Skip to main content
Log in

Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

It is documented that some plant-growth-promoting rhizobacteria (PGPR) enhance plant salt tolerance. However, as to how PGPR may influence two crucial components of plant salt tolerance such as, root hydraulic characteristics and aquaporin regulation has been almost unexplored. Here, maize (Zea mays L.) plants were inoculated with a Bacillus megaterium strain previously isolated from a degraded soil and characterized as PGPR. Inoculated plants were found to exhibit higher root hydraulic conductance (L) values under both unstressed and salt-stressed conditions. These higher L values in inoculated plants correlated with higher plasma membrane type two (PIP2) aquaporin amount in their roots under salt-stressed conditions. Also, ZmPIP1;1 protein amount under salt-stressed conditions was higher in inoculated leaves than in non-inoculated ones. Hence, the different regulation of PIP aquaporin expression and abundance by the inoculation with the B. megaterium strain could be one of the causes of the different salt response in terms of root growth, necrotic leaf area, leaf relative water content and L by the inoculation treatment.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7

Similar content being viewed by others

Abbreviations

L :

Root hydraulic conductance

PGPR:

Plant-growth-promoting rhizobacteria

PIP:

Plasma membrane aquaporins

References

  • Alguacil MM, 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 58:942–951

    Article  CAS  Google Scholar 

  • Aroca R, Ruiz-Lozano JM (2009a) Induction of tolerance to semi-arid environments by beneficial soil microorganisms––a review. In: Lichtfouse E (ed) Sustainable agriculture reviews 2. Climate change, intercropping, pest control and beneficial microorganisms. Springer, Dordrecht, pp 121–136

    Chapter  Google Scholar 

  • Aroca R, Ruiz-Lozano JM (2009b) Root water transport under abiotic stress conditions. In: Devane RT (ed) New plant physiology research. Nova Science Publisher, New York, pp 97–110

    Google Scholar 

  • Aroca R, Vernieri P, Irigoyen JJ, Sánchez-Díaz M, Tognoni F, Pardossi A (2003) Involvement of abscisic acid in leaf and root of maize (Zea mays L.) in avoiding chilling-induced water stress. Plant Sci 165:671–679

    Article  CAS  Google Scholar 

  • Aroca R, Amodeo G, Fernández-Illescas S, Herman EM, Chaumont F, Chrispeels MJ (2005) The role of aquaporins and membrane damage in chilling and hydrogen peroxide induced changes in the hydraulic conductance of maize roots. Plant Physiol 137:341–353

    Article  CAS  PubMed  Google Scholar 

  • Aroca R, Ferrante A, Vernieri P, Chrispeels MJ (2006) Drought, abscisic acid and transpiration rate effects on the regulation of PIP aquaporins gene expression and abundance in Phaseolus vulgaris plants. Ann Bot 98:1301–1310

    Article  CAS  PubMed  Google Scholar 

  • 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 173:808–816

    Article  CAS  PubMed  Google Scholar 

  • Bashan Y, Salazar B, Puente ME (2009) Responses of native legume desert trees used for reforestation in the Sonoran Desert to plant growth-promoting microorganisms in screen house. Biol Fertil Soil 45:655–662

    Article  Google Scholar 

  • Benabdellah K, Ruiz-Lozano JM, Aroca R (2009) Hydrogen peroxide effects on root hydraulic properties and plasma membrane aquaporin regulation in Phaseolus vulgaris. Plant Mol Biol 70:647–661

    Article  CAS  PubMed  Google Scholar 

  • Benes SE, Aragües R, Grattan SR, Austin RB (1996a) Foliar and root absorption of Na+ and Cl in maize and barley: implications for salt tolerance screening and the use of saline sprinkler irrigation. Plant Soil 180:75–86

    Article  CAS  Google Scholar 

  • Benes SE, Aragües R, Austin RB, Grattan SR (1996b) Brief pre- and post-irrigation sprinkling with freshwater reduces foliar salt uptake in maize and barley sprinkler irrigated with saline water. Plant Soil 180:87–95

    Article  CAS  Google Scholar 

  • Boursiac Y, Chen S, Luu DT, Sorieul M, Van den Dries N, Maurel C (2005) Early effects of salinity on water transport in Arabidopsis roots. Molecular and cellular features of aquaporin expression. Plant Physiol 139:790–805

    Article  CAS  PubMed  Google Scholar 

  • Cassaniti C, Leonardi C, Flowers TJ (2009) The effects of sodium chloride on ornamental shrubs. Sci Hortic 122:586–593

    Article  CAS  Google Scholar 

  • Chaumont F, Barrieu F, Wojcik E, Chrispeels MJ, Jung R (2001) Aquaporins constitute a large and highly divergent protein family in maize. Plant Physiol 125:1206–1215

    Article  CAS  PubMed  Google Scholar 

  • Cui H, Takeoka Y, Wada T (1995) Effect of sodium chloride on the panicle and spikelet morphogenesis in rice. I. External shoot morphology during young panicle formation. Jpn J Crop Sci 64:587–592

    CAS  Google Scholar 

  • Dabuxilatu, Ikeda M (2005) Distribution of K, Na and Cl in root and leaf cells of soybean and cucumber plants grown under salinity conditions. Soil Sci Plant Nutr 51:1053–1057

  • Dimkpa C, Weinand T, Asch F (2009) Plant-rhizobacteria interactions alleviate abiotic stress conditions. Plant Cell Environ 32:1682–1694

    Article  CAS  PubMed  Google Scholar 

  • Ferdose J, Kawasaki M, Taniguchi M, Miyake H (2009) Differential sensitivity of rice cultivars to salinity and its relation to ion accumulation and root tip structure. Plant Prod Sci 12:453–461

    Article  CAS  Google Scholar 

  • Fetter K, Van Wilder V, Moshelion M, Chaumont F (2004) Interactions between plasma membrane aquaporins modulate their water channel activity. Plant Cell 16:215–228

    Article  CAS  PubMed  Google Scholar 

  • Fricke W, Leigh RA, Tomos AD (1996) The intercellular distribution of vacuolar solutes in the epidermis and mesophyll of barley leaves changes in response to NaCl. J Exp Bot 47:1413–1426

    Article  CAS  Google Scholar 

  • Gray EJ, Smith DL (2005) Intracellular and extarcellular PGPR: commonalities and distinctions in the plant-bacterium signalling processes. Soil Biol Biochem 37:395–412

    Article  CAS  Google Scholar 

  • Gupta AB, Sankararamakrishnan R (2009) Genome-wide analysis of major intrinsic proteins in the tree plant Populus trichocarpa: characterization of XIP subfamily of aquaporins from evolutionary perspective. BMC Plant Biol 9:134

    Article  PubMed  CAS  Google Scholar 

  • Hachez C, Moshelion M, Zelazny E, Cavez D, Chaumont F (2006) Localization and quantification of plasma membrane aquaporin expression in maize primary root: a clue to understanding their role as cellular plumbers. Plant Mol Biol 62:305–323

    Article  CAS  PubMed  Google Scholar 

  • Hachez C, Heinen RB, Draye X, Chaumont F (2008) The expression pattern of plasma membrane aquaporins in maize leaves highlights their role in hydraulic regulation. Plant Mol Biol 68:337–353

    Article  CAS  PubMed  Google Scholar 

  • Javot H, Lauvergeat V, Santoni V, Martin-Laurent F, Guclu J, Vinh J, Frank KI, Schaffner AR, Bouchez D, Maurel C (2003) Role of a single aquaporin isoform in root water uptake. Plant Cell 15:509–522

    Article  CAS  PubMed  Google Scholar 

  • Johansson I, Karlsson M, Shukla VK, Chrispeels MJ, Larsson C, Kjellbom P (1998) Water transport activity of the plasma membrane aquaporin PM28A is regulated by phosphorylation. Plant Cell 10:451–459

    Article  CAS  PubMed  Google Scholar 

  • Kawasaki S, Borchert C, Deyholos M, Wang H, Brazille S, Kwai K, Galbraith D, Bohnert HJ (2001) Gene expression profiles during the initial phase of salt stress in rice. Plant Cell 13:889–905

    Article  CAS  PubMed  Google Scholar 

  • Kay R, Chau A, Daly M (1987) Duplication of CaMV 35S promoter sequences creates a strong enhancer for plants genes. Science 236:1299–1302

    Article  CAS  PubMed  Google Scholar 

  • Kohler J, Hernández JA, Caravaca F, Roldán A (2009) Induction of antioxidant enzymes is involved in the greater effectiveness of a PGPR versus AM fungi with respect to increasing the tolerance of lettuce to severe salt stress. Environ Exp Bot 65:245–252

    Article  CAS  Google Scholar 

  • Liddycoat SM, Greenberg BM, Wolyn DJ (2009) The effect of plant growth-promoting rhizobacteria on asparagus seedlings and germinating seeds subjected to water stress under green house conditions. Can J Microbiol 55:388–394

    Article  CAS  PubMed  Google Scholar 

  • Lin WL, Peng YH, Li GW, Arora R, Tang ZC, Su WA, Cai WM (2007) Isolation and functional characterization of PgTIP1 a hormone-autotrophic cell-specific tonoplast aquaporin in ginseng. J Exp Bot 58:947–956

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−Ct method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lugtenberg B, Kamilova F (2009) Plant-growth promoting rhizobacteria. Annu Rev Microbiol 63:541–556

    Article  CAS  PubMed  Google Scholar 

  • Martínez-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 160:689–697

    Article  PubMed  Google Scholar 

  • Martínez-Ballesta MC, Silva C, López-Berenguer C, Cabañero FJ, Carvajal M (2006) Plant aquaporins: new perspectives on water and nutrient uptake in saline environments. Plant Biol 8:535–546

    Article  PubMed  CAS  Google Scholar 

  • Marulanda A, Barea JM, Azcón R (2009) Stimulation of plant growth and drought tolerance by native microorganisms (AM fungi and bacteria) from dry environments: mechanisms related to bacterial effectiveness. J Plant Growth Regul 28:115–124

    Article  CAS  Google Scholar 

  • Marulanda-Aguirre A, Azcón R, Ruiz-Lozano JM, Aroca R (2008) Differential effects of a Bacillus megaterium strain on Lactuca sativa plant growth depending on the origin of the arbuscular mycorrhizal fungus coinoculated: physiologic and biochemical traits. J Plant Growth Regul 27:10–18

    Article  CAS  Google Scholar 

  • Maurel C, Verdoucq L, Luu DT, Santoni V (2008) Plant aquaporins: membrane channels with multiple integrated functions. Annu Rev Plant Biol 59:595–624

    Article  CAS  PubMed  Google Scholar 

  • Mut P, Bustamante C, Martínez G, Alleva K, Sutka M, Civello M, Amadeo G (2008) A fruit-specific plasma membrana aquaporin subtype PIP1;1 is regulated during strawberry (Fragaria x ananassa) fruit ripening. Physiol Plant 132:538–551

    Article  CAS  PubMed  Google Scholar 

  • 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 53:1141–1149

    Article  CAS  PubMed  Google Scholar 

  • Pan B, Bai YM, Leibovitch S, Smith DL (1999) Plant-growth-promoting rhizobacteria and kinetin as ways to promote corn growth and yield in a short-growing-season area. Eur J Agron 11:179–186

    Article  CAS  Google Scholar 

  • Postaire O, Tournaire-Roux C, Grondin A, Boursiac Y, Morillon R, Schäffner AR, Maurel C (2010) A PIP1 aquaporin contributes to hydrostatic pressure-induced water transport in both the root and rosette of Arabidopsis. Plant Physiol 152:1418–1430

    Article  CAS  PubMed  Google Scholar 

  • Quian YL, Whilhem SJ, Marcum KB (2001) Comparative responses of two Kentucky bluegrass cultivars to salinity stress. Crop Sci 41:1895–1900

    Article  Google Scholar 

  • Rincon A, Valladares F, Gimeno TE, Pueyo JJ (2008) Water stress responses of two Mediterranean tree species influenced by native soil microorganisms and inoculation with a plant growth promoting rhizobacterium. Tree Physiol 28:1693–1701

    CAS  PubMed  Google Scholar 

  • Ruiz-Lozano JM, Alguacil MM, Bárzana G, Vernieri P, Aroca R (2009) Exogenous ABA accentuates the differences in root hydraulic properties between mycorrhizal and non mycorrhizal maize plants through regulation of PIP aquaporins. Plant Mol Biol 70:565–579

    Article  CAS  PubMed  Google Scholar 

  • Ryan PR, Dessaux Y, Thomashow LS, Weller DM (2009) Rhizosphere engineering and management for sustainable agriculture. Plant Soil 321:363–383

    Article  CAS  Google Scholar 

  • Sade N, Gebretsadik M, Seligmann R, Schwartz A, Wallach R, Moshelion M (2010) The role of tobacco Aquaporin1 in improving water use efficiency, hydraulic conductivity, and yield production under salt stress. Plant Physiol 152:245–254

    Article  CAS  PubMed  Google Scholar 

  • Sarig S, Okon Y, Blum A (1992) Effect of Azospirillum brasilense inoculation on growth dynamics and hydraulic conductivity of Shorgum bicolour roots. J Plant Nutr 15:805–819

    Article  Google Scholar 

  • Siefritz F, Tyree MY, Lovisolo C, Schubert A, Kaldenhoff R (2002) PIP1 plasma membrane aquaporins in tobacco: from cellular effects to function in plants. Plant Cell 14:869–876

    Article  CAS  PubMed  Google Scholar 

  • Silva C, Martínez V, Carvajal M (2008) Osmotic versus toxic effects of NaCl on pepper plants. Biol Plant 52:72–79

    Article  CAS  Google Scholar 

  • Staiger D, Zecca L, Kirk DAW, Apel K, Eckstein L (2003) The circadian clock regulated RNA-binding protein AtGRP7 autoregulates its expression by influencing alternative splicing of its own pre-mRNA. Plant J 33:361–371

    Article  CAS  PubMed  Google Scholar 

  • Tyree MT, Velez V, Dalling JV (1998) Growth dynamics of root and shoot hydraulic conductance in seedlings of five neotropical tree species: scaling to show possible adaptation to differing light regimes. Oecologia 114:293–298

    Article  Google Scholar 

  • Uehlein N, Lovisolo C, Siefritz F, Kaldenhoff R (2003) The tobacco aquaporin NtAQP1 is a membrane CO2 pore with physiological functions. Nature 425:734–737

    Article  CAS  PubMed  Google Scholar 

  • Uehlein N, Otto B, Hanson DT, Fischer M, McDowell N, Kaldenhoff R (2008) Function of Nicotiana tabacum aquaporins as chloroplast gas pores challenges the concept of membrane CO2 permeability. Plant Cell 20:648–657

    Article  CAS  PubMed  Google Scholar 

  • Van Wilder V, Miecielica U, Degand H, Derua R, Waelkens E, Chaumont F (2008) Maize plasma membrane aquaporins belonging to the PIP1 and PIP2 subgroups are in vivo phosphorylated. Plant Cell Physiol 49:1364–1377

    Article  PubMed  CAS  Google Scholar 

  • Vázquez MM, César S, Azcón R, Barea JM (2000) Interactions between arbuscular mycorhizal fungi and other microbial inoculants (Azospirillum, Pseudomonas, Trichoderma) and their effects on microbial population and enzyme activities in the rhizosphere of maize plants. Appl Soil Ecol 15:261–272

    Article  Google Scholar 

  • Vessey JK (2003) Plant growth promoting rhizobacteria as biofertilizers. Plant Soil 255:571–586

    Article  CAS  Google Scholar 

  • Wang Y, Li K, Li X (2009) Auxin redistribution modulates plastic development of root system architecture under salt stress in Arabidopsis thaliana. J Plant Physiol 166:1637–1645

    Article  CAS  PubMed  Google Scholar 

  • Werner M, Uehlein N, Proksch P, Kaldenhoff R (2001) Characterization of two tomato aquaporins and expression during the incompatible interaction of tomato with the plant parasite Cuscuta reflexa. Planta 213:550–555

    Article  CAS  PubMed  Google Scholar 

  • Zelazny E, Borst JW, Muylaert M, Batoko H, Hemminga MA, Chaumont F (2007) FRET imaging in living maize cells reveals that plasma membrane aquaporins interact to regulate their subcellular localization. Proc Natl Acad Sci USA 104:12359–12364

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

Authors thank Prof. M. Carvajal (Centro de Edafología y Biología Aplicada del Segura, CSIC, Murcia, Spain) for the analyses of plant mineral contents. Also, authors thank Mr. José Antonio Paz for his technical assistant during the experiments. F. Chaumont was supported by grants from the Belgian National Fund for Scientific Research (FNRS), the Interuniversity Attraction Poles Programme–Belgian Science Policy, and the “Communauté française de Belgique–Actions de Recherches Concertées”.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Ricardo Aroca.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Marulanda, A., Azcón, R., Chaumont, F. et al. Regulation of plasma membrane aquaporins by inoculation with a Bacillus megaterium strain in maize (Zea mays L.) plants under unstressed and salt-stressed conditions. Planta 232, 533–543 (2010). https://doi.org/10.1007/s00425-010-1196-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-010-1196-8

Keywords

Navigation