Skip to main content
Log in

Process of aerenchyma formation and reactive oxygen species induced by waterlogging in wheat seminal roots

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

The development and regulation of aerenchyma in waterlogged conditions were studied in the seminal roots of wheat. Evans blue staining and the first cell death position indicated that the cortical cell death began at the root mid-cortex cells in flooding conditions. Continuous waterlogging treatment caused the spread of cell death from the mid-cortex to the neighboring cells and well-developed aerenchyma was formed after 72 h. Meanwhile, the formation of radial oxygen loss barrier was observed in the exodermis owing to the induction of Casparian bands and lignin deposition. Analysis of aerenchyma along the wheat root revealed that aerenchyma formed at 10 mm from the root tip, significantly increased toward the center of the roots, and decreased toward the basal region of the root. In situ detection of radial oxygen species (ROS) showed that ROS accumulation started in the mid-cortex cells, where cell death began indicating that cell death was probably accompanied by ROS production. Further waterlogging treatments resulted in the accumulation of ROS in the cortical cells, which were the zone for aerenchyma development. Accumulation and distribution of H2O2 at the subcellular level were revealed by ultracytochemical localization, which further verified the involvement of ROS in the cortical cell death process (i.e., aerenchyma formation). Furthermore, gene expression analysis indicated that ROS production might be the result of up-regulation of genes encoding for ROS-producing enzymes and the down-regulation of genes encoding for ROS-detoxifying enzymes. These results suggest that aerenchyma development in wheat roots starts in the mid-cortex cells and its formation is regulated by ROS.

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.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Abbreviations

CBs:

Casparian bands

DAB:

3,3-Diaminobenzidine

H2DCF-DA:

2′,7′-Dichlorodi-hydrofluorescein diacetate

MOPS:

3-(N-morpholino) propanesulphonic acid

MT:

Metallothionein

NBT:

Nitroblue tetrazolium

PCD:

Programmed cell death

ROL:

Radial oxygen loss

ROS:

Reactive oxygen species

TEM:

Transmission electron microscopy

References

  • Abiko T, Kotula L, Shiono K, Malik AI, Colmer TD, Nakazono M (2012) Enhanced formation of aerenchyma and induction of a barrier to radial oxygen loss in adventitious roots of Zea nicaraguensis contribute to its waterlogging tolerance as compared with maize (Zea mays ssp. mays). Plant Cell Environ 35:1618–1630

    Article  PubMed  CAS  Google Scholar 

  • Aguilar EA, Turne DW, Sivasithamparam K (1999) Aerenchyma formation in roots of four banana (Musa spp.) cultivars. Sci Hortic 80:57–72

    Article  Google Scholar 

  • Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  PubMed  CAS  Google Scholar 

  • Armstrong W (1971) Radial oxygen losses from intact rice roots as affected by distance from the apex, respiration and waterlogging. Physiol Plant 25:192–197

    Article  Google Scholar 

  • Beckman KB, Ames BN (1997) Oxidative decay of DNA. J Biol Chem 272:19633–19636

    Article  PubMed  CAS  Google Scholar 

  • Berg C, Willemsen Hage W, Weisbeek P, Scheres B (1995) Cell fate in the Arabidopsis root meristem determined by directional signaling. Nature 378:62–65

    Article  PubMed  Google Scholar 

  • Berlett BS, Stadtman ER (1997) Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 272:20313–20316

    Article  PubMed  CAS  Google Scholar 

  • Bestwick CS, Bennett MH, Mansfield JW (1995) Hrp mutant of Pseudomonas syringae pv phaseolicola induces cell wall alterations but not membrane damage leading to the hypersensitive reaction in lettuce (Lactuca sativa). Plant Physiol 108:503–516

    PubMed  CAS  Google Scholar 

  • Boka K, Orban N, Kristof Z (2007) Dynamics and localization of H2O2 production in elicited plant cells. Protoplasma 230:89–97

    Article  PubMed  CAS  Google Scholar 

  • Bouranis DL, Chorianopoulou SN, Siyiannis VF, Protonotarios VE, Hawkesford MJ (2003) Aerenchyma formation in roots of maize during sulphate starvation. Planta 217:382–391

    Article  PubMed  CAS  Google Scholar 

  • Bouranis DL, Chorianopoulou SN, Kollias C, Maniou P, Protonotarios VE, Siyiannis VF, Hawkesford MJ (2006) Dynamics of Aerenchyma distribution in the cortex of sulfate-deprived adventitious roots of maize. Ann Bot 7:695–704

    Article  Google Scholar 

  • Colmer TD (2003a) Aerenchyma and an inducible barrier to radial oxygen loss facilitate root aeration in upland, paddy and deep-water rice (Oryza sativa L.). Ann Bot 9:301–309

    Article  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Colmer TD, Gibberd MR, Wiengweera A, Tinh TK (1998) The barrier to radial oxygen loss from roots of rice (Oryza sativa L.) is induced by growth in stagnant solution. J Exp Bot 49:1431–1436

    CAS  Google Scholar 

  • Danon A, Miersch O, Felix G, Camp RG, Apel K (2005) Concurrent activation of cell death-regulating signaling pathways by singlet oxygen in Arabidopsis thaliana. Plant J 41:68–80

    Article  PubMed  CAS  Google Scholar 

  • de Jong AJ, Yakimova ET, Kapchina VM, Woltering EJ (2002) A critical role for ethylene in hydrogen peroxide release during programmed cell death in tomato suspension cells. Planta 214:537–545

    Article  Google Scholar 

  • de Pinto MC, Paradiso A, Leonetti P, De Gara L (2006) Hydrogen peroxide, nitric oxide and cytosolic ascorbate peroxidase at the crossroad between defence and cell death. Plant J 48:784–795

    Article  PubMed  Google Scholar 

  • Dennis ES, Dolferus R, Ellis M, Rahman M, Wu Y, Hoeren FU, Grover A, Ismond KP, Good AG, Peacock WJ (2000) Molecular strategies for improving waterlogging tolerance in plants. J Exp Bot 51:89–97

    Article  PubMed  CAS  Google Scholar 

  • Drew MC, He CJ, Morgan PW (2000) Programmed cell death and aerenchyma formation in roots. Trends Plant Sci 5:123–127

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Fleury C, Mignotte B, Vayssière JL (2002) Mitochondrial reactive oxygen species in cell death signaling. Biochimie 84:131–141

    Article  PubMed  CAS  Google Scholar 

  • Garthwaite AJ, von Bothmer R, Colmer TD (2003) Diversity in root aeration traits associated with waterlogging tolerance in genus Hordeum. Funct Plant Biol 30:875–889

    Article  Google Scholar 

  • Gechev TS, Hille J (2005) Hydrogen peroxide as a signal controlling plant programmed cell death. J Cell Biol 168:17–20

    Article  PubMed  CAS  Google Scholar 

  • Gunawardena AH, Pearce DM, Jackson MB, Hawes CR, Evans DE (2001) Characterisation of programmed cell death during aerenchyma formation induced by ethylene or hypoxia in roots of maize (Zea mays L.). Planta 212:205–214

    Article  PubMed  CAS  Google Scholar 

  • Haque ME, Abe F, Kawaguchi K (2010) Formation and extension of lysigenous aerenchyma in seminal root cortex of spring wheat (Triticum aestivum cv. Bobwhite line SH 98 26) seedlings under different strengths of waterlogging. Plant Root 4:31–39

    Article  Google Scholar 

  • Houot V, Etienne P, Petitot AS, Barbier S, Blein JP, Suty L (2001) Hydrogen peroxide induces programmed cell death features in cultured tobacco BY-2 cells, in a dose-dependent manner. J Exp Bot 52:1721–1730

    Article  PubMed  CAS  Google Scholar 

  • Jackson MB, Drew MC (1984) Effects of flooding on growth and metabolism of herbaceous plants. In: Kozlowski T (ed) Flooding and plant growth. Academic Press, Orlando, pp 47–128

    Chapter  Google Scholar 

  • Jensen WA (1962) Botanical histochemistry. N.H. Freeman & Co., San Francisco

    Google Scholar 

  • Jiang Z, Song XF, Zhou ZQ, Wang LK, Li JW, Deng XY, Fan HY (2010) Aerenchyma formation: programmed cell death in adventitious roots of winter wheat (Triticum aestivum) under waterlogging. Funct Plant Biol 37:748–755

    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 

  • Kawai M, Samarajeewa PK, Barrero RA, Nishiguchi M, Uchimiya H (1998) Cellular dissection of the degradation pattern of cortical cell death during aerenchyma formation of rice roots. Planta 204:277–287

    Article  CAS  Google Scholar 

  • Kotula L, Ranathunge K, Schreiber L, Steudle E (2009) Functional and chemical comparison of apoplastic barriers to radial oxygen loss in roots of rice (Oryza sativa L.) grown in aerated or deoxygenated solution. J Exp Bot 60:2155–2167

    Article  PubMed  CAS  Google Scholar 

  • Lamb C, Dixon RA (1997) The oxidative burst in plant disease resistance. Annu Rev Plant Physiol Plant Mol Biol 48:251–275

    Article  PubMed  CAS  Google Scholar 

  • Lambeth JD (2004) NOX enzymes and the biology of reactive oxygen. Nat Rev Immunol 4:181–189

    Article  PubMed  CAS  Google Scholar 

  • Lenochová Z, Soukup A, Votrubová O (2009) Aerenchyma formation in maize roots. Biol Plant 53:263–270

    Article  Google Scholar 

  • Levine A, Tenhaken R, Dixon R, Lamb C (1994) H2O2 from the oxidative burst orchestrates the plant hypersensitive disease resistance response. Cell 79:583–593

    Article  PubMed  CAS  Google Scholar 

  • Lorrain S, Vailleau F, Balagué C, Roby D (2003) Lesion mimic mutants: keys for deciphering cell death and defense pathways in plants? Trends Plant Sci 8:263–271

    Article  PubMed  CAS  Google Scholar 

  • Lulai EC, Morgan WC (1992) Histochemical probing of potato periderm with neutral red: a sensitive cytofluorochrome for the hydrophobic domain of suberin. Biotech Histochem 67:185–195

    Article  PubMed  CAS  Google Scholar 

  • 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 26:1713–1722

    Article  Google Scholar 

  • McDonald MP, Galwey NW, Colmer TD (2001a) Waterlogging tolerance in the tribe Triticeae: the adventitious roots of Critesion marinum have a relatively high porosity and a barrier to radial oxygen loss. Plant Cell Environ 24:585–596

    Article  Google Scholar 

  • McDonald MP, Galwey NW, Ellneskog-Staam P, Colmer TD (2001b) Evaluation of Lophopyrum elongatum as a source of genetic diversity to increase waterlogging tolerance of hexaploid wheat (Triticum aestivum). New Phytol 151:369–380

    Article  Google Scholar 

  • McDonald MP, Galwey NW, Colmer TD (2002) Similarity and diversity in adventitious root anatomy as related to root aeration among a range of wetland and dryland grass species. Plant Cell Environ 25:441–451

    Article  Google Scholar 

  • Mergemann H, Saute M (2000) Ethylene induces epidermal cell death at the site of adventitious root emergence in rice. Plant Physiol 124:609–614

    Article  PubMed  CAS  Google Scholar 

  • Mittler R, Rizhsky L (2000) Transgene-induced lesion mimic. Plant Mol Biol 44:335–344

    Article  PubMed  CAS  Google Scholar 

  • Moeder W, Barry CS, Tauriainen AA, Betz C, Tuomainen J, Utriainen M, Grierson D, Sandermann H, Langebartels C, Kangasjärvi J (2002) Ethylene synthesis regulated by biphasic induction of ACC synthase and ACC oxidase genes is required for H2O2 accumulation and cell death in ozone-exposed tomato. Plant Physiol 130:1918–1926

    Article  PubMed  CAS  Google Scholar 

  • Montillet JL, Chamnongpol S, Rustérucci C, Dat J, van de Cotte B, Agnel JP, Battesti C, Inzé D, Van Breusegem F, Triantaphylidès C (2005) Fatty acid hydroperoxides and H2O2 in the execution of hypersensitive cell death in tobacco leaves. Plant Physiol 138:1516–1526

    Article  PubMed  CAS  Google Scholar 

  • Overmyer K, Tuominen H, Kettunen R, Betz C, Langebartels C, Sandermann HJ, Kangasjärvi J (2000) Ozone-sensitive arabidopsis rcd1 mutant reveals opposite roles for ethylene and jasmonate signaling pathways in regulating superoxide-dependent cell death. Plant Cell 12:1849–1862

    PubMed  CAS  Google Scholar 

  • 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 107:1335–1343

    Article  PubMed  CAS  Google Scholar 

  • Ren D, Yang H, Zhang S (2002) Cell death mediated by MAPK is associated with hydrogen peroxide production in Arabidopsis. J Biol Chem 277:559–565

    Article  PubMed  CAS  Google Scholar 

  • Ros Barceló A (1998) The generation of H2O2 in the xylem of Zinnia elegans is mediated by an NADPH-oxidase-like enzyme. Planta 207:207–216

    Article  Google Scholar 

  • Samuel MA, Ellis BE (2002) Double jeopardy: both overexpression and suppression of a redox-activated plant mitogen-activated protein kinase render tobacco plants ozone sensitive. Plant Cell 14:2059–2069

    Article  PubMed  CAS  Google Scholar 

  • Steffens B, Sauter M (2005) Epidermal cell death in rice (Oryza sativa L.) is regulated by ethylene, gibberellin and abscisic acid. Plant Physiol 139:713–721

    Article  PubMed  CAS  Google Scholar 

  • Steffens B, Sauter M (2009) Epidermal cell death in rice is confined to cells with a distinct molecular identity and is mediated by ethylene and H2O2 through an autoamplified signal pathway. Plant Cell 21:184–196

    Article  PubMed  CAS  Google Scholar 

  • Steffens B, Geske T, Sauter M (2011) Aerenchyma formation in the rice stem and its promotion by H2O2. New Phytol 190:369–378

    Article  PubMed  CAS  Google Scholar 

  • Thomson CJ, Colmer TD, Watkins 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 

  • Watkin ELJ, Thomson CJ, Greenway H (1998) Root development and aerenchyma formation in two wheat cultivars and one triticale cultivar grown in stagnant agar and aerated nutrient solution. Ann Bot 81:349–354

    Article  Google Scholar 

  • Wong HL, Sakamoto T, Kawasaki T, Umemura K, Shimamoto K (2004) Downregulation of metallothionein, a reactive oxygen scavenger, by the small GTPase OsRac1 in rice. Plant Physiol 135:1447–1456

    Article  PubMed  CAS  Google Scholar 

  • Xiong HY, Li YS, Li LJ (2006) A unique form of cell death occurring in meristematic root tips of completely submerged maize seedlings. Plant Sci 171:624–631

    Article  CAS  Google Scholar 

  • Yamauchi T, Rajhi I, Nakazono M (2011) Lysigenous aerenchyma formation in maize root is confined to cortical cells by regulation of genes related to generation and scavenging of reactive oxygen species. Plant Signal Behav 6:759–761

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Chen Chunli for stimulating discussions. We also thank Tan Yuan for TEM technical supports. This work was supported by the National Foundation of China (Grant Nos. 31071347 and 31171469), and we declare that the authors have no conflict of interest.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Z. Q. Zhou.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Xu, Q.T., Yang, L., Zhou, Z.Q. et al. Process of aerenchyma formation and reactive oxygen species induced by waterlogging in wheat seminal roots. Planta 238, 969–982 (2013). https://doi.org/10.1007/s00425-013-1947-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-013-1947-4

Keywords

Navigation