, 214:220 | Cite as

Screening of diverse tall fescue population for salinity tolerance based on SSR marker-physiological trait association

  • Erick Amombo
  • Xiaoning Li
  • Guangyang Wang
  • Shugao Fan
  • An Shao
  • Yinkun Zhang
  • Jinmin FuEmail author


Soil salinity is a notorious abiotic stress which constrains plant growth and limits crop productivity. Recent advances in phytogenetics especially the discovery of marker-trait association have facilitated the efficient selection of stress-tolerant crops. The objective of this study was to evaluate tall fescue (Festuca arundinacea Schreb.) accessions growing under salt stress in order to identify salt-tolerant and salt-sensitive genotypes using physiological and molecular markers. The population consisted of 114 diverse tall fescue accessions which were assessed using 99 simple sequence repeat (SSR) markers and five functional physiological traits i.e., turf quality, leaf water content, chlorophyll content, relative growth rate, and evapotranspiration rate. Salinity stress induced great variations among the functional physiological traits and there were significant correlations among them. The population structure analysis revealed two distinct populations, while association mapping between the SSRs and phenotypic traits identified significant associations. In addition, the accessions that maintained relatively higher physiological traits had a significantly lower accumulation of Na+ and Cl in the roots compared to those whose functional traits declined. We identified six most salt-tolerant accessions due to their high values of physiological parameters and significantly low accumulation of Na+ and Cl in the roots. Similarly, we identified six accessions we considered to be most salt-sensitive as observed by high Na+ and Cl accumulation plus a decline in the physiological activities. Our findings are helpful to tall fescue breeders with a goal of producing tall fescue cultivars with enhanced salt tolerance.


Tall fescue Salt stress Functional traits Association mapping Population structure 



This work was funded by the China National Science Foundation (NSFC) (Grant Nos. 31470363 and 31772662. We thank Dr Li Huiying and Xie Yan for their advice during data analysis.

Supplementary material

10681_2018_2281_MOESM1_ESM.xlsx (690 kb)
Supplementary material 1 (XLSX 690 kb)


  1. Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399PubMedCrossRefGoogle Scholar
  2. Aranda R, Syvertsen JP (1996) The influence of foliar-applied urea nitrogen and saline solutions on net gas exchange of citrus leaves. J Am Soc Hortic Sci 121:501–506Google Scholar
  3. Bajaj D, Saxena M, Kujur S, Das A, Badoni S, Tripathi S, Hari DU, Gowda CL, Shivali S, Sube S, Tyagi AK, Parida SK (2015) Genome-wide conserved non-coding microsatellite (CNMS) marker-based integrative genetical genomics for quantitative dissection of seed weight in chickpea. J Exp Bot 66:1271–1290PubMedCrossRefGoogle Scholar
  4. Banach K, Banach AM, Lamers LP, De Kroon H, Bennicelli RP, Antoine JM, Eric JW (2009) Differences in flooding tolerance between species from two wetland habitats with contrasting hydrology—implications for vegetation development in future floodwater retention areas. Ann Bot 103:341–351PubMedCrossRefGoogle Scholar
  5. Bettany AJ, Dalton E, Timms SJ, Morris P (1998) Stability of transgene expression during vegetative propagation of protoplast-derived tall fescue (Festuca arundinacea Schreb.) plants. J Exp Bot 49:1797–1804CrossRefGoogle Scholar
  6. Blum T, Soni A, Winggae M (1999) Growth and water-use efficiency of 10 Triticum aestivum cultivars at different water availability in relation to allocation of biomass. Plant, Cell Environ 20:200–210Google Scholar
  7. Bowman DC, Cramer GR, Devitt DA (2006) Effect of salinity and nitrogen status on nitrogen uptake by tall fescue turf. J Plant Nutr 29:1481–1490CrossRefGoogle Scholar
  8. Bradbury PJ, Zhang Z, De Kroon H, Casstevens TM, Ramdoss Y, Ramdoss Y, Buckler S (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23:2633–2635PubMedCrossRefGoogle Scholar
  9. Buckler ES, Thornsberry JM (2002) Plant molecular diversity and applications to genomics. Curr Opin Plant Biol 5:107–111PubMedCrossRefGoogle Scholar
  10. Buckner RC, Powel JB, Frakes RV (1979) Tall fescue: historical development. In: Buckner RC, Bush LP (eds) ASA, CSSA, and SSSA Editions, Agronomy and Monogronomy. Madison, pp 31–39Google Scholar
  11. Cao YJ, Wei Q, Liao Y, Song HL, Li X, Xiang CB, Kuai BK (2009) Ectopic overexpression of AtHDG11 in tall fescue resulted in enhanced tolerance to drought and salt stress. Plant Cell Rep 2028:579–588CrossRefGoogle Scholar
  12. Carrow RN, Duncan RR (1998) Salt-affected turfgrass sites: assessment and management. Ann Arbor Press, ChelseaGoogle Scholar
  13. Chen W, Gao Y, Xie W, Gong L, Lu K, Wang W, Li Y, Liu X, Zhang H, Dong H, Zhang W, Zhang L, Yu S, Wang G, Lian S, Luo J (2014) Genome-wide association analyses provide genetic and biochemical insights into natural variation in rice metabolism. Nat Genet 46:714–721PubMedCrossRefGoogle Scholar
  14. Dean DE, Devitt DA, Verchick LS, Morris RL (1996) Turfgrass quality, growth, and water use influenced by salinity and water stress. Agron J 88:844–849CrossRefGoogle Scholar
  15. Deokar AL, Ramsay A, Sharpe G, Diapari M, Sindhu A (2014) Genome-wide SNP identification in chickpea for use in the development of a high-density genetic map and improvement of the chickpea reference genome assembly. BMC Genomics 15:708–713PubMedPubMedCentralCrossRefGoogle Scholar
  16. Doyle JJ (1991) DNA protocols for plants: CTAB total DNA isolation. In: Hewitt GM, Johnston A (eds) Molecular techniques in taxonomy. Springer, Berlin, pp 283–293CrossRefGoogle Scholar
  17. Epstein E (1980) Responses of plants to saline environments. In: Rains DW, Valentine RC, Hollaender A (eds) Genetic engineering of osmoregulation. Plenum Press, New York, pp 7–21CrossRefGoogle Scholar
  18. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2618CrossRefGoogle Scholar
  19. FAO (2000) Global network on integrated soil management for sustainable use of salt-affected soils.
  20. Fu J, Huang B (2001) Involvement of antioxidant and lipid peroxidation in the adaptation of two cool-season grasses to localized drought stress. Environ Expt Bot 45:105–114CrossRefGoogle Scholar
  21. Gao Y, Li D (2014) Growth responses of tall fescue (Festuca arundinacea Schreb.) to salinity stress. Eur J Hortic Sci 79:123–128Google Scholar
  22. Gitelson AA, Gritz U, Merzlyak MN (2003) Relationships between leaf chlorophyll content and spectral reflectance and algorithms for non-destructive chlorophyll assessment in higher plant leaves. J Plant Physiol 160:271–282PubMedCrossRefGoogle Scholar
  23. Gorham J, Wyn RG, Bristol A (1990) Partial characterization of the trait for enhanced K+–Na+ discrimination in the d genome of wheat. Planta 180:590–597PubMedCrossRefGoogle Scholar
  24. Greenway H, Munns R (1980) Mechanisms of salt tolerance in non-halophytes. Annu Rev Plant Physiol Plant Mol Biol 31:149–190CrossRefGoogle Scholar
  25. Gupta B, Huang B (2014) Mechanism of salinity tolerance in plants: physiological, biochemical, and molecular characterization. Int J Genomics. PubMedPubMedCentralCrossRefGoogle Scholar
  26. Ha SB, Wu FS, Thorn TK (1992) Transgenic turf type tall fescue (Festuca arundinacea) plants regenerated from protoplasts. Plant Cell Rep 11:601–604PubMedCrossRefGoogle Scholar
  27. Hasegawa PM, Bressan RA, Zhu JK, Bohnert HJ (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Biol 51:463–499CrossRefGoogle Scholar
  28. Henry T, James AR, Humphreys MW (1999) Effects of water stress on leaf growth in tall fescue, Italian ryegrass and their hybrid: rheological properties of expansion zones of leaves, measured on growing and killed tissue. J Exp Bot 331:221–231Google Scholar
  29. Hu T, Li HY, Zhang XZ, Luo HJ, Fu JM (2011) Toxic effect of NaCl on ion metabolism, antioxidative enzymes and gene expression of perennial ryegrass. Ecotoxicol Environ Saf 77:2050–2056CrossRefGoogle Scholar
  30. Hu T, Chen K, Hu L, Amombo E, Fu J (2016) H2O2 and Ca2+-based signaling and associated ion accumulation, antioxidant systems, and secondary metabolism orchestrate the response to NaCl stress in perennial ryegrass. Sci Rep. PubMedPubMedCentralCrossRefGoogle Scholar
  31. Huang B, Fry JD (1998) Root anatomical, morphological, and physiological responses to drought stress for tall fescue cultivars. Crop Sci 38:1017–1022CrossRefGoogle Scholar
  32. Huang B, Gao H (1999) Physiological responses of diverse tall fescue cultivars to drought stress. HortScience 34:897–901Google Scholar
  33. Huang N, MewMagpantay A, McCouch G, Guider-doni S, Xu J, Subudhi P, Angeles ER, Khush GS (1997) RFLP mapping of isozymes, RAPD and QTLs for grain shape, brown planthopper resistance in a doubled haploid rice population. Mol Breed 3:105–113CrossRefGoogle Scholar
  34. Kaiser WM (1987) Effects of water deficit on photosynthetic capacity. Physiol Plant 71:142–149CrossRefGoogle Scholar
  35. Khan MA, Shirazi MU, Khan MA, Mujtaba SM, Islam E, Mumtaz S, Shereen A, Ansari RU, Ashraf MY (2009) Role of proline, K/Na ratio and chlorophyll content in salt tolerance of wheat (Triticum aestivum L.). Pakistan J Bot 41:633–638Google Scholar
  36. Kuai B, Dalton SJ, Bettany AJ (1999) Regeneration of fertile transgenic tall fescue plants with stable highly expressed foreign gene. Plant Cell, Tissue Organ Cult 58:149–154CrossRefGoogle Scholar
  37. Leksungnoen N, Paul G, Roger KK (2012) Physiological responses of turfgrass species to drought stress under high desert conditions. HortScience 47:105–111Google Scholar
  38. Lou Y, Hu L, Chen L, Sun X, Yang Y, Liu H (2015) Association analysis of simple sequence repeats (SSR) markers with agronomic traits in tall fescue (Festuca arundinacea Schreb.). PLoS ONE 10:7–18Google Scholar
  39. Ma DM, Xu W, Li HW, Jin FX, Guo LN, Wang DJ, Xu X (2014) Co-expression of the Arabidopsis SOS genes enhances salt tolerance in transgenic tall fescue (Festuca arundinacea Schreb.). Protoplasma 251:219–231PubMedCrossRefGoogle Scholar
  40. Medrano HT, Magdalena S, Martorell F, Jaume E, Hernández J, Rossell A, Pou JM, Bota J (2015) From leaf to whole-plant water use efficiency (WUE) in complex canopies: Limitations of leaf WUE as a selection target. Crop J 3:220–228CrossRefGoogle Scholar
  41. Mian M, Hopkins A, Zwonitzer J (2002) Determination of genetic diversity in tall fescue with AFLP markers. Crop Sci 42:944–950CrossRefGoogle Scholar
  42. Molazem D, Qurbanov EM, Dunyamaliyev SA (2010) Role of proline, Na and chlorophyll content in salt tolerance of corn (Zea mays L.). Am Eurasian J Agric Environ Sci 9:319–324Google Scholar
  43. Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell Environ 28:239–250CrossRefGoogle Scholar
  44. Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  45. Munns R, Richard A, Lauchli A (2006) Approaches to increasing the salt tolerance of wheat and other cereals. J Exp Bot 57:1025–1043PubMedCrossRefGoogle Scholar
  46. Nawaz K, Hussain K, Majeed A, Khan F, Afghan S, Ali K (2010) Fatality of salt stress to plants: morphological, physiological and biochemical aspects. Afr J Biotechnol 9:5475–5480Google Scholar
  47. Norris IB, Thomas H (1982) Variation in growth of varieties and ecotypes of Lolium, Dactylis and Festuca exposed to drought conditions. J Appl Ecol 19:881–889CrossRefGoogle Scholar
  48. Poehlman JM, Sleper DA (1995) Breeding field crops, 5th edn. Wiley-Blackwell. ISBN: 978-0-8138-2428-4 424Google Scholar
  49. Qian YL, Fry JD, Upham WS (1997) Rooting and drought avoidance of warm-season turfgrasses and tall fescue in Kansas. Crop Sci 37:905–910CrossRefGoogle Scholar
  50. Richardson AD, Duigan SP, Berlyn GP (2002) An evaluation of non-invasive methods to estimate foliar chlorophyll content. New Phytol 153:185–194CrossRefGoogle Scholar
  51. Robredo A, López P, Maza U, González-Moro H, Lacuesta B, Mena-Petite M, Alberto MR (2007) Elevated CO2 alleviates the impact of the drought on barley improving water status by lowering stomatal conductance and delaying its effects on photosynthesis. Environ Exp Bot 59:252–263CrossRefGoogle Scholar
  52. Rose-Flicker CA, Fraser MI, Meyer WA, Funk CR (1999) Registration of ‘Gold’ Colorado tall fescue. Crop Sci 39:288Google Scholar
  53. Roylance JT, Hill NS, Parrott WA (1994) Detection of somaclonal variation in tissue culture regenerants of tall fescue. Crop Sci 39:288–289Google Scholar
  54. Saha MC, Mian J, Zwonitzer CK, Chekhovskiy AH (2005) An SSR- and AFLP-based genetic linkage map of tall fescue (Festuca arundinacea Schreb.). Theor Appl Genet 110:323–336PubMedCrossRefGoogle Scholar
  55. Saha MC, Cooper JD, Mian MR (2006) Tall fescue genomic SSR markers: development and transferability across multiple grass species. Theor Appl Genet 8:1449–1458CrossRefGoogle Scholar
  56. Seemann JR, Critchley C (1985) Effects of salt stress on the growth, ion contents, stomatal behaviour and photosynthetic capacity of a salt sensitive species. Phaseolus vulgaris L. Planta 164:66–69CrossRefGoogle Scholar
  57. Shearman R, Morris KN (1996) National zoysiagrass test-1991. Final report NTEP No. 96-15Google Scholar
  58. Singh KN, Chatrath R (2001) Salinity tolerance. In: Reynolds MP, Ortiz-Monasterio JJ, McNab A (eds) Application of physiology in wheat breeding. CIMMYT, MexicoGoogle Scholar
  59. Sukumaran S, Xiang W, Bean S, Jeffrey F, Stephen P, Mitchell K (2012) Association mapping for grain quality in a diverse sorghum collection. Plant Genome 5:126–135CrossRefGoogle Scholar
  60. Sun X, Zhimin D, Jin R, Fu J (2015a) Association of SSR markers with functional traits from heat stress in diverse tall fescue accessions. BMC Plant Biol 15:116PubMedPubMedCentralCrossRefGoogle Scholar
  61. Sun X, Xie Y, Bi Y, Liu J, Amombo E, Hu T, Fu J (2015b) Comparative study of diversity based on heat tolerant-related morpho-physiological traits and molecular markers in tall fescue accessions. Sci Rep 5:18213PubMedPubMedCentralCrossRefGoogle Scholar
  62. Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Ann Bot 91:503–527PubMedPubMedCentralCrossRefGoogle Scholar
  63. Tian M, Yoshie E, Chou L, Roe J, Paula X, Michael D (2009) Candidate gene association mapping of Arabidopsis flowering time. Genetics 183:325–335CrossRefGoogle Scholar
  64. Tuteja N (2007) Mechanisms of high salinity tolerance in plants. Methods Enzymol 428:419–438PubMedCrossRefGoogle Scholar
  65. Upadhyaya HD, Bajaj D, Narnoliya L, Das S, Kumar V (2016) Genome-wide scans for delineation of candidate genes regulating seed-protein content in chickpea. Front Plant Sci 7:302PubMedPubMedCentralCrossRefGoogle Scholar
  66. Volenec JJ, Nelson CJ (1981) Cell dynamics in leaf meristems of contrasting tall fescue genotypes. Crop Sci 21:381–385CrossRefGoogle Scholar
  67. Wang Z, Hopkins A, Mian R (2001) Forage and turfgrass biotechnology. Crit Rev Plant Sci 20:573–619CrossRefGoogle Scholar
  68. Watkins ES, Fei D, Gardner J, Stier S, Bughrarali D (2011) Low-input turfgrass species for the North Central United States. Appl Turfgrass Sci. CrossRefGoogle Scholar
  69. Xu WW, Sleper DA, Chao S (1995) Genome mapping of polyploidy tall fescue (Festuca arundinacea Shcreb.) with RFLP markers. Theor Appl Genet 91:9347–9955Google Scholar
  70. Yadav RK, Sigh SP, Lal D, Kumar A (2007) Fodder production and soil health with conjunctive use of saline and good quality water in ustipsamments of a semi-arid region. Land Degrad Dev 18:153–161CrossRefGoogle Scholar
  71. Yan J, Warburton M, Crouch J (2011) Association mapping for enhancing maize (Zea mays L.) genetic improvement. Crop Sci 51:433–449CrossRefGoogle Scholar
  72. Yan H, Yu Z, Zeng B, Yin G, Zhang X, Ji Y (2016) Genetic diversity and association of EST-SSR and SCoT markers with rust traits in orchardgrass (Dactylis glomerata L.). Molecules 21:66–69PubMedCrossRefGoogle Scholar
  73. Yu X, Guihua B, Na L, Zhenbang C, Shuwei L, Jianxiu L (2011) Association of simple sequence repeats (SSR) markers with submergence tolerance in diverse populations of perennial ryegrass. Plant Sci 4:391–398CrossRefGoogle Scholar
  74. Zhao J, Zhi D, Xue Z, Liu H, Xia G (2007) Enhanced salt tolerance of transgenic progeny of tall fescue (Festuca arundinacea) expressing a vacuolar Na+/H+ antiporter gene from arabidopsis. J Plant Physiol 164:1377–1383PubMedCrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Erick Amombo
    • 1
  • Xiaoning Li
    • 1
  • Guangyang Wang
    • 1
  • Shugao Fan
    • 2
  • An Shao
    • 2
  • Yinkun Zhang
    • 2
  • Jinmin Fu
    • 2
    Email author
  1. 1.Key Laboratory of Plant Germplasm Enhancement and Specialty Agriculture, Wuhan Botanical GardenThe Chinese Academy of ScienceWuhanChina
  2. 2.Coastal Salinity Tolerant Grass Engineering and Technology Research CenterLudong UniversityYantaiChina

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