Skip to main content
SpringerLink
Log in

Antioxidative responses and morpho-anatomical adaptations to waterlogging in Sesbania virgata

  • Original Paper
  • Published:
Trees Aims and scope Submit manuscript

Abstract

Sesbania virgata (Leguminosae) is tolerant of long periods of soil inundation. However, its morphological adaptations to anoxia and its response to possible damage from oxidative stress are still unknown. Here, we provide new information that helps to explain the ability of S. virgata plants to grow in flooded environments. Plants containing six expanded leaves were placed in masonry tanks and were subjected to the following conditions: control (well watered), soil waterlogging (water to the setup level of 1 cm above the soil surface—roots and parts of the stems flooded), and complete submergence (whole plant flooded). Plants exposed to flooding (soil waterlogging and complete submergence) significantly increased their production of hydrogen peroxide (H2O2), indicating the extent of oxidative injury posed by stress conditions. We demonstrate that plants exposed to flooding develop an efficient scavenger of ROS (generated during stress) in the roots through the coordinated action of nonenzymatic ascorbic acid (Asc) and dehydroascorbate (DHA) as well as the enzymatic antioxidants superoxide dismutase (SOD), ascorbate peroxidase (APX), dehydroascorbate reductase (DHAR), and glutathione reductase (GR) that are present in the tissues. Moreover, we observed the development of morpho-anatomical structures such as adventitious roots, lenticels, and cracks in the stem of plants under soil waterlogging. The secondary root of plants under soil waterlogging showed a thinner cortex and larger number of elements of small diameter vessels. Numerous aerenchymas were observed in the newly formed in the adventitious roots. We conclude that these antioxidative responses and morpho-anatomical adaptations in the roots are part of a suite of adaptations that allow S. virgata plants to survive long periods of flooding, notably under waterlogged conditions.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Ahmed S, Nawata E, Sakuratani T (2002) Effects of waterlogging at vegetative and reproductive growth stages on photosynthesis, leaf water potential and yield in mungbean. Plant Prod Sci 5:117–123

    Article  Google Scholar 

  • Ahsan N, Lee D-G, Lee S-H, Lee K-W, Bahk J-D, Lee B-H (2007) A proteomic screen and identification of waterlogging regulated proteins in tomato roots. Plant Soil 295:37–51

    Article  CAS  Google Scholar 

  • Alam I, Lee D, Kim K, Park C, Sharmin SA, Lee H, Oh K, Yun B, Lee B (2010) Proteome analysis of soybean roots under waterlogging stress at an early vegetative stage. J Biol Sci 35:49–62

    CAS  Google Scholar 

  • Arakawa N, Tsutsumi K, Sanceda NG, Kurata T, Inagaki C (1981) A rapid and sensitive method for the determination of ascorbic acid using 4,7-diphenyl-1,10-phenanthroline. Agric Biol Chem 45:1289–1290

    Article  CAS  Google Scholar 

  • Araki H, Hossain MA, Takahashi T (2012) Waterlogging and hypoxia have permanent effects on wheat root growth and respiration. J Agro Crop Sci 198:264–275

    Article  Google Scholar 

  • Azevedo RA, Alas RM, Smith RJ, Lea PJ (1998) Response from elevated carbon dioxide to air and ozone fumigation in leaves and roots of wild type and a catalase-deficient mutant of barley. Physiol Plantarum 104:280–292

    Article  CAS  Google Scholar 

  • Bai T, Li C, Ma F, Feng F, Shu F (2010) Response of growth and antioxidant system to root-zone hypoxia stress in two Malus species. Plant Soil 325:95–105

    Article  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Bansal R, Srivastava JP (2012) Antioxidative defense system in pigeonpea roots under waterlogging stress. Acta Physiol Plant 34:515–522

    Article  CAS  Google Scholar 

  • Blokhina O, Virolainen E, Fagerstedt KV (2003) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot 91:179–194

    Article  PubMed  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  PubMed  CAS  Google Scholar 

  • Buege JA, Aust SD (1978) Microsomal lipid peroxidation. Methods Enzymol 52:302–310

    Article  PubMed  CAS  Google Scholar 

  • Cakmak I, Strbac D, Marschner H (1993) Activities of hydrogen peroxide-scavenging enzymes in germination wheat seeds. J Exp Bot 44:127–132

    Article  CAS  Google Scholar 

  • Campbell R, Drew MC (1983) Electron-microscopy of gas space (aerenchyma) formation in adventitious roots of Zea mays L. subjected to oxygen shortage. Planta 157:350–357

    Article  Google Scholar 

  • Crawford RMM, Braendle R (1996) Oxygen deprivation stress in a changing environment. J Exp Bot 47:145–159

    Article  CAS  Google Scholar 

  • Deuner S, Alves JD, Zanandrea I, Goulart PFP, Silveira NM, Henrique PC, Mesquita AC (2011) Stomatal behavior and components of the antioxidative system in coffee plants under water stress. Sci Agric 68:77–85

    Article  CAS  Google Scholar 

  • Dolferus R, Klok EJ, Delessert C, Wilson S, Ismond KP, Good AG, Peacock WJ, Dennis ES (2003) Enhancing the anaerobic response. Ann Bot 91:111–117

    Article  PubMed  CAS  Google Scholar 

  • Drew MC (1997) Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annu Rev Plant Physiol Plant Mol Biol 48:223–250

    Article  PubMed  CAS  Google Scholar 

  • Evans DE (2003) Aerenchyma formation. New Phytol 161:35–49

    Article  Google Scholar 

  • Fernandes-Corrêa AF, Furch B (1992) Investigations on the tolerance of several trees to submergence and blackwater (Igapo) and withewater (Várzea) inundation forests near Manaus, central Amazonia. Amazoniana 12:71–84

    Google Scholar 

  • Ferreira L (1997) Effects of the duration of flooding on species richness and floristic composition in three hectares in the Jaú National Park in floodplain forests in Central Amazonia. Biodivers Conserv 6:1353–1363

    Article  Google Scholar 

  • Ghugh V, Kaur N, Gupta A (2011) Role of antioxidant and anaerobic metabolism enzymes in providing tolerance to maize (Zea mays L.) seedlings against waterlogging. Indian J Anim Sci 48:346–352

    Google Scholar 

  • Giannopolitis CN, Ries SK (1977) Superoxide dismutases. I. Occurrence in higher plants. Plant Physiol 59:309–314

    Article  PubMed  CAS  Google Scholar 

  • Godoy JR, Petts G, Salo J (1999) Riparian flooded forests of the Orinoco and Amazon basins: a comparative review. Riparian flooded forests of the Orinoco and Amazon basins: a comparative review. Biodivers Conserv 8:551–586

    Article  Google Scholar 

  • Gunawardena A, Pearce DME, Jackson MB, Hawes CR, Evans DE (2001) Rapid changes in cell wall pectic polysaccharides are closely associated with early stages of aerenchyma formation, a spatially localized form of programmed cell death in roots of maize (Zea mays L.) promoted by ethylene. Plant Cell Environ 24:1369–1375

    Article  CAS  Google Scholar 

  • Guo WQ, Chen BL, Liu RX, Zhou ZG (2010) Effects of nitrogen application rate on cotton leaf antioxidant enzyme activities and endogenous hormone contents under short-term waterlogging at flowering and boll-forming stage. Ying Yong Sheng Tai Xue Bao 21:53–61

    PubMed  CAS  Google Scholar 

  • He CJ, Finlayson SA, Drew MC, Jordan WR, Morgan PW (1996) Ethylene biosynthesis during aerenchyma formation in roots of maize subjected to mechanical impedance and hypoxia. Plant Physiol 112:1679–1685

    PubMed  CAS  Google Scholar 

  • Holbrook NM, Zwieniecki MA (1999) Embolism repair and xylem tension: do we need a miracle? Plant Physiol 120:7–70

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Hossain Z, Lopez-Climent MF, Arbona V, Perez-Clemente RM, Gomez-Cadenas A (2009) Modulation of the antioxidant system in citrus under waterlogging and subsequent drainage. J Plant Physiol 166:1391–1404

    Article  PubMed  CAS  Google Scholar 

  • Hossain MA, Araki H, Takahashi T (2011) Poor grain filling induced by waterlogging is similar to that in abnormal early ripening in wheat in Western Japan. Field Crop Res 123:100–108

    Article  Google Scholar 

  • Huang S, Greenway H, Colmer TD, Millar AH (2005) Protein synthesis by rice coleoptiles during prolonged anoxia: implications for glycolysis, growth and energy utilization. Ann Bot 96:703–715

    Article  PubMed  CAS  Google Scholar 

  • Jackson MB (1985) Ethylene and responses of plants to soil waterlogging and submergence. Annu Rev Plant Physiol 36:145–174

    Article  CAS  Google Scholar 

  • Johansen DA (1940) Plant microtechnique. McGraw-Hill, New York

    Google Scholar 

  • Junk WJ (1989) Flood tolerance and tree distribution in central Amazonia. In: Holm-Nielsen LB et al. (eds) Tropical forest botanical dynamics, speciation and diversity. Academic Press, London, pp 47–64

  • Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES (2002) Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. Plant Cell 14:2481–2494

    Article  PubMed  CAS  Google Scholar 

  • Kolb RM, Dolder H, Cortelazzo AL (2004) Effect of anoxia on root ultrastructure of four neotropical trees. Protoplasma 224:99–105

    PubMed  CAS  Google Scholar 

  • Kreuzwieser J, Hauberg J, Howell KA, Carroll A, Rennenberg H, Millar AH, Whelan J (2009) Differential response of gray poplar leaves and roots underpins stress adaptation during hypoxia. Plant Physiol 149:461–473

    Article  PubMed  CAS  Google Scholar 

  • Licausi F, Perata P (2009) Low oxygen signaling and tolerance in plants. Adv Bot Res 50:139–198

    Article  CAS  Google Scholar 

  • Lin KHR, Weng CC, Lo HF, Chen JT (2004) Study of the root antioxidative system of tomatoes and eggplants under waterlogged conditions. Plant Sci 167:355–365

    Article  CAS  Google Scholar 

  • Liu F, VanToai T, Moy LP, Bock G, Linford LD, Quackenbush J (2005) Global transcription profiling reveals comprehensive insights into hypoxic response in Arabidopsis. Plant Physiol 137:1115–1129

    Article  PubMed  CAS  Google Scholar 

  • Mallick N, Mohn FH (2000) Reactive oxygen species: response of algal cells. J Plant Physiol 157:183–193

    Article  CAS  Google Scholar 

  • Medina CL, Sanches MC, Tucci MLS, Sousa CAF, Cuzzuol GRF, Joly CA (2009) Erythrina speciosa (Leguminosae-Papilionoideae) under soil water saturation: morphophysiological and growth responses. Ann Bot 104:671–680

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) The reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

    Article  PubMed  CAS  Google Scholar 

  • Monk LS, Fagerstedt KV, Crawford RMM (1987) Superoxide dismutase as an anaerobic polypeptide. A key factor in recovery from oxygen deprivation in Iris pseudacorus. Plant Physiol 85:1016–1020

    Article  PubMed  CAS  Google Scholar 

  • Mühlenbock P, Plaszczyca M, Plaszczyca M, Mellerowicz E, Karpinski S (2007) Lysigenous aerenchyma formation in Arabidopsis is controlled by lesion simulating disease. Plant Cell 19:3819–3830

    Article  PubMed  Google Scholar 

  • Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbato-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

    CAS  Google Scholar 

  • Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Annu Rev Plant Biol 49:249–279

    Article  CAS  Google Scholar 

  • Poot P, Bakker R, Lambers H (2008) Adaptations to winter-wet ironstone soils: a comparison between rare ironstone Hakea (Proteaceae) species and their common congeners. Aust J Bot 56:58–574

    Article  Google Scholar 

  • Porto BN, Alves JD, Magalhães PC, Castro EM, Campos NA, Souza KRD, Magalhães MM, Andrade CA, Santos MO (2012) Calcium-dependent tolerant response of cell wall in maize mesocotyl under flooding stress. J Agro Crop Sci. doi:10.1111/j.1439-037X.2012.00535.x

  • Potters G, Horemans N, Jansen MAK (2010) The cellular redox state in plant stress biology e a charging concept. Plant Physiol Biochem 48:292–300

    Article  PubMed  CAS  Google Scholar 

  • Rk Sairam, Kumutha D, Ezhilmathi K, Deshmukh Ps, Srivastava Gc (2008) Physiology and biochemistry of waterlogging tolerance in plants. Biol Plantarum 52:401–412

    Article  Google Scholar 

  • Santiago EF, Paoli AAS (2007) Respostas morfológicas em Guibourtia hymenifolia (Moric.) J. Leonard (Fabaceae) e Genipa americana L. (Rubiaceae), submetidas ao estresse por deficiência nutricional e alagamento do substrato. Revista Brasileira de Botânica 30:129–138 (in Portuguese, with abstract in English)

    Google Scholar 

  • Sinha S, Saxena R, Singh S (2005) Chromium induced lipid peroxidation the plants of Pistia stratiotes L.: role of antioxidants and antioxidant enzymes. Chemosphere 58:595–604

    Article  PubMed  CAS  Google Scholar 

  • Tanaka K, Masumori M, Yamanoshita T, Tange T (2011) Morphological and anatomical changes of Melaleuca cajuputi under submergence. Trees 25:695–704

    Article  Google Scholar 

  • Vartapetian BB (1982) Pasteur effect visualization by electron microscopy. Naturwissenschaften 69:99

    Article  PubMed  CAS  Google Scholar 

  • Waters I, Morrell S, Greenway H, Colmer TD (1991) Effects of anoxia on wheat seedlings. II. Influence of O2 supply prior to anoxia on tolerance to anoxia, alcoholic fermentation, and sugar levels. J Exp Bot 42:1437–1447

    Article  CAS  Google Scholar 

  • Wollenweber-Ratzer B, Crawford RMM (1994) Enzymatic defence against post-anoxic injury in higher plants. Proc R Soc Edinb 102:381–390

    Google Scholar 

  • Zanandrea I, Alves JD, Deuner S, Goulart PFP, Henrique PC, Silveira NM (2010) Tolerance of S. virgata plants to flooding. Aust J Bot 57:661–669

    Article  Google Scholar 

Download references

Acknowledgments

This study was supported by the National Council for Scientific and Technological Development (CNPq), with a research fellowship to JDA, and by the Foundation for Research Support of Minas Gerais (FAPEMIG). Thanks to Dr Richard Ladle for editing and proofreading the manuscript.

Author information

Authors and Affiliations

  1. Departamento de Biologia, Universidade Federal de Lavras, Lavras, MG, 37200-000, Brazil

    José D. Alves, Kamila R. D. de Souza & Meline de O. Santos

  2. Departamento de Botânica, Universidade Federal de Pelotas, Pelotas, RS, 96010-900, Brazil

    Ilisandra Zanandrea

  3. Embrapa Cerrados, Planaltina, DF, 73310-970, Brazil

    Sidnei Deuner

  4. Centro Universitario de Lavras, Lavras, MG, 37200-000, Brazil

    Patrícia de F. P. Goulart

Authors
  1. José D. Alves
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Ilisandra Zanandrea
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Sidnei Deuner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Patrícia de F. P. Goulart
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Kamila R. D. de Souza
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Meline de O. Santos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to José D. Alves.

Additional information

Communicated by R. Matyssek.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Alves, J.D., Zanandrea, I., Deuner, S. et al. Antioxidative responses and morpho-anatomical adaptations to waterlogging in Sesbania virgata . Trees 27, 717–728 (2013). https://doi.org/10.1007/s00468-012-0827-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00468-012-0827-z

Keywords

Search

Navigation