Abstract
In response to adverse environmental conditions, plants modify their metabolism to adapt to the new conditions. To differentiate common responses to abiotic stress from specific adaptation to a certain stress condition, two citrus rootstocks (Carrizo citrange and Cleopatra mandarin) with a different ability to tolerate stress were subjected to soil flooding and drought, two water stress conditions. In response to these conditions, both genotypes showed altered root proline and phenylpropanoid levels, especially cinnamic acid, which was a common feature to Carrizo and Cleopatra. This was correlated with alterations in the levels of phenylpropanoid derivatives likely involved in lignin biosynthesis. In the regulatory part, levels of both stress hormones abscisic acid (ABA) and jasmonic acid (JA) decreased in response to soil flooding irrespective of the genotype’s relative flooding tolerance, but, on the other hand, the concentration of both metabolites increased in response to drought, showing a transient accumulation of JA after a few days and a progressive pattern of ABA increase. These responses are probably associated with different regulatory processes under soil flooding and drought. In addition, alterations in indole acetic acid (IAA) levels in citrus roots seemed to be associated with particular stress tolerance. Moreover, both genotypes exhibited a low degree of overlap in the metabolites induced under similar stress conditions, indicating a specific mechanism to cope with stress in plant species. Results also indicated a different metabolic basal status in both genotypes that could contribute to stress tolerance.
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References
Arbona V, Gómez-Cadenas A (2008) Hormonal modulation of citrus responses to flooding. J Plant Growth Regul 27:241–250
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 44:388–394
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 25:1–9
Arbona V, Hossain Z, López-Climent MF, Pérez-Clemente RM, Gómez-Cadenas A (2008) Antioxidant enzymatic activity is linked to waterlogging stress tolerance in citrus. Physiol Plant 132:452–466
Arbona V, Iglesias DJ, Talón M, Gómez-Cadenas A (2009a) Plant phenotype demarcation using nontargeted LC-MS and GC-MS metabolite profiling. J Agric Food Chem 57:7338–7347
Arbona V, López-Climent MF, Pérez-Clemente RM, Gómez-Cadenas A (2009b) Maintenance of a high photosynthetic performance is linked to flooding tolerance in citrus. Environ Exp Bot 66:135–142
Arbona V, Argamasilla R, Gómez-Cadenas A (2010) Common and divergent physiological, hormonal and metabolic responses of Arabidopsis thaliana and Thellungiella halophila to water and salt stress. J Plant Physiol 167:1342–1350
Ballizany WL, Hofmann RW, Jahufer MZZ, Barrett BA (2012) Genotype×environment analysis of flavonoid accumulation and morphology in white clover under contrasting field conditions. Field Crops Res 128:156–166
Bates LS, Waldren RP, Teare ID (1973) Rapid determination of free proline for water-stress studies. Plant Soil 39:205–207
Cabane M, Afif D, Hawkins S (2012) Lignins and abiotic stresses. Adv Bot Res 61:219–262
Cidade LC, de Oliveira TM, Mendes AFS, Macedo AF, Floh EIS, Gesteira AS, Soares-Filho WS, Costa MGC (2012) Ectopic expression of a fruit phytoene synthase from Citrus paradisi Macf. promotes abiotic stress tolerance in transgenic tobacco. Mol Biol Rep 39:10201–10209
Dai A, Nie Y, Yu B, Li Q, Lu L, Bai J (2012) Cinnamic acid pretreatment enhances heat tolerance of cucumber leaves through modulating antioxidant enzyme activity. Environ Exp Bot 79:1–10
De Ollas C, Hernando B, Arbona V, Gómez-Cadenas A (2013) Jasmonic acid transient accumulation is needed for abscisic acid increase in citrus roots under drought stress conditions. Physiol Plant 147(3):296–306
Des Marais DL, Juenger TE (2010) Pleiotropy, plasticity, and the evolution of plant abiotic stress tolerance. Ann N Y Acad Sci 1206:56–79
Djoukeng JD, Arbona V, Argamasilla R, Gómez-Cadenas A (2008) Flavonoid profiling in leaves of citrus genotypes under different environmental situations. J Agric Food Chem 56:11087–11097
Durgbanshi A, Arbona V, Pozo O, Miersch O, Sancho JV, Gómez-Cadenas A (2005) Simultaneous determination of multiple phytohormones in plant extracts by liquid chromatography–electrospray tandem mass spectrometry. J Agric Food Chem 53:8437–8442
Glauser G, Grata E, Rudaz S, Wolfender J (2008) High-resolution profiling of oxylipin-containing galactolipids in Arabidopsis extracts by ultra-performance liquid chromatography/time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 22:3154–3160
Gómez-Cadenas A, Tadeo FR, Talon M, Primo-Millo E (1996) Leaf abscission induced by ethylene in water-stressed intact seedlings of Cleopatra mandarin requires previous abscisic acid accumulation in roots. Plant Physiol 112:401–408
Gómez-Cadenas A, Pozo OJ, Garcia-Augustin P, Sancho JV (2002) Direct analysis of abscisic acid in crude plant extracts by liquid chromatography–electrospray/tandem mass spectrometry. Phytochem Anal 13:228–234
Kristl J, Veber M, Krajničič B, Orešnik K, Slekovec M (2005) Determination of jasmonic acid in Lemna minor (L.) by liquid chromatography with fluorescence detection. Anal Bioanal Chem 383:886–893
Lee B, Muneer S, Jung W, Avice J, Ourry A, Kim T (2012a) Mycorrhizal colonization alleviates drought-induced oxidative damage and lignification in the leaves of drought-stressed perennial ryegrass (Lolium perenne). Physiol Plant 145:440–449
Lee M, Jung J, Han D, Seo PJ, Park WJ, Park C (2012b) Activation of a flavin monooxygenase gene YUCCA7 enhances drought resistance in Arabidopsis. Planta 235:923–938
Li Z, Peng Y, Ma X (2012) Different response on drought tolerance and post-drought recovery between the small-leafed and the large-leafed white clover (Trifolium repens L.) associated with antioxidative enzyme protection and lignin metabolism. Acta Physiol Plant 35:213–222
Liu P, Sun F, Gao R, Dong H (2012) RAP2.6L overexpression delays waterlogging induced premature senescence by increasing stomatal closure more than antioxidant enzyme activity. Plant Mol Biol 79:609–622
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 62:176–184
Mehterov N, Balazadeh S, Hille J, Toneva V, Mueller-Roeber B, Gechev T (2012) Oxidative stress provokes distinct transcriptional responses in the stress-tolerant atr7 and stress-sensitive loh2 Arabidopsis thaliana mutants as revealed by multi-parallel quantitative real-time PCR analysis of ROS marker and antioxidant genes. Plant Physiol Biochem 59:20–29
Merchant A, Richter A, Popp M, Adams M (2006) Targeted metabolite profiling provides a functional link among eucalypt taxonomy, physiology and evolution. Phytochemistry 67:402–408
Moura JC, Bonine CA, de Oliveira Fernandes Viana J, Dornelas MC, Mazzafera P (2010) Abiotic and biotic stresses and changes in the lignin content and composition in plants. J Integr Plant Biol 52:360–376
Moya JL, Gómez-Cadenas A, Primo-Millo E, Talon M (2003) Chloride absorption in salt-sensitive Carrizo citrange and salt-tolerant Cleopatra mandarin citrus rootstocks is linked to water use. J Exp Bot 54:825–833
Munns R (2011) Plant adaptations to salt and water stress: differences and commonalities. Adv Bot Res 57:1–32
Qin F, Shinozaki K, Yamaguchi-Shinozaki K (2011) Achievements and challenges in understanding plant abiotic stress responses and tolerance. Plant Cell Physiol 52:1569–1582
Sun W, Nie Y, Gao Y, Dai A, Bai J (2012) Exogenous cinnamic acid regulates antioxidant enzyme activity and reduces lipid peroxidation in drought-stressed cucumber leaves. Acta Physiol Plant 34:641–655
Vincent D, Lapierre C, Pollet B, Cornic G, Negroni L, Zivy M (2005) Water deficits affect caffeate O-methyltransferase, lignification, and related enzymes in maize leaves. A proteomic investigation. Plant Physiol 137:949–960
Witt S, Galicia L, Lisec J, Cairns J, Tiessen A, Araus JL, Palacios-Rojas N, Fernie AR (2012) Metabolic and phenotypic responses of greenhouse-grown maize hybrids to experimentally controlled drought stress. Mol Plant 5:401–417
Acknowledgments
This study was supported by the Spanish Ministerio de Economía y Competitividad (MINECO) and Universitat Jaume I/Fundació Bancaixa through grants AGL2010-22195-C03-01/AGR and P11B2009-01, respectively. VA was the recipient of a “Ramón y Cajal” contract from the MINECO. Mass spectrometry analyses were performed at the central facilities (Servei Central d’Instrumentació Científica, SCIC) of Universitat Jaume I.
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Argamasilla, R., Gómez-Cadenas, A. & Arbona, V. Metabolic and Regulatory Responses in Citrus Rootstocks in Response to Adverse Environmental Conditions. J Plant Growth Regul 33, 169–180 (2014). https://doi.org/10.1007/s00344-013-9359-z
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DOI: https://doi.org/10.1007/s00344-013-9359-z