam Toxicol 55:33–42. doi:10.1007/s00244-007-9097-y

    Article  CAS  PubMed  Google Scholar 

  84. Lakzian A, Murphy P, Turner A et al (2002) Rhizobium leguminosarum bv. viciae populations in soils with increasing heavy metal contamination: abundance, plasmid profiles, diversity and metal tolerance. Soil Biol Biochem 34:519–529. doi:10.1016/S0038-0717(01)00210-3

    Article  CAS  Google Scholar 

  85. Wani PA, Khan MS (2013) Nickel detoxification and plant growth promotion by multi metal resistant plant growth promoting Rhizobium species RL9. Bull Environ Contam Toxicol 91:117–124. doi:10.1007/s00128-013-1002-y

    Article  CAS  PubMed  Google Scholar 

  86. Joseph B, Patra R, Lawrence R (2007) Characterization of plant growth promoting rhizobacteria associated with chickpea (Cicer arietinum L.). Int J Plant Prod 1:141–151

    Google Scholar 

  87. Rajkumar MA, Ae N, Prasad MN, Freitas H (2010) Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends Biotechnol 28:142–149. doi:10.1016/j.tibtech.2009.12.002

    Article  CAS  PubMed  Google Scholar 

  88. Glick BR (2010) Using soil bacteria to facilitate phytoremediation. Biotechnol Adv 28:367–374. doi:10.1016/j.biotechadv.2010.02.001

    Article  CAS  PubMed  Google Scholar 

  89. Glick BR, Stearns JC (2011) Making phytoremediation work better: maximizing a plant’s growth potential in the midst of adversity. Int J Phytoremediation 13:4–16. doi:10.1080/15226514.2011.568533

    Article  PubMed  Google Scholar 

  90. Hao X, Xie P, Johnstone L et al (2012) Genome sequence and mutational analysis of plant-growth-promoting bacterium Agrobacterium tumefaciens CCNWGS0286 isolated from a zinc-lead mine tailing. Appl Environ Microbiol 78:5384–5394. doi:10.1128/AEM.01200-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by FEDER Funds through the Operational Programme for Competitiveness Factors—COMPETE and National Funds through FCT-Foundation for Science and Technology under the Project UID/AGR/00115/2013 and Project no. FCOMP-01-0124-FEDER-028316 (PTDC/BIA-EVF/4158/2012), the European Union Seventh Framework Programme (FP7/2007-2013) under grant agreement no. 247669, and InAlentejo Project ALENT-07-0262-FEDER-001871. C. Brígido acknowledges a FCT fellowship (SFRH/BPD/94751/2013). B.R. Glick was supported by the Natural Science and Engineering Research Council of Canada.

Author information

Authors and Affiliations

  1. ICAAM—Instituto de Ciências Agrárias e Ambientais Mediterrânicas (Laboratório de Microbiologia do Solo), Universidade de Évora, Núcleo da Mitra, Ap. 94, 7002-554, Évora, Portugal

    Clarisse Brígido & Solange Oliveira

  2. IIFA—Instituto de Investigação e Formação Avançada, Universidade de Évora, Ap. 94, 7002-554, Évora, Portugal

    Clarisse Brígido

  3. Department of Biology, University of Waterloo, Waterloo, ON, N2L 3G1, Canada

    Bernard R. Glick

Authors
  1. Clarisse Brígido
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Bernard R. Glick
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Solange Oliveira
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Solange Oliveira.

Electronic Supplementary Material

Below is the link to the electronic supplementary material.

Supplementary Fig. 1

Maximum likelihood phylogeny of chickpea mesorhizobia isolates and type strains, based on partial 16S rRNA gene analysis (alignment length 579 bp). Kimura’s two-parameter model with a discrete gamma distribution and invariant sites was used. The three main clusters generated are marked with letters A to C. (JPG 226 kb)

Supplementary Table 1

Results obtained from the Portuguese chickpea mesorhizobia characterization in terms of specific plant growth-promoting traits and tolerance to heavy metals. nd- not determined; Classes of P solubilization: 0- no solubilization; 1-low solubilization; 2- high solubilization. Classes of siderophore production: 0 no production, 1- low production, 2- medium production, 3- high production. (JPG 31 kb)

Supplementary Table 2

Some characteristics of the soils used to obtain chickpea rhizobia isolates [data from 30 and 32]. Classes of soil pH: 1) soils with pH values below 6.5 (acid soils), 2) soils with pH values ranging from 6.5 to 7.4 (neutral soils), 3) soils with pH values above 7.4 (alkaline soils). nd- not determined (JPG 17 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brígido, C., Glick, B.R. & Oliveira, S. Survey of Plant Growth-Promoting Mechanisms in Native Portuguese Chickpea Mesorhizobium Isolates. Microb Ecol 73, 900–915 (2017). https://doi.org/10.1007/s00248-016-0891-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00248-016-0891-9

Keywords

Search

Navigation