Skip to main content
Log in

Mapping quantitative trait loci for root development under hypoxia conditions in soybean (Glycine max L. Merr.)

  • Original Article
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

Key message

Greatest potential, QTLs for hypoxia and waterlogging tolerance in soybean roots were detected using a new phenotypic evaluation method.

Abstract

Waterlogging is a major environmental stress limiting soybean yield in wet parts of the world. Root development is an important indicator of hypoxia tolerance in soybean. However, little is known about the genetic control of root development under hypoxia. This study was conducted to identify quantitative trait loci (QTLs) responsible for root development under hypoxia. Recombinant inbred lines (RILs) developed from a cross between a hypoxia-sensitive cultivar, Tachinagaha, and a tolerant landrace, Iyodaizu, were used. Seedlings were subjected to hypoxia, and root development was evaluated with the value change in root traits between after and before treatments. We found 230 polymorphic markers spanning 2519.2 cM distributed on all 20 chromosomes (Chrs.). Using these, we found 11 QTLs for root length (RL), root length development (RLD), root surface area (RSA), root surface area development (RSAD), root diameter (RD), and change in average root diameter (CARD) on Chrs. 11, 12, 13 and 14, and 7 QTLs for hypoxia tolerance of these root traits. These included QTLs for RLD and RSAD between markers Satt052 and Satt302 on Chr. 12, which are important markers of hypoxia tolerance in soybean; those QTLs were stable between 2 years. To validate the QTLs, we developed a near-isogenic line with the QTL region derived from Iyodaizu. The line performed well under both hypoxia and waterlogging, suggesting that the region contains one or more genes with large effects on root development. These findings may be useful for fine mapping and positional cloning of gene responsible for root development under hypoxia.

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

Access this article

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

CARD:

Change in average root diameter

Chr.:

Chromosome

DAS:

Days after sowing

HTI:

Hypoxia tolerance index

LG:

Linkage group

NIL:

Near-isogenic line

QTL:

Quantitative trait loci

RD:

Root diameter

RDW:

Root dry weight

RIL:

Recombinant inbred lines

RL:

Root length

RLD:

Root length development

RSA:

Root surface area

RSAD:

Root surface area development

SDW:

Shoot dry weight

References

  • Araki H, Hossain MA, Takahashi A (2012) Waterlogging and hypoxia have permanent effects on wheat root growth and respiration. J Agron Crop Sci 198:264–275. doi:10.1111/j.1439-037X.2012.00510.x

    Article  Google Scholar 

  • Armstrong W (1980) Aeration in higher plants. Adv Bot Res 7:225–332

    Article  Google Scholar 

  • Armstrong W, Drew MC (2002) Root growth and metabolism under oxygen deficiency. In: Yoav W, Amram E, Uzi K (ed) Plant root: the hidden half 3rd edn. Marcel Dekker Inc., New York, pp 729–761

    Google Scholar 

  • Bacanamwo M, Purcell LC (1999) Soybean dry matter and N accumulation responses to flooding stress, N sources and hypoxia. J Exp Bot 50:689–696. doi:10.1093/jxb/50.334.689

    Article  CAS  Google Scholar 

  • Cho JW, Yamakawa T (2006) Effects on growth and seed yield of small soy bean cultivars of flooding conditions in paddy field. J Fac Agr Kyu Univ 52:189–193

    Google Scholar 

  • Colmer TD (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ 26:17–36. doi:10.1046/j.1365-3040.2003.00846.x

    Article  CAS  Google Scholar 

  • Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Funct Plant Biol 36:665–681. doi:10.1071/FP09144

    Article  Google Scholar 

  • Cornelious BP, Chen P, Chen N, de Leon N, Shannon JG, Wang D (2005) Identification of QTLs underlying waterlogging tolerance in soybean. Mol Breed 16:103–112. doi:10.1007/s11032-005-5911-2

    Article  Google Scholar 

  • Drew MC (1992) Soil aeration and plant root metabolism. Soil Sci 154:259–268

    Article  Google Scholar 

  • Githiri SM, WananabeS, HaradaK, Takahashi R (2006) QTL analysis of flooding tolerance in soybean at an early vegetative growth stage. Plant Breed 125:613–618. doi:10.1111/j.1439-0523.2006.01291.x

    Article  CAS  Google Scholar 

  • Henshaw TL, Gilbert RA, Scholberg JMS, Sinclair TR (2007a) Soya bean (Glycine max L. Merr.) genotype response to early-season flooding: I. root and nodule development. J Agron Crop Sci 193:177–188. doi:10.1111/j.1439-037X.2007.00257.x

  • Henshaw TL, Gilbert RA, Scholberg JMS, Sinclair TR (2007b) Soya bean (Glycine max L. Merr.) genotype response to early-season flooding: II. Aboveground growth and biomass. J Agron Crop Sci 193:189–197. doi:10.1111/j.1439-037X.2007.00258.x

  • Hisano H, Sato S, Isobe S, Sasamoto S, Wada T, Matsuo A, Fujishiro T, Yamada M, Nakayama S, Nakamura Y, Watanabe S, Harada K, Tabata S (2007) Characterization of the soybean genome using EST-derived microsatellite markers. DNA Res 14:271–281. doi:10.1093/dnares/dsm025

    Article  CAS  PubMed  Google Scholar 

  • Hossain MA, Uddin SN (2011) Mechanism of waterlogging tolerance in wheat: morphological and metabolic adaptations under hypoxia or anoxia. Aust J Crop Sci 5:1094–1101

    CAS  Google Scholar 

  • Jitsuyama Y (2015) Morphological root responses of soybean to rhizosphere hypoxia reflect waterlogging tolerance. Can J Plant Sci 95:999–1005. doi:10.4141/CJPS-2014-370

    Article  CAS  Google Scholar 

  • Kaga A, Shimizu T, Watanabe S, Tsubokura Y, Katayose Y, Harada K, Vaughan DA, Tomooka N (2012) Evaluation of soybean germplasm conserved in NIAS genebank and development of mini core collections. Breed Sci 61:566–592. doi:10.1270/jsbbs.61.566

  • Kokubun M (2013) Genetic and cultural improvement of soybean for waterlogged conditions in Asia. Field Crops Res 152:3–7. doi:10.1016/j.fcr.2012.09.022

    Article  Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow, Daly MJ, Lincoln, Newberg LA (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181. doi:10.1016/0888-7543(87)90010-3

    Article  CAS  PubMed  Google Scholar 

  • Linkemer G, Board JE, Musgrave ME (1998) Waterlogging effects on growth and yield components in late-planted soybean. Crop Sci 38:1576–1584. doi:10.2135/cropsci1998.0011183X003800060028x

    Article  CAS  PubMed  Google Scholar 

  • Mano Y, Omori F (2007) Breeding for flooding tolerant maize using “teosinte” as a germplasm resource. Plant Root 1: 17–21. doi:10.3117/plantroot.1.17

    Article  CAS  Google Scholar 

  • McNamara ST, Mitchell CA (1990) Adaptive stem and adventitious root responses of two tomato genotypes to flooding. Hort Sci 25(1):100–103

    Google Scholar 

  • Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen VT, Vuong TD, VanToai T, Lee JD, Wu X, Rouf Mian MA, Dorrance AE, Shannon JG, Nguyen HT (2012) Mapping of quantitative trait loci associated with resistance to Phytophthora sojae and flooding tolerance in soybean. Crop Sci 52:2481–2493. doi:10.2135/cropsci2011.09.0466

    Article  CAS  Google Scholar 

  • Oosterhuis DM, Scott HD, Hampton RE, Wullschleger SD (1990) Physiological responses of two soybean [Glycine max (L.) Merr] cultivars to short-term flooding. Environ Exp Bot 30:85–92. doi:10.1016/0098-8472(90)90012-S

    Article  Google Scholar 

  • Pedó T, Koch F, Martinazzo EG, Villela FA, Aumonde TZ (2015) Physiological attributes, growth and expression of vigor in soybean seeds under soil waterlogging. Afr J Agric Res 10: 3791–3797. doi:10.5897/AJAR2015.9661

    Google Scholar 

  • Reyna N, Cornelious B, Shannon JG, Sneller CH (2003) Evaluation of a QTL for waterlogging tolerance in southern soybean germplasm. Crop Sci 43 :2077–2082 .doi:10.2135/cropsci2003.2077

  • Rhine MD, Stevens G, Shannon G, Wrather A, Sleper D (2010) Yield and nutritional responses to waterlogging of soybean cultivars. Irrig Sci 28:135–142. doi:10.1007/s00271-009-0168-x

    Article  Google Scholar 

  • Rich S, Ludwig M, Colmer T (2012) Aquatic adventitious root development in partially and completely submerged wetland plants Cotula coronopifolia and Meionectes brownii. Ann Bot 110:405–414. doi:10.1093/aob/mcs051

    Article  PubMed  PubMed Central  Google Scholar 

  • Sakazono S, Nagata T, Matsuo R, Kajihara S, Watanabe M, Ishimoto M, Shimamura S, Harada K, Takahashi R, Mochizuki T (2014) Variation in root development response to flooding among 92 soybean lines during early growth stages. Plant Pro Sci 17:228–236. doi:10.1626/pps.17.228

    Article  Google Scholar 

  • Sallam A, Scott HD (1987) Effects of prolonged flooding on soybeans during early vegetative growth. Soil Sci 144:61–66

    Article  Google Scholar 

  • Sauter M (2013) Root responses to flooding. Curr Opin Plant Bol 16:282–286. doi:10.1016/j.pbi.2013.03.013

    Article  Google Scholar 

  • Sayama T, Nakazaki T, Ishikawa G, Yagasaki K, Yamada N, Hirota N, Hirat K, Yoshikawa T, Saito H, Teraishi M, Okumoto Y, Tsukiyama T, Tanisaka T (2009) QTL analysis of seed-flooding tolerance in soybean (Glycine max [L.] Merr.). Plant Sci 176:514–521. doi:10.1016/j.plantsci.2009.01.007

    Article  CAS  PubMed  Google Scholar 

  • Shimamura S, Mochizuki T, Nada Y, Fukuyama M (2003) Formation and function of secondary aerenchyma in hypocotyl, roots and nodules of soybean (Glycine max) under flooded conditions. Plant Soil 251:351–359. doi:10.1023/A:1023036720537

    Article  CAS  Google Scholar 

  • Song QJ, Marek LF, Shoemaker RC, Lark KG, Concibido VC, Delannay X, Specht JE, Cregan PB (2004) A new integrated genetic linkage map of the soybean. Theor Appl Genet 109:122–128. doi:10.1007/s00122-004-1602-3

    Article  CAS  PubMed  Google Scholar 

  • Souza TC, Castro EM, Magalhães PC, Alves ET, Pereira FJ (2012) Early characterization of maize plants in selection cycles under soil flooding. Plant Breed 131:439–501. doi:10.1111/j.1439-0523.2012.01973.x

    Article  Google Scholar 

  • Thomas AL, Guerreiro SMC, Sodek L (2005) Aerenchyma formation and recovery from hypoxia of the flooded root system of nodulated soybean. Ann Bot 96:1191–1198. doi:10.1093/aob/mci272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trought MCT, Drew MC (1980) The development of waterlogging damage in wheat seedlings (Triticum aestivum L.) I. Shoot and root growth in relation to changes in the concentrations of dissolved gases and solutes in the soil. Plant Soil 54:77–94. doi:10.1007/BF02182001

    Article  CAS  Google Scholar 

  • Vandamme E, Pypers P, Smolders E, Merckx R (2016) Seed weight affects shoot and root growth among and within soybean genotypes beyond the seedling stage: implications for low P tolerance screening. Plant Soil 401:65–78. doi:10.1007/s11104-015-2564-8

    Article  CAS  Google Scholar 

  • VanToai TT, Beuerlein JE, Schmitthenner AF, Martin SKSt (1994) Genetic variability for flooding tolerance in soybeans. Crop Sci 34:1112–1115. doi:10.2135/cropsci1994.0011183X003400040051x

    Article  Google Scholar 

  • VanToai TT, Martin SKSt, Chase K, Boru G, Schnipke V, Schmitthennr AF, Lark KG (2001) Identification of a QTL associated with tolerance of soybean to soil waterlogging. Crop Sci 41:1247–1252. doi:10.2135/cropsci2001.4141247x

    Article  Google Scholar 

  • VanToai TT, Hoa TTC, Hue NTN, Nguyen HT, Shannon JG, Rahman MA (2010) Flooding tolerance of soybean [Glycine max (L.) Merr.] germplasm from Southeast Asia under field and screen-house environments. Open Agric J 4:38–46. doi:10.2174/1874331501004010038

    Article  Google Scholar 

  • Visser EJW, Colmer TD, Blom CWPM, Voesenek LACJ (2000) Changes in growth, porosity, and radial oxygen loss from adventitious roots of selected mono- and dicotyledonous wetland species with contrasting types of aerenchyma. Plant Cell Environ 23:1237–1245. doi:10.1046/j.1365-3040.2000.00628.x

    Article  Google Scholar 

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

    Google Scholar 

  • Wiengweera A, Greenway H, Thomson CJ (1997) The use of agar nutrient solution to simulate lack of convection in waterlogging soils. Ann Bot 80:115–123. doi:10.1006/anbo.1996.0405

    Article  Google Scholar 

  • Yamane K, Iijima M (2016) Nodulation control of crack fertilization technique reduced the growth inhibition of soybean caused by short-term waterlogging at early vegetative stage. Plant Prot Sci 19(3):438–448. doi:10.1080/1343943X.2016.1164573

    Article  Google Scholar 

  • Yamauchi T, Abe F, Kawaguchi K, Oyanagi A, Nakazono M (2014) Adventitious roots of wheat seedlings that emerge in oxygen-deficient conditions have increased root diameters with highly developed lysigenous aerenchyma. Plant Signal Behav 9:e28506

    Article  PubMed Central  Google Scholar 

  • Zaidi PH, Rafique S, Singh NN (2003) Response of maize (Zea mays L.) genotypes to excess soil moisture stress: morpho-physiological effects and basis of tolerance. Eur J Agron 19: 383–399

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by a grant from the Ministry of Agriculture, Forestry and Fisheries of Japan (Genomics-based Technology for Agricultural Improvement, SFC-1005).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Loc Van Nguyen.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Brian Diers.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Van Nguyen, L., Takahashi, R., Githiri, S.M. et al. Mapping quantitative trait loci for root development under hypoxia conditions in soybean (Glycine max L. Merr.). Theor Appl Genet 130, 743–755 (2017). https://doi.org/10.1007/s00122-016-2847-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-016-2847-3

Keywords

Navigation