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Physiological and biochemical responses of Eucalyptus seedlings to hypoxia

  • Eduardo F. MedinaEmail author
  • Gustavo C. V. Mayrink
  • Cleide R. Dias
  • Camilo E. Vital
  • Dimas M. Ribeiro
  • Ivo R. Silva
  • Andrew Merchant
Research Paper

Abstract

Key message

Hypoxia promoted distinct changes in the levels of hormones, amino acids and organic acids in the roots and shoots of a seedling from 2 Eucalyptus clones. These results indicate that modulation of hormone production, as well as specific chemical constituents associated with primary metabolism, contributes to the regulation of growth of Eucalyptus seedlings under hypoxic conditions.

Context

Although floods in areas under Eucalyptus cultivation in Brazil negatively affect plant growth, chemical markers and/or indicators of hypoxia contributes to the regulation.s

Aims

This study aimed to evaluate the hormonal and metabolic alterations induced by hypoxia on seedling growth.

Methods

Seedlings of Eucalyptus urograndis clones VCC 975 and 1004 were grown in liquid solution and submitted to bubbling with air or with nitrogen. Levels of indol-3-acetic acid (IAA), abscisic acid (ABA), ethylene, 1-aminocyclopropane-1-carboxylic acid (ACC), primary metabolite profile and photosynthetic parameters were evaluated after fourteen days.

Results

Hypoxia did not affect shoot dry mass of the seedlings. However, it decreased stomatal conductance and photosynthetic CO2 assimilation rate, and increased levels of ABA in the shoot. Hypoxia greatly reduced the dry mass and volume of roots, concomitantly with higher ACC and ethylene production. Moreover, hypoxia promoted distinct changes in IAA levels, and in amino acid and organic acid metabolism in roots and shoots.

Conclusion

The biosynthesis of ABA, ethylene and IAA and its quantity in root tissues indicates the regulation of metabolism in response to hypoxia in Eucalyptus clones.

Keywords

Growth inhibition Hormones Photosynthetic response Primary metabolism 

Notes

Acknowledgments

Discussions with Professor Timothy Colmer (University of Western Australia) were highly valuable in the development of this work. My gratitude is also extended to the NUBIOMOL (Núcleo de Análises de Biomoléculas) for the support with the LC-MS analysis.

Funding

EFM would like to thank CAPES (Coordination of Personal Improvement at the Higher Level) and CNPq (Brazilian Council for Advancement of Science and Technology) for the financial support.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Supplementary material

13595_2018_789_MOESM1_ESM.docx (1.7 mb)
Supplementary material 1 Supplementary figures and tables (DOCX 1712 kb)
13595_2018_789_MOESM2_ESM.pdf (48 kb)
Supplementary material 2 Two-Way ANOVA data (PDF 47 kb)

References

  1. Abraf, Anuário Estatístico da Abraf (2013) Ano base 2012. Associação Brasileira de Produtores de Florestas Plantadas, Brasília, 2012.148 pGoogle Scholar
  2. Araújo WL, Martins AO, Fernie AR, Tohge T (2014) 2-Oxoglutarate: linking TCA cycle function with amino acid, glucosinolate, flavonoid, alkaloid, and gibberellin biosynthesis. Front Plant Sci 5:552PubMedPubMedCentralGoogle Scholar
  3. 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 38:1189–1199.  https://doi.org/10.1111/pce.12473 CrossRefPubMedGoogle Scholar
  4. Bai T, Yin R, Li C, Ma F, Yue Z, Shu H (2011) 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.  https://doi.org/10.1007/s00344-010-9173-9 CrossRefGoogle Scholar
  5. Bailey-Serres J, Voesenek LACJ (2008) Flooding stress: acclimations and genetic diversity. Annu Rev Plant Biol 59:313–339.  https://doi.org/10.1146/annurev.arplant.59.032607.092752 CrossRefPubMedGoogle Scholar
  6. Bailey-Serres J, Fukao T, Gibbs DJ, Holdsworth MJ, Lee SC, Licausi F, Perata P, LACJ V, van Dongen JT (2012) Making sense of low oxygen sensing. Trends Plant Sci 17(3):129–138.  https://doi.org/10.1016/j.tplants.2011.12.004 CrossRefPubMedGoogle Scholar
  7. Beckman TG, Perry RL, Flore JA (1992) Short-term flooding affects gas exchange characteristics of containerized sour cherry trees. HortScience 27:1297–1301 http://hortsci.ashspublications.org/content/27/12/1297.short Google Scholar
  8. Bison O, Ramalho MAP, Rezende GDSP, Rezende MDV (2006) Comparison between open pollinated progenies and hybrids performance in Eucalyptus grandis and Eucalyptus urophylla. Silvae Genet 55(4/5):192–196.  https://doi.org/10.1515/sg-2006-0026 CrossRefGoogle Scholar
  9. Branco-Price C, Kaiser KA, Jang CJH, Larive CK, Bailey-Serres J (2008) Selective mRNA translation coordinates energetic and metabolic adjustments to cellular oxygen deprivation and reoxygenation in Arabidopsis thaliana. Plant J 56:743–755.  https://doi.org/10.1111/j.1365-313X.2008.03642.x CrossRefPubMedGoogle Scholar
  10. Cao WH, Liu J, He XJ, Mu RL, Zhou HL, Chen SY, Zhang JS (2007) Modulation of ethylene responses affects plant salt-stress responses. Plant Physiol 143:707–719.  https://doi.org/10.1104/pp.106.094292 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Clark R (1975) Characterization of phosphatase of intact maize roots. J Agric Food Chem 23:458–460.  https://doi.org/10.1021/jf60199a002 CrossRefPubMedGoogle Scholar
  12. Colmer TD, Voesenek LACJ (2009) Flooding tolerance: suites of plant traits in variable environments. Funct Plant Biol 36:665–681.  https://doi.org/10.1071/FP09144 CrossRefGoogle Scholar
  13. Dethloff F, Erban A, Orf I, Alpers J, Fehrle I, Beine-Golovchuk O, Schmidt S, Schwachtje J, Kopka J (2014) Profiling methods to identify cold-regulated primary metabolites using gas chromatography coupled to mass spectrometry. Method Mol Biol 1166:171–197.  https://doi.org/10.1007/978-1-4939-0844-8_14 CrossRefGoogle Scholar
  14. Dreyer E (1994) Compared sensitivity of seedlings from 3 woody species (Quercus robur L., Quercus rubra L and Fagus sylvatica L.) to waterlogging and associated root hypoxia: effects on water relations and photosynthesis. Ann For Sci 51:417–429.  https://doi.org/10.1051/forest:19940407 CrossRefGoogle Scholar
  15. Feng X, Porporato A, Rodriguez-Iturbe I (2013) Changes in rainfall seasonality in the tropics. Nat Clim Chang 3(9):811–815.  https://doi.org/10.1038/nclimate1907 CrossRefGoogle Scholar
  16. Geisler-Lee J, Caldwell C, Gallie DR (2010) Expression of the ethylene biosynthetic machinery in maize roots is regulated in response to hypoxia. J Exp Bot 61:857–871.  https://doi.org/10.1093/jxb/erp362 CrossRefPubMedGoogle Scholar
  17. Genty B, Briantais JM, Baker NR (1989) The relationship between the quantum yield of photosynthetic electron transport and quenching of chlorophyll fluorescence. Biochim Biophys Acta Gen Subj 990(1):87–92.  https://doi.org/10.1016/S0304-4165(89)80016-9 CrossRefGoogle Scholar
  18. Gonçalves JLM, Alvares CA, Souza AHBN, Arthur Junior JC (2016) Caracterização edafoclimática e manejo de solos das áreas com plantações de eucalipto. In: Schumacher MV, Viera M, organizadores. Silvicult Euc Brasil. Santa Maria: Editora UFSM; p.111–54Google Scholar
  19. Graf A, Schlereth A, Stitt M, Smith AM (2010) Circadian control of carbohydrate availability for growth in Arabidopsis plants at night. Proc Natl Acad Sci U S A 107:9458–9463.  https://doi.org/10.1073/pnas.0914299107 CrossRefPubMedPubMedCentralGoogle Scholar
  20. Harguindeguy I, Castro GF, Novais SV, Vergutz L, Araujo WL, Novais RF (2017) Physiological responses to hypoxia and manganese in Eucalyptus clones with differential tolerance to Vale do Rio Doce shoot dieback. Rev Bras Cienc Solo 41:e0160550.  https://doi.org/10.1590/18069657rbcs20160550 CrossRefGoogle Scholar
  21. Harrington JT, Mexal JG, Fisher JT (1994) Volume displacement provides a quick and accurate way to quantify new root production. Tree Plant Notes 45:121–124Google Scholar
  22. Ibrahim MH, Jaafar HZE (2013) Abscisic acid induced changes in production of primary and secondary metabolites, photosynthetic capacity, antioxidant capability, antioxidant enzymes and lipoxygenase inhibitory activity of Orthosiphon stamineus Benth. Molecules 18:7957–7976.  https://doi.org/10.3390/molecules18077957 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Indústria brasileira de árvores. Iba 2014. http://www.iba.org/shared/iba_2014_pt.pdf
  24. Kreuzwieser J, Rennenberg H (2014) Molecular and physiological responses of trees to waterlogging stress. Plant Cell Environ 37:2245–2259.  https://doi.org/10.1111/pce.12310 CrossRefPubMedGoogle Scholar
  25. Leite FP, Novais RF, Silva IR, Barros NF, Neves JCL, Medeiros AGB, Ventrella MC, Villani EMA (2014) Manganese accumulation and its relation to “eucalyptus shoot blight in the Vale do Rio Doce”. Rev Bras Cienc Solo 38:193–204.  https://doi.org/10.1590/S0100-06832014000100019 CrossRefGoogle Scholar
  26. Lisec J, Schauer N, Kopka J, Willmitzer L, Fernie AR (2006) Gas chromatography mass spectrometry–based metabolite profiling in plants. Nat Protoc 1:387–396.  https://doi.org/10.1038/nprot.2006.59 CrossRefPubMedGoogle Scholar
  27. Loreti E, van Veen H, Perata P (2016) Plant responses to flooding stress. Curr Opin Plant Biol 33:64–71.  https://doi.org/10.1016/j.pbi.2016.06.005 CrossRefPubMedGoogle Scholar
  28. Luedemann A, Strassburg K, Erban A, Kopka J (2008) TagFinder for the quantitative analysis of gas chromatography-mass spectrometry (GC-MS)-based metabolite profiling experiments. Bioinformatics 24(5):732–737.  https://doi.org/10.1093/bioinformatics/btn023 CrossRefPubMedGoogle Scholar
  29. Mergemann H, Sauter M (2000) Ethylene induces epidermal cell death at the site of adventitious root emergence in rice. Plant Physiol 124(2):609–614.  https://doi.org/10.1104/pp.124.2.609 CrossRefPubMedPubMedCentralGoogle Scholar
  30. Michaeli S, Fait A, Lagor K, Nunes-Nesi A, Grillich N, Yellin A, Bar D, Khan M, Fernie AR, Turano FJ, Fromm H (2011) A mitochondrial GABA permease connects the GABA shunt and the TCA cycle, and is essential for normal carbon metabolism. Plant J 67(3):485–498.  https://doi.org/10.1111/j.1365-313X.2011.04612.x CrossRefPubMedGoogle Scholar
  31. Müller M, Munné-Bosch S (2011) Rapid and sensitive hormonal profiling of complex plant samples by liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Plant Methods 7(1):37.  https://doi.org/10.1186/1746-4811-7-37 CrossRefPubMedPubMedCentralGoogle Scholar
  32. Paul MV, Iyer S, Amerhauser C, Lehmann M, van Dongen JT, Geigenberger P (2016) Oxygen sensing via the ethylene response transcription factor RAP2.12 affects plant metabolism and performance under both normoxia and hypoxia. Plant Physiol 172:141–153.  https://doi.org/10.1104/pp.16.00460 CrossRefPubMedPubMedCentralGoogle Scholar
  33. Peng HP, Lin TY, Wang NN, Shih MC (2005) Differential expression of genes encoding 1-aminocyclopropane-1-carboxylate synthase in Arabidopsis during hypoxia. Plant Mol Biol 58:15–25.  https://doi.org/10.1007/s11103-005-3573-4 CrossRefPubMedGoogle Scholar
  34. Pierik R, Sasidharan R, Voesenek LACJ (2007) Growth control by ethylene: adjusting phenotypes to the environment. J Plant Growth Regul 26(2):188–200.  https://doi.org/10.1007/s00344-006-0124-4 CrossRefGoogle Scholar
  35. Renault H, El Amrani A, Berger A, Mouille G, Soubigou-TaconnaT L, Bouchereau A, Deleu C (2013) γ-Aminobutyric acid transaminase deficiency impairs central carbon metabolism and leads to cell wall defects during salt stress in Arabidopsis roots. Plant Cell Environ 36(5):1009–1018.  https://doi.org/10.1111/pce.12033 CrossRefPubMedGoogle Scholar
  36. Rocha M, Licausi F, Araújo WL, Nunes-Nesi A, Sodek L, Fernie AR, van Dongen JT (2010) Glycolysis and the tricarboxylic acid cycle are linked by alanine aminotransferase during hypoxia induced by waterlogging of Lotus japonicus. Plant Physiol 152(3):1501–1513.  https://doi.org/10.1104/pp.109.150045 CrossRefPubMedPubMedCentralGoogle Scholar
  37. Rockwood DL, Rudie AW, Ralph SA, Zhu JY, Winandy JE (2008) Energy product options for eucalyptus species grown as short rotation woody crops. Int J Mol Sci 9(8):1361–1378.  https://doi.org/10.3390/ijms9081361 CrossRefPubMedPubMedCentralGoogle Scholar
  38. Silva PO, Medina EF, Barros RS, Ribeiro DM (2014) Germination of salt-stressed seeds as related to the ethylene biosynthesis ability in three Stylosanthes species. J Plant Physiol 171(1):14–22.  https://doi.org/10.1016/j.jplph.2013.09.004 CrossRefPubMedGoogle Scholar
  39. Steffens B, Rasmussen A (2016) The physiology of adventitious roots. Plant Physiol 170(2):603–617.  https://doi.org/10.1104/pp.15.01360 CrossRefPubMedGoogle Scholar
  40. 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.  https://doi.org/10.1105/tpc.108.061887 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Steffens B, Sauter M (2014) Role of ethylene and other plant hormones in orchestrating the responses to low oxygen conditions. Plant Cell Monographs 21:117–132.  https://doi.org/10.1007/978-3-7091-1254-0_7 CrossRefGoogle Scholar
  42. Steffens B, Steffen-Heins A, Sauter M (2013) Reactive oxygen species mediate growth and death in submerged plants. Front Plant Sci 4:179.  https://doi.org/10.3389/fpls.2013.00179 CrossRefPubMedPubMedCentralGoogle Scholar
  43. Sulpice R, Flis A, Ivakov AA, Apelt F, Krohn N, Encke B, Abel C, Feil R, Lunn JE, Stitt M (2014) Arabidopsis coordinates the diurnal regulation of carbon allocation and growth across a wide range of photoperiods. Mol Plant 7(1):137–155.  https://doi.org/10.1093/mp/sst127 CrossRefPubMedGoogle Scholar
  44. Van de Poel B, Van Der Straeten D (2014) 1-aminocyclopropane-1-carboxylic acid (ACC) in plants: more than just the precursor of ethylene! Front Plant Sci 5:640.  https://doi.org/10.3389/fpls.2014.00640 CrossRefPubMedPubMedCentralGoogle Scholar
  45. Vartapetian BB, Jackson MB (1997) Plant adaptations to anaerobic stress. Ann Bot 79:3–20.  https://doi.org/10.1093/oxfordjournals.aob.a010303 CrossRefGoogle Scholar
  46. Vidoz ML, Loreti E, Mensuali A, Alpi A, Perata P (2010) Hormonal interplay during adventitious root formation in flooded tomato plants. Plant J 63:551–562.  https://doi.org/10.1111/j.1365-313X.2010.04262.x CrossRefPubMedGoogle Scholar
  47. Voesenek LACJ, Bailey-Serres J (2015) Flood adaptive traits and processes: an overview. New Phytol 206:57–73.  https://doi.org/10.1111/nph.13209 CrossRefPubMedGoogle Scholar
  48. Voesenek LACJ, Banga M, Thier RH, Mudde CM, Harren FJM, Barendse GWM, Blom CWPM (1993) Submergence-induced ethylene synthesis, entrapment, and growth in two plant species with contrasting flooding resistances. Plant Physiol 103(3):783–790.  https://doi.org/10.1104/pp.103.3.783 CrossRefPubMedPubMedCentralGoogle Scholar
  49. Wang L, Ruan YL (2013) Regulation of cell division and expansion by sugar and auxin signaling. Front Plant Sci 4:163.  https://doi.org/10.3389/fpls.2013.00163 CrossRefPubMedPubMedCentralGoogle Scholar
  50. Yamauchi T, Watanabe K, Fukazawa A, Mori H, Abe F, Kawaguchi K, Oyanagi A, Nakazono M (2013) Ethylene and reactive oxygen species are involved in root aerenchyma formation and adaptation of wheat seedlings to oxygen-deficient conditions. J Exp Bot 65(1):261–273.  https://doi.org/10.1093/jxb/ert371 CrossRefPubMedPubMedCentralGoogle Scholar
  51. Yukiyoshi K, Karahara I (2014) Role of ethylene signalling in the formation of constitutive aerenchyma in primary roots of rice. AoB Plants 6:plu043.  https://doi.org/10.1093/aobpla/plu043 CrossRefPubMedPubMedCentralGoogle Scholar
  52. Zou J, Li X, Ratnasekera D, Wang C, Liu W, Song L, Zhang W, Wu W (2015) Arabidopsis calcium-dependent protein kinase8 and catalase3 function in abscisic acid-mediated signaling and H2O2 homeostasis in stomatal guard cells under drought stress. Plant Cell 27(5):1445–1460.  https://doi.org/10.1105/tpc.15.00144 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© INRA and Springer-Verlag France SAS, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Departamento de Solos e Nutrição de PlantasUniversidade Federal de ViçosaViçosaBrazil
  2. 2.Departamento de EntomologiaUniversidade Federal de ViçosaViçosaBrazil
  3. 3.Núcleo de Análises de BiomoléculasViçosaBrazil
  4. 4.Departamento de Biologia VegetalUniversidade Federal de ViçosaViçosaBrazil
  5. 5.Faculty of ScienceThe University of SydneySydneyAustralia

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