Impact of a natural soil salinity gradient on fungal endophytes in wild barley (Hordeum maritimum With.)

  • Haifa Hammami
  • Paula BaptistaEmail author
  • Fátima Martins
  • Teresa Gomes
  • Chedly Abdelly
  • Ouissal Metoui-Ben Mahmoud
Original Paper


Occurrence and distribution pattern of fungal endophytes in different tissues of halophytic plants across saline depressions are poorly studied. We investigated the endophytic fungal communities inhabiting roots, stems and leaves of Hordeum maritimum collected in a soil salinity gradient, i.e. non-saline, slightly saline and saline, using a culture-dependent approach. A total of 20 taxa belonging to Ascomycota phylum were identified by ITS rRNA gene sequence. Pyronema domesticum and Alternaria spp. were the most frequently isolated. Roots host higher diversity and were more frequently colonized by endophytes than aboveground organs. Endophytic composition of all organs surveyed differed according to salinity gradient. Contrary to expectations, the colonization rate of roots increased with soil salinity, indicating that under salt stress the endophyte-plant association is promoted. All the isolates exhibited in vitro saline tolerance, especially those belonging to genera Xylaria, Chalastospora, Alternaria and Pyronema. Fungal tolerance to NaCl under in vitro conditions appears to be more dependent on the isolates than on the sites of their isolation, suggesting that under natural conditions other factors, beyond soil salinity, should be taken into account. These findings highlight the importance of fungal endophytes in the protection and/or adaptation of both interacting species (plant-fungus) to salt stress under natural conditions.

Graphical Abstract


Endophytic communities Halophytes Saline depression Similarity Tolerance index 



This work is funded by the Foundation for Science and Technology–FCT–in the scope of the Transnational Cooperation Portugal–Tunisia project nº 6818 and partially by FEDER through the Operational Competitiveness Program–COMPETE–and by national funds through FCT–in the scope of the project PTDC/AGR-PRO/4354/2012.

Supplementary material

11274_2016_2142_MOESM1_ESM.docx (20 kb)
Supplementary material 1 (DOCX 19 kb)


  1. Bray JR, Curtis JT (1957) An ordination of the upland forest communities of southern Wisconsin. Ecol Monogr 27:325–349CrossRefGoogle Scholar
  2. Bulgarelli D, Schlaeppi K, Spaepen S, van Themaat EVL, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838CrossRefGoogle Scholar
  3. Clarke J (1993) Non-parametric multivariate analyses of changes in community structure. Aust J Ecol 18:117–143CrossRefGoogle Scholar
  4. Clarke KR, Gorley RN (2015) PRIMER v7: User Manual/Tutorial. PRIMER-E, PlymouthGoogle Scholar
  5. El-Morsy EM (2000) Fungi isolated from the endorhizosphere of halophytic plants from the Red Sea Coast of Egypt. Fungal Divers 5:43–54Google Scholar
  6. FAO (1988) Salt-affected soils and their management. FAO Soils Bull. 39. FAO, Rome, ItalyGoogle Scholar
  7. Frohlich-Nowoisky J, Burrows SM, Xie Z et al (2012) Biogeography in the air: fungal diversity over land and oceans. Biogeosciences 9:1125–1136CrossRefGoogle Scholar
  8. Gunde-Cimerman N, Zalar P (2014) Extremely Halotolerant and Halophilic Fungi Inhabit Brine in Solar Salterns Around the Globe. Food Technol Biotech 52:170–179Google Scholar
  9. Gunde-Cimerman N, Ramosb J, Plemenitas A (2009) Halotolerant and halophilic fungi. Mycol Res 113:1231–1241CrossRefGoogle Scholar
  10. Hafsi C, Lakhdhar A, Rabhi M, Debez A, Abdelly C, Ouerghi Z (2007) Interactive effects of salinity and potassium availability on growth, water status, and ionic composition of Hordeum maritimum. J Plant Nutr Soil Sci 170:469–473CrossRefGoogle Scholar
  11. Henderson PA, Seaby RMH (2007) Community Analysis Package 4.0. Pisces Conservation Ltd, Lymington, UKGoogle Scholar
  12. Kannan KP, Kumar DM, Ramya PR, Nika SM, Meenatchi G, Sowmya AN, Bhuvaneswari S (2014) Diversity of endophytic fungi from salt tolerant plants. Int J ChemTech Res 6:4084–4088Google Scholar
  13. Khan AL, Hamayun M, Ahmad N, Hussain J, Kang SM, Kim YH, Adnan M, Tang DS, Waqas M, Radhakrishnan R, Hwang YH, Lee IJ (2011) Salinity stress resistance offered by endophytic fungal interaction between Penicillium minioluteum LHL09 and glycine max. L J Microbiol Biotechnol 21:893–902CrossRefGoogle Scholar
  14. Khan AL, Waqas M, Khan AR, Hussain J, Kang SM, Gilani SA, Hamayun M, Shin JH, Kamran M, Al-Harrasi A, Yun BW, Adnan M, Lee IJ (2013) Fungal endophyte Penicillium janthinellum LK5 improves growth of ABA-deficient tomato under salinity. World J Microbiol Biotechnol 29:2133–2144CrossRefGoogle Scholar
  15. Kralj Kuncic M, Kogej T, Drobne D, Gunde-Cimerman N (2010) Morphological response of the halophilic fungal genus Wallemia to high salinity. Appl Environ Microbiol 76:329–337CrossRefGoogle Scholar
  16. Lindow SE, Brandl MT (2003) Microbiology of the phyllosphere. Appl Environ Microbiol 69:1875–1883CrossRefGoogle Scholar
  17. Lombardi T, Lupi B (2006) Salt-tolerance in wild Hordeum (poaceae) species: differences between H. maritimum with. and H. hystrix roth. Atti Soc tosc Sci nat, Mem, Serie B 113:31–35Google Scholar
  18. Maciá-Vicente JG, Ferraro V, Burruano S, Lopez-Llorca LV (2012) Fungal assemblages associated with roots of halophytic and non-halophytic plant species vary differentially along a salinity gradient. Microb Ecol 64:668–679CrossRefGoogle Scholar
  19. Magurran AE (2004) Measuring Biological Diversity. Blackwell, HobokenGoogle Scholar
  20. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681CrossRefGoogle Scholar
  21. Oliveira I, Pereira JA, Lino-Neto T, Bento A, Baptista P (2012) Fungal diversity associated to the olive moth, Prays oleae Bernard: a survey for potential entomopathogenic fungi. Microb Ecol 63:964–974CrossRefGoogle Scholar
  22. Plemenitaš A, Lenassi M, Konte T, Kejžar A, Zajc J, Gostinčar C, Gunde-Cimerman N (2014) Adaptation to high salt concentrations in halotolerant/halophilic fungi: a molecular perspective. Front Microbiol 5:199Google Scholar
  23. Rabhi M, Hafsi C, Lakhdar A, Hajji S, Barhoumi Z, Hamrouni MH, Abdelly C, Smaoui A (2009) Evaluation of the capacity of three halophytes to desalinize their rhizosphere as grown on saline soils under nonleaching conditions. Afr J Ecol 47:463–468CrossRefGoogle Scholar
  24. Redman RS, Kim YO, Woodward CJDA, Greer C, Espino L, Doty SL, Rodriguez RJ (2011) Increased fitness of rice plants to abiotic stress via habitat adapted symbiosis: a strategy for mitigating impacts of climate change. PLoS ONE 6:e14823CrossRefGoogle Scholar
  25. Rodriguez RJ, Henson J, Van Volkenburgh E, Hoy M, Wright L, Beckwith F, Kim YO, Redman RS (2008) Stress tolerance in plants via habitat-adapted symbiosis. ISME J 2:404–416CrossRefGoogle Scholar
  26. Rodriguez RJ, Woodward CS, Redman RS (2012) Fungal Influence on Plant Tolerance to stress. In: Southworth D, Wiley J & Sons (ed) Biocomplexity of Plant-Fungal Interactions. Wiley-Blackwell, Hoboken, pp 155-164Google Scholar
  27. Seaby RM, Henderson PA (2006) Species Diversity and Richness Version 4Google Scholar
  28. Shrivastava P, Kumar R (2015) Soil salinity: a serious environmental issue and plant growth promoting bacteria as one of the tools for its alleviation. Saudi J Biol Sci 22:123–131CrossRefGoogle Scholar
  29. Smallwood MF, Calvert CM, Bowles DJ (1999) Plant Responses to Environmental Stress. BIOS Scientific Publishers Limited, OxfordGoogle Scholar
  30. Sun Y, Wang Q, Lu XD, Okane I, Kakishima M (2011) Endophytic fungi associated with two Suaeda species growing in alkaline soil in China. Mycosphere 2:239–248Google Scholar
  31. Suryanarayanan TS, Kumaresan V (2000) Endophytic fungi of some halophytes from an estuarine mangrove forest. Mycol Res 104:1465–1467CrossRefGoogle Scholar
  32. Tedersoo L, Bahram M, Toots M et al (2014) Global diversity and geography of soil fungi. Science 346:1256688CrossRefGoogle Scholar
  33. Wang F, Li A, Dai D, Xu X, Li D (2013) New halotolerant species of Alternaria from Qinghai-Tibet Plateau, China. Mycotaxon 123:251–253CrossRefGoogle Scholar
  34. Waqas M, Khan AL, Kamran M, Hamayun M, Kang SM, Kim YH, Lee IJ (2012) Endophytic fungi produce gibberellins and indoleacetic acid and promotes host-plant growth during stress. Molecules 17:10754–10773CrossRefGoogle Scholar
  35. Wearn JA, Sutton BC, Morley NJ, Gange AC (2012) Species and organ specificity of fungal endophytes in herbaceous grassland plants. J Ecol 100:1085–1092CrossRefGoogle Scholar
  36. White TJ, Bruns T, Lee S, Taylor J (1990) Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: Innis MA, Gelfand DH, Sninsky JJ, White TJ (eds) PCR Protocols: A guide to Methods and Applications. Academic Press, San Diego, pp 315–322Google Scholar
  37. Yancey PH (2005) Organic osmolytes as compatible, metabolic and counteracting cytoprotectants in high osmolarity and other stresses. J Exp Biol 208:2819–2830CrossRefGoogle Scholar
  38. Yensen NP (2008) Halophyte uses for the twenty-first century. In: Khan MA, Weber DJ (eds) Ecophysiology of High Salinity Tolerant Plants. Springer, Dordrecht, pp 367–396Google Scholar
  39. You YH, Yoon H, Kang SM, Shin JH, Choo YS, Lee IJ, Lee JM, Kim JG (2012) Fungal diversity and plant growth promotion of endophytic fungi from Six halophytes in Suncheon bay. J Microbiol Biotechnol 22:1549–1556CrossRefGoogle Scholar
  40. Zajc J, Kogej T, Galinski EA, Ramos J, Gunde-Cimerman N (2014) The osmoadaptation strategy of the most halophilic fungus, Wallemia ichthyophaga, growing optimally at salinities above 15% NaCl. Appl Environ Microbiol 80:247–256CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2016

Authors and Affiliations

  • Haifa Hammami
    • 1
  • Paula Baptista
    • 2
    Email author
  • Fátima Martins
    • 2
  • Teresa Gomes
    • 2
  • Chedly Abdelly
    • 1
  • Ouissal Metoui-Ben Mahmoud
    • 1
  1. 1.Laboratoire des Plantes ExtrêmophilesCentre de Biotechnologie de Borj-CédriaHammam-LifTunisia
  2. 2.REQUIMTE-LAQV, School of AgriculturePolytechnic Institute of BragançaBragançaPortugal

Personalised recommendations