Plant Growth Regulation

, Volume 85, Issue 3, pp 399–409 | Cite as

Morpho-anatomical and physiological responses to waterlogging stress in different barley (Hordeum vulgare L.) genotypes

  • Haiye Luan
  • Baojian Guo
  • Yuhan Pan
  • Chao Lv
  • Huiquan Shen
  • Rugen Xu
Original paper


Waterlogging is one of the major stresses limiting crop production worldwide. The understanding of the mechanisms of plant adaptations to waterlogging stress helps improve plant tolerance to stress. In this study, physiological responses and morpho-anatomical adaptations of seven different barley genotypes were investigated under waterlogging stress. The results showed that the waterlogging-tolerant varieties (TX9425, Yerong, TF58) showed less reduction in plant height, SPAD (soil–plant analyses development analyses) value, tillers, shoot and root biomasses than did the waterlogging-sensitive varieties (Franklin, Naso Nijo, TF57). Under waterlogging stress condition, the tolerant genotypes also showed a much larger number of adventitious roots than did the sensitive genotypes. More intercellular spaces and better integrated chloroplast membrane structures were observed in the leaves of the waterlogging-tolerant cultivars, which is likely due to increased ethylene content, decreased ABA content and less accumulation of O2.−. The ability to form new adventitious roots and intercellular spaces in shoots can also be used as selection criteria in breeding barley for waterlogging tolerance.


Barley (Hordeum vulgare L.) Waterlogging Adventitious root Leaf aerenchyma Chloroplast ultrastructure 



This research was funded by the National Natural Science Foundation of China (31571648), the National Barley and Highland Barley Industrial Technology Specially Constructive Foundation of China (CARS-05), the opening project of Jiangsu Key Laboratory of Biochemistry and Biotechnology of Marine Wetland (K2016-03), the funds institute of Agricultural Science in Jiangsu Coastal Areas (YHS201605), and a Project Funded by the Priority Academic Program Development of Jiangsu Higher Education Institutions.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

Supplementary material

10725_2018_401_MOESM1_ESM.doc (7.3 mb)
Supplementary material 1 (DOC 7507 KB)


  1. Argus RE, Colmer TD, Grierson PF (2015) Early physiological flood tolerance is followed by slow post-flooding root recovery in the dryland riparian tree Eucalyptus camaldulensis subsp. refulgens. Plant Cell Environ 38:1189–1199CrossRefPubMedGoogle Scholar
  2. Arias-Moreno DM, Jiménez-Bremont JF, Maruri-López I, Delgado-Sánchez P (2017) Effects of catalase on chloroplast arrangement in Opuntia streptacantha chlorenchyma cells under salt stress. Sci Rep 7:8656CrossRefPubMedPubMedCentralGoogle Scholar
  3. Benschop JJ, Jackson MB, Gühl K, Vreeburg RA, Croker SJ, Peeters AJ, Voesenek LA (2005) Contrasting interactions between ethylene and abscisic acid in Rumex species differing in submergence tolerance. Plant J 44:756–768CrossRefPubMedGoogle Scholar
  4. Broughton S, Zhou GF, Teakle NL, Matsuda R, Zhou MX, O’Leary RA, Colmer T, Li CD (2015) Waterlogging tolerance is associated with root porosity in barley. Mol Breeding 35:27CrossRefGoogle Scholar
  5. Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560CrossRefPubMedGoogle Scholar
  6. Chen XM, Qiu LL, Guo HP, Wang Y, Yuan HW, Yan DL, Zheng BS (2017) Spermidine induces physiological and biochemical changes in southern highbush blueberry under drought stress. Braz J Bot 40:841–851CrossRefGoogle Scholar
  7. Colmer TD (2003) Long-distance transport of gases in plants: a perspective on internal aeration and radial oxygen loss from roots. Plant Cell Environ 26:17–36CrossRefGoogle Scholar
  8. Colmer TD, Pedersen O (2008) Oxygen dynamics in submerged rice (Oryza sativa). New Phytol 178:326–334CrossRefPubMedGoogle Scholar
  9. Colmer TD, Voesenek LACJ. (2009) Flooding tolerance: suites of plant traits in variable environments. Funct Plant Biol 36:665–681CrossRefGoogle Scholar
  10. Crozier A, Sandberg G, Monteiro AM, Sundberg B (1986) The use of immunological techniques in plant hormone analysis. In: Bopp M (ed) Plant growth substances 1985. Springer, Berlin, pp 13–21CrossRefGoogle Scholar
  11. Dawood T, Rieu I, Wolters-Arts M, Derksen EB, Mariani C, Visser EJ (2014) Rapid flooding-induced adventitious root development from preformed primordia in Solanum dulcamara. AoB Plants 6:490–552CrossRefGoogle Scholar
  12. Jackson MB, Colmer TD (2005) Response and adaptation by plants to flooding stress. Ann Bot 96:501–505CrossRefPubMedPubMedCentralGoogle Scholar
  13. Jiang M, Zhang J (2002) Water stress-induced abscisic acid accumulation triggers the increased generation of reactive oxygen species and up-regulates the activities of antioxidant enzymes in maize leaves. J Exp Bot 53:2401–2410CrossRefPubMedGoogle Scholar
  14. Jung J, Lee SC, Choi HK (2008) Anatomical patterns of aerenchyma in aquatic and wetland plants. J Plant Biol 51:428–439CrossRefGoogle Scholar
  15. Kim YH, Hwang SJ, Waqas M, Khan AL, Lee JH, Lee JD, Nguyen T, Lee H IJ (2015) Comparative analysis of endogenous hormones level in two soybean (Glycine max L.) lines differing in waterlogging tolerance. Front Plant Sci 6:714PubMedPubMedCentralGoogle Scholar
  16. Malik AI, Colmer TD, Lambers H, Schortemeyer M (2003) Aerenchyma formation and radial O2 loss along adventitious roots of wheat with only the apical root portion exposed to O2 deficiency. Plant Cell Environ 26:1713–1722CrossRefGoogle Scholar
  17. Mano Y, Omori F (2008) Verification of QTL controlling root aerenchyma formation in a maize × teosinte “Zea nicaraguensis” advanced backcross population. Breed Sci 58:217–223CrossRefGoogle Scholar
  18. Mano Y, Omori F (2013) Relationship between constitutive root aerenchyma formation and flooding tolerance in Zea nicaraguensis. Plant Soil 370:447–460CrossRefGoogle Scholar
  19. Mano Y, Omori F, Loaisiga CH, Bird RMK (2009) QTL mapping of above-ground adventitious roots during flooding in maize × teosinte “Zea nicaraguensis” backcross population. Plant Root 3:3–9CrossRefGoogle Scholar
  20. Matsukura C, Kawai M, Toyofuku K, Barrero RA, Uchimiya H, Yamaguchi J (2000) Transverse vein differentiation associated with gas space formation-fate of the middle cell layer in leaf sheath development of rice. Ann Bot 85:19–27CrossRefGoogle Scholar
  21. Parlanti S, Kudahettige NP, Lombardi L, Mensuali-Sodi A, Alpi A, Perata P, Pucciariello C (2011) Distinct mechanisms for aerenchyma formation in leaf sheaths of rice genotypes displaying a quiescence or escape strategy for flooding tolerance. Ann Bot 107:1335–1343CrossRefPubMedPubMedCentralGoogle Scholar
  22. Rajhi I, Yamauchi T, Takahashi H, Nishiuchi S, Shiono K, Watanabe R, Mliki A, Nagamura Y, Tsutsumi N, Nishizawa NK, Nakazono M (2011) Identification of genes expressed in maize root cortical cells during lysigenous aerenchyma formation using laser microdissection and microarray analyses. New Phytol 190:351–368CrossRefPubMedGoogle Scholar
  23. Ren BZ, Zhang JW, Dong ST, Liu P, Zhao B (2016) Effects of waterlogging on leaf mesophyll cell ultrastructure and photosynthetic characteristics of summer maize. PLoS ONE 11:e0161424CrossRefPubMedPubMedCentralGoogle Scholar
  24. Romina P, Abeledo LG, Miralles DJ (2014) Identifying the critical period for waterlogging on yield and its components in wheat and barley. Plant Soil 378:265–277CrossRefGoogle Scholar
  25. Sauter M (2013) Root responses to flooding. Curr Opin Plant Biol 16:282–286CrossRefPubMedGoogle Scholar
  26. Setter TL, Waters I (2003) Review of prospects for germplasm improvement for waterlogging tolerance in wheat, barley and oats. Plant Soil 253:1–34CrossRefGoogle Scholar
  27. Shao QS, Wang HZ, Gou HP, Zhou AC, Huang YQ, Sun YL, Li MY (2014) Effects of shade treatment on photosynthetic characteristics, chloroplast ultrastructure, and physiology of Anoectochilus roxburghii. PLoS ONE 9:1–10Google Scholar
  28. Shimamura S, Yoshioka T, Yamamoto R, Hiraga S, Nakamura T, Shimada S, Komatsu S (2014) Role of abscisic acid in flood-induced secondary aerenchyma formation in soybean (Glycine max) hypocotyls. Plant Prod Sci 17:131–137CrossRefGoogle Scholar
  29. Steffens B (2014) The role of ethylene and ROS in salinity, heavy metal, and flooding responses in rice. Front Plant Sci 5:685CrossRefPubMedPubMedCentralGoogle Scholar
  30. Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170:603–617CrossRefPubMedGoogle Scholar
  31. Steffens B, Geske T, Sauter M (2011) Aerenchyma formation in the rice stem and its promotion by H2O2. New Phytol 190:369–378CrossRefPubMedGoogle Scholar
  32. Vidoz ML, Loreti E, Mensuali A, Alpi A, Perata P (2010) Hormonal interplay during adventitious root formation in flooded tomato plants. Plant J 63:551–562CrossRefPubMedGoogle Scholar
  33. Visser EJW, Voesenek LACJ (2004) Acclimation to soil flooding-sensing and signal-transduction. Plant Soil 254:197–214Google Scholar
  34. Wang LH, Li DH, Zhang YX, Yuan G, Yu JY, Sauter X, Zhang XR (2016) Tolerant and susceptible sesame genotypes reveal waterlogging stress response patterns. PLoS ONE 11:e0149912CrossRefPubMedPubMedCentralGoogle Scholar
  35. Wang RF, Dai HX, Shi M, Ahmed IM, Liu WX, Chen ZH, Zhang GP, Wu FB (2017) Genotype-dependent effects of phosphorus supply on physiological and biochemical responses to Al-stress in cultivated and Tibetan wild barley. Plant Growth Regul 82:259–270CrossRefGoogle Scholar
  36. Wei WL, Li DH, Wang LH, Wang LH, Ding X, Zhang YX, Gao Y, Zhang XR (2013) Morpho-anatomical and physiological responses to waterlogging of sesame (Sesamum indicum L.). Plant Sci 208:102–111CrossRefPubMedGoogle Scholar
  37. Xu S, Li JL, Zhang XQ, Wei H, Cui LJ (2006) Effects of heat acclimation pretreatment on changes of membrane lipid peroxidation, antioxidant metabolites, and ultrastructure of chloroplasts in two cool-season turfgrass species under heat stress. Environ Exp Bot 56:274–285CrossRefGoogle Scholar
  38. Xu XW, Ji J, Xu Q, Q XH, Chen XH (2017) Inheritance and quantitative trail loci mapping of adventitious root numbers in cucumber seedlings under waterlogging conditions. Mol Genet Genomics 292:353CrossRefPubMedGoogle Scholar
  39. Yamauchi T, Watanabe K, Fukazawa A, Mori H, Kawaquchi K, Oyanagi A, Nakazono M (2014) Ethylene and reactive oxygen species are involved in root aerenchyma formation and adaptation of wheat seedlings to oxygen-deficient conditions. J Exp Bot 65:261–273CrossRefPubMedGoogle Scholar
  40. Yordanova RY, Christov KN, Popova LP (2004) Antioxidative enzymes in barley plants subjected to soil flooding. Environ Exp Bot 51:93–101CrossRefGoogle Scholar
  41. Zhang H, Xue YG, Wang ZQ, Yang JC, Zhang JH (2009) Morphological and physiological traits of roots and their relationships with shoot growth in “super’’ rice. Field Crop Res 113:31–40CrossRefGoogle Scholar
  42. Zhang XC, Shabala S, Koutoulis A, Shabala L, Johnson P, Hayes D, Nichols DS, Zhou MX (2015a) Waterlogging tolerance in barley is associated with faster aerenchyma formation in adventitious roots. Plant Soil 394:355–372CrossRefGoogle Scholar
  43. Zhang YJ, Song XZ, Yang GZ, Li ZH, Lu HQ, Kong XQ, Eneji AE, Dong HZ (2015b) Physiological and molecular adjustment of cotton to waterlogging at peak-flowering in relation to growth and yield. Field Crop Res 179:164–172CrossRefGoogle Scholar
  44. Zhang M, Jin ZQ, Zhao J, Zhang GP, Wu FB (2015c) Physiological and biochemical responses to drought stress in cultivated and Tibetan wild barley. Plant Growth Regul 75:567–574CrossRefGoogle Scholar
  45. Zhang XC, Zhou GF, Shabala S, Koutoulis A, Shabala L, Johnson P, Li CD, Zhou MX (2016) Identification of aerenchyma formation related QTL in barley that can be effective in breeding for waterlogging tolerance. Theor Appl Genet 129:1167–1177CrossRefPubMedGoogle Scholar
  46. Zheng YK, Wang Z (2011) Contrast observation and investigation of wheat endosperm transfer cells and nucellar projection transfer cells. Plant Cell Rep 30:1281–1288CrossRefPubMedGoogle Scholar
  47. Zheng CF, Jiang D, Liu FL, Dai TB, Jing Q, Cao WX (2009) Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. Plant Sci 176:575–582CrossRefPubMedGoogle Scholar
  48. Zhou MX (2012) Accurate phenotyping reveals better QTL for waterlogging tolerance in barley. Plant Breed 130:203–208CrossRefGoogle Scholar
  49. Zhou MX, Li HB, Mendham NJ (2007) Combining ability of waterlogging tolerance in barley. Crop Sci 47:278–284CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V., part of Springer Nature 2018

Authors and Affiliations

  • Haiye Luan
    • 1
    • 2
  • Baojian Guo
    • 1
  • Yuhan Pan
    • 1
  • Chao Lv
    • 1
  • Huiquan Shen
    • 2
  • Rugen Xu
    • 1
  1. 1.Jiangsu Key Laboratory of Crop Genetics and Physiology/Co-Innovation Center for Modern Production Technology of Grain Crops, Key Laboratory of Plant Functional Genomics of the Ministry of Education, Barley Research Institution of Yangzhou UniversityYangzhou UniversityYangzhouChina
  2. 2.Institute of Agricultural Science in Jiangsu Coastal AreasYanchengChina

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