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β-Aminobutyric acid increases drought tolerance and reorganizes solute content and water homeostasis in flax (Linum usitatissimum)

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Abstract

β-Aminobutyric acid (BABA) is a non-protein amino acid that induces drought tolerance in plants. The mechanisms involved in this tolerance are still poorly understood. In the present study, metabolomic and ionomic profiling performed in flax (Linum usitatissimum) leaves revealed that BABA induces a major reorganization in solute content. This reorganization resulted in increased accumulation of non-structural carbohydrates and proline and a decrease in inorganic solutes. This response has high similarities with that obtained when flax is exposed to an osmotic stress. BABA treatment also induced a decrease in osmotic potential and a change in water status of flax leaves. These modifications are accompanied by an improvement in drought tolerance.

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References

  • Alcazar, R., Marco, F., Cuevas, J. C., Patron, M., Ferrando, A., Carrasco, P., et al. (2006). Involvement of polyamines in plant response to abiotic stress. Biotechnology Letters, 28, 1867–1876.

    Article  CAS  PubMed  Google Scholar 

  • Ali, Q., & Ashraf, M. (2011). Induction of drought tolerance in maize (Zea mays L.) due to exogenous application of trehalose: Growth, photosynthesis, water relations and oxidative defence mechanism. Journal of Agronomy and Crop Science, 197, 258–271.

    Article  CAS  Google Scholar 

  • Ali, Q., Ashraf, M., & Athar, H. R. (2007). Exogenously applied proline at different growth stages enhances growth of two maize cultivars grown under water deficit conditions. Pakistan Journal of Botany, 39, 1133–1144.

    Google Scholar 

  • Arbona, V., Manzi, M., de Ollas, C., & Gómez-Cadenas, A. (2013). Metabolomics as a tool to investigate abiotic stress tolerance in plants. International Journal of Molecular Sciences, 14, 4885–4911.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ashraf, M., Akram, N. A., Al-Qurainy, F., & Foolad, M. R. (2011). Drought tolerance: roles of organic osmolytes, growth regulators, and mineral nutrients. In L. S. Donald (Ed.), Advances in Agronomy (pp. 249–296). New York: Academic Press.

    Google Scholar 

  • Avonce, N., Leyman, B., Mascorro-Gallardo, J. O., Van Dijck, P., Thevelein, J. M., & Iturriaga, G. (2004). The Arabidopsis trehalose-6-P synthase AtTPS1 gene is a regulator of glucose, abscisic acid, and stress signaling. Plant Physiology, 136, 3649–3659.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Baena-Gonzalez, E., & Sheen, J. (2008). Convergent energy and stress signaling. Trends in Plant Science, 13, 474–482.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Barbosa, J. M., Singh, N. K., Cherry, J. H., & Locy, R. D. (2010). Nitrate uptake and utilization is modulated by exogenous γ-aminobutyric acid in Arabidopsis thaliana seedlings. Plant Physiology and Biochemistry, 48, 443–450.

    Article  CAS  PubMed  Google Scholar 

  • Bengtsson, T., Weighill, D., Proux-Wéra, E., Levander, F., Resjö, S., Burra, D. D., et al. (2014). Proteomics and transcriptomics of the BABA-induced resistance response in potato using a novel functional annotation approach. BMC Genomics, 15, 315.

    Article  PubMed Central  PubMed  Google Scholar 

  • Bruce, T. J. A., Matthes, M. C., Napier, J. A., & Pickett, J. A. (2007). Stressful ‘‘memories’’ of plants: Evidence and possible mechanisms. Plant Science, 173, 603–608.

    Article  CAS  Google Scholar 

  • Cao, S. Q., Jiang, L., Yuan, H. B., Jian, H., Ren, G., Bian, X., et al. (2008). β-Amino-butyric acid protects Arabidopsis against low potassium stress. Acta Physiologiae Plantarum, 30, 309–314.

    Article  CAS  Google Scholar 

  • Cao, S. Q., Ren, G., Jiang, L., Yuan, H. B., & Ma, G. H. (2009). The role of β-aminobutyric acid in enhancing cadmium tolerance in Arabidopsis thaliana. Russian Journal of Plant Physiology, 56, 575–579.

    Article  CAS  Google Scholar 

  • Casa, R., Russell, G., Lo Cascio, B., & Rossini, F. (1999). Environmental effects on linseed (Linum usitatissimum L.) yield and growth of flax at different stand densities. European Journal of Agronomy, 11, 267–278.

    Article  Google Scholar 

  • Chantreau, M., Portelette, A., Dauwe, R., Kiyoto, S., Crônier, D., Morreel, K., et al. (2014). Ectopic lignification in the flax lignified bast fiber 1 mutant stem is associated with tissue-specific modifications in gene expression and cell wall composition. The Plant Cell Online, 26(11), 4462–4482.

    Article  CAS  Google Scholar 

  • Claeys, H., & Inzé, D. (2013). The agony of choice: How plants balance growth and survival under water-limiting conditions. Plant Physiology, 162, 1768–1779.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Cohen, Y., Rubin, A. E., & Kilfin, G. (2010). Mechanisms of induced resistance in lettuce against Bremia lactucae by dl-β-amino-butyric acid (BABA). European Journal of Plant Pathology, 126, 553–573.

    Article  CAS  Google Scholar 

  • Cortina, C., & Culianez-Macia, F. A. (2005). Tomato abiotic stress enhanced tolerance by trehalose biosynthesis. Plant Science, 169, 75–82.

    Article  CAS  Google Scholar 

  • Du, Y. L., Wang, Z. Y., Fan, J. W., Turner, C., Wang, T., & Li, F. M. (2012). β-Aminobutyric acid increases abscisic acid accumulation and desiccation tolerance and decreases water use but fails to improve grain yield in two spring wheat cultivars under soil drying. Journal of Experimental Botany, 63, 4849–4860.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Fernandez, O., Bethencourt, L., Quéro, A., Sangwan, R. S., & Clement, C. (2010). Trehalose and plant stress responses: Friend or foe? Trends in Plant Science, 15, 409–417.

    Article  CAS  PubMed  Google Scholar 

  • Gagneul, D., Ainouche, A., Duhaze, C., Lugan, R., Larher, F. R., & Bouchereau, A. (2007). A reassessment of the function of the so-called compatible solutes in the halophytic plumbaginaceae Limonium latifolium. Plant Physiology, 144, 1598–1611.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gamir, J., Pastor, V., Kaever, A., Cerezo, M., & Flors, V. (2014). Targeting novel chemical and constitutive primed metabolites against Plectosphaerella cucumerina. The Plant Journal, 78, 227–240.

    Article  CAS  PubMed  Google Scholar 

  • Garg, A. K., Kim, J. K., Owens, T. G., Ranwala, A. P., Choi, Y. D., Kochian, L. V., et al. (2002). Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proceedings of the National Academy of Sciences of the United States of America, 99, 15898–15903.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hare, P. D., & Cress, W. A. (1997). Metabolic implications of stress-induced proline accumulation in plants. Plant Growth Regulation, 21, 79–102.

    Article  CAS  Google Scholar 

  • Hoagland, D. R., & Arnon, D. I. (1938). The water culture method for growing plant without soil (Vol. 347, pp. 1–39). Berkeley, CA: California Agricultural Experiment Station.

    Google Scholar 

  • Hong, Z., Lakkineni, K., Zhang, Z., & Verma, D. P. (2000). Removal of feedback inhibition of delta(1)-pyrroline-5-carboxylate synthetase results in increased proline accumulation and protection of plants from osmotic stress. Plant Physiology, 122, 1129–1136.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Huis, R., Morreel, K., Fliniaux, O., Lucau-Danila, A., Fénart, S., Grec, S., et al. (2012). Natural hypolignification is associated with extensive oligolignol accumulation in flax stems. Plant Physiology, 158(4), 1893–1915.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hummel, I., Pantin, F., Sulpice, R., Piques, M., Rolland, G., Dauzat, M., et al. (2010a). Arabidopsis plants acclimate to water deficit at low cost through changes of carbon usage: an integrated perspective using growth, metabolite, enzyme, and gene expression analysis. Plant Physiology, 154, 357–372.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hummel, J., Strehmel, N., Selbig, J., Walther, D., & Kopka, J. (2010b). Decision tree supported substructure prediction of metabolites from GC-MS profiles. Metabolomics, 6, 322–333.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Hussain, M., Malik, M. A., Farooq, M., Ashraf, M. Y., & Cheema, M. A. (2008). Improving drought tolerance by exogenous application of glycinebetaine and salicylic acid in sunflower. Journal of Agronomy and Crop Science, 194, 193–199.

    Article  CAS  Google Scholar 

  • Jakab, G., Cottier, V., Toquin, V., Rigoli, G., Zimmerli, L., Métraux, J. P., et al. (2001). β-Aminobutyric acid-induced resistance in plants. European Journal of Plant Pathology, 107, 29–37.

    Article  CAS  Google Scholar 

  • Jakab, G., Ton, J., Flors, V., Zimmerli, L., Metraux, J. P., & Mauch-Mani, B. (2005). Enhancing Arabidopsis salt and drought stress tolerance by chemical priming for its abscisic acid responses. Plant Physiology, 139, 267–274.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Jiang, L., Yang, R. Z., Lu, Y. F., Cao, S. Q., Ci, L. K., & Zhang, J. J. (2012). β-Aminobutyric acid mediated tobacco tolerance to potassium deficiency. Russian Journal of Plant Physiology, 59, 781–787.

    Article  CAS  Google Scholar 

  • Jung, S. (2004). Variation in antioxidant metabolism of young and mature leaves of Arabidopsis thaliana subjected to drought. Plant Science, 166, 459–466.

    Article  CAS  Google Scholar 

  • Lamblin, F., Hano, C., Fliniaux, O., Mesnard, F., Fliniaux, M. A., & Lainé, E. (2008). Intérêt des lignanes dans la prévention et le traitement de cancers. Médecine/Sciences, 24, 511–519.

    Article  Google Scholar 

  • Last, R. L., Jones, D., & Shachar-Hill, Y. (2007). Towards the plant metabolome and beyond. Nature Reviews Molecular Cell Biology, 8, 167–174.

    Article  CAS  PubMed  Google Scholar 

  • Lisec, J., Schauer, N., Kopka, J., Willmitzer, L., & Fernie, A. R. (2006). Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols, 1, 387–396.

    Article  CAS  PubMed  Google Scholar 

  • Liu, T., Jiang, X., Shi, W., Chen, J., Pei, Z., & Zheng, H. (2011). Comparative proteomic analysis of differentially expressed proteins in β-aminobutyric acid enhanced Arabidopsis thaliana tolerance to simulated acid rain. Proteomics, 11, 2079–2094.

    Article  CAS  PubMed  Google Scholar 

  • Liu, W. X., Zhang, F. C., Zhang, W. Z., Song, L. F., Wei-Hua, W., & Chen, Y. F. (2013). Arabidopsis Di19 functions as a transcription factor and modulates PR1, PR2, and PR5 expressions in response to drought stress. Molecular Plant, 6, 1487–1502.

    Article  CAS  PubMed  Google Scholar 

  • Lugan, R., Niogret, M. F., Kervazo, L., Larher, F. R., Kopka, J., & Bouchereau, A. (2009). Metabolome and water status phenotyping of Arabidopsis under abiotic stress cues reveals new insight into ESK1 function. Plant, Cell and Environment, 32, 95–108.

    Article  CAS  PubMed  Google Scholar 

  • Luna, E., van Hulten, M., Zhang, Y., Berkowitz, O., López, A., Pétriacq, P., et al. (2014). Plant perception of β-aminobutyric acid is mediated by an aspartyl-tRNAsynthetase. Nature Chemical Biology, 10, 450–456.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Macarisin, D., Wisniewski, M. E., Bassett, C., & Thannhauser, T. (2009). Proteomic analysis of β-aminobutyric acid priming and abscisic acid—Induction of drought resistance in crabapple (Malus pumila): Effect on general metabolism, the phenylpropanoid pathway and cell wall enzymes. Plant, Cell and Environment, 32, 1612–1631.

    Article  CAS  Google Scholar 

  • Okazaki, Y., & Saito, K. (2012). Recent advances of metabolomics in plant biotechnology. Plant Biotechnology Reports, 6, 1–15.

    Article  PubMed Central  PubMed  Google Scholar 

  • Pastor, V., Balmer, A., Gamir, A., Flors, V., & Mauch-Mani, B. (2014). Preparing to fight back: generation and storage of priming compounds. Frontiers in Plant Science, 5, 245.

    Google Scholar 

  • Quéro, A., Béthencourt, L., Pilard, S., Fournet, A., Guillot, X., Sangwan, R. S., et al. (2013). Trehalose determination in linseed subjected to osmotic stress. HPAEC-PAD analysis: An inappropriate method. Physiologia Plantarum, 147, 261–269.

    Article  PubMed  Google Scholar 

  • Quéro, A., Molinié, R., Elboutachfaiti, R., Petit, E., Pau-Roblot, C., Guillot, X., et al. (2014). Osmotic stress alters the balance between organic and inorganic solutes in flax (Linum usitatissimum). Journal of Plant Physiology, 171, 55–64.

    Article  PubMed  Google Scholar 

  • Raghavendra, A. S., Gonugunta, V. K., Christmann, A., & Grill, E. (2010). ABA perception and signalling. Trends in Plant Science, 15, 395–401.

    Article  CAS  PubMed  Google Scholar 

  • Ramsay, A., Fliniaux, O., Fang, J., Molinie, R., Roscher, A., Grand, E., et al. (2014). Development of an NMR metabolomics-based tool for selection of flaxseed varieties. Metabolomics, 10, 1258–1267.

    Article  CAS  Google Scholar 

  • Renault, R., Roussel, V., El Amrani, A., Arzel, M., Renault, D., Bouchereau, A., et al. (2010). The Arabidopsis pop 2-1 mutant reveals the involvement of GABA transaminase in salt stress tolerance. BMC Plant Biology, 10, 20.

    Article  PubMed Central  PubMed  Google Scholar 

  • Romero, C., Belles, J. M., Vaya, J. L., Serrano, R., & Culianez-Macia, F. A. (1997). Expression of the yeast trehalose-6-phosphate synthase gene in transgenic tobacco plants: Pleiotropic phenotypes include drought tolerance. Planta, 201, 293–297.

    Article  CAS  PubMed  Google Scholar 

  • Saradhi, P. P., Alia Arora, S., & Prasad, K. V. (1995). Proline accumulates in plants exposed to UV radiation and protects them against UV induced peroxidation. Biochemical and Biophysical Research Communications, 209, 1–5.

    Article  CAS  PubMed  Google Scholar 

  • Seki, M., Umezawa, T., Urano, K., & Shinozaki, K. (2007). Regulatory metabolic networks in drought stress responses. Current Opinion in Plant Biology, 10, 296–302.

    Article  CAS  PubMed  Google Scholar 

  • Seo, P. J., Lee, A. K., Xiang, F., & Park, C. M. (2008). Molecular and functional profiling of arabidopsis pathogenesis-related genes: Insights into their roles in salt response of seed germination. Plant and Cell Physiology, 49, 334–344.

    Article  CAS  PubMed  Google Scholar 

  • Shulaev, V., Cortesa, D., Miller, G., & Mittler, R. (2008). Metabolomics for plant stress response. Physiologia Plantarum, 132, 199–208.

    Article  CAS  PubMed  Google Scholar 

  • Singh, P., Wu, C. C., & Zimmerli, L. (2010). β-Aminobutyric acid priming by stress imprinting. Plant Signaling and Behavior, 5, 878–880.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sperdouli, I., & Moustakas, M. (2012). Interaction of proline, sugars, and anthocyanins during photosynthetic acclimation of Arabidopsis thaliana to drought stress. Journal of Plant Physiology, 169, 577–585.

    Article  CAS  PubMed  Google Scholar 

  • Summerscales, J., Dissanayake, N., Virk, A. S., & Hall, W. (2010). A review of bast fibres and their composites: Part 1—Fibres as reinforcements. Composites Part A Applied Science and Manufacturing, 41, 1329–1335.

    Article  Google Scholar 

  • Szabados, L., Kovács, H., Zilberstein, A., & Bouchereau, A. (2011). Plants in extreme environments: Importance of protective compounds in stress tolerance. In I. Turkan (Ed.), Advances in botanical research: Plant responses to drought and salinity stress—Developments in a post-genomic era (pp. 105–150). Amsterdam: Elsevier Ltd.

    Chapter  Google Scholar 

  • Szabados, L., & Savoure, A. (2010). Proline: A multifunctional amino acid. Trends in Plant Science, 15, 89–97.

    Article  CAS  PubMed  Google Scholar 

  • Tocquin, P., Corbesier, L., Havelange, A., Pieltain, A., Kurtem, E., Bernier, G., et al. (2003). A novel high efficiency, low maintenance, hydroponic system for synchronous growth and flowering of Arabidopsis thaliana. BMC Plant Biology, 3, 2.

    Article  PubMed Central  PubMed  Google Scholar 

  • Ton, J., Jakab, G., Toquin, V., Flors, V., Iavicoli, A., Maeder, M. N., et al. (2005). Dissecting the β-aminobutyric acid-induced priming phenomenon in Arabidopsis. The Plant Cell, 17, 987–999.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Touré, A., & Xu, X. M. (2010). Flaxseed lignans: Source, biosynthesis, metabolism, antioxidant activity, bio-active components, and health benefits. Comprehensive Reviews in Food Science and Food Safety, 9, 261–269.

    Article  Google Scholar 

  • Verslues, P. E., Agarwal, M., Katiyar-Agarwal, S., Zhu, J., & Zhu, J. K. (2006). Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. The Plant Journal, 45, 523–539.

    Article  CAS  PubMed  Google Scholar 

  • Walter, J., Nagy, L., Hein, R., Rascher, U., Beierkuhnlein, C., Willner, E., et al. (2011). Do plants remember drought? Hints towards a drought-memory in grasses. Environmental and Experimental Botany, 71, 34–40.

    Article  Google Scholar 

  • Walters, D. R., Ratsep, J., & Havis, N. D. (2013). Controlling crop diseases using induced resistance: Challenges for the future. Journal of Experimental Botany, 64, 1263–1280.

    Article  CAS  PubMed  Google Scholar 

  • Wu, C. C., Singh, P., Chen, M. C., & Zimmerli, L. (2010). l-Glutamine inhibits beta-aminobutyric acid-induced stress resistance and priming in Arabidopsis. Journal of Experimental Botany, 61, 995–1002.

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zimmerli, L., Hou, B. H., Tsai, C. H., Jakab, G., Mauch-Mani, B., & Somerville, S. (2008). The xenobiotic β-aminobutyric acid enhances Arabidopsis thermotolerance. The Plant Journal, 53, 144–156.

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This work was supported by the French Picardie Region. FM wishes to acknowledge COST Action FA 1006 Plant Metabolic Engineering for High Value Products.

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All the authors declare that they have no conflict of interest.

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This article does not contain any studies with human participants or animals performed by any of the authors.

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Correspondence to François Mesnard.

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Josiane Courtois and François Mesnard have contributed equally to the article.

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Quéro, A., Fliniaux, O., Elboutachfaiti, R. et al. β-Aminobutyric acid increases drought tolerance and reorganizes solute content and water homeostasis in flax (Linum usitatissimum). Metabolomics 11, 1363–1375 (2015). https://doi.org/10.1007/s11306-015-0792-9

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