535
Views
49
CrossRef citations to date
0
Altmetric
Original Articles

Effect of halotolerant endophytic bacteria isolated from Salicornia europaea L. on the growth of fodder beet (Beta vulgaris L.) under salt stress

, , , , &
Pages 1404-1418 | Received 20 Jul 2016, Accepted 20 Jan 2017, Published online: 08 Feb 2017

References

  • Abo-Kassem EE-DM. 2007. Effects of salinity: calcium interaction of growth and nucleid acid metabolism in five species of Chenopodiaceae. Turk J Bot. 31:125–134.
  • Ali S, Carles TC, Glick BR. 2014. Amelioration of high salinity stress damage by plant growth-promoting bacterial endophytes that contain ACC deaminase. Plant Physiol Biochem. 80:160–167.
  • Alvarado AD, Bradford KJ, Hewitt JD. 1987. Osmotic priming of tomato seeds. Effects on germination, field emergence, seedling growth and fruit yield. J Am Soc Hortic Sci. 112:427–432.
  • Arteca RN. 1996. Plant growth substances: principles and applications. New York, USA: Capan and Hall Press.
  • Asfaw GK. 2011. Effects of salinity on seedling biomass production and relative water content of twenty sorghum (Sorghum bicolor L. Moench) accessions. Asian J Agric Sci. 3:242–249.
  • Ashour NI, Yakout GM. 1993. Productivity of fodder beet grown under saline conditions in Sinai. In: Lieth, H, Al Masoom, A, editors. Towards the rational use of high salinity tolerant plants 2. Dordrecht: Kluver Academic Publishers; p. 209–212.
  • Bagheri A, Hasanvandi MS. 2013. Analysis of safflower leaf growth indices using regression modeling. Int J Agri Crop Sci. 5:2752–2760.
  • Bagwell CE, Dantzler M, Bergholz PW, Lovell CR. 2001. Host-specific ecotype diversity of rhizoplane diazotrophs of the perennial glasswort Salicornia virginica and selected salt marsh grasses. Aquati Microb Ecol. 23:293–300.
  • Bashan Y, Moreno M, Troyo E. 2000. Growth promotion of the sea-water irrigated oilseed halophyte Salicornia bigelovii inoculated with mangrove rhizosphere bacteria and halotolerant Azospirillum ssp. Biol Fertil Soils. 32:265–272.
  • Biancardi E, Panella LW, Lewellen RT. 2012. Beta maritima, the origin of beets. New York,NY: Springer.
  • Black M, Pritchard HW. 2002. Desiccation and survival in plants drying without dying. New York, NY: CABI publishing.
  • Dadkhah A. 2011. Effect of salinity on growth and leaf photosynthesis of two sugar beet (Beta vulgaris L.) cultivars. J Agr Sci Tech. 13:1001–1012.
  • Davy AJ, Bishop GF, Costa CSB. 2001. Salicornia L. (Salicornia pusilla J. Woods, S. ramosissima J. Woods, S. europaea L., S. obscura P.W. Ball & Tutin, S. nitens P.W. Ball & Tutin, S. fragilis P.W. Ball & Tutin and S. dolichostachya Moss). J Ecol. 89:681–707.
  • Evelin H, Kapoor R, Giri B. 2009. Arbuscular mycorrhizal fungi in alleviation of salt stress: a review. Ann Bot. 104:1263–1280.
  • Flowers TJ, Colmer TD. 2008. Salinity tolerance in halophytes. New Pytol. 179:945–963.
  • Flowers TJ, Galal HK, Bromham L. 2010. Evolution of halophytes: multiple origins of salt tolerance in land plants. Function Plant Biol. 37:604–612.
  • Geressu K, Gezahagne M. 2008. Response of some lowland growing sorghum (Sorghum bicolor L. Moench) accessions to salt stress during germination and seedling growth. Afr J Agric Res. 3:044–048.
  • Ghoulam C, Fores K. 2001. Effect of salinity on seed germination and early seedlings growth of sugar beet (Beat vulgaris L.). Seed Sci Technol. 29:357–364.
  • Ghoulam C, Foursy A, Fores K. 2002. Effects of salt stress on growth, inorganic ions and proline accumulation in relation to osmotic adjustment in five sugar beet cultivars. Environ Exp Bot. 47:39–50.
  • Gutterman Y. 1993. Seed germination in desert plants. Berlin: Springer-Verlag.
  • Habutamu A, Estifanos E, Muluken E, Mulugeta T, Nuguse S. 2014. Seed germination and early seedling growth of haricot bean (Phaseolus vulgaris L.) cultivars as influenced by salinity stress. Int J Agric Sci. 4:125–130.
  • Hajiboland R, Joudmand A, Fotouchi K. 2009. Mild salinity improves sugar beet (Beta vulgaris L.) quality. Acta Agric Scandinavica Sec B – Soil and Plant Sci. 59:295–305.
  • Hallmann J, Quadt-Hallmann A, Mahaffee WF, Kloepper JW. 1997. Bacterial endophytes in agricultural crops. Can J Microbiol. 43:895–914.
  • Hasanuzzaman M, Kamrun N, Masayuki F. 2013. Plant response to salt stress and role of exogenous protectants to mitigate salt-induced demages. In: Ahmad, P, Azooz, MM, Prasad, MNV, editors. Ecophysiology and responses of plant under salt stress. New York: Springer-Verlag; p. 25–87.
  • Hrynkiewicz K, Baum C, Leinweber P. 2010. Density, metabolic activity, and identity of cultivable rhizosphere bacteria on Salix viminalis in disturbed arable and landfill soils. J Plant Nut Soil Sci. 173:747–756.
  • Hubbard M, Germida J, Vujanovic V. 2012. Fungal endophytes improve wheat seed germination under heat and drought stress. Bot. 90:137–149.
  • Hulisz P, Charzyński P, Giani L. 2010. Application of the WRB classification to salt-affected soils in Poland and Germany. Polish J Soil Sci. 43:81–92.
  • Ibrahim YM. 2005. Ranges and forage (In Arabic). Khartoum, Sudan: Dar Azza for Publication.
  • Jafari B, Hanifezadeh M, Maryam Parvin MSJ. 2012. Molecular study of bacteria associated with Salicornia symbiotic bacteria as a candidate for Hormozgan salty zone culturing by Persian Gulf water irrigation. Afr J Mic Res. 6:4687–4695.
  • Jafarzadeh AA, Aliasgharzad N. 2007. Salinity and salt composition effects on seed germination and root lenght of four sugar beet cultivars. Biol. 62:562–564.
  • Jamil M, Deog Bae L, Kwang Yong J, Ashraf M, Sheong Chun L, Eui Shik R. 2006. Effect of salt (NaCl) stress on germination and early seedling growth of four vegetable species. J Central Europ Agri. 7:273–282.
  • Janette S, Craig R, Lynch JP. 2002. Salinity tolerance of Phaseolus species during germination and early seedlings growth. Crop Sci. 42:1584–1594.
  • Jha B, Gontia I, Hartmann A. 2011. The roots of the halophyte Salicornia brachiata are a source of new halotolerant diazotrophic bacteria with plant growth-promoting potential. Plant Soil. 356:265–277.
  • Jiang D, Huang L, Lin Y, Nie L, Kuang SLT, Li Y. 2012. Inhibitory effect of Salicornia europaea on the marine alga Skeletonema costatum. Sci China Life Sci. 55:551–558.
  • Kaffka S, Hembree K. 2004. Effects of saline soil, Irrigation, and seed treatments on sugar beet stand establishment. J Sugar Beet Res. 41:61–72.
  • Kaya CA, Tunab L, Ashrafc M, Altunlud H. 2007. Improved salt tolerance of melon (Cucumis melo L.) by the addition of proline and potassium nitrate. Environ Exp Bot. 60:397–403.
  • Kaya MD, Ozturk A. 2003. Effect of different soil salinity levels on germination and seedling growth of safflower (Carthamus tinctorious L. Turk J Agric. 27:221–227.
  • Khavari-Nejad RA, Najafi F, Khavari-Nejad S. 2008. Growth and some physiological parameters of four sugar beet (Beta vulgaris L.) cultivars as affected by salinity. Pakistan J Biol Sci. 11:1390–1393.
  • Khogali ME, Dagash YMI, EL-Hag MG. 2011. Productivity of fodder beet (Beta vulgaris var. crassa) cultivars affected by nitrogen and plant spacing. Agric Biol J N Am. 2:791–798.
  • Kigel J. 1995. Seed germination in arid and semiarid region. In: Kigel, J, Gallili, G, editors. Seed development and germination. New York: Marcel Dekker; p. 654–697.
  • Kremmydas GF, Tampakaki AP, Georgakopoulos DG. 2013. Characterization of the biocontrol activity of Pseudomonas fluorescens strain X reveals novel genes regulated by glucose. Plos One. 8:e61808.
  • Ladeiro B. 2012. Saline agriculture in the 21st century: using salt contaminated resources to cope food requirements. J Bot Article ID. 310705:1–7.
  • Liu L, Ueda A, Saneoka H. 2013. Physiological responses of white Swiss chard (Beta vulgaris L. subsp. cicla) to saline and alkaline stress. Australian J Crop Sci. 7:1046–1052.
  • Mahajan S, Tuteja N. 2005. Cold, salinity and drought stresses: an overview. Arch Biochem Biophys. 444:139–158.
  • Martin JH, Leonard WH, Stamp DL. 1976. Principles of field crop production. Third ed. New York: MacMillan Publishing Co., Inc.
  • Mayak S, Tirosh T, Glick BR. 2004. Plant growth-promoting bacteria that confer resistance to water stress in tomatoes and pepper. Plant Sci. 166:525–530.
  • Miliute I, Buzaite O, Banilus D, Stanys V. 2015. Bacterial endophytes in agricultural crops and their role in stress tolerance: a review. Zemdirbyste-Agric. 102:465–478.
  • Mordi P, Zavareh M. 2013. Effect of salinity on germination and early seedling growth of cheackpea (Cicer arientum L.) cultivars. Int J Farming Allied Sci. 2:70–74.
  • Munns R, Tester M. 2008. Mechanisms of salinity tolerance. Ann Rev Plant Biol. 59:651–681.
  • Niazi BH 2007. Response of fodder beet to salinity. Introduction of a non-conventional fodder crop (Fodderbeet) to salt affected lands of Pakistan. PhD-thesis Vrije Universiteit, Amsterdam.
  • Nishma KS, Adrisyanti B, Anusha SH, Rupali P, Sneha K, Jayamohan NS, Kumudini BS. 2014. Induced growth promotion under in vitro salt stress tolerance on solanum lycopersicum by fluorescent pseudomonas associated with rhizosphere. Int J Appl Sci Engineering Res. 3:422–430.
  • Patten CL, Glick BR. 2002. Role of Pseudomonas putida indoleacetic acid in development of the host plant root system. Appl Environ Microbiol. 68:3795–3801.
  • Piernik A. 2005. Vegetation-environment relations on inland saline habitats in Central Poland. Phytocoenologia. 35:19–38.
  • Piernik A. 2012. Ecological pattern of inland salt marsh vegetation in Central Europe. Toruń: NCU Press.
  • Piernik A, Hulisz P, Rokicka A. 2015. Micropattern of halophytic vegetation on technogenic soils affected by the soda industry. Soil Sci Plant Nutr. 61:98–112.
  • Raheem A, Basharat A. 2015. Halotolerant rhizobacteria: beneficial plant metabolites and growth enhancement of Triticum aestivum L. in salt-amended soils. Arch Agron Soil Sci. 61:1691–1705.
  • Rhee MH, Park H-J, Cho JY. 2009. Salicornia herbacea: botanical, chemical and pharmacological review of halophyte marsh plant. J Medic Plants Res. 3:548–555.
  • Richardson AD, Duigan PS, Berlyn GP. 2002. An evaluation of noninvasive methods to estimate foliar chlorophyll content. New Phytol. 153:185–194.
  • Rozema J. 1991. Growth, water, and ion relationships of halophytic monocotyledone and dicotyledone: a unified concept. Aquatic Bot. 39:3–16.
  • Rozema J, Cornelisse D, Zhang Y, Li H, Bruning B, Katching D, Broekman R, Ji B, Van Bodegom P. 2014. Comparing salt tolerance of beet sultivars and their halophytic ancestor: consequences of domestication and breeding programmes. Aob Plants. 7:plu083.
  • Rozema J, Schat H. 2013. Salt tolerance of halophytes, research questions reviewed in the perspective of saline agriculture. Environ Exp Bot. 92:83–95.
  • Ruan S, Xue Q, Tylkowska K. 2002. The influence of priming on germination of rice (Oryza sativa L.) seeds and seedling emergence and performance in flooded soil. Seed Sci Technol. 30:61–67.
  • Rueda-Puente EO, Farmohammadi S, Moghaddam A, Zakeri O. 2011. Plant growth promoting bacteria associated to Salicornia rhyzosphere in Abbas, Iran. Agric Sci Res J. 1:155–165.
  • Santoyo G, Moreno-Hagelsieb G, Orozco-Mosqueda M, Glick BR. 2016. Plant growth promoting bacterial endophytes. Microbiol Res. 183:92–99.
  • Seyed NM, Morteza EN. 2013. Effect of NaCl and CaCl stress on germination indicators and seedling growth of canola. Int J Farming Allied Sci. 2:32–37.
  • Sgroy V, Cassán F, Masciarelli O, Del Papa MF, Lagares A, Luna V. 2009. Isolation and characterization of endophytic plant growth-promoting (PGPB) or stress homeostasisregulating (PSHB) bacteria associated to the halophyte Prosopis strombulifera. Appl Microbiol Biotechnol. 85:371–381.
  • Shabala S, Mackay A. 2011. Ion transport in halophytes. Advances Bot Res. 57:151–199.
  • Shi Y, Lou K, Li C. 2009. Isolation, quantity distribution and characterization of endophytic microorganisms within sugar beet. African J Biotechnol. 8:835–840.
  • Shi Y, Lou K, Li C. 2010. Growth and photosynthetic efficiency promotion of sugar beet (Beta vulgaris L.) by endophytic bacteria. Photosynth Res. 105:5–13.
  • Shi Y, Lou K, Li C, Wang L, Zhao Z, Zhao S, Tian C. 2015. Ilumina-based analysis of bacterial diversity related to halophytes Salicornia europaea and Suaeda aralocaspica. J Microbiol. 53:678–685.
  • StatSoft 2006. Elektroniczny Podręcznik Statystyki PL [Electronic Guide for Statistics PL]. Kraków, WEB: http://www.statsoft.pl/textbook/stathome.html.
  • Steppuhn H, Van Genuchten MT, Grieve CM. 2005. Root-zone salinity: II. Indices for tolerance in agricultural crops. Crop Sci. 45:221–232.
  • Szymańska S, Piernik A, Baum C, Złoch M, Hrynkiewicz K. 2014. Metabolic profiles of microorganisms associated with the halophyte Salicornia europaea in soils with different levels of salinity. Ecoscience. 21:114–122.
  • Szymańska S, Płociniczak T, Piotrowska-Seg Z, Hrynkiewicz K. 2016. Endophytic and rhizosphere bacteria associated with the roots of the halophyte Salicornia europaea L. – community structure and metabolic potential. Microbiol Res. 192:37–51.
  • Taghavi S, Garafola C, Monchy S, Newman L, Hoffman A, Weyens N, Barac T, Vangronsveld J, van der Lelie D. 2009. Genome survey and characterization of endophytic bacteria exhibiting a beneficial effect on growth development of oplar trees. Appl Environ Microbiol. 53:1195–1202.
  • Tanimoto E. 2005. Regulation of root growth by plant hormones – role of auxin and gibberellins. Crit Rev Plant Sci. 24:249–265.
  • Ter Braak CJF, Šmilauer P. 2002. CANOCO reference manual and CanoDraw for Windows User’s guide: software for Canonical Community Ordination (version 4.5). Ithaca, NY, USA: Microcomputer Power.
  • Truyens S, Weyens N, Cuypers A, Vangronsveld J. 2015. Bacterial seed endophytes: genera, vertical transmission and interaction with plants. Environ Microbiol Reports. 7:40–50.
  • Wang B, Seiler JR, Mei C. 2016. A microbial endophyte enhanced growth of switchgrass under two drought cycles improving leaf physiology and leaf development. Environ Exp Bot. 122:100–108.
  • Waqas M, Khan AL, Muhammad K, Kamran M, Hamayun M, Kang SM, Kim YH, Jung HY, Lee JH, Lee IJ. 2012. Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules. 17:10754–10773.
  • Weilharter A, Mitter B, Shin MV, Chain PS, Nowak J, Sessitsch A. 2011. Complete genome sequence of the plant growth-promoting endophyte Burkholderia phytofirmans strain PsJN. J Bacteriol. 193:3383–3384.
  • Zhu JK. 2001. Plant salt tolerance. Trends Plant Sci. 6:66–71.
  • Zohary D, Hopf M. 2000. Domestication of plants in the world. 3rd ed. New York: Oxford University Press.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.