Physiological and biochemical responses of Eucalyptus seedlings to hypoxia
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.
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
This study aimed to evaluate the hormonal and metabolic alterations induced by hypoxia on seedling growth.
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.
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.
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.
KeywordsGrowth inhibition Hormones Photosynthetic response Primary metabolism
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.
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.
- Abraf, Anuário Estatístico da Abraf (2013) Ano base 2012. Associação Brasileira de Produtores de Florestas Plantadas, Brasília, 2012.148 pGoogle Scholar
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- 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
- Indústria brasileira de árvores. Iba 2014. http://www.iba.org/shared/iba_2014_pt.pdf
- 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
- National Register of Cultivars Website: http://sistemas.agricultura.gov.br/snpc/cultivarweb/cultivares_registradas.php
- 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
- 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
- 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
- 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
- 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
- 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
- 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