Restoration of Growth of Durum Wheat (Triticum durum var. waha) Under Saline Conditions Due to Inoculation with the Rhizosphere Bacterium Azospirillum brasilense NH and Extracts of the Marine Alga Ulva lactuca

Abdel-Ghaffar BA, El-Shourbagy MN, Basha EM (1998) Responses of NaCl stressed wheat to IAA. In: Proceedings of the 6th Egyptian botanical conference, 24–26 November 1998, Cairo University, Giza, Egypt. WJAS/AEJAES 6:79–88 Alvey S, Yang CH, Buerkert D, Crowley DE (2003) Cereal/legume rotation effects on rhizosphere bacterial community structure in West African soils. Biol Fert Soils 37:73–82 Amann RI, Binder BJ, Olson RJ, Chisholm SW, Devereux R, Stahl DA (1990) Combination of 16S rRNA-targeted oligonucleotide probes with flow cytometry for analyzing mixed microbial populations. Appl Environ Microbiol 56:1919–1925 Ashraf MY, Khan MA, Maqvi SSM (1991) Effect of salinity on seedling growth and solutes accumulation in two wheat genotypes. Rachis 10:30–31 Aßmus B, Hutzler P, Kirchhof G, Amann R, Lawrence JR, Hartmann A (1995) In situ localization of Azospirillum brasilense in the rhizosphere of wheat with fluorescently labeled, rRNA-targeted oligonucleotide probes and scanning confocal laser microscopy. Appl Environ Microbiol 61:1013–1019 Bakker EP, Booth IR, Dinnbier U, Epstein W, Gajewska A (1987) Evidence for multiple K+ export systems in Escherichia coli. J Bacteriol 169:3743–3749 Baldani VLD, Döbereiner J (1980) Host-plant specificity in the infection of cereals with Azospirillum spp. Soil Biol Biochem 12:433–439 Barbieri P, Galli E (1993) Effect on wheat root development of inoculation with an Azospirillum brasilense mutant with altered indole-3-acetic acid production. Res Microbiol 144:69–75 Bartels D, Sunkar R (2005) Drought and salt tolerance in plants. Crit Rev Plant Sci 24:23–58 Bashan Y, Holguin G (1997) Azospirillum–plant relationships, environmental and physiological advances. Can J Microbiol 43:103–121 Bashan Y, Levanony H (1990) Current status of Azospirillum inoculation technology. Azospirillum as a challenge for agriculture. Can J Microbiol 36:591–607 Bashan Y, Moreno M, Troyo E (2000) Growth promotion of the seawater-irrigated oilseed halophyte Salicornia bigelovii inoculated with mangrove rhizosphere bacteria and halotolerant Azospirillum spp. Biol Fert Soils 32:265–272 Bengston C, Klockare B, Klockare R, Larsson S, Sudquist C (1978) The after-effect of water stress on chlorophyll formation during greening and the level of abscisic acid and proline in dark growth wheat seedlings. Plant Physiol 43:205–212 Blaha D, Prigent-Combaret C, Mirza MS, Moënne-Loccoz Y (2006) Phylogeny of the 1-aminocyclopropane-1-carboxylic acid deaminase-encoding gene acdS in phytobeneficial and pathogenic Proteobacteria and relation with strain biogeography. FEMS Microbiol Ecol 56:455–470 Brenda C, Fermin TS, Hahm JA, Radinsky RJ, Kratochvil JE, Hall Y, Martin L (2005) Effect of proline and glutamine on the functional properties of wheat dough in winter wheat varieties. J Food Sci 70:273–278 Brown CM, Dilworth MJ (1975) Ammonia assimilation by Rhizobium cultures and bacteroids. J Gen Microbiol 122:61–67 Carpita NC (1985) Tensile strength of cell walls of living cells. Plant Physiol 79:485–488 Cayla M (1995) Découvrez les algues: propriétés, applications, recettes. Chairon, Paris, pp 23–25 Cordovilla MP, Ligero F, Lluch C (1994) The effect of salinity on N-fixation on growth, symbiotic performance and nitrogen assimilation in Faba bean (Vicia faba L.) under salt stress. Plant Soil 172:289–297 Creus CM, Sueldo RJ, Barassi CA (1998) Water relations in Azospirillum-inoculated wheat seedlings under osmotic stress. Can J Bot 76:238–244 Daims H, Bruhl A, Amann R, Schleifer K-H, Wagner M (1999) The domain-specific probe EUB338 is insufficient for the detection of all bacteria: development and evaluation of a more comprehensive probe set. Syst Appl Microbiol 22:434–444 Dobbelaere S, Croonenborghs A, Amber T, Ptacek D, Vanderleyden J, Dutto P, Labandera-Gonzalez C, Caballero-Mellado J, Aguirre JF, Kapulnik Y, Shimon B, Burdman S, Kadouri D, Sarig S, Okon Y (2001) Responses of agronomically important crops to inoculation with Azospirillum. Aust J Plant Physiol 28:1–9 Dobbelaere S, Vanderleyden J, Okon Y (2003) Plant growth-promoting effects of diazotrophs in the rhizosphere. Crit Rev Plant Sci 22:107–149 Egamberdiyeva D (2005) Characterization of Pseudomonas species isolated from the rhizosphere of plants grown in serozem soil, semi arid region of Uzbekistan. Sci World J 5:501–509 El-Haddad EHM, O’Leary JW (1994) Effect of salinity and K/Na ratio of irrigation water on growth and solute content of Atriplex amnicola and Sorghum bicolor. Irrigation Sci 14:127–133 Epstein W (1986) Osmoregulation by potassium transport in Escherichia coli. FEMS Microbiol Lett 39:73–78 Evans LT (1993) Crop evolution, adaptation and yield. Cambridge University Press, Cambridge Ferreira MCB, Fernandes MS, Döbereiner J (1987) Role of Azospirillum brasilense nitrate reductase in nitrate assimilation by wheat plants. Biol Fert Soils 4:47–53 Francois LE, Maas EV, Donovan TJ, Youngs VL (1986) Effect of salinity on grain yield and quality, vegetative growth, and germination of semi-dwarf and durum wheat. Agron J 78:1053–1058 Galinski EA (1995) Osmoadaptation in bacteria. Adv Microb Physiol 37:274–325 Gallé Á, Csiszár J, Tari I, Erdei L (2002) Changes in water and chlorophyll fluorescence parameters under osmotic stress in wheat cultivars. Acta Biol Szeged 46:85–86 Ghoul M (1990) L’halotolérance de E. coli. Effet des osmoprotecteurs naturels. Doctorate thesis, Université of Rennes 1, Rennes, France Ghoul M, Minet J, Bernard T, Dupray E, Cormier M (1995) Marine macroalgae as a source for osmoprotection for Escherichia coli. Microb Ecol 30:171–181 Gill PK, Sharma AD, Singh P, Bhullar SS (2002) Osmotic stress-induced changes in germination, growth and soluble sugar content of Sorghum bicolour (L.) Moench seeds. Bulg J Plant Physiol 28(3–4):12–25 Glick BR, Penrose DM, Li J (1998) A model for the lowering of plant ethylene concentrations by plant growth promoting bacteria. J Theor Biol 190:63–68 Gunes A, Inal A, Alpaslan M (1996) Effect of salinity on stomatal resistance, proline, and mineral composition of pepper. J Plant Nutr 19:389–396 Hartmann A, Baldani JI (2006) The genus Azospirillum. In: Dworkin M, Falkow S, Rosenberg E, Schleifer K-H, Stackebrandt E (eds) The prokaryotes, vol 5: Proteobacteria: alpha and beta subclasses (chap 3.1.5). Springer, New York, pp 115–140 Hartmann A, Singh M, Klingmüller W (1983) Isolation and characterization of Azospirillum mutants excreting high amounts of indole acetic acid. Can J Microbiol 29:916–923 Iqbal R, Mahmood A (1992) Structural studies on root nodules of Leucaena leucocephola with particular reference to the infection process. Pak J Bot 24:142–152 Jofré E, Fischer S, Rivarola V, Balegno H, Mori G (1998) Saline stress affects the attachment of Azospirillum brasilense Cd to maize and wheat roots. Can J Microbiol 44:416–422 Kapulnik Y, Okon Y, Henis Y (1985) Changes in root morphology of wheat caused by Azospirillum inoculation. Can J Microbiol 31:881–887 Kapulnik Y, Okon Y, Henis Y (1987) Yield response of spring wheat (Triticum aestivum) to inoculation with Azospirillum brasilense under field conditions. Biol Fert Soils 4:27–35 Kerepesi I, Galiba G (2000) Osmotic and salt stress-induced alteration in soluble carbohydrate content in wheat seedlings. Crop Sci 40:482–487 Kogut M, Russell NJ (1987) Life at the limits: considerations on how bacteria can grow at extremes of temperature and pressure or with high concentrations of ions and solutes. Sci Prog 71:381–400 Konnova SA, Makarov OE, Skvortsov IM, Ignatov VV (1994) Isolation, fractionation and some properties of polysaccharides produced in a bound form by Azospirillum brasilense and their possible involvement in Azospirillum–wheat root interactions. FEMS Microbiol Lett 118:93–99 Malmstrom RR, Kiene RP, Cottrell MT, Kirchman DL (2004) Contribution of SAR11 bacteria to dissolved dimethylsulfoniopropionate and amino acid uptake in the north Atlantic Ocean. Appl Environ Microbiol 70:4129–4135 Marshall KC (1975) Clay mineralogy in relation to survival of soil bacteria. Annu Rev Phytopathol 13:357–373 Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria that confer resistance in tomato to salt stress. Plant Physiol Biochem 42:565–572 Morel JL, Habib L, Plantureux S, Guckert A (1991) Influence of maize root mucilage on soil aggregate stability. Plant Soil 136:111–119 Nabti E, Sahnoune M, Adjrad S, Van Dommelen A, Ghoul M, Schmid M, Hartmann A (2007) A halophilic and osmotolerant Azospirillum brasilense strain from Algerian soil restores wheat growth under saline conditions. Eng Life Sci 7:354–360 Nedzarek A, Rakusa-Suszczewski S (2004) Decomposition of macroalgae and the release of nutrient in Admiralty Bay, King George Island, Antarctica. Polar Biosci 17:26–35 Okon Y, Kapulnik Y (1986) Development and function of Azospirillum-inoculated roots. Plant Soil 90:3–16 Okon Y, Labandera-Gonzalez C (1994) Agronomic applications of Azospirillum: an evaluation of 20 years world-wide field inoculation. Soil Biol Biochem 26:1591–1601 Okon Y, Vanderleyden J (1997) Root-associated Azospirillum species can stimulate plants. ASM News 63:366–370 Perrig D, Boiero ML, Masciarelli OA, Penna C, Ruiz OA, Cassan FD, Luna MV (2007) Plant-growth-promoting compounds produced by two agronomically important strains of Azospirillum brasilense, and implications for inoculant formulation. Appl Microbiol Biotechnol 75(5):1143–1150 Phillips DA, Joseph CM, Maxwell CA (1992) Trigonelline and stachydrine released from alfalfa seeds activate NodD2 protein in Rhizobium meliloti. Plant Physiol 99:1526–1531 Pichereau V, Pocard J-A, Hamelin J, Blanco C, Bernard T (1998) Differential effects of dimethylsulfoniopropionate, dimethylsulfonioacetate, and other S-methylated compounds on the growth of Sinorhizobium meliloti at low and high osmolarities. Appl Environ Microbiol 64:1420–1429 Qureshi RH, Ahmed R, Ilyas M, Aslam Z (1980) Screening of wheat (Triticum aestivum L.) for salt tolerance. Pak J Agric Sci 27:9–26 Rashid A (1986) Mechanism of salt tolerance in wheat (Triticum aestivum L.). PhD thesis, University of Agriculture, Faisalabad, Pakistan Reddy PS, Veeranjaneyulu K (1991) Proline metabolism in senescing leaves of hosgram (Macrotyloma uniflorum lam.). J Physiol 137:381–383 Reed RH (1983) Measurement and osmotic significance of ß-dimethylsulphoniopropionate in marine macroalgae. Mar Biol Lett 34:173–181 Rengasamy P (2002) Transient salinity and subsoil constraints to dryland farming in Australian sodic soils: an overview. Aust J Exp Agric 42:351–361 Rengasamy P, Chittleborough D, Helyar K (2003) Root-zone constraints and plant-based solutions for dryland salinity. Plant Soil 257:249–260 Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44:357–384 Rodrigues O, Didonet AD, Gouveia JA, Soares C (2000) Nitrogen translocation in wheat inoculated with Azospirillum and fertilized with nitrogen. Pesqui Agropecu Bras 35:1473–1481 Rosenblueth M, Martinez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Mol Plant Microbe Interact 19:827–837 Rothballer M, Schmid M, Hartmann A (2003) In situ localization and PGPR effect of Azospirillum brasilense strains colonizing roots of different wheat varieties. Symbiosis 34:261–279 Sakhabutdinova AR, Fatkhutdinova DR, Bezrukova MV, Shakirova FM (2003) Salicylic acid prevents the damaging action of stress factors on wheat plants. Bulg J Plant Physiol 33:314–319 Saqib M, Akhtar J, Qureshi RH (2004) Pot study on wheat growth in saline and waterlogged compacted soil: I. Grain yield and yield components. Soil Till Res 77:169–177 Sayre KD, Rajaram S, Fischer RA (1997) Yield potential progress in short bread wheats in northwest Mexico. Crop Sci 37:36–42 Schloter M, Hartmann A (1998) Endophytic and surface colonization of wheat roots (Triticum aestivum) by different Azospirillum brasilense strains studies with strain-specific monoclonal antibodies. Symbiosis 25:159–179 Schulz B, Boyle C, Sieber N (2006) Microbial root endophytes. Springer, New York Sepaskhah AR, Bazrafshan-Jahromi AR, Shirmohammadi-Aliakbarkhani Z (2006) Development and evaluation of a model for yield production of wheat, maize and sugarbeet under water and salt stresses. Biosyst Eng 93:139–152 Sharma RC, Gupta NK, Gupta S, Hasegawa H (2005) Effect of NaCl salinity on photosynthetic rate, transpiration rate, and oxidative stress tolerance in contrasting wheat genotype. Photosynthesis 43:609–613 STAT-ITCF (1992) Logiciels et manuels d’utilisation. ITCF, Paris. STATSOFT (2004) Statistica, version 7.0. StatSoft, Inc, Tulsa, OK Stoffels M, Castellanos T, Hartmann A (2001) Design and application of new 16S rRNA-targeted oligonucleotide probes for the Azospirillum-Skermanella-Rhodocista-cluster. Syst Appl Microbiol 24:83–97 Termaat A, Passioura JB, Munns R (1985) Shoot turgor does not limit shoot growth of NaCl-affected wheat and barley. Plant Physiol 77:869–872 Tripathi AK, Nagarajan T, Verma SC, Le Rudulier D (2002) Inhibition of biosynthesis and activity of nitrogenase in Azospirillum brasilense Sp7 under salinity stress. Curr Microbiol 44:363–367 Vande Broek A, Lambrecht M, Vanderleyden J (1998) Bacterial chemotactic motility is important for the initiation of wheat root colonization by Azospirillum brasilense. Microbiology 144:2599–2606 Xiong L, Zhu J-K (2002) Molecular and genetic aspects of plant responses to osmotic stress. Plant Cell Environ 25:131–139 Zahran HH (1999) Rhizobium-legume symbiosis and nitrogen fixation under severe conditions and in an arid climate. Microbiol Mol Biol Rev 63:968–989 Zilber-Rosenberg I, Rosenberg E (2008) Role of microorganisms in the evolution of animals and plants: the hologenome theory of evolution. FEMS Microbiol Rev 32:723–735