Skip to main content
Log in

Comparative Analysis of Endogenous Hormones in Leaves and Roots of Two Contrasting Malus Species in Response to Hypoxia Stress

  • Published:
Journal of Plant Growth Regulation Aims and scope Submit manuscript

Abstract

Plant hormones play important roles in regulating developmental processes and signaling networks involved in plant responses to biotic and abiotic stresses. We comparatively studied the growth and endogenous hormonal levels in leaves and roots in two Malus species (M. sieversii and M. hupehensis) differing in hypoxia tolerance under normoxic and hypoxia stress. The results showed that hypoxia stress inhibited growth of seedlings of both Malus species, but with significant differences in intensity. Exposure to hypoxia altered the levels of endogenous hormones in leaves and roots in both Malus seedlings. Leaf and root abscisic acid (ABA) contents increased in response to hypoxia stress in both genotypes despite different extents. Compared with M. hupehensis, M. sieversii was more responsive to hypoxia stress, resulting in larger increases in leaf and root ABA contents. The changes in leaf and root ABA contents correlating with the different tolerance levels of the genotypes confirm the involvement of this hormone in plant responses to hypoxia stress. Gibberellins (GAs; GA1 + GA4) continuously increased in leaves and roots during the whole period of stress, whereas indole-3-acetic acid (IAA) showed a sharp increase at the early stage in both Malus seedlings. In addition, zeatin riboside (ZR), dihydrozeatin riboside (DHZR), and isopentenyl adenine (IPA) differed in their pattern of changes in both Malus seedlings under hypoxia stress. Based on variations in endogenous hormonal levels in both Malus species that differ in their ability to tolerate hypoxia, we conclude that not a single hormone but multiple hormones and their interplay are responsible for hypoxia tolerance.

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

Access this article

Price includes VAT (Canada)

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Arbona V, Gómez-Cadenas A (2008) Hormonal modulation of citrus responses to flooding. J Plant Growth Regul 27:241–250

    Article  CAS  Google Scholar 

  • Azuma T, Hirano T, Deki Y, Uchida N, Yasuda T, Yamaguchi T (1995) Involvement of the decrease in levels of abscisic-acid in the internodal elongation of submerged floating rice. J Plant Physiol 146:323–332

    CAS  Google Scholar 

  • Bai T, Li C, Ma F, Shu H, Han M (2008) Physiological responses and analysis of tolerance of apple rootstocks to root-zone hypoxia stress. Agric Sci China 41:4140–4148

    CAS  Google Scholar 

  • Bai T, Li C, Ma F, Shu H, Han M (2009) Exogenous salicylic acid alleviates growth inhibition and oxidative stress induced by hypoxia stress in Malus robusta Rehd. J Plant Growth Regul 28:358–366

    Article  CAS  Google Scholar 

  • Bai T, Li C, Ma F, Feng F, Shu H (2010) Responses of growth and antioxidant system to root-zone hypoxia stress in two Malus species. Plant Soil 327:95–105

    Article  CAS  Google Scholar 

  • Bailey-Serres J, Chang R (2005) Sensing and signaling in response to oxygen deprivation in plants and other organisms. Ann Bot 96:507–518

    Article  PubMed  CAS  Google Scholar 

  • Balbi V, Devoto A (2008) Jasmonate signaling network in Arabidopsis thaliana: crucial regulatory nodes and new physiological scenarios. New Phytol 177:301–318

    Article  PubMed  CAS  Google Scholar 

  • Branco-Price C, Kawaguchi R, Ferreira R, Bailey-Serres J (2005) Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Ann Bot 96:647–660

    Article  PubMed  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  PubMed  CAS  Google Scholar 

  • Dat JF, Capelli N, Folzer H, Bourgeade P, Badot PM (2004) Sensing and signaling during plant flooding. Plant Physiol Biochem 42:273–282

    Article  PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Ellis MH, Dennis ES, Peacock WJ (1999) Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance. Plant Physiol 119:57–64

    Article  PubMed  CAS  Google Scholar 

  • Fukao T, Bailey-Serres J (2008) Ethylene—a key regulator of submergence responses in rice. Plant Sci 175:43–51

    Article  CAS  Google Scholar 

  • Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18:2021–2034

    Article  PubMed  CAS  Google Scholar 

  • Garcia-Martinez JL, Gil J (2002) Light regulation of gibberellin biosynthesis and mode of action. J Plant Growth Regul 20:354–368

    Article  Google Scholar 

  • Garnczarska M, Bednarski W (2004) Effect of a short-term hypoxic treatment followed by re-aeration on free radicals level and antioxidative enzymes in lupine roots. Plant Physiol Biochem 42:233–240

    Article  PubMed  CAS  Google Scholar 

  • He Z (1993) a laboratory guide to chemical control technology on field crop. Beijing Agricultural University Press, Beijing, pp 60–68

    Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agriculture Experiment Station Circular 347

  • Hwang S, VanToai TT (1991) Abscisic acid induces Anaerobiosis tolerance in corn. Plant Physiol 97:593–597

    Article  PubMed  CAS  Google Scholar 

  • Jackson MB (1990) Hormones and developmental change in plants subjected to submergence or soil waterlogging. Aquat Bot 38:49–72

    Article  CAS  Google Scholar 

  • Jackson MB, Young SF, Hall KC (1988) Are roots a source of abscisic-acid for the shoots of flooded pea-plants? J Exp Bot 39:1631–1637

    Article  CAS  Google Scholar 

  • Kato-Noguchi H (2000) Abscisic acid and hypoxic induction of anoxia tolerance in roots of lettuce seedlings. J Exp Bot 51:1939–1944

    Article  PubMed  CAS  Google Scholar 

  • Koiwa H, Bressan RA, Hasegawa PA (1997) Regulation of proteinase inhibitors and plant defense. Trends Plant Sci 2:379–384

    Article  Google Scholar 

  • Liu X, Huang B (2005) Root physiological factors involved in cool-season grass response to high soil temperature. Environ Exp Bot 53:233–245

    Article  Google Scholar 

  • Mahouachi J, Arbona V, Gómez-Cadenas A (2007) Hormonal changes in papaya seedlings subjected to progressive water stress and re-watering. Plant Growth Regul 53:43–51

    Article  CAS  Google Scholar 

  • Olivella C, Biel C, Vendrell M, Save R (2000) Hormonal and physiological responses of Gerbera jamesonii to flooding stress. HortScience 35:222–225

    CAS  Google Scholar 

  • Pierik R, Sasidharan R, Voesenek LACJ (2007) Growth control by ethylene: adjusting phenotypes to the environment. J Plant Growth Regul 26:188–200

    Article  CAS  Google Scholar 

  • Rawyler A, Arpagaus S, Braendle R (2002) Impact of oxygen stress and energy availability on membrane stability of plant cells. Ann Bot 90:499–507

    Article  PubMed  CAS  Google Scholar 

  • Reid DM, Wample RL (1985) Water relations and plant hormones. In: Pharis RP, Reid DM (eds) Encyclopedia of plant physiology. Springer, Berlin, pp 513–578

    Google Scholar 

  • Robert-Seilaniantz A, Navarro L, Bari R, Jones JDG (2007) Pathological hormone imbalances. Curr Opin Plant Biol 10:372–379

    Article  PubMed  CAS  Google Scholar 

  • Sasaki-Sekimoto Y, Taki N, Obayashi T, Aono M, Matsumoto F, Sakurai N, Suzuki H, Hirai MY, Noji M, Saito K, Masuda T, Takamiya K, Shibata D, Ohta H (2005) Coordinated activation of metabolic pathways for antioxidants and defense compounds by jasmonates and their roles in stress tolerance in Arabidopsis. Plant J 44:653–668

    Article  PubMed  CAS  Google Scholar 

  • Valdés AE, Fernández B, Centeno ML (2004) Hormonal changes throughout maturation and ageing in Pinus pinea. Plant Physiol Biochem 42:335–340

    Article  PubMed  Google Scholar 

  • van Zanten M, Voesenek LACJ, Peeters AJM, Millenaar FF (2009) Hormone- and light-mediated regulation of heat-induced differential petiole growth in Arabidopsis. Plant Physiol 151:1446–1458

    Article  PubMed  Google Scholar 

  • Voesenek LACJ, Benschop JJ, Bou J, Cox MCH, Groeneveld HW, Millenaar FF, Vreeburg RAM, Peeters AJM (2003) Interactions between plant hormones regulate submergence-induced shoot elongation in the flooding-tolerant dicot Rumex palustris. Ann Bot 91:205–211

    Article  PubMed  CAS  Google Scholar 

  • Wang Q, Zhang L, Guan Y, Wang Z (2006) Endogenous hormone concentration in developing tuberous roots of different sweet potato genotypes. Agric Sci China 5:919–927

    CAS  Google Scholar 

  • Wasternack C (2007) Jasmonates: an update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697

    Article  PubMed  CAS  Google Scholar 

  • Weiler EW, Jordan PS, Conrad W (1981) Levels of indole-3-acetic acid in intact and decapitated coleoptiles as determined by a specific and highly sensitive solid-phase enzyme immunoassay. Planta 153:561–571

    Article  CAS  Google Scholar 

  • Weyers JDB, Paterson NW (2001) Plant hormones and the control of physiological processes. New Phytol 152:375–407

    Article  CAS  Google Scholar 

  • Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought, and salt stress. Plant Cell 14:165–183

    Article  Google Scholar 

  • Yang J, Zhang J, Wang Z, Zhu Q, Wang W (2001) Hormonal changes in the grains of rice subjected to water stress during grain filling. Plant Physiol 127:315–323

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported in part by the Agriculture Ministry of China (2006-G28), China Postdoctoral Science Foundation-funded project (20060390310), and the Modern Agricultural Industry Technology System in China. We thank Dr. Kenong Xu for providing advice and critical reading of the manuscript and Mr. Xuanchang Fu for his technical assistance in growing and management of the plant materials.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Fengwang Ma.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bai, T., Yin, R., Li, C. et al. Comparative Analysis of Endogenous Hormones in Leaves and Roots of Two Contrasting Malus Species in Response to Hypoxia Stress. J Plant Growth Regul 30, 119–127 (2011). https://doi.org/10.1007/s00344-010-9173-9

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00344-010-9173-9

Keywords

Navigation

-