Hormonal Modulation of Citrus Responses to Flooding

Article

Abstract

In this work, variations in endogenous levels of several hormones were measured in citrus under conditions of continuous flooding following a time-course design. The use of three genotypes differing in their ability to tolerate waterlogging has allowed the discrimination between common and specific hormonal responses. Data suggest an essential involvement of the aerial part in the regulation of tolerance to flooding, whereas in roots more general responses were detected. The progressive increase in leaf abscisic acid (ABA) correlating with the different tolerance of genotypes confirms the involvement of this hormone in plant responses to stress. The late increase in 1-aminocyclopropane-1-carboxylic acid, concomitant with severe leaf injury, points to ethylene as a promoter of leaf senescence in citrus. Leaf putrescine increased in all flooded genotypes, suggesting a general protective role, whereas a higher protective ability of spermidine and spermine was enforced by their exclusive accumulation in the sensitive genotype. Leaf jasmonic acid (JA) increased rapidly and transiently under flooding, suggesting a role for this hormone in triggering downstream responses. In stressed roots, while indole-3-acetic acid increased, JA and ABA levels rapidly decreased to reach almost complete depletion in all flooded citrus genotypes. This suggests that not only should the increase in the so-called stress hormones be considered a signal but also their reduction. The results contribute to the understanding of the intricate set of connections between plant hormones that regulate physiologic responses to stress.

Keywords

Abscisic acid 1-Aminocyclopropane-1-carboxylic acid Indole-3-acetic acid Jasmonic acid Putrescine Spermidine Spermine Waterlogging 

Notes

Acknowledgements

This work was supported by the Spanish Ministerio de Educación y Ciencia and Universitat Jaume I/Fundació Bancaixa through grants No. AGL2007-65437-C04-03/AGR and P1IB2006-02, respectively. Hormone determinations were performed in the central facilities (Servei Central d’Instrumentació Científica, SCIC) of Universitat Jaume I. Authors are grateful to Gerald Rix (M.D.) for proofreading the text.

References

  1. Arbona V, Flors V, Jacas J, Garcia-Agustin P, Gomez-Cadenas A (2003) Enzymatic and non-enzymatic antioxidant responses of carrizo citrange, a salt-sensitive citrus rootstock, to different levels of salinity. Plant Cell Physiol 44:388-394PubMedCrossRefGoogle Scholar
  2. Arbona V, Lopez-Climent MF, Mahouachi J, Perez-Clemente RM, Abrams SR, Gomez-Cadenas A (2006) Use of persistent analogs of abscisic acid as palliatives against salt-stress induced damage in citrus plants. J Plant Growth Regul 25:1–9CrossRefGoogle Scholar
  3. Arbona V, Hossain Z, Lopez-Climent MF, Perez-Clemente RM, Gomez-Cadenas A (2008) Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus. Physiol Plant 132:452–466 PubMedCrossRefGoogle Scholar
  4. 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 146:323–328Google Scholar
  5. Bouchereau A, Aziz A, Larher F, Martin-Tanguy J (1999) Polyamines and environmental challenges: recent development. Plant Sci 140:103–125CrossRefGoogle Scholar
  6. Castonguay Y, Nadeau P, Simard RR (1993) Effects of flooding on carbohydrate and ABA levels in roots and shoots of alfalfa. Plant Cell Environ 16:695–702CrossRefGoogle Scholar
  7. Cox MCH, Benschop JJ, Vreeburg RAM, Wagemaker CAM, Moritz T, Peeters AJM, Voesenek LACJ (2004) The roles of ethylene, auxin, abscisic acid, and gibberellin in the hyponastic growth of submerged rumex palustris petioles. Plant Physiol 136:2948–2960PubMedCrossRefGoogle Scholar
  8. Dat JF, Capelli N, Folzer H, Bourgeade P, Badot PM (2004) Sensing and signalling during plant flooding. Plant Physiol Biochem 42:273–282PubMedCrossRefGoogle Scholar
  9. Devoto A, Turner JG (2005) Jasmonate-regulated Arabidopsis stress signaling network. Physiol Plant 124:161–172CrossRefGoogle Scholar
  10. Dodd IC (2003) Hormonal interactions and stomatal responses. J Plant Growth Regul 22:32–46CrossRefGoogle Scholar
  11. Durgbanshi A, Arbona V, Pozo O, Miersch O, Sancho JV, Gomez-Cadenas A (2005) Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography-electrospray tandem mass spectrometry. J Agric Food Chem 53:8437–8442PubMedCrossRefGoogle Scholar
  12. Else MA, Hall KC, Arnold GM, Davies WJ, Jackson MB (1995) Export of abscisic-acid, 1-aminocyclopropane-1-carboxylic acid, phosphate, and nitrate from roots to shoots of flooded tomato plants—accounting for effects of xylem sap flow-rate on concentration and delivery. Plant Physiol 107:377–384PubMedGoogle Scholar
  13. Else MA, Tiekstra AE, Croker SJ, Davies WJ, Jackson MB (1996) Stomatal closure in flooded tomato plants involves abscisic acid and a chemically unidentified anti-transpirant in xylem sap. Plant Physiol 112:239–247PubMedGoogle Scholar
  14. Else MA, Coupland D, Dutton L, Jackson MB (2001) Decreased root hydraulic conductivity reduces leaf water potential, initiates stomatal closure and slows leaf expansion in flooded plants of castor oil (Ricinus communis) despite diminished delivery of ABA from the roots to shoots in xylem sap. Physiol Plant 111:46–54CrossRefGoogle Scholar
  15. Ford HW (1968) Water management of wetland citrus in Florida. In: Proc 1st int citrus symp, vol 3, pp 1759–1770Google Scholar
  16. Gómez-Cadenas A, Tadeo FR, Talón M, PrimoMillo E (1996) Leaf abscission induced by ethylene in water-stressed intact seedlings of Cleopatra mandarin requires previous abscisic acid accumulation in roots. Plant Physiol 112:401–408PubMedGoogle Scholar
  17. Gómez-Cadenas A, Tadeo FR, Primo-Millo E, Talón M (1998) Involvement of abscisic acid and ethylene in the responses of citrus seedlings to salt shock. Physiol Plant 103:475–484CrossRefGoogle Scholar
  18. Gómez-Cadenas A, Mehouachi J, Tadeo FR, Primo-Millo E, Talón M (2000) Hormonal regulation of fruitlet abscission induced by carbohydrate shortage in citrus. Planta 210:636–643PubMedCrossRefGoogle Scholar
  19. Gómez-Cadenas A, Pozo OJ, García-Agustín P, Sancho JV (2002) Direct analysis of abscisic acid in crude plant extracts by liquid chromatography-electrospray/tandem mass spectrometry. Phytochem Anal 13:228–234PubMedCrossRefGoogle Scholar
  20. Ho T-HD, Gómez-Cadenas A, Zentella R, Casaretto J (2003) Crosstalk between giberellins and abscisic acid in cereal aleurone. J Plant Growth Regul 22:185–194CrossRefGoogle Scholar
  21. Hunter KJ (1998) A dansyl chloride HPLC method for the determination of polyamines. In: Morgan D (ed) Methods in molecular biology. Polyamine protocols. Humana Press, Totowa, NJ, pp 119–123Google Scholar
  22. Hurng WP, Kao CH (1993) Endogenous polyamine levels and flooding-enhanced leaf senescence of tobacco. Plant Sci 91:121–125CrossRefGoogle Scholar
  23. Hurng WP, Lur HS, Liao CK, Kao CH (1994) Role of abscisic acid, ethylene and polyamines in flooding-promoted senescence of tobacco leaves. J Plant Physiol 143:102–105Google Scholar
  24. Jackson MB, Young SF, Hall KC (1988) Are roots a source of abscisic-acid for the shoots of flooded pea-plants. J Exp Bot 39:1631–1637CrossRefGoogle Scholar
  25. Kristl J, Veber M, Krajnicic B, Oresnik K, Slekovec M (2005) Determination of jasmonic acid in Lemna minor (L.) by liquid chromatography with fluorescence detection. Anal Bioanal Chem 383:886–893PubMedCrossRefGoogle Scholar
  26. Larson KD, Schaffer B, Davies FS (1993) Floodwater oxygen-content, ethylene production and lenticel hypertrophy in flooded mango (Mangifera indica L) trees. J Exp Bot 44:665–671CrossRefGoogle Scholar
  27. López-Climent MF, Arbona V, Pérez-Clemente RM, Gómez-Cadenas A (2008) Relationship between salt tolerance and photosynthetic machinery performance in citrus. Environ Exp Bot 62:176–184CrossRefGoogle Scholar
  28. Mahouachi J, Arbona V, Gómez-Cadenas A (2007) Hormonal changes in papaya seedlings subjected to progressive water stress and re-watering. Plant Growth Regul 53:43–51CrossRefGoogle Scholar
  29. Nada K, Iwatani E, Doi T, Tachibana S (2006) Effect of putrescine pretreatment to roots on growth and lactate metabolism in the root of tomato (Lycopersicon esculentum Mill.) under root-zone hypoxia. J Jpn Soc Hort Sci 73:337–339CrossRefGoogle Scholar
  30. Nayyar H, Chander S (2004) Protective effects of polyamines against oxidative stress induced by water and cold stress in chickpea. J Agron Crop Sci 190:355–365CrossRefGoogle Scholar
  31. O’Donnell PJ, Schmelz E, Block A, Miersch O, Wasternack C, Jones JB, Klee HJ (2003) Multiple hormones act sequentially to mediate a susceptible tomato pathogen defense response. Plant Physiol 133:1181–1189PubMedCrossRefGoogle Scholar
  32. Olivella C, Biel C, Vendrell M, Save R (2000) Hormonal and physiological responses of Gerbera jamesonii to flooding stress. HortScience 35:222–225Google Scholar
  33. Pedranzani H, Racagni G, Alemano S, Miersch O, Ramirez I, Pena-Cortes H, Taleisnik E, Machado-Domenech E, Abdala G (2003) Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regul 41:149–158CrossRefGoogle Scholar
  34. Pierik R, Sasidharan R, Voesenek LACJ (2007) Growth control by ethylene: adjusting phenotypes to the environment. J Plant Growth Regul 26:188–200CrossRefGoogle Scholar
  35. Pollmann S, Müller A, Weiler EW (2006) Many roads lead to “Auxin”: of nitrilases, synthases, and amidases. Plant Biol 8:326–333PubMedCrossRefGoogle Scholar
  36. Seidel C, Walz A, Park S, Cohen JD, Ludwig-Müller J (2006) Indole-3-acetic acid protein conjugates: novel players in auxin homeostasis. Plant Biol 8:340–345PubMedCrossRefGoogle Scholar
  37. 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 91:205–211PubMedCrossRefGoogle Scholar
  38. Wasternack C (2007) Jasmonates: An update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann Bot 100:681–697PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2008

Authors and Affiliations

  1. 1.Departmento de Ciències Agràries i del Medi Natural Universitat Jaume ICastelló de la PlanaSpain

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