Applied Microbiology and Biotechnology

, Volume 90, Issue 4, pp 1389–1397 | Cite as

Response to saline stress and aquaporin expression in Azospirillum-inoculated barley seedlings

  • Myriam S. Zawoznik
  • Mayra Ameneiros
  • María P. Benavides
  • Susana Vázquez
  • María D. Groppa
Applied Microbial and Cell Physiology

Abstract

The ability of two strains of Azospirillum brasilense to mitigate NaCl stress in barley plants was evaluated. Barley seedlings were inoculated and subjected to 200 mM NaCl for 18 days. Several days after NaCl treatment, a significant decline in biomass as well as in height was observed in uninoculated plants. However, smaller reductions in biomass and height were detected in plants inoculated with strain Az39. All the stressed plants showed significantly higher Na+ but lower K+ contents in their shoots. The growth rate of uninoculated plants was adversely affected by saline treatment, which was associated with higher putrescine content and lower levels of HvPIP2;1 transcripts in the roots. Azospirillum inoculation triggered the transcription of this gene. Our results suggest that barley plants inoculated with A. brasilense may be better prepared to thrive under saline conditions. To our knowledge, this is the first report showing an effect of Azospirillum inoculation on the expression of PIP2;1, a gene involved in the synthesis of root water channels.

Keywords

Azospirillum Barley Saline stress Aquaporins Polyamines 

Notes

Acknowledgments

This work was supported by the University of Buenos Aires (UBACYT B410) and CONICET (PIP 0097). María D. Groppa and María P. Benavides are researchers at the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). We thank Ing. Agr. Alejandro Perticari (IMYZA-INTA) for providing the A. brasilense strain Az39 and Dr. José Luis López (Cátedra de Virología, FFYB, UBA) for his valuable advice on RT-PCR procedures.

References

  1. Alcázar R, Marco F, Cuevas JC, Patron M, Ferrando A, Carrasco P, Tiburcio AF, Altabella T (2006) Involvement of polyamines in plant response to abiotic stress. Biotechnol Lett 28:1867–1876CrossRefGoogle Scholar
  2. Alguacil M, Kohler J, Caravaca F, Roldán A (2009) Differential effects of Pseudomonas mendocina and Glomus intraradices on lettuce plants. Physiological response and aquaporin PIP2 gene expression under elevated atmospheric CO2 and drought. Microb Ecol 58:942–951CrossRefGoogle Scholar
  3. Aroca R, Porcel R, Ruiz-Lozano JM (2007) How does arbuscular mycorrhizal symbiosis regulate root hydraulic properties and plasma membrane aquaporins in Phaseolus vulgaris under drought, cold or salinity stresses? New Phytol 173:808–816CrossRefGoogle Scholar
  4. Barassi CA, Ayrault G, Creus CM, Sueldo RJ, Sobrero MT (2006) Seed inoculation with Azospirillum mitigates NaCl effects on lettuce. Sci Hortic 109:8–14CrossRefGoogle Scholar
  5. Bashan Y, Holguin G, de Bashan LE (2004) Azospirillum–plant relationships: physiological, molecular, agricultural, and environmental advances (1997–2003). Can J Microbiol 50:521–577CrossRefGoogle Scholar
  6. Casanovas EM, Barassi CA, Sueldo RJ (2002) Azospirillum inoculation mitigates water stress effects in maize seedlings. Cereal Res Commun 30:343–350Google Scholar
  7. Cassan F, Maiale S, Masciarelli O, Vidal A, Luna V, Ruiz O (2009) Cadaverine production by Azospirillum brasilense and its possible role in plant growth promotion and osmotic stress mitigation. Eur J Soil Biol 45:12–19CrossRefGoogle Scholar
  8. Chaumont F, Barrieu F, Jung R, Chrispeels MJ (2000) Plasma membrane intrinsic proteins from maize cluster in two sequence subgroups with differential aquaporin activity. Plant Physiol 122:1025–1034CrossRefGoogle Scholar
  9. Chaumont F, Moshelion M, Daniels MJ (2005) Regulation of plant aquaporin activity. Biol Cell 97:749–764CrossRefGoogle Scholar
  10. Creus CM, Sueldo RJ, Barassi CA (1998) Water relations in Azospirillum-inoculated wheat seedlings under osmotic stress. Can J Bot 76:238–244Google Scholar
  11. Creus CM, Sueldo RJ, Barassi CA (2004) Water relations and yield in Azospirillum-inoculated wheat exposed to drought in the field. Can J Bot 82:273–281CrossRefGoogle Scholar
  12. Cushman JC (2001) Osmoregulation in plants: implications for agriculture. Amer Zool 41:758–769CrossRefGoogle Scholar
  13. Dalla Santa OR, Hernández RF, Alvarez GLM, Ronzelli P Jr, Soccol CR (2004) Azospirillum sp. inoculation in wheat, barley and oats seeds. Greenhouse experiments. Braz Arch Biol Technol 47:843–850CrossRefGoogle Scholar
  14. Dimkpa C, Weinand T, Asch F (2009) Plant–rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694CrossRefGoogle Scholar
  15. Döbereiner J (1980) Forage grasses and grain crops. In: Bergersen FL (ed) Methods for evaluating biological nitrogen. Wiley, New York, pp 535–555Google Scholar
  16. Döbereiner J, Baldani JI, Baldani VLD (1995) Como isolar e identificar bactérias diazotróficas de plantas não-leguminosas. EMBRAPA-SPI, BrasiliaGoogle Scholar
  17. Flowers TJ (2004) Improving crop salt tolerance. J Exp Bot 55:307–319CrossRefGoogle Scholar
  18. Friedman R, Altman A, Levin N (1989) The effect of salt stress on polyamine biosynthesis and content in mung bean plants and in halophytes. Physiol Plant 76:295–302Google Scholar
  19. Groppa MD, Benavides MP (2008) Polyamines and abiotic stress: recent advances. Amino Acids 34:35–45CrossRefGoogle Scholar
  20. Hamaoui B, Abbadi JM, Burdman S, Rashid A, Sarig S, Okon Y (2001) Effects of inoculation with Azospirillum brasilense on chickpeas (Cicer arietinum) and faba beans (Vicia faba) under different growth conditions. Agronomie 21:553–560CrossRefGoogle Scholar
  21. Hamdia ABE, Shaddad MAK, Doaa MM (2004) Mechanisms of salt tolerance and interactive effects of Azospirillum brasilense inoculation on maize cultivars grown under salt stress conditions. Plant Growth Regul 44:165–174CrossRefGoogle Scholar
  22. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499CrossRefGoogle Scholar
  23. Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. Calif Agric Exp Stat Univ Calif Berkeley Circ 347:1–32Google Scholar
  24. Katsuhara M, Shibasaka M (2007) Barley root hydraulic conductivity and aquaporins expression in relation to salt tolerance. Soil Sci Plant Nutr 53:466–470CrossRefGoogle Scholar
  25. Katsuhara M, Akiyama Y, Koshio K, Shibasaka M, Kasamo K (2002) Functional analysis of water channels in barley roots. Plant Cell Physiol 43:885–893CrossRefGoogle Scholar
  26. Krishnamurthy R, Bhagwat KA (1989) Polyamines as modulators of salt tolerance in rice cultivar. Plant Physiol 91:500–504CrossRefGoogle Scholar
  27. Marjanovic Z, Uehlein N, Kaldenhoff R, Zwiazek JJ, Weib M, Hampp R, Nehls U (2005) Aquaporins in poplar: what a difference a symbiont makes! Planta 222:258–268CrossRefGoogle Scholar
  28. Martinez-Ballesta MC, Aparicio F, Pallás V, Martínez V, Carvajal M (2003) Influence of saline stress on root hydraulic conductance and PIP expression in Arabidopsis. J Plant Physiol 160:689–697CrossRefGoogle Scholar
  29. Martinez-Ballesta MC, Silva C, Lopez-Berenguer C, Cabanero FJ, Carvajal M (2006) Plant aquaporins: new challenge for water and nutrient uptake in saline environment. Plant Biol 8:535–546CrossRefGoogle Scholar
  30. Marulanda A, Azcón R, Chaumont F, Ruiz-Lozano JM, Aroca R (2010) Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L) under unstressed and salt-stressed conditions. Planta 232:533–543CrossRefGoogle Scholar
  31. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572CrossRefGoogle Scholar
  32. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Ann Rev Plant Biol 59:651–681CrossRefGoogle Scholar
  33. Munns R, Gardner PA, Tunnet ML, Rawson HM (1988) Growth and development in NaCl-treated plants. II. Do Na+ or Cl concentrations in dividing or expanding tissues determine growth in barley? Aust J Plant Physiol 15:529–540CrossRefGoogle Scholar
  34. Nadeem SM, Zahir ZA, Naveed M, Arshad M (2007) Preliminary investigations on inducing salt tolerance in maize through inoculation with rhizobacteria containing ACC deaminase activity. Can J Microbiol 53:1141–1149CrossRefGoogle Scholar
  35. Parida AK, Das AB (2005) Salt tolerance and salinity effects on plants: a review. Ecotoxicol Environ Saf 60:324–349CrossRefGoogle Scholar
  36. Pereyra MA, Zalazar CA, Barassi CA (2006) Root phospholipids in Azospirillum-inoculated wheat seedlings exposed to water stress. Plant Physiol Biochem 44:873–879CrossRefGoogle Scholar
  37. 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 75:1143–1150CrossRefGoogle Scholar
  38. Ribaudo CM, Krumpholz EM, Cassan FD, Bottini R, Cantore ML, Cura JA (2006) Azospirillum sp. promotes root hair development in tomato plants through a mechanism that involves ethylene. J Plant Growth Regul 24:175–185CrossRefGoogle Scholar
  39. Rodriguez-Kessler M, Alpuche-Solís AG, Ruiz OA, Jiménez-Bermont JF (2006) Effect of salt stress on the regulation of maize (Zea mays L.) genes involved in polyamine biosynthesis. Plant Growth Regul 48:175–185CrossRefGoogle Scholar
  40. Rodríguez-Salazar J, Suárez R, Caballero-Mellado J, Iturriaga G (2009) Trehalose accumulation in Azospirillum brasilense improves drought tolerance and biomass in maize plants. FEMS Microbiol Lett 296:52–59CrossRefGoogle Scholar
  41. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  42. Smith BN, Meeuse BJD (1966) Production of volatiles amines and skatole at anthesis in some Arum lily species. Plant Physiol 41:343–347CrossRefGoogle Scholar
  43. Taleisnik E, Grunberg K (2006) Ion balance in tomato cultivars differing in salt tolerance. I. Sodium and potassium accumulation and fluxes under moderate salinity. Physiol Plant 92:528–534CrossRefGoogle Scholar
  44. Tarrand JJ, Krieg NR, Döbereiner J (1978) A taxonomic study of the Spirillum lipoferum group, with descriptions of a new genus, Azospirillum gen. nov. and two species, Azospirillum lipoferum (Beijerinck) comb. nov. and Azospirillum brasilense sp. nov. Can J Microbiol 8:967–980CrossRefGoogle Scholar
  45. Tripathi AK, Mishra BM, Tripathi P (1998) Salinity stress responses in the plant growth promoting rhizobacteria, Azospirillum spp. J Biosci 23:463–471CrossRefGoogle Scholar
  46. Uehlein N, Fileschi K, Eckert M, Bienert G, Bertl A, Kaldenhoff R (2007) Arbuscular mycorrhizal symbiosis and plant aquaporin expression. Phytochemistry 68:122–129CrossRefGoogle Scholar
  47. Viégas RA, Silveira JAG, Lima Junior AR, Queiroz JE, Fausto MJM (2001) Effects of NaCl-salinity on growth and inorganic solute accumulation of young cashew plants. Braz J Agric Environ Eng Campina Grande 5:216–222Google Scholar
  48. Wang Q, Garrity GM, Tiedje JM, Cole JR (2007) Naïve Bayesian classifier for rapid assignment of rRNA sequences into the new bacterial taxonomy. Appl Environ Microbiol 73:5261–5267CrossRefGoogle Scholar
  49. Widodo PJH, Newbigin E, Tester M, Bacic A, Roessner U (2009) Metabolic responses to salt stress of barley (Hordeum vulgare L.) cultivars, Sahara and Clipper, which differ in salinity tolerance. J Exp Bot 60:4089–4103CrossRefGoogle Scholar
  50. Yuwono T, Handayani D, Soedarsono J (2005) The role of osmotolerant rhizobacteria in rice growth under different drought conditions. Aust J Agr Res 56:715–721CrossRefGoogle Scholar

Copyright information

© Springer-Verlag 2011

Authors and Affiliations

  • Myriam S. Zawoznik
    • 1
  • Mayra Ameneiros
    • 1
  • María P. Benavides
    • 1
  • Susana Vázquez
    • 1
  • María D. Groppa
    • 1
  1. 1.Cátedra de Química Biológica Vegetal, Facultad de Farmacia y BioquímicaUniversidad de Buenos AiresBuenos AiresArgentina

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