Journal of Applied Genetics

, Volume 57, Issue 2, pp 151–163 | Cite as

Regions of the bread wheat D genome associated with variation in key photosynthesis traits and shoot biomass under both well watered and water deficient conditions

  • Svetlana OsipovaEmail author
  • Alexey Permyakov
  • Marina Permyakova
  • Tatyana Pshenichnikova
  • Vasiliy Verkhoturov
  • Alexandr Rudikovsky
  • Elena Rudikovskaya
  • Alexandr Shishparenok
  • Alexey Doroshkov
  • Andreas Börner
Plant Genetics • Original Paper


A quantitative trait locus (QTL) approach was taken to reveal the genetic basis in wheat of traits associated with photosynthesis during a period of exposure to water deficit stress. The performance, with respect to shoot biomass, gas exchange and chlorophyll fluorescence, leaf pigment content and the activity of various ascorbate-glutathione cycle enzymes and catalase, of a set of 80 wheat lines, each containing a single chromosomal segment introgressed from the bread wheat D genome progenitor Aegilops tauschii, was monitored in plants exposed to various water regimes. Four of the seven D genome chromosomes (1D, 2D, 5D, and 7D) carried clusters of both major (LOD >3.0) and minor (LOD between 2.0 and 3.0) QTL. A major QTL underlying the activity of glutathione reductase was located on chromosome 2D, and another, controlling the activity of ascorbate peroxidase, on chromosome 7D. A region of chromosome 2D defined by the microsatellite locus Xgwm539 and a second on chromosome 7D flanked by the marker loci Xgwm1242 and Xgwm44 harbored a number of QTL associated with the water deficit stress response.


Asc-GSH cycle enzyme activity Chlorophyll fluorescence Gas exchange Leaf pigment content QTL mapping Water deficit stress Wheat 



This research was financially supported by the Russian Foundation for Basic Research (15-04-02762). Statistical processing and analysis of dataset has been made at the expense of Russian Scientific Foundation (№14-14-00734). All experiments were carried out on the experimental basis of the Baikal Analytical Center of Collective Use “Phytotron SIFIBR SB RAS”.

Supplementary material

13353_2015_315_MOESM1_ESM.docx (19 kb)
Table S1 (DOCX 18 kb)
13353_2015_315_MOESM2_ESM.docx (19 kb)
Table S2 (DOCX 19 kb)
13353_2015_315_MOESM3_ESM.jpg (376 kb)
Fig. S1 QTL interval analysis along 1D, 2D, 4D, 5D and 7D chromosomes for physiological and biochemical traits in well-watered (WW) and water deficient conditions (WD). To the left: LOD max (3.0) is pointed with a dotted line. Separate traits are marked in different colors. Designations as in Tables 1 and 5 (JPEG 376 kb)
13353_2015_315_MOESM4_ESM.jpg (343 kb)
Fig. S1 Continuation (JPEG 342 kb)


  1. Aebi H (1984) Catalase in vitro. Methods Enzymol 105:121–126CrossRefPubMedGoogle Scholar
  2. Arraiano LS, Worland AJ, Ellenbrook C, Brown JKM (2001) Chromosomal location of a gene for resistance to Septoria tritici blotch (Mycosphaerella graminicola) in the hexaploid wheat synthetic 6x. Theor Appl Genet 103:758–764CrossRefGoogle Scholar
  3. Baier M, Noctor G, Foyer C, Dietz KJ (2000) Antisense suppression of 2-cysteine peroxiredoxin in Arabidopsis specifically enhances the activities and expression of enzymes associated with ascorbate metabolism but not glutathione metabolism. Plant Physiol 124:823–832CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bartoli CG, Guiamet JJ, Kiddle G, Pastory GM, Cagno R, Theodoulou FL, Foyer CH (2005) Ascorbate content of wheat leaves is not determined by maximal l-galactono-1,4-lactone dehydrogenase (GalLDH) activity under drought stress. Plant Cell Environ 28:1073–1081CrossRefGoogle Scholar
  5. Bencze S, Bamberger Z, Janda T, Balla K, Bedő Z, Veisz O (2011) Drought tolerance in cereals in terms of water retention, photosynthesis and antioxidant enzyme activities. Cent Eur J Biol 6:376–387Google Scholar
  6. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248--254Google Scholar
  7. Czyczylo-Mysza I, Tyrka M, Marcińska I, Skrzypek E, Karbarz M, Dziurka M, Hura T, Dziurka K, Quarrie SA (2013) Quantitative trait loci for leaf chlorophyll fluorescence parameters, chlorophyll and carotenoid contents in relation to biomass and yield in bread wheat and their chromosome deletion bin assignments. Mol Breed 32:189–210CrossRefPubMedPubMedCentralGoogle Scholar
  8. De Lamotte F, Vianey-Liaud N, Duviau M, Kobrehel K (2000) Glutathione reductase in wheat grain. 1. Isolation and characterization. J Agric Food Chem 48:4978–4983. doi: 10.1021/jf0003808 CrossRefPubMedGoogle Scholar
  9. Dospekhov BA (1985) The technique of field experiment (with the basic statistical processing of experimantsl results). Agropromizdat, MoskvaGoogle Scholar
  10. Foyer CH, Shigeoka S (2011) Understanding oxidative stress and antioxidant functions to enhance photosynthesis. Plant Physiol 155:93–100CrossRefPubMedPubMedCentralGoogle Scholar
  11. Gallie DR (2013) L-ascorbic acid: a multifunctional molecule supporting plant growth and development. Scientifica Article ID 795964, doi: 10.1155/2013/795964
  12. Giannopolitis CN, Ries SK (1977) Superoxide dismutase. 1. Occurrence in higher plants. Plant Physiol 59:309–314CrossRefPubMedPubMedCentralGoogle Scholar
  13. Hammer O, Harper DAT, Ryan PD (2001) PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron 4:9Google Scholar
  14. Huseynova IM (2012) Photosynthetic characteristics and enzymatic antioxidant capacity of leaves from wheat cultivars exposed to drought. Biochim Biophys Acta 1817:1516–1523CrossRefPubMedGoogle Scholar
  15. Ivanov BN (2014) Role of ascorbic acid in photosynthesis. Biochem Mosc 79:282–289CrossRefGoogle Scholar
  16. Jia J, Zhao S, Kong X, Li Y, Zhao G, He W, Appels R, Pfeifer M, Tao Y, Zhang X, Jing R, Zhang C, Ma Y, Gao L, Gao C et al (2013) Aegilops tauschii draft genome sequence reveals a gene repertoire for wheat adaptation. Nature 496:91–95. doi: 10.1038/nature12028 CrossRefPubMedGoogle Scholar
  17. Kiddle G, Pastori GM, Bernard S, Pignocchi C, Antoniw J, Verrier PJ, Foyer CH (2003) Effects of leaf ascorbate content on defense and photosynthesis gene expression in Arabidopsis thaliana. Antioxid Redox Signal 5:23–32CrossRefPubMedGoogle Scholar
  18. Kocsy G, Tari I, Vankova R, Zechman B, Gulyas Z, Poor P, Galiba G (2013) Redox control of plant growth and development. Plant Sci 211:77–91CrossRefPubMedGoogle Scholar
  19. Kumar S, Sehgal SK, Kumar U, Prasad PVV, Joshi AK, Gill BS (2012) Genomic characterization of drought tolerance-related traits in spring wheat. Euphytica 186:265–276CrossRefGoogle Scholar
  20. Landjeva S, Lohwasser U, Bőrner A (2010) Genetic mapping within the wheat D genome reveals QTL for germination, seed vigour and longevity, and early seedling growth. Euphytica 17:129–143. doi: 10.1007/s10681-009-0016-3 CrossRefGoogle Scholar
  21. Li WL, Faris JD, Chittoor JM, Leach JE, Hulbert SH, Liu DJ, Chen PD, Gill BS (1999) Genomic mapping of defense response genes in wheat. Theor Appl Genet 98:226–233CrossRefGoogle Scholar
  22. Liu L, Sun G, Ren X, Li C, Sun D (2015) Identification of QTL underlying physiological and morphological traits of flag leaf in barley. BMC Genet. doi: 10.1186/s12863-015-0187-y Google Scholar
  23. Makino A (2011) Photosynthesis, grain yield and nitrogen utilization in rice and wheat. Plant Physiol 155:125–129CrossRefPubMedPubMedCentralGoogle Scholar
  24. McFadden ES, Sears ER (1946) The origin of Triticumspelta and its free-threshing hexaploid relative. J Hered 37:81–89PubMedGoogle Scholar
  25. McIntyre LC, Mathews KL, Rattey A, Chapman SC, Drenth J, Ghaderi M, Reynolds M, Shorter R (2010) Molecular detection of genomic regions associated with grain yield and yield-related components in an elite bread wheat cross evaluated under irrigated and rainfed conditions. Theor Appl Genet 120:527–541CrossRefPubMedGoogle Scholar
  26. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880Google Scholar
  27. Narain P (2010) Quantitative genetics: past and present. Mol Breed 26:135–143. doi: 10.1007/s11032-010-9406-4 CrossRefGoogle Scholar
  28. Nelson JC (1997) QGENE: software for mapping – based genomic analysis and breeding. Mol Breed 3:239–245CrossRefGoogle Scholar
  29. Neuman PR, Hart GE (1986) Genetic control of the mitochondrial form of superoxide dismutase in hexaploid wheat. Biochem Genet 24:435–446CrossRefPubMedGoogle Scholar
  30. Osipova S, Permyakov A, Permyakova M, Pshenichnikova T, Börner A (2011) Leaf dehydroascorbate reductase and catalase activity is associated with soil drought tolerance in bread wheat. Acta Physiol Plant 33:2169–2177CrossRefGoogle Scholar
  31. Osipova SV, Permyakov AV, Permyakova MD, Pshenichnikova TA, Genaev MA, Börner A (2013) The antioxidant enzymes activity in leaves of inter – varietal substitution lines of 35:2455–2465. doi: 10.1007/S11738-013-1280-3
  32. Pang CH, Wang BS (2010) Role of ascorbate peroxidase and glutathione reductase in ascorbate-glutathione cycle and stress tolerance in plants. In: Anjum NA, Umar S, Chan MT (eds) Ascorbate-glutathione pathway and stress tolerance in plants. Springer, Dordrecht, pp 91–113CrossRefGoogle Scholar
  33. Panio G, Motzo R, Mastrangelo AM, Marone D, Cattivelli L, Giunta F, De Vita P (2013) Molecular mapping of stomatal-conductance-related traits in durum wheat (Triticum turgidum ssp. durum). Ann Appl Biol 162:258–270CrossRefGoogle Scholar
  34. Pestsova EG, Börner A, Röder MS (2001) Development of a set of Triticum aestivumAegilops tauschii introgression lines. Hereditas 135:139–143CrossRefPubMedGoogle Scholar
  35. Pestsova EC, Börner A, Röder MS (2006) Development and QTL assessment of Triticum aestivum-Aegilops tauschii introgression lines. Theor Appl Genet 112:634–647CrossRefPubMedGoogle Scholar
  36. Polesskaya OG, Kashirina EI, Alekhina ND (2004) Changes in the activity of antioxidant enzymes in wheat leaves and roots as a function of nitrogen form and rate in the nutrient medium. Russ J Plant Physiol 51:686–691Google Scholar
  37. Reynolds M, Foulkes MJ, Slafer GA, Berry P, Parry MA, Snape JW, Angus WJ (2009) Raising yield potential in wheat. J Exp Bot 60:1899–1918. doi: 10.1093/jxb/erp016 CrossRefPubMedGoogle Scholar
  38. Simon MR, Ayala FM, Cordo CA, Röder MS, Börner A (2007) The use of wheat/goatgrass introgression lines for the detection of gene(s) determining resistance to septoria tritici blotch (Mycosphaerella graminicola). Euphytica 154:249–254CrossRefGoogle Scholar
  39. Steinhauser M, Steinhauser D, Gibon Y, Bolger M, Arrivault S, Usadel B, Zamir D, Fernie AR, Stitt M (2011) Identification of enzyme activity quantitative trait loci in a Solanuml ycopersicum × Solanum pennellii introgression line population. Plant Physiol 157:998–1014. doi: 10.1104/pp.111.181594 CrossRefPubMedPubMedCentralGoogle Scholar
  40. Trethowan RM, Mujeeb-Kazi A (2008) Novel germplasm resources for improving environmental stress tolerance of hexaploid wheat. Crop Sci 48:1255–1265CrossRefGoogle Scholar
  41. Van Eeuwijk FA, Bink M, Chenu K, Chapman SC (2010) Detection and use of QTL for complex traits in multiple environments. Curr Opin Plant Biol 13:193–205CrossRefPubMedGoogle Scholar
  42. Verma V, Foulkes MJ, Worland AJ, Sylvester-Bradley R, Caligari PDS, Snape JW (2004) Mapping quantitative trait loci for flag leaf senescence as a yield determinant in winter wheat under optimal and drought-stressed environments. Euphytica 135:255–263CrossRefGoogle Scholar
  43. Wettstein D (1957) Chlorophyll-letale und der submikroskopische form wechsel der Plastiden. Exp Cell Res 12:427–506CrossRefGoogle Scholar
  44. Wu G, Wilen RW, Robertson AJ, Gusta LV (1999) Isolation, chromosomal localization, and differential expression of mitochondrial manganese superoxide dismutase and chloroplastic copper/zinc superoxide dismutase genes in wheat. Plant Physiol 120:513–520CrossRefPubMedPubMedCentralGoogle Scholar
  45. Yang D, Jing R, Chang X, Li W (2007) Quantitative trait loci mapping for chlorophyll fluorescence and associated traits in wheat (Triticum aestivum). J Integr Plant Biol 49:646–654CrossRefGoogle Scholar
  46. Zhang N, Gibon Y, Gur A, Chen C, Lepak N, Hohne M, Zhang Z, Kroon D, Tschoep H, Stitt M, Buckler E (2010) Fine quantitative trait loci mapping of carbon and nitrogen metabolism enzyme activities and seedling biomass in the maize IBM mapping population. Plant Physiol 154:1753–1765CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Institute of Plant Genetics, Polish Academy of Sciences, Poznan 2015

Authors and Affiliations

  • Svetlana Osipova
    • 1
    • 5
    Email author
  • Alexey Permyakov
    • 1
  • Marina Permyakova
    • 1
  • Tatyana Pshenichnikova
    • 2
  • Vasiliy Verkhoturov
    • 3
  • Alexandr Rudikovsky
    • 1
  • Elena Rudikovskaya
    • 1
  • Alexandr Shishparenok
    • 1
  • Alexey Doroshkov
    • 2
  • Andreas Börner
    • 4
  1. 1.Siberian Institute of Plant Physiology and Biochemistry SB RASIrkutskRussia
  2. 2.Institute of Cytology and Genetics SB RASNovosibirskRussia
  3. 3.National Research Irkutsk State Technical UniversityIrkutskRussia
  4. 4.Leibniz Institute of Plant Genetics and Crop Plant ResearchGaterslebenGermany
  5. 5.Irkutsk State UniversityIrkutskRussia

Personalised recommendations