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Plant function and evolutionary biology
RESEARCH ARTICLE

Improvement of salt and waterlogging tolerance in wheat: comparative physiology of Hordeum marinum-Triticum aestivum amphiploids with their H. marinum and wheat parents

Saud A. Alamri A B C , Edward G. Barrett-Lennard A B , Natasha L. Teakle A B E and Timothy D. Colmer A D F
+ Author Affiliations
- Author Affiliations

A School of Plant Biology, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

B Centre for Ecohydrology, Department of Agriculture and Food of Western Australia and The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

C Botany and Microbiology Department, College of Science Bild. 5, King Saud University, PO Box 2455 – Riyadh 11451, Kingdom of Saudi Arabia.

D Institute of Agriculture, The University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

E Present address: Graduate Research School, Edith Cowan University, 270 Joondalup Drive, Joondalup, WA 6027, Australia.

F Corresponding author. Email: timothy.colmer@uwa.edu.au

Functional Plant Biology 40(11) 1168-1178 https://doi.org/10.1071/FP12385
Submitted: 20 December 2012  Accepted: 29 April 2013   Published: 3 June 2013

Abstract

Hordeum marinum Huds. is a waterlogging-tolerant halophyte that has been hybridised with bread wheat (Triticum aestivum L.) to produce an amphiploid containing both genomes. This study tested the hypothesis that traits associated with waterlogging and salinity tolerances would be expressed in H. marinum-wheat amphiploids. Four H. marinum accessions were used as parents to produce amphiploids with Chinese Spring wheat, and their responses to hypoxic and 200 mM NaCl were evaluated. Relative growth rate (RGR) in the hypoxic-saline treatment was better maintained in the amphiploids (58–71% of controls) than in wheat (56% of control), but the amphiploids were more affected than H. marinum (68–97% of controls). In hypoxic-saline conditions, leaf Na+ concentrations in the amphiploids were lower than in wheat (30–41% lower) but were 39–47% higher than in the H. marinum parents. A strong barrier to radial oxygen loss formed in basal root zones under hypoxic conditions in two H. marinum accessions; this barrier was moderate in the amphiploids, absent in wheat, and was weaker for the hypoxic-saline treatment. Porosity of adventitious roots increased with the hypoxic treatments; values were 24–38% in H. marinum, 16–27% in the amphiploids and 16% in wheat. Overall, the amphiploids showed greater salt and waterlogging tolerances than wheat, demonstrating the expression of relevant traits from H. marinum in the amphiploids.

Additional keywords: leaf potassium, leaf sodium and chloride, Na+ exclusion, radial O2 loss, root porosity, sea barleygrass, wide hybridisation, wild Triticeae.


References

Armstrong W (1979) Aeration in higher plants. Advances in Botanical Research 7, 225–332.
Aeration in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL3cXhsVeiu7c%3D&md5=86c43c19845f9491aaed39144f6c209eCAS |

Armstrong W (1994) Polarographic oxygen electrodes and their use in plant aeration studies. Proceedings of the Royal Society of Edinburgh 102, 511–527.

Armstrong W, Wright EJ (1975) Radial oxygen loss from roots: the theoretical basis for the manipulation of flux data obtained by the cylindrical platinum electrode technique. Physiologia Plantarum 35, 21–26.
Radial oxygen loss from roots: the theoretical basis for the manipulation of flux data obtained by the cylindrical platinum electrode technique.Crossref | GoogleScholarGoogle Scholar |

Barrett-Lennard EG (2003) The interaction between waterlogging and salinity in higher plants: causes, consequences and implications. Plant and Soil 253, 35–54.
The interaction between waterlogging and salinity in higher plants: causes, consequences and implications.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVemsbk%3D&md5=a46fbd122186d4e690bf50aab4cd8500CAS |

Barrett-Lennard EG, Shabala SN (2013) The waterlogging/salinity interaction in higher plants revisited – focusing on the hypoxia-induced disturbance to K+ homeostasis. Functional Plant Biology
The waterlogging/salinity interaction in higher plants revisited – focusing on the hypoxia-induced disturbance to K+ homeostasis.Crossref | GoogleScholarGoogle Scholar | in press.

Barrett-Lennard EG, van Ratingen P, Mathie MH (1999) The developing pattern of damage in wheat (Triticum aestivum L.) due to the combined stresses of salinity and hypoxia: experiments under controlled conditions suggest a methodology for plant selection. Australian Journal of Agricultural Research 50, 129–136.
The developing pattern of damage in wheat (Triticum aestivum L.) due to the combined stresses of salinity and hypoxia: experiments under controlled conditions suggest a methodology for plant selection.Crossref | GoogleScholarGoogle Scholar |

Colmer TD (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant, Cell & Environment 26, 17–36.
Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXhtlKrtLs%3D&md5=e80503627222f82665ec0f1c8e0f2122CAS |

Colmer TD, Flowers TJ (2008) Flooding tolerance in halophytes. New Phytologist 179, 964–974.
Flooding tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtFWqurzM&md5=42000ad7cdadbc6b288c74a91150d853CAS | 18482227PubMed |

Colmer TD, Greenway H (2011) Ion transport in seminal and adventitious roots of cereals during O2 deficiency. Journal of Experimental Botany 62, 39–57.
Ion transport in seminal and adventitious roots of cereals during O2 deficiency.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFamurnE&md5=00b92cbcc1649e26a963a26ffc260d5dCAS | 20847100PubMed |

Colmer TD, Garthwaite AJ, Islam AKMR, Islam S, Malik AI, von Bothmer R (2005) ‘Salinity and waterlogging tolerance in wild Hordeum species: physiological basis and prospects for use in cereal improvement.’ pp. 8–9. (The 15th International Plant Nutrition Colloquium: Beijing, China)

Colmer TD, Flowers TJ, Munns R (2006) Use of wild relatives to improve salt tolerance in wheat. Journal of Experimental Botany 57, 1059–1078.
Use of wild relatives to improve salt tolerance in wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xis1Gls7s%3D&md5=62a57757a166a1df340760b85a38679bCAS | 16513812PubMed |

Cuin TA, Miller AJ, Laurie SA, Leigh RA (2003) Potassium activities in cell compartments of salt-grown barley leaves. Journal of Experimental Botany 54, 657–661.
Potassium activities in cell compartments of salt-grown barley leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXit1arurw%3D&md5=699c9ac06bfab18576f20730e648ad62CAS | 12554708PubMed |

Garthwaite AJ, von Bothmer R, Colmer TD (2003) Diversity in root aeration traits associated with waterlogging tolerance in the genus Hordeum. Functional Plant Biology 30, 875–889.
Diversity in root aeration traits associated with waterlogging tolerance in the genus Hordeum.Crossref | GoogleScholarGoogle Scholar |

Garthwaite AJ, von Bothmer R, Colmer TD (2005) Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl– into the shoots. Journal of Experimental Botany 56, 2365–2378.
Salt tolerance in wild Hordeum species is associated with restricted entry of Na+ and Cl into the shoots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXhtVahtLvJ&md5=7888a39cb3a91baf58cb0e41bd7a787aCAS | 16014366PubMed |

Garthwaite AJ, Armstrong W, Colmer TD (2008) Assessment of O2 diffusivity across the barrier to radial O2 loss in adventitious roots of Hordeum marinum. New Phytologist 179, 405–416.
Assessment of O2 diffusivity across the barrier to radial O2 loss in adventitious roots of Hordeum marinum.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpsVOgtL8%3D&md5=e8762e48c17745eeb7a63c1cf867cae7CAS | 19086178PubMed |

Hunt R (1978) ‘Plant growth analysis.’ (Edward Arnold Limited: London)

Islam S, Malik AI, Islam AKMR, Colmer TD (2007) Salt tolerance in a Hordeum marinum-Triticum aestivum amphiploid, and its parents. Journal of Experimental Botany 58, 1219–1229.
Salt tolerance in a Hordeum marinum-Triticum aestivum amphiploid, and its parents.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXktlWjsbs%3D&md5=fc5d5283b05f6327e24b9512a6507ac0CAS | 17283374PubMed |

Jackson MB, Armstrong W (1999) Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence. Plant Biology 1, 274–287.
Formation of aerenchyma and the processes of plant ventilation in relation to soil flooding and submergence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXjsVKjsbk%3D&md5=a44e71273b9cab84badc1a81871b11e6CAS |

Justin SHFW, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytologist 106, 465–495.
The anatomical characteristics of roots and plant response to soil flooding.Crossref | GoogleScholarGoogle Scholar |

Maas EV (1986) Salt tolerance of plants. Applied Agricultural Research 1, 12–26.

Maathuis FJM, Amtmann A (1999) K+ nutrition and Na+ toxicity: the basis of cellular K+ : Na+ ratios. Annals of Botany 84, 123–133.
K+ nutrition and Na+ toxicity: the basis of cellular K+ : Na+ ratios.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXltVCgtL4%3D&md5=ef0d422684c723bba2a783c048c48b92CAS |

Malik AI, English JP, Colmer TD (2009a) Tolerance of Hordeum marinum accessions to O2 deficiency, salinity and these stresses combined. Annals of Botany 103, 237–248.
Tolerance of Hordeum marinum accessions to O2 deficiency, salinity and these stresses combined.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXjsFCktbc%3D&md5=2dfba4634434084198c78fff1a9e2ed0CAS | 18701600PubMed |

Malik AI, English JP, Shepherd KA, Islam AKMR, Colmer TD (2009b) Tolerance of combined salinity and O2 deficiency in Hordeum marinum accessions from the grain-belt of Western Australia. In ‘The Proceedings of the International Plant Nutrition Colloquium. XVI’. p. 1277. (International Plant Nutrition Colloquium: Davis, CA, USA)

Malik AI, Islam AKMR, Colmer TD (2011) Transfer of the barrier to radial oxygen loss in roots of Hordeum marinum to wheat (Triticum aestivum): evaluation of four H. marinum-wheat amphiploids. New Phytologist 190, 499–508.
Transfer of the barrier to radial oxygen loss in roots of Hordeum marinum to wheat (Triticum aestivum): evaluation of four H. marinum-wheat amphiploids.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC3MzjvFaruw%3D%3D&md5=3f69ba52d23960194fbdcc010e980112CAS | 21054414PubMed |

McDonald MP, Galwey NW, Colmer TD (2001) Waterlogging tolerance in the tribe Triticeae: the adventitious roots of Critesion marinum have a relatively high porosity and a barrier to radial oxygen loss. Plant, Cell & Environment 24, 585–596.
Waterlogging tolerance in the tribe Triticeae: the adventitious roots of Critesion marinum have a relatively high porosity and a barrier to radial oxygen loss.Crossref | GoogleScholarGoogle Scholar |

Munns R (1993) Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses. Plant, Cell & Environment 16, 15–24.
Physiological processes limiting plant growth in saline soils: some dogmas and hypotheses.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXks1yjsr0%3D&md5=a884c868738a00c05e702ebf444e38dbCAS |

Munns R (2002) Comparative physiology of salt and water stress. Plant, Cell & Environment 25, 239–250.
Comparative physiology of salt and water stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xhslakurw%3D&md5=4b241e0ff1eba2f3fa3d1e323ab7e87aCAS |

Munns R, James RA (2003) Screening methods for salinity tolerance: a case study with tetraploid wheat. Plant and Soil 253, 201–218.
Screening methods for salinity tolerance: a case study with tetraploid wheat.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVemsbc%3D&md5=aa01ce01ce313fb5da5c0e864a48405eCAS |

Munns R, Termaat A (1986) Whole-plant responses to salinity. Functional Plant Biology 13, 143–160.

Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annual Review of Plant Physiology 59, 651–681.

Munns R, Schachtman DP, Condon AG (1995) The significance of a two-phase growth response to salinity in wheat and barley. Functional Plant Biology 22, 561–569.

Munns R, James RA, Islam AKMR, Colmer TD (2011) Hordeum marinum-wheat amphiploids maintain higher leaf K+ : Na+ and suffer less leaf injury than wheat parents in saline conditions. Plant and Soil 348, 365–377.
Hordeum marinum-wheat amphiploids maintain higher leaf K+ : Na+ and suffer less leaf injury than wheat parents in saline conditions.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXht1Gnt7rF&md5=6f27272480ca8ea88633504a4fb94b01CAS |

Pang JY, Newman I, Mendham N, Zhou M, Shabala S (2006) Microelectrode ion and O2 fluxes measurements reveal differential sensitivity of barley root tissues to hypoxia. Plant, Cell & Environment 29, 1107–1121.
Microelectrode ion and O2 fluxes measurements reveal differential sensitivity of barley root tissues to hypoxia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlvFakuro%3D&md5=5affc3f281b1dc9ac2dbe520e72dc874CAS |

Rogers ME, Colmer TD, Nichols PGH, Hughes SJ, Frost K, Cornwall D, Chandra S, Miller SM, Craig AD (2011) Salinity and waterlogging tolerance amongst accessions of Messina (Melilotus siculus). Crop and Pasture Science 62, 225–235.
Salinity and waterlogging tolerance amongst accessions of Messina (Melilotus siculus).Crossref | GoogleScholarGoogle Scholar |

Rubio F, Schwarz M, Gassmann W, Schroeder JI (1999) Genetic selection of mutations in the high affinity K+ transporter HKT1 that define functions of a loop site for reduced Na+ permeability and increased Na+ tolerance. The Journal of Biological Chemistry 274, 6839–6847.
Genetic selection of mutations in the high affinity K+ transporter HKT1 that define functions of a loop site for reduced Na+ permeability and increased Na+ tolerance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvFWru78%3D&md5=3b362129d8a22206eb62881bde6fa0e2CAS | 10066736PubMed |

Setter TL, Waters I (2003) Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. Plant and Soil 253, 1–34.
Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXltVemsb4%3D&md5=8d47390dedc71a36d2502276db14066eCAS |

Szabolcs I (1994) Soils and salinization. In ‘Handbook of plant and crop stress’. (Ed. M Pessarakali) pp. 3–11. (Marcel Dekkar: New York)

Tester M, Davenport R (2003) Na+ tolerance and Na+ transport in higher plants. Annals of Botany 91, 503–527.
Na+ tolerance and Na+ transport in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsVyisbk%3D&md5=88eb811f9dc3f2cd8aa877eaee28c69dCAS | 12646496PubMed |

Thomson CJ, Armstrong W, Waters I, Greenway H (1990) Aerenchyma formation and associated oxygen movement in seminal and nodal roots of wheat. Plant, Cell & Environment 13, 395–403.
Aerenchyma formation and associated oxygen movement in seminal and nodal roots of wheat.Crossref | GoogleScholarGoogle Scholar |

von Bothmer R, Jacobsen N, Baden C, Jorgensen RB, Linde-Laursen I (1991) ‘An ecogeographical study of the genus Hordeum. Systematic and ecogeographic studies on crop genepools. Vol. 7’. pp. 73–78. (International Board for Plant Genetic Resources: Rome)

Wiengweera A, Greenway H (2004) Performance of seminal and nodal roots of wheat in stagnant solution: K+ and P uptake and effects of increasing O2 partial pressures around the shoot on nodal root elongation. Journal of Experimental Botany 55, 2121–2129.
Performance of seminal and nodal roots of wheat in stagnant solution: K+ and P uptake and effects of increasing O2 partial pressures around the shoot on nodal root elongation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnsVyit74%3D&md5=ea45a5cd97644ac78f0ff3c5bd111ac4CAS | 15310817PubMed |

Wiengweera A, Greenway H, Thomson CJ (1997) The use of agar nutrient solution to simulate lack of convection in waterlogged soils. Annals of Botany 80, 115–123.
The use of agar nutrient solution to simulate lack of convection in waterlogged soils.Crossref | GoogleScholarGoogle Scholar |