Plant Growth-Promoting Bacteria Associated to the Halophyte Suaeda maritima (L.) in Abbas, Iran

  • Edgar Omar Rueda-PuenteEmail author
  • Oscar Bianciotto
  • Saifolah Farmohammadi
  • Omid Zakeri
  • Jesús López Elías
  • Luis Guillermo Hernández-Montiel
  • Murillo Amador Bernardo
Part of the Tasks for Vegetation Science book series (TAVS, volume 49)


Suaeda maritima (L.), regarded as a promising halophyte, is widely distributed along the coastal plains of Abbas, Iran. Suaeda maritima has been highly incorporated with the traditional agriculture to support the Iranian agricultural economy. However, its productivity is limited by a lack of available nitrogen. Application of halotolerant plant growth-promoting rhizobacteria (PGPR) suggested being an alternative biological fertilizer. Increasing the knowledge of halotolerant PGPR associated to the native crops remains important. Nine endemic colonies were isolated from the roots of S. maritima. Those isolates were cultured in different salinity conditions (0, 0.25, 0.5, and 0.75 M NaCl) and maintained at different temperature regimes (30 and 55 °C). The nitrogen fixation ability of the isolated endemic colonies was screened by acetylene reduction assay. Among them, only one showed high acetylene reduction activity and capacity to solubilize phosphates. This bacterium was identified as Bacillus amyloliquefaciens. Seeds inoculated with Bacillus amyloliquefaciens, in conjunction with Azospirillum halopraeferens as a biological control, were tested for seed germination and early growth promotions of S. maritima exposed to high salinities under in vitro conditions. Bacillus amyloliquefaciens showed a high specificity for the wild S. maritima. This is the first report of Bacillus amyloliquefaciens as nitrogen-fixing bacterium associated with the oilseed S. maritima a novel halophyte crop. Through this work, a reliable biological method was found, based on beneficial bacteria, to contribute to maintain or improve the fertility of soils sustaining Suaeda fields.


Arid desert Halophytes Nitrogen fixation 



This work was supported by Academic Center for Education Culture and Research (ACECR) of Hormozgan, Iran. Thanks to Universidad de Sonora and Project of CONACYT (Apoyoscomplementarios para la consolidacióninstitucional de grupos de investigación) 2007; code: 74592 of Dr. Bernardo Murillo Amador, CIBNOR.


  1. Akhavan K, Campbell W, Jurinak J, Dudley L (1991) Effects of CaSO4, CaCl2, and NaCl on leaf nitrogen, nodule weight, and acetylene reduction activity in Phaseolus vulgaris L. Arid Soil Res Rehabil 5:97–103CrossRefGoogle Scholar
  2. Arsac J, Lamothe C, Mulard D, Fages J (1990) Growth enhancement of maize (Zea mays L) through Azospirillum lipoferum inoculation: effect of plant genotype and bacterial concentration. Agronomie 10:640–654CrossRefGoogle Scholar
  3. Bashan Y, Holguin G, Puente M (1992) Alternativaagrícola regional por fertilizantesbacterianosenuso y manejo de los recursos naturales en la Sierra de la Laguna Baja California Sur. In: Ortega R (ed) Uso y Manejo de los Recursos Naturales en la Sierra de la Laguna, B.C.S. Centro de InvestigacionesBiológicas del Noroeste, La Paz, pp 46–67Google Scholar
  4. Bagwell C, Dantzler M, Bergholz P, Llovell C (2001) Host-specific ecotype diversity of rhizoplane diazotrophs of the perennial glasswort Salicornia virginica and selected salt mash grasses. J Aqu Microbiol Ecol 23:293–300CrossRefGoogle Scholar
  5. Baldani V, Dobereiner I (1980) Host-plant specificity in the infection of cereals with Azospirillum spp. Soil Biol Biochem 12:443–439CrossRefGoogle Scholar
  6. Banwari I, Rao V (1990) Effect of Azospirillum brasilense on growth and nitrogen content of Cynodon dactylon under different moisture regimens. Ind. J Plant Physiol 33:210–213Google Scholar
  7. Barnes H, Blackstock J (1973) Estimation of lipids in marine animal and tissues: detailed investigation of sulphophosphovanil method for ‘total’ lipids. J Exp Mar Biol Ecol 12:103–118CrossRefGoogle Scholar
  8. Carrillo A; Puente ME, Castellanos E, Bashan Y (1998) Aplicaciones Biotecnológicas de EcologíaMicrobiana. Pontificia Universidad Javeriana, Santa Fe de Bogotá, Colombia and Centro de InvestigacionesBiológicas del Noroeste Manual de Laboratorio, Manual de Laboratorio, La Paz, B.C.S., México, pp 15–20Google Scholar
  9. Craven PA, Hayasaka S (1982) Inorganic phosphate solubilization by rhizosphere bacteria in a Zostera marina community. Can J Microbiol 28:605–610CrossRefGoogle Scholar
  10. De Troch P, Vaderleyden J (1996) Surface properties and motility of rhizobium and Azospirillum in relation to plant root attachment. Microb Ecol 32:149–169CrossRefGoogle Scholar
  11. Díaz V, Ferrera C, Almaraz S, Alcántar G (2001) Inoculation of plant growth-promoting bacteria in lettuce. Terrain 19:327–335Google Scholar
  12. Food and Agriculture Organization, FAO (1998) Red Latinoamericana de CooperaciónTécnicaen SistemasAgroforestales. EspeciesArbóreas y Arbustivas para las zonas Áridas y Semiáridas de América Latina, p 320Google Scholar
  13. Felker P, Clark PR, Laag AE, Pratt P (1981) Salinity tolerance of the tree legumes mesquite (Prosopis glandulosa var torreyana, P. velutina, and P. articulate) algarrobo (P. chilensis), Kiawe (P. pallida) and tamarugo (P. tamarugo) grown in sand culture on nitrogen free media. Plant Soil 61:311–317CrossRefGoogle Scholar
  14. Goodfriend W, Olsenm M, Frye R (2000) Soil microfloral and microfaunal response to Salicornia bigelovii planting density and soil residue amendment. Plant Soil 1:23–32CrossRefGoogle Scholar
  15. Hamdi H (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in arid climate. Microb. Mol Biol Rev 63:968–989Google Scholar
  16. Holguin G, Guzman M, Bashan Y (1992) Two new nitrogen-fixing bacteria from the rhizosphere of mangrove trees: isolation, identification and in vitro interaction with rhizosphere Staphylococcus sp. Federation of European Microbiological Societies. Microbiol Ecol 101:207–216Google Scholar
  17. Khan MA, Gul B (1998) High salt tolerance in germinating dimorphic seeds of Arthrocnemum indicum. Int J Plant Sci 159:826–832CrossRefGoogle Scholar
  18. Khan MA, Gul B (2002) Salt tolerant plants of coastal Sabkhas of Pakistan. In: Sabkha A, Barth H, Boer B (eds) Ecosystems. Kluwer Academic Press, DordrechtGoogle Scholar
  19. Khan MA, Gul B, Weber DJ (2000) Germination response of Salicornia rubra to temperature and salinity. J Arid Environ 45:207–214CrossRefGoogle Scholar
  20. Little EL (1950) Southwestern trees – a guide to the native species of New Mexico and Arizona. USD, Handbook No. 9, Government Printing Office, Washington, DC, 560 pGoogle Scholar
  21. Liu W, Wang X, Wu L, Chen M, Tu C, Luo Y, Christie P (2012) Isolation, identification and characterization of Bacillus amyloliquefaciens BZ-6, a bacterial isolate for enhancing oil recovery from oily sludge. Chemosphere 87(10):1105–1110CrossRefGoogle Scholar
  22. Lovell C, Piceno Y, Bagwell C (2000) Molecular analysis of diazotroph diversity in the rhizosphere of the smooth cordgrass, Spartina alterniflora. Appl Environ Microbiol 66:3814–3822CrossRefGoogle Scholar
  23. Maguire J (1962) Speed of germination-aid in selection and evaluation for seedling emergence and vigour. Crop Sci 2:176–177CrossRefGoogle Scholar
  24. Munns R (2005) Genes and salt tolerance: bringing them together. New Phytol 167:645–663CrossRefGoogle Scholar
  25. Nielsen I, Finster K, Welsch A, Donelly R, Herbert R, De Wit L, Lomstein B (2001) Sulphate reduction and nitrogen fixation rates associated with roots, rhizomes and sediments from Zostera noltii and Spartina maritima meadows. Environ Microbiol 3:63–71CrossRefGoogle Scholar
  26. Okon Y, Hadar Y (1987) Microbial inoculants as crop-yield enhancers. CRC Crit Rev Biotechnol 6:6–85CrossRefGoogle Scholar
  27. Puente M (2004) Poblacionesbacterianasendófitas y del rizoplano de plantas del desiertodegradadotas de roca y suefectosobre el crecimiento del cardón (Pachycereuspringlei [S. WATS] BRITT. and ROSS). Doctoral thesis, Centro de Investigaciones Biológicas del Noroeste, La Paz, B.C.S., México, pp 1–166Google Scholar
  28. Rennie R (1981) A single medium for the isolation of acetylene reducing (dinitrogen-fixing bacteria from soil). Can J Microbiol 27:8–14CrossRefGoogle Scholar
  29. Reinhold B, Hurek T, Fendrik I, Pot B, Gillis M, Kersters K, Thielmans S, De Ley J (1987) Azospirillum halopraeferens sp. novo a nitrogen-fixing organism associated with roots of Kallar grass (Leptochloa fusca L. Kunth). Int J Syst Bacteriol 37:43–51CrossRefGoogle Scholar
  30. Rodelas B, González I, Salmeron V, Pozo C, Martinez T (1996) Enhancement of nodulation, N-2 fixation and growth of faba bean (Viciafaba L.) by combined inoculation with Rhizobium leguminosarum by Viceaesp and Azospirillum brasilense. Symbiosis 21:175–186Google Scholar
  31. Rojas A, Holguin G, Glick B, Bashan Y (2001) Synergism between Phyllobacterium sp (N2-fixer) and Bacillus licheniformis (P-solubilizer), both from a semiarid mangrove rhizosphere. Microb Ecol 35:181–187CrossRefGoogle Scholar
  32. Rueda PEO, Barrón H, Jojanes H (2009a) BacteriasPromotoras Del Crecimiento Vegetal. Editorial Plaza y Valdes, México, p 112Google Scholar
  33. Rueda PEO, Barrón H, Tarazón H, Preciado R (2009b) La Salinidad: Un Problema o Una Opción Para La Agricultura? Editorial Plaza y Valdes, México City, p 264Google Scholar
  34. Rueda PEO, Castellanos T, Troyo E, De León J (2004) Effect of Klebsiella pneumoniae and Azospirillum halopraeferens on the growth and development of two Salicornia bigelovii genotypes. Aust J Exp Agric 44:65–74CrossRefGoogle Scholar
  35. Rueda PEO, Félix A, Beltrán M, Ruíz H, Valdez C, García H, Ávila N, Partida L, Murillo B (2011) Sustainable options for soil management in arid zones: uses of the halophyte Salicornia bigelovii (Torr.) and biofertilizers in the modern agriculture. Trop Subtrop Agroecosyst 13:157–167Google Scholar
  36. Robles AB, Ruiz M, Ramos ME, González R (2009) Role of livestock grazing in sustainable use, naturalness promotion in naturalization of marginal ecosystems of southeastern Spain (Andalusia). In: Rigueiro-Rodriguez A, McAdam J, Mosquera-Losada MR (eds) Agroforesty in Europe. Editorial Springer, Lugo, p 445Google Scholar
  37. Saitou N, Nei M (1987) The neighbour-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425PubMedGoogle Scholar
  38. SAS, Institute (2001) SAS/STAT User’s Guide. Version 6.12 SAS Institute, Cary, NCGoogle Scholar
  39. Sasser M (1990) Identification of bacteria through fatty acid analysis. In: Clement Z (ed) Methods in Phytobacteriology, vol 565. Akadamiai RU Kiado, BudapestGoogle Scholar
  40. Snedecor G (1956) In: Freeman SR (ed) Statistical methods applied to experiments in agriculture and biology. The Iowa State College Press, AmesGoogle Scholar
  41. Sokal R, Rohlf F (1988) Biometry. In: Freeman SR (ed) The principles and practice of statistics in biological research, San Francisco, p 650Google Scholar
  42. Song J, Fan H, Zhao YY, Jia YH, Du XH, Wang BS (2008) Effect of salinity on germination, seedling emergence, seedling growth and ion accumulation of a euhalophyte Suaeda salsa in an intertidal zone and on saline inland. Aquat Bot 88:331–337CrossRefGoogle Scholar
  43. Strickl J, Parsons T (1972) A practical handbook of sea water analysis. Bull Fish Res Can 167:49–52Google Scholar
  44. Sundara-Rao W, Sinha M (1963) Phosphate dissolving micro-organisms in the soil and rhizosphere. Indian J Microbiol 41:999–1011Google Scholar
  45. Towhidi A, Zhandi M (2007) Chemical composition, in vitro digestibility and palatability of nine plant species for dromedary camels in the province of Semnan. Iran Egypt J Biol 9:47–52Google Scholar
  46. Ungar I (2000) Ecophysiology of vascular halophytes. Department of Botany, CRC Press, Ohio University, Athens, p 209Google Scholar
  47. Vázquez P, Holguin G, Puente M, López-Cortes A, Bashan Y (2000) Phosphate-solubilizing microorganisms associated with the rhizosphere of mangroves in a semiarid coastal lagoon. Biol Fertil Soils 30:460–468CrossRefGoogle Scholar
  48. Velarde M, Felker P, Degano C (2003) Evaluation of argentine and Peruvian Prosopis germplasm for growth at seawater salinities. J Arid Environ 55:515–531CrossRefGoogle Scholar
  49. Villegas E, Rueda PEO, Puente ME, Muñiz SR, Avilés MS, Grimaldo JO, Murillo A, Preciado R (2010) First report of plant growth promoting bacteria from mesquite (Prosopis glandulosa) rhizosphere on volcans of Sonora desert. 12 International symposium on microbial ecology, Cairns, Australia, pp 15–25Google Scholar
  50. Wang BS, Luttge U, Ratajczak R (2004) Specific regulation of SOD isoforms by NaCl and osmotic stress in leaves of the C3 halophyte Suaeda salsa L. J Plant Physiol 161:285–293CrossRefGoogle Scholar
  51. Whipps J (2000) Microbial interactions and biocontrol in the rhizosphere. J Exp Bot 52:487–511CrossRefGoogle Scholar
  52. Yokoishi T, Tanimoto S (1994) Seed germination of the halophyte Suaeda japonica under salt stress. J Plant Res 107:385–388CrossRefGoogle Scholar
  53. Zexun I, Wei S (2000) Effect of cultural conditions on IAA biosynthesis by Klebsiella oxytoca SG-11. Chinese J Appl Environ Biol 6:66–69Google Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Edgar Omar Rueda-Puente
    • 1
    Email author
  • Oscar Bianciotto
    • 2
  • Saifolah Farmohammadi
    • 3
  • Omid Zakeri
    • 3
  • Jesús López Elías
    • 1
  • Luis Guillermo Hernández-Montiel
    • 4
  • Murillo Amador Bernardo
    • 4
  1. 1.Agriculture DepartmentSonora UniversityHermosilloMexico
  2. 2.Universidad Nacional de Tierra del Fuego A.I.A.SUshuaiaArgentina
  3. 3.Academic Center for Education Culture and Research (ACECR) of Hormozgan, Iran and Province Department of Natural ResourcesPlantation OfficeTehranIran
  4. 4.Center of Biological Researchers of NorwestInstituto Politécnico NacionalLa PazMéxico

Personalised recommendations