Log in

Tolerance of wheat to vegetative stage soil waterlogging is conditioned by both constitutive and adaptive QTL

  • Published:
Euphytica Aims and scope Submit manuscript

Abstract

Soil waterlogging is a primary constraint to crop yield both globally and in the United States, yet little is known about the genetic control of waterlogging tolerance in wheat. The objective of this study was to characterize genetic variation for key adaptive traits influencing waterlogging tolerance at the vegetative stage and to identify associated quantitative trait loci (QTL). Traits measured included shoot and root biomass, root length, tiller number, seedling height, stem elongation, and chlorophyll content. Waterlogging reduced traits means by 8–58 % in the greenhouse and by 22–32 % in the field, with the largest reduction observed for root length. Both root biomass and root length showed significant genotype by treatment interaction indicating an adaptive growth response in waterlogged versus non-waterlogged soils and a possible mechanism of tolerance. A positive correlation was observed between chlorophyll content and shoot biomass, and between root and shoot biomass under waterlogging, which may make indirect selection possible. QTL analysis identified 48 individual QTL that clustered into 10 genomic regions consistently detected in both the greenhouse and field experiments. While most clusters were constitutively expressed, regions on chromosomes 1B and 6D were found to be adaptive to conditions of soil waterlogging, with no QTL detected in the non-waterlogged controls. A QTL region on chromosome 1D specific for chlorophyll content was significant across environments and repeated measurements, explaining up to 24 % of the phenotypic variation. This study provides the first reported QTL for waterlogging tolerance in wheat identified under both field and greenhouse conditions. The QTL can be targeted by breeders for future genetic improvement.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3

Similar content being viewed by others

Abbreviations

QTL:

Quantitative trait locus

RIL:

Recombinant inbred line

FTI:

Flooding tolerance index

PCA:

Principal component analysis

WGH:

Greenhouse waterlogging

CGH:

Greenhouse control

WF:

Field waterlogging

CF:

Field control

References

  • Armstrong W (1979) Aeration in higher plants. In: Woolhouse HW (ed) Advances in botanical research. Academic Press Inc., New York, pp 225–332

    Google Scholar 

  • Bacon RK, Kelly JT, Milus GA (1998) Registration of ‘Jaypee’ Wheat. Crop Sci 38:1723

    Article  Google Scholar 

  • Bai C, Liang Y, Hawkesford MJ (2013) Identification of QTLs associated with seedling root traits and their correlation with plant height in wheat. J Exp Bot 64:1745–1753

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Bailey-Serres J, Voesenek LACJ (2008) Flooding Stress: acclimations and Genetic Diversity. Annu Rev Plant Biol 59:313–339

    Article  CAS  PubMed  Google Scholar 

  • Barrett-Lennard EG (2003) The interaction between waterlogging and salinity in higher plants: causes, consequences and implications. Plant Soil 253:35–54

    Article  CAS  Google Scholar 

  • Boru G, van Ginkel M, Kronstad WE, Boersma L (2001) Expression and inheritance of tolerance to waterlogging stress in wheat. Euphytica 117:91–98

    Article  Google Scholar 

  • Brisson N, Rebiere B, Zimmer D, Renault P (2002) Response of the root system of a winter wheat crop to waterlogging. Plant Soil 243:43–55

    Article  CAS  Google Scholar 

  • Christianson JA, Llewellyn DJ, Dennis ES, Wilson IW (2010) Global gene expression responses to waterlogging in roots and leaves of cotton (Gossypium hirsutum L.). Plant Cell Physiol 51:21–37

    Article  CAS  PubMed  Google Scholar 

  • Collaku A, Harrison SA (2002) Losses in wheat due to waterlogging. Crop Sci 42:444–450

    Article  Google Scholar 

  • Colmer TD, Greenway H (2011) Ion transport in seminal and adventitious roots of cereals during O2 deficiency. J Exp Biol 62:39–57

    CAS  Google Scholar 

  • Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Funct Plant Biol 36:665–681

    Article  Google Scholar 

  • Cornelious B, Chen P, Chen Y, De Leon N, Shannon JG, Wang D (2005) Identification of QTLs underlying waterlogging tolerance in soybean. Mol Breed 16:103–112

    Article  Google Scholar 

  • Dickin E, Bennett S, Wright D (2009) Growth and yield responses of UK wheat cultivars to winter waterlogging. J Agric Sci 147:127–140

    Article  Google Scholar 

  • Gardner WK, Flood RG (1993) Less waterlogging damage with long season wheats. Cereal Res Commun 21:337–343

    Google Scholar 

  • Griffiths S, Simmonds J, Leverington M, Wang Y, Fish L, Sayers L, Alibert L, Orford S, Wingen L, Snape J (2012) Meta-QTL analysis of the genetic control of crop height in elite European winter wheat germplasm. Mol Breed 29:159–171

    Article  Google Scholar 

  • Hall MD, Tucker D, Griffey CA, Liu S, Sneller C, Guttieri M, Van Sanford D, Costa J, Marshall D, Brown-Guedira GL (2010) Registration of USG 3209/Jaypee wheat recombinant inbred line map** population. J Plant Regist 4:159–162

    Article  Google Scholar 

  • Huang B, Johnson JW, NeSmith DS, Bridges DC (1994a) Root and shoot growth of wheat genotypes in response to hypoxia and subsequent resumption of aeration. Crop Sci 34:1538–1544

    Article  Google Scholar 

  • Huang B, Johnson JW, Nesmith S, Bridges DC (1994b) Growth, physiological and anatomical responses of two wheat genotypes to waterlogging and nutrient supply. J Exp Bot 45:193–202

    Article  Google Scholar 

  • Justin SHFW, Armstrong W (1987) The anatomical characteristics of roots and plant response to soil flooding. New Phytol 106:465–495

    Article  Google Scholar 

  • Kato K, Miura H, Sawada S (1999) QTL map** of genes controlling ear emergence time and plant height on chromosome 5A of wheat. Theor Appl Genet 98:472–477

    Article  CAS  Google Scholar 

  • Lee T, Jang C, Kim J, Seong R, Kim I, Kim D, Seo Y (2007a) Expressed sequence tags from wheat roots under hypoxia. Russ J Plant Physiol 54:659–668

    Article  CAS  Google Scholar 

  • Lee TG, Jang CS, Kim JY, Kim DS, Park JH, Kim DY, Seo YW (2007b) A Myb transcription factor (TaMyb1) from wheat roots is expressed during hypoxia: roles in response to the oxygen concentration in root environment and abiotic stresses. Physiol Plant 129:375–385

    Article  CAS  Google Scholar 

  • Li H, Vaillancourt RE, Mendham N, Zhou M (2008) Comparative map** of quantitative trait loci associated with waterlogging tolerance in barley (Hordeum vulgare L.). BMC Genom 9:401

    Article  Google Scholar 

  • Lopes MS, Reynolds MP (2010) Partitioning of assimilates to deeper roots is associated with cooler canopies and increased yield under drought in wheat. Funct Plant Biol 37:147–156

    Article  Google Scholar 

  • Malik AI, Colmer TD, Lambers H, Schortemeyer M (2001) Changes in physiological and morphological traits of roots and shoots of wheat in response to different depths of waterlogging. Funct Plant Biol 28:1121–1131

    Article  Google Scholar 

  • Malik AI, Colmer TD, Lambers H, Setter TL, Schortemeyer M (2002) Short-term waterlogging has long-term effects on the growth and physiology of wheat. New Phytol 153:225–236

    Article  Google Scholar 

  • Mano Y, Omori F, Muraki M, Takamizo T (2005) QTL map** of adventitious root formation under flooding conditions in tropical maize (Zea mays L.) seedlings. Breed Sci 55:343–347

    Article  Google Scholar 

  • Mano Y, Muraki M, Takamizo T (2006) Identification of QTL controlling flooding tolerance in reducing soil conditions in maize (Zea mays L.) seedlings. Plant Prod Sci 9:176–181

    Article  CAS  Google Scholar 

  • Mason RE, Mondal S, Beecher F, Pacheco A, Jampala B, Ibrahim A, Hays DB (2010) QTL associated with heat susceptibility index in wheat (Triticum aestivum L.) under short-term reproductive stage heat stress. Euphytica 174:423–436

    Article  Google Scholar 

  • Mehlich A (1984) Mehlich 3 soil test extractant: a modification of Mehlich 2 extractant. Commun Soil Sci Plant Anal 15:1409–1416

    Article  CAS  Google Scholar 

  • Meyer WS, Barrs HD (1988) Response of wheat to single short-term waterlogging during and after stem elongation. Aust J Agric Res 39:11–20

    Article  Google Scholar 

  • Musgrave ME, Ding N (1998) Evaluating wheat cultivars for waterlogging tolerance. Crop Sci 38:90–97

    Article  Google Scholar 

  • NRCS (2013) “Stuttgart” the Arkansas State Soil. February 14 2013 edn. Natural resources conservation service (NRCS). http://www.ar.nrcs.usda.gov/soils/state_soil.html, p 1

  • Paux E, Sourdille P, Salse J, Saintenac C, Choulet F, Leroy P, Korol A, Michalak M, Kianian S, Spielmeyer W, Lagudah E, Somers D, Kilian A, Alaux M, Vautrin S, Berges H, Eversole K, Appels R, Safar J, Simkova H, Dolezel J, Bernard M, Feuillet C (2008) A physical map of the 1-gigabase bread wheat chromosome 3B. Science 322:101–104

    Article  CAS  PubMed  Google Scholar 

  • Qiu F, Zheng Y, Zhang Z, Xu S (2007) Map** of QTL associated with waterlogging tolerance during the seedling stage in maize. Ann Bot 99:1067–1081

    Article  PubMed Central  PubMed  Google Scholar 

  • Rebetzke GJ, Ellis MH, Bonnett DG, Richards RA (2007) Molecular map** of genes for coleoptile growth in bread wheat (Triticum aestivum L.). Theor Appl Genet 114:1173–1183

    Article  CAS  PubMed  Google Scholar 

  • Rocha M, Licausi F, Araújo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT (2010) Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 152:1501–1513

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Setter TL, Waters I (2003) Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. Plant Soil 253:1–34

    Article  CAS  Google Scholar 

  • Shabala S (2011) Physiological and cellular aspects of phytotoxicity tolerance in plants: the role of membrane transporters and implications for crop breeding for waterlogging tolerance. New Phytol 190:289–298

    Article  CAS  PubMed  Google Scholar 

  • St. Burgos M, Messmer MM, Stamp P, Schmid JE (2001) Flooding tolerance of spelt (Triticum spelta L.) compared to wheat (Triticum aestivum L.)—A physiological and genetic approach. Euphytica 122:287–295

    Article  Google Scholar 

  • Thomson CJ, Colmer TD, Watkin ELJ, Greenway H (1992) Tolerance of wheat (Triticum aestivum cvs Gamenya and Kite) and triticale (Triticosecale cv. Muir) to waterlogging. New Phytol 120:335–344

    Article  Google Scholar 

  • Too**da T, Siangliw M, Tragoonrung S, Vanavichit A (2003) Molecular genetics of submergence tolerance in rice: QTL analysis of key traits. Ann Bot 91:243–253

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • USDA (1998) Catalogue of gene symbols for wheat http://wheat.pw.usda.gov/engages/wag/98/Contents

  • VanToai TT, St. Martin SK, Chase K, Boru G, Schnipke V, Schmitthenner A, Lark KG (2001) Identification of a QTL associated with tolerance of soybean to soil waterlogging. Crop Sci 41:1247–1252

    Article  Google Scholar 

  • Voorrips RE (2002) MapChart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Basten CJ, Zeng ZB (2007) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh, NC

  • Yu M, Chen G-Y (2013) Conditional QTL map** for waterlogging tolerance in two RILs populations of wheat. SpringerPlus 2:1–7

    Article  Google Scholar 

  • Zhou M (2011) Accurate phenoty** reveals better QTL for waterlogging tolerance in barley. Plant Breed 130:203–208

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by the Agriculture and Food Research Initiative competitive Grant #2012-67013-19436 of the USDA National Institute of Food and Agriculture and the Arkansas Center for Plant Powered Production (P3) funded through the RII: Arkansas ASSET Initiatives (AR EPSCoR) I (EPS-0701890) and II (EPS-1003970) by the National Science Foundation and the Arkansas Science and Technology Authority to Esten Mason. Preliminary data for this study was supported by a grant from the Arkansas Wheat Promotion Board.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to R. Esten Mason.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ballesteros, D.C., Mason, R.E., Addison, C.K. et al. Tolerance of wheat to vegetative stage soil waterlogging is conditioned by both constitutive and adaptive QTL. Euphytica 201, 329–343 (2015). https://doi.org/10.1007/s10681-014-1184-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10681-014-1184-3

Keywords

Navigation