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Polar Biology

, Volume 41, Issue 10, pp 1973–1982 | Cite as

Antarctic rhizobacteria improve salt tolerance and physiological performance of the Antarctic vascular plants

  • Jorge Gallardo-Cerda
  • Juana Levihuan
  • Paris Lavín
  • Romulo Oses
  • Cristian Atala
  • Cristian Torres-Díaz
  • Marely Cuba-Díaz
  • Andrea Barrera
  • Marco A. Molina-Montenegro
Original Paper
  • 201 Downloads

Abstract

The two native Antarctic vascular plants, Deschampsia antarctica and Colobanthus quitensis, are mostly restricted to coastal habitats where they are often exposed to sea spray with high levels of salinity. Most of the studies regarding the ability of C. quitensis and D. antarctica to cope with abiotic stress have been focused on their physiological adaptations to tolerate cold stress, but little is known about their tolerance to salinity. We investigated whether rhizospheric bacteria associated to D. antarctica and C. quitensis improve the ability of Antarctic plants to tolerate salt stress. Salt tolerance was assayed in rhizospheric bacteria, and also their effects on the ecophysiological performance (photochemical efficiency of PSII, growth, and survival) of both plants were assessed under salt stress. A total of eight bacterial rhizospheric strains capable of growing at 4 °C were isolated. The strains isolated from D. antarctica showed higher levels of salt tolerance than those strains isolated from C. quitensis. The ecophysiological performance of C. quitensis and D. antarctica was significantly increased when plants were inoculated with rhizospheric bacteria. Our results suggest that rhizospheric bacteria improve the ability of both plants to tolerate salinity stress with positive effects on the adaptation and survival of vascular plants to current conditions in Antarctic ecosystem.

Keywords

Salt tolerance Antarctica Plant growth-promoting rhizobacteria Colobanthus quitensis Deschampsia antarctica 

Notes

Acknowledgements

We acknowledge the financial and logistic support of the Chilean Antarctic Institute (INACH Projects: RT-14-08 and RT-11-13. This study was supported by the FONDECYT 3160333 project. This article contributes to the SCAR biological research programs: “Antarctic Thresholds—Ecosystem Resilience and Adaptation” (AnT-ERA) and “State of the Antarctic Ecosystem” (Ant-Eco). The funding was provided by CONICYT (Grant Number: PII20150126).

References

  1. Acuña-Rodríguez IS, Torres-Díaz C, Molina-Montenegro MA (2017) Asymmetric responses to simulated global warming by populations of Colobanthus quitensis along a latitudinal gradient. PeerJ 5:e3718CrossRefGoogle Scholar
  2. Ahemad M, Kibret M (2014) Mechanisms and applications of plant growth promoting rhizobacteria: current perspective. J King Saud Univ Sci 26:1–20CrossRefGoogle Scholar
  3. Alberdi M, Bravo LA, Gutierrez A, Gidekel M, Corcuera LJ (2002) Ecophysiology of Antarctic vascular plants. Physiol Plant 115:479–486CrossRefPubMedCentralGoogle Scholar
  4. Azad K, Kaminskyj S (2016) A fungal endophyte strategy for mitigating the effect of salt and drought stress on plant growth. Symbiosis 68:73–78CrossRefGoogle Scholar
  5. Bano A, Fatima M (2009) Salt tolerance in Zea mays (L). Following inoculation with Rhizobium and Pseudomonas. Biol Fertil Soils 45:405–413CrossRefGoogle Scholar
  6. Berríos G, Cabrera G, Gidekel M, Gutiérrez-Moraga A (2013) Characterization of a novel antarctic plant growth-promoting bacterial strain and its interaction with antarctic hair grass (Deschampsia antarctica Desv). Polar Biol 23:349–362CrossRefGoogle Scholar
  7. Bhuvaneswari TV, Turgeon BG, Bauer WD (1980) Early events in the infection of soybean (Glycine max L. Merr) by Rhizobium japonicum I. Localization of infectible root cells. Plant Physiol 66:1027–1031CrossRefGoogle Scholar
  8. Bohnert HJ, Nelson DE, Jensen RG (1995) Adaptations to environmental stresses. Plant Cell 7:1099CrossRefGoogle Scholar
  9. Brosius JJL, Palmer HP, Kennedy H, Noller F (1978) Complete nucleotide sequence of a 16S ribosomal RNA gene from Escherichia coli. Proc Natl Acad Sci USA 75:4801–4805CrossRefGoogle Scholar
  10. Cannone N, Guglielmin M, Convey P, Worland M, Favero-Longo S (2016) Vascular plants changes in extreme environments: effect of multiple drivers. Clim Change 134:651–665CrossRefGoogle Scholar
  11. Chakrabarty A, Aditya M, Dey N, Banik N, Bhattacharjee S (2016) Antioxidant signaling and redox regulation in drought-and salinity-stressed plants. In: Drought stress tolerance in plants, vol 1. Springer International Publishing, pp 465–498Google Scholar
  12. Chew O, Lelelan S, John UP, Spangerberg GC (2012) Cold acclimation induces rapid and dynamic changes in freeze tolerance mechanisms in the cryophile Deschampsia antarctica E. Desv. Plant Cell Environ 35:829–837CrossRefGoogle Scholar
  13. Convey P (2008) Antarctic terrestrial life—challenging the history of the frozen continent? Biol Rev 83:103–117CrossRefPubMedCentralGoogle Scholar
  14. Convey P, Chown SL, Clarke A, Barnes DKA, Cummings V, Ducklow H, Frati F, Green TGA, Gordon S, Griffiths H, Howard-Williams C, Huiskes AHL, Laybourn-Parry J, Lyons B, McMinn A, Peck LS, Quesada A, Schiaparelli S, Wall D (2014) The spatial structure of Antarctic biodiversity. Ecol Monogr 84:203–244CrossRefGoogle Scholar
  15. de Zelicourt A, Al-Yousif M, de Hirt H (2013) Rhizosphere microbes as essential partners for plant stress tolerance. Mol Plant 6:242–245CrossRefPubMedCentralGoogle Scholar
  16. Egamberdieva D, Jabborova D, Wirth S (2013) Alleviation of salt stress in legumes by co-inoculation with Pseudomonas and Rhizobium. In: Arora NK (ed) Plant microbe symbiosis—fundamentals and advances. Springer, India, pp 291–303CrossRefGoogle Scholar
  17. Egamberdieva D, Botir H, Hashem A, Abd-Allah EF (2014) Characterization of salt tolerant Enterobacter hormaechei strain associated with tomato root grown in arid saline soil. J Pure Appl Microbiol 8:4231–4239Google Scholar
  18. Egamberdieva D, Jabborova D, Hashem A (2015) Pseudomonas induces salinity tolerance in cotton (Gossypium hirsutum) and resistance to Fusarium root rot through the modulation of indole-3-acetic acid. Saudi J Biol Sci 22:773–779CrossRefGoogle Scholar
  19. ElSayed AI, Rafudeen MS, Golldack D (2014) Physiological aspects of raffinose family oligosaccharides in plants: protection against abiotic stress. Plant Biol 16:1–8CrossRefGoogle Scholar
  20. FAO (2014) The state of food insecurity in the world. Food and Agriculture Organization of the United Nations, Rome, p 55Google Scholar
  21. Fedoroff NV, Battisti DS, Beachy RN, Cooper PJM, Fischhoff DA et al (2010) Radically rethinking agriculture for the 21st century. Science 327:833–834CrossRefGoogle Scholar
  22. Fowbert JA, Smith RIL (1994) Rapid population increases in native vascular plants in the Argentine islands, Antarctic Peninsula. Arct Alp Res 26:290–296CrossRefGoogle Scholar
  23. Fox GA (1993) Failure time analysis: emergence, flowering, survivorship, and other waiting times. In: Scheiner SM, Gurevitch J (eds) Design and analysis of ecological experiments. Oxford University Press, New York, pp 253–289Google Scholar
  24. Ganzert L, Bajerski F, Mangelsdorf K, Lipski A, Wagner D (2011) Arthrobacter livingstonensis sp. nov. and Arthrobacter cryotolerans sp. nov., salt-tolerant and psychrotolerant species from Antarctic soil. Int J Syst Evol Microbiol 61:979–984CrossRefGoogle Scholar
  25. Glick BR (2014) Bacteria with ACC deaminase can promote plant growth and help to feed the world. Microbiol Res 139:30–39CrossRefGoogle Scholar
  26. Habib SH, Kausar K, Saud HM (2016) Plant growth-promoting Rhizobacteria enhance salinity stress tolerance in Okra through ROS-scavenging enzymes. Biomed Res Int.  https://doi.org/10.1155/2016/6284547 CrossRefPubMedPubMedCentralGoogle Scholar
  27. Hadi F, Bano A (2010) Effect of diazotrophs (Rhizobium and Azatebactor) on growth of maize (Zea mays L.) and accumulation of lead (Pb) in different plant parts. Pak J Bot 42:4363–4370Google Scholar
  28. Hasanuzzaman Md, Shabala L, Rodribb TJ, Zhou M, Shabala S (2017) Assessing the suitability of various screening methods as a proxy for drought tolerance in barley. Funct Plant Biol 44:253–266CrossRefGoogle Scholar
  29. Hill PW, Farrar J, Roberts P, Farrell M, Grant H, Newsham KK, Hopkins DW, Bardgett RD, Jones DL (2011) Vascular plant success in a warming Antarctic may be due to efficient nitrogen acquisition. Nat Clim Change 1:50–53CrossRefGoogle Scholar
  30. Hirt H (2009) Plant stress biology: from genomics to systems biology. Wiley, West SussexCrossRefGoogle Scholar
  31. Holtom A, Greene SW (1967) The growth and reproduction of Antarctica flowering plants. Philos Trans Soc Lond B 252:323–337CrossRefGoogle Scholar
  32. IPCC (2014) Climate change 2014: impacts, adaptation, and vulnerability. Part A: global and sectoral aspects. In: Field CB, Barros VR, Dokken DJ, Mach KJ, Mastrandrea MD, Bilir TE, Chatterjee M, Ebi KL, Estrada YO, Genova RC, Girma B, Kissel ES, Levy AN, MacCracken S, Mastrandrea PR, White LL (eds) Contribution of working group II to the fifth assessment report of the intergovernmental panel on climate change. Cambridge University Press, Cambridge and New York, p 1132Google Scholar
  33. Karthikeyan B, Joe MM, Islam MR, Sa T (2012) ACC deaminase containing diazotrophic endophytic bacteria ameliorate salt stress in Catharanthus roseus through reduced ethylene levels and induction of antioxidative defense systems. Symbiosis 56:77–86CrossRefGoogle Scholar
  34. Lee J, Noh EK, Choi H-S, Shin SC, Park H, Lee H (2013) Transcriptome sequencing of the Antarctic vascular plant Deschampsia antarctica Desv. under abiotic stress. Planta 237:823–836CrossRefPubMedCentralGoogle Scholar
  35. Liu Y, Chen L, Zhang N, Li Z, Zhang G, Xu Y, Zhang R (2016) Plant-microbe communication enhances auxin biosynthesis by a root-associated bacterium, Bacillus amyloliquefaciens SQR9. Mol Plant-Microbe Int 29:324–330CrossRefGoogle Scholar
  36. Maxwell K, Johnson GN (2000) Chlorophyll fluorescence a practical guide. J Exp Bot 51:659–668CrossRefPubMedCentralGoogle Scholar
  37. Mayak S, Tirosh T, Glick BR (2004) Plant growth-promoting bacteria confer resistance in tomato plants to salt stress. Plant Physiol Biochem 42:565–572CrossRefPubMedCentralGoogle Scholar
  38. Mbah EI, Wakil SM (2012) Elimination of bacteria from in vitro yam tissue cultures using antibiotics. J Plant Pathol 94:53–58Google Scholar
  39. Molina-Montenegro MA, Salgado-Luarte C, Oses R, Torres-Díaz C (2013) Is physiological performance a good predictor for fitness? Insights from an invasive plant species. PLoS ONE 8:e76432CrossRefGoogle Scholar
  40. Molina-Montenegro MA, Oses R, Torres-Díaz C, Atala C, Núñez MA, Armas C (2015) Fungal endophytes associated with roots of nurse cushion species have positive effects on native and invasive beneficiary plants in an alpine ecosystem. Perspect Plant Ecol 17:218–226CrossRefGoogle Scholar
  41. Molina-Montenegro MA, Galleguillos C, Oses R, Acuña-Rodríguez IS, Lavín P, Gallardo-Cerda J, Atala C (2016) Adaptive phenotypic plasticity and competitive ability deployed under a climate change scenario may promote the invasion of Poa annua in Antarctica. Biol Invasions 18:603–618CrossRefGoogle Scholar
  42. Moore DM (1970) Studies in Colobanthus quitensis (Kunth) Bartl. and Deschampsia antarctica Desv. II. Taxonomy, distribution and relationships. Brit Antarct Surv B 23:63–80Google Scholar
  43. Olave-Concha N, Bravo LA, Ruiz-Lara S, Corcuera LJ (2005) Differential accumulation of dehydrin-like proteins by abiotic stresses in Deschampsia antarctica Desv. Polar Biol 28:506–513CrossRefGoogle Scholar
  44. Ørskov J (1922) Method for the isolation of bacteria in pure culture from single cells and procedure for the direct tracing of bacterial growth on a solid medium. J Bacteriol 7:537PubMedPubMedCentralGoogle Scholar
  45. Osakabe Y, Arinaga N, Umezawa T, Katsura S, Nagamachi K, Tanaka H, Yoshimura E (2013) Osmotic stress responses and plant growth controlled by potassium transporters in Arabidopsis. Plant Cell 25:609–624CrossRefGoogle Scholar
  46. Pedranzani H, Rodríguez-Rivera M, Gutiérrez M, Porcel R, Hause B, Ruiz-Lozano JM (2016) Arbuscular mycorrhizal symbiosis regulates physiology and performance of Digitaria eriantha plants subjected to abiotic stresses by modulating antioxidant and jasmonate levels. Mycorrhiza 26:141–152CrossRefPubMedCentralGoogle Scholar
  47. Pérez-Torres E, Dinamarca J, Bravo LA, Corcuera LJ (2004) Responses of Colobanthus quitensis (Kunth) Bartl. to high light and low temperature. Polar Biol 27:183–189CrossRefGoogle Scholar
  48. Pointing SB, Büdel B, Convey P, Gillman LN, Körner C, Leuzinger S, Vincent WF (2015) Biogeography of photoautotrophs in the high polar biome. Front Plant Sci 6:692CrossRefGoogle Scholar
  49. Potvin C, Tardif S (1988) Sources of variability and experimental designs in growth chambers. Funct Ecol 2:122–130CrossRefGoogle Scholar
  50. Qin S, Zhang Y, Yuan B, Xu P, Xing K, Wang J, Jiang J (2014) Isolation of ACC deaminase-producing habitat-adapted symbiotic bacteria associated with halophyte Limonium sinense (Girard) Kuntze and evaluating their plant growth-promoting activity under salt stress. Plant Soil 374:753–766CrossRefGoogle Scholar
  51. Rajput LUBNA, Imran A, Mubeen FATHIA, Hafeez FY (2013) Salt-tolerant PGPR strain Planococcus rifietoensis promotes the growth and yield of wheat (Triticum aestivum L.) cultivated in saline soil. Pak J Bot 45:1955–1962Google Scholar
  52. Rhuland C, Krna M (2010) Effects of salinity and temperature on Deschampsia antarctica. Polar Biol 33:1007–1012CrossRefGoogle Scholar
  53. Robinson S, Wasley J, Tobin L (2003) Living on the edge—plants and global change in continental and maritime Antarctica. Glob Change Biol 9:1681–1717CrossRefGoogle Scholar
  54. Ruiz-Carrasco K, Antognoni F, Coulibaly AK, Lizardi S, Covarrubias A, Martínez EA, Zurita-Silva A (2011) Variation in salinity tolerance of four lowland genotypes of quinoa (Chenopodium quinoa Willd.) as assessed by growth, physiological traits, and sodium transporter gene expression. Plant Physiol Biochem 49:1333–1341CrossRefPubMedCentralGoogle Scholar
  55. Sairam RK, Tyagi A (2004) Physiology and molecular biology of salinity stress tolerance in plants. Curr Sci 86:407–421Google Scholar
  56. Smith RIL (1984) Terrestrial plant biology of the sub-Antarctic and Antarctic. In: Laws RM (ed) Antarctic Ecology, vol 1. Academic Press, London, pp 61–162Google Scholar
  57. Smith RIL (2003) The enigma of Colobanthus quitensis and Deschampsia antarctica in Antarctica. In: Huiskes AHL et al (eds) Antarctic biology in a global context. Backhuys Publications, Leiden, pp 234–239Google Scholar
  58. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. WH Freeman, San FranciscoGoogle Scholar
  59. Tapia-Valdebenito D, Ramirez LAB, Arce-Johnson P, Gutiérrez-Moraga A (2016) Salt tolerance traits in Deschampsia antarctica Desv. Antarct Sci 28:1–11CrossRefGoogle Scholar
  60. Thawatchai M, Seiichi T, Ratana R (2008) Impregnation of silver nanoparticles into bacterial cellulose for antimicrobial wound dressing. Carbohydr Polym 72:43–51CrossRefGoogle Scholar
  61. Wang CJ, Yang W, Wang C, Gu C, Niu DD, Liu HX, Guo JH (2012) Induction of drought tolerance in cucumber plants by a consortium of three plant growth-promoting rhizobacterium strains. PLoS ONE 7:e52565CrossRefGoogle Scholar
  62. Wang Q, Dodd IC, Belimov AA, Jiang F (2016) Rhizosphere bacteria containing 1-aminocyclopropane-1-carboxylate deaminase increase growth and photosynthesis of pea plants under salt stress by limiting Na+ accumulation. Funct Plant Biol 43:161–172CrossRefGoogle Scholar
  63. Wasley J (2006) Climate change manipulations show Antarctic flora is more strongly affected elevated nutrients than water. Glob Change Biol 12:1800–1812CrossRefGoogle Scholar
  64. Xiong FS, Ruhland TC, Day TA (1999) Photosynthetic temperature response of the Antarctic vascular plants Colobanthus quitensis and Deschampsia antarctica. Physiol Plant 106:276–286CrossRefGoogle Scholar
  65. Xiong FS, Mueller EC, Day TA (2000) Photosynthetic and respiratory acclimation and growth response of Antarctic vascular plants to contrasting temperatures regimes. Am J Bot 87:700–710CrossRefGoogle Scholar
  66. Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 53:247–273CrossRefGoogle Scholar
  67. Zhu JK (2007) Plant salt stress. Wiley, ChichesterCrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  • Jorge Gallardo-Cerda
    • 1
  • Juana Levihuan
    • 2
  • Paris Lavín
    • 3
  • Romulo Oses
    • 4
  • Cristian Atala
    • 5
  • Cristian Torres-Díaz
    • 6
  • Marely Cuba-Díaz
    • 7
  • Andrea Barrera
    • 1
  • Marco A. Molina-Montenegro
    • 1
    • 8
  1. 1.Centro de Estudios en Ecología Molecular y Funcional, Instituto de Ciencias BiológicasUniversidad de TalcaTalcaChile
  2. 2.Laboratorio de Biorrecursos AntárticosInstituto Antártico Chileno (INACH)Punta ArenasChile
  3. 3.Laboratorio de Complejidad Microbiana y Ecología FuncionalUniversidad de AntofagastaAntofagastaChile
  4. 4.Centro Regional de Investigación y Desarrollo Sustentable de Atacama (CRIDESAT). Av. Copayapu n° 485Universidad de AtacamaCopiapóChile
  5. 5.Laboratorio de Anatomía y Ecología Funcional de Plantas (AEF), Instituto de Biología, Facultad de CienciasPontificia Universidad Católica de ValparaísoValparaísoChile
  6. 6.Grupo de Biodiversidad y Cambio Global (BCG), Departamento de Ciencias BásicasUniversidad del Bío-BíoChillanChile
  7. 7.Departamento de Ciencias y Tecnología Vegetal, Campus Los ÁngelesUniversidad de ConcepciónLos ÁngelesChile
  8. 8.Centro de Estudios Avanzados en Zonas Áridas (CEAZA), Facultad de Ciencias del MarUniversidad Católica del NorteCoquimboChile

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