Effects of Salinity and Abscisic Acid on Lipid Transfer Protein Accumulation, Suberin Deposition and Hydraulic Conductance in Pea Roots
Abstract
:1. Introduction
2. Materials and Methods
2.1. Materials
2.2. Plant Growth Conditions and Treatments
2.3. Characteristics of Water Relations
2.4. Microscopic Study
2.5. RNA Extraction and Analysis of Abundance of LTP mRNA
2.6. Computational Molecular Docking to Study the Interaction of ABA with LTPs
2.7. Fluorescence Spectroscopy to Study of LTP Binding of ABA In Vitro
2.8. Statistics
3. Results
4. Discussion
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Acknowledgments
Conflicts of Interest
References
- Edqvist, J.; Blomqvist, K.; Nieuwland, J.; Salminen, T.A. Plant lipid transfer proteins: Are we finally closing in on the roles of these enigmatic proteins? J. Lipid Res. 2018, 59, 1374–1380. [Google Scholar] [CrossRef] [Green Version]
- Jülke, S.; Ludwig-Müller, J. Response of Arabidopsis thaliana roots with altered lipid transfer protein (LTP) gene expression to the clubroot disease and salt stress. Plants 2016, 5, 2. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Melnikova, D.N.; Mineev, K.S.; Finkina, E.I.; Arseniev, A.S.; Ovchinnikova, T.V. A novel lipid transfer protein from the dill Anethum graveolens L.: Isolation, structure, heterologous expression, and functional characteristics. J. Pept. Sci. 2016, 22, 59–66. [Google Scholar] [CrossRef] [PubMed]
- Blein, J.-P.; Coutos-Thévenot, P.; Marion, D.; Ponchet, M. From elicitins to lipid-transfer proteins: A new insight in cell signalling involved in plant defence mechanisms. Trends Plant Sci. 2002, 7, 293–296. [Google Scholar] [CrossRef]
- García-Garrido, J.M.; Menossi, M.; Puigdoménech, P.; Martínez-Izquierdo, J.A.; Delseny, M. Characterization of a gene encoding an abscisic acid-inducible type-2 lipid transfer protein from rice. FEBS Lett. 1998, 428, 193–199. [Google Scholar] [CrossRef] [Green Version]
- Moraes, G.P.; Benitez, L.C.; do Amara, M.N.; Vighi, I.L.; Auler, P.A.; da Maia, L.C.; Bianchi, V.J.; Braga, E.J.B. Expression of LTP genes in response to saline stress in rice seedlings. Genet. Mol. Res. 2015, 14, 8294–8305. [Google Scholar] [CrossRef] [PubMed]
- Deeken, R.; Saupe, S.; Klinkenberg, J.; Riedel, M.; Leide, J.; Hedrich, R.; Mueller, T.D. The nonspecific lipid transfer protein ATLTPI-4 is involved in suberin formation of Arabidopsis thaliana crown gall. Plant Physiol. 2016, 172, 1911–1927. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shao, Y.; Cheng, Y.; Pang, H.; Chang, M.; He, F.; Wang, M.; Davis, D.J.; Zhang, S.; Oliver Betz, O.; Fleck, C.; et al. Investigation of salt tolerance mechanisms across a root developmental gradient in almond rootstocks. Front. Plant Sci. 2020, 11, 595055. [Google Scholar] [CrossRef] [PubMed]
- Xu, Y.; Zheng, X.; Song, Y.; Zhu, L.; Yu, Z.; Gan, L.; Zhou, S.; Liu, H.; Wen, F.; Zhu, C. NtLTP4, a lipid transfer protein that enhances salt and drought stresses tolerance in Nicotiana tabacum. Sci. Rep. 2018, 8, 1–14. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Rahman, M.M.; Mostofa, M.G.; Rahman, M.A.; Miah, M.G.; Saha, S.R.; Karim, M.A.; Keya, S.S.; Akter, M.; Islam, M.; Phan, L.-S. Insight into salt tolerance mechanisms of the halophyte Achras sapota: An important fruit tree for agriculture in coastal areas. Protoplasma 2019, 256, 181–191. [Google Scholar] [CrossRef] [PubMed]
- Coffey, O.; Bonfield, R.; Florine Corre, F.; Sirigiri, J.A.; Meng, D.; Fricke, W. Root and cell hydraulic conductivity, apoplastic barriers and aquaporin gene expression in barley (Hordeum vulgare L.) grown with low supply of potassium. Ann. Bot. 2018, 122, 1131–1141. [Google Scholar] [CrossRef] [Green Version]
- Finkelstein, R. Abscisic acid synthesis and response. Arab. Book 2013, 11, e0166. [Google Scholar] [CrossRef] [Green Version]
- Wang, C.; Yang, C.; Gao, C.; Wang, Y. Cloning and expression analysis of 14 lipid transfer protein genes from Tamarix hispida responding to different abiotic stresses. Tree Physiol. 2009, 29, 1607–1619. [Google Scholar] [CrossRef] [Green Version]
- Akhiyarova, G.R.; Finkina, E.I.; Ovchinnikova, T.N.; Veselov, D.S.; Kudoyarova, G.R. Role of pea LTPs and abscisic acid in salt-stressed roots. Biomolecules 2020, 10, 15. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barbaglia, A.M.; Tamot, B.; Greve, V.; Hoffmann-Benning, S. Phloem proteomics reveals new lipid-binding proteins with a putative role in lipid-mediated signaling. Front. Plant Sci. 2016, 7, 563. [Google Scholar] [CrossRef] [Green Version]
- Bogdanov, I.V.; Shenkarev, Z.O.; Finkina, E.I.; Melnikova, D.N.; Rumynskiy, E.I.; Arseniev, A.S.; Ovchinnikova, T.V. A novel lipid transfer protein from the pea Pisum sativum: Isolation, recombinant expression, solution structure, antifungal activity, lipid binding, and allergenic properties. BMC Plant Biol. 2016, 16, 107–124. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gizatullina, A.K.; Finkina, E.I.; Mineev, K.S.; Melnikova, D.N.; Bogdanov, I.V.; Telezhinskaya, I.N.; Balandin, S.V.; Shenkarev, Z.; Arseniev, A.S.; Ovchinnikova, T.V. Recombinant production and solution structure of lipid transfer protein from lentil Lens culinaris. Biochem. Biophys. Res. Commun. 2013, 439, 427–432. [Google Scholar] [CrossRef]
- Arkhipova, T.; Martynenko, E.; Sharipova, G.; Kuzmina, L.; Ivanov, I.; Garipova, M.; Kudoyarova, G. Effects of plant growth promoting rhizobacteria on the content of abscisic acid and salt resistance of wheat plants. Plants 2020, 9, 1429. [Google Scholar] [CrossRef]
- Bogdanov, I.V.; Finkina, E.I.; Balandin, S.V.; Melnikova, D.N.; Stukacheva, E.A.; Ovchinnikova, T.V. Structural and functional characterization of recombinant isoforms of the lentil lipid transfer protein. Acta Nat. 2015, 7, 65–73. [Google Scholar] [CrossRef] [Green Version]
- Sharipova, G.; Veselov, D.; Kudsoyarova, G.; Fricke, W.; Dodd, I.; Katsuhara, M.; Furuichi, T.; Ivanov, I.; Veselov, S. Exogenous application of abscisic acid (ABA) increases root and cell hydraulic conductivity and abundance of some aquaporin isoforms in the ABA deficient barley mutant Az34. Ann. Bot. 2016, 118, 777–785. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Efetova, M.; Zeier, J.; Riederer, M.; Lee, C.W.; Stingl, N.; Mueller, M.; Hartung, W.; Hedrich, R.; Deeken, R. A central role of abscisic acid in drought stress protection of Agrobacterium-induced tumors on Arabidopsis. Plant Physiol. 2007, 145, 853–862. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Finkina, E.I.; Melnikova, D.N.; Bogdanov, I.V.; Ovchinnikova, T.V. Lipid transfer proteins as components of the plant innate immune system: Structure, functions, and applications. Acta Nat. 2016, 8, 47–61. [Google Scholar] [CrossRef]
- Pettersen, E.F.; Goddard, T.D.; Huang, C.C.; Couch, G.S.; Greenblatt, D.M.; Meng, E.C.; Ferrin, T.E. UCSF Chimera—A visualization system for exploratory research and analysis. J. Comput. Chem. 2004, 25, 1605–1612. [Google Scholar] [CrossRef] [Green Version]
- Trott, O.; Olson, A.J. AutoDock Vina: Improving the speed and accuracy of docking with a new scoring function, efficient optimization, and multithreading. J. Comput. Chem. 2009, 31, 455–461. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dassault Systèmes BIOVIA. Discovery Studio Visualizer; v20.1.0.19295; Dassault Systèmes: San Diego, CA, USA, 2020. [Google Scholar]
- Buhot, N.; Gomès, E.; Milat, M.-L.; Ponchet, M.; Marion, D.; Lequeu, J.; Delrot, S.; Coutos-Thévenot, P.; Blein, J.-P. Modulation of the biological activity of a tobacco LTP1 by lipid complexation. Mol. Biol. Cell. 2004, 15, 5047–5052. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Edstam, M.M.; Laurila, M.; Höglund, A.; Raman, A.; Dahlström, K.M.; Salminen, T.A.; Edqvist, J.; Blomqvist, K. Characterization of the GPI-anchored lipid transferproteins in the moss Physcomitrella patens. Plant Physiol. Biochem. 2014, 75, 55–69. [Google Scholar] [CrossRef]
- Manzi, M.; Lado, J.; Rodrigo, M.J.; Zacarías, L.; Arbona, V.; Aurelio Gómez-Cadenas, A. Root ABA accumulation in long-term water-stressed plants is sustained by hormone transport from aerial organs. Plant Cell Physiol. 2015, 56, 2457–2466. [Google Scholar] [CrossRef]
- Safi, H.; Saibi, W.; Alaoui, M.M.; Hmyene, A.; Masmoudi, K.; Hanin, M.; Brini, F. A wheat lipid transfer protein (TdLTP4) promotes tolerance to abiotic and biotic stress in Arabidopsis thaliana. Plant Physiol. Biochem. 2015, 89, 64–75. [Google Scholar] [CrossRef]
- Hartung, W.; Sauter, A.; Hose, E. Abscisic acid in the xylem: Where does it come from, where does it go to? J. Exp. Bot. 2002, 53, 27–33. [Google Scholar] [CrossRef]
- Hijaz, F.; Killiny, N. Collection and chemical composition of phloem sap from Citrus sinensis L. Osbeck (sweet orange). PLoS ONE 2014, 9, e101830. [Google Scholar] [CrossRef] [Green Version]
- Lee, S.B.; Suh, M.-C. Disruption of glycosylphosphatidylinositol-anchored lipid transfer protein 15 affects seed coat permeability in Arabidopsis. Plant J. 2018, 96, 1206–1217. [Google Scholar] [CrossRef] [PubMed]
- Rains, M.K.; de Silva, N.D.G.; Molina, I. Reconstructing the suberin pathway in poplar by chemical and transcriptomic analysis of bark tissues. Tree Physiol. 2018, 38, 340–361. [Google Scholar] [CrossRef] [PubMed]
- Baxter, I.; Hosmani, P.S.; Ana Rus, A.; Lahner, B.; Borevitz, J.; Muthukumar, B.; Mickelbart, M.V.; Schreiber, L.; Franke, R.B.; Salt, D.E. Root suberin forms an extracellular barrier that affects water relations and mineral nutrition in Arabidopsis. PLoS Genet. 2009, 5, e1000492. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Benning, U.F.; Tamot, B.; Guelette, B.S.; Hoffmann-Benning, S. New aspects of phloem-mediated long-distance lipid signaling in plants. Front. Plant Sci. 2012, 3, 53. [Google Scholar] [CrossRef] [Green Version]
- Guelette, B.S.; Benning, U.F.; Hoffmann-Benning, S. Identification of lipids and lipid-binding proteins in phloem exudates from Arabidopsis thaliana. J. Exp. Bot. 2012, 63, 3603–3616. [Google Scholar] [CrossRef] [Green Version]
- Wang, X.; Wang, H.; Cao, K.; Ge, X. A rice lipid transfer protein binds to plasma membrane proteinaceous sites. Mol. Biol. Rep. 2009, 36, 745–750. [Google Scholar] [CrossRef]
Transpiration | LWP | OPNS | Hydraulic Conductance | |
---|---|---|---|---|
2 days after ABA treatment | ||||
Control (without ABA) | 0.23 ± 0.04 | −0.4 ± 0.05 | −0.01 ± 0.01 | 1.49 ± 0.24 |
ABA treatment | 0.05 ± 0.01 * | −0.52 ± 0.04 * | −0.01 ± 0.01 | 0.27 ± 0.16 * |
4 days after salt treatment | ||||
Control (without NaCl) | 0.3 ± 0.02 | −0.33 ± 0.08 | −0.01 ± 0.01 | 0.93 ± 0.11 |
NaCl treatment | 0.23 ± 0.03 * | −0.91 ± 0.1 * | −0.26 ± 0.04 * | 0.35 ± 0.13 * |
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Akhiyarova, G.R.; Ivanov, R.S.; Ivanov, I.I.; Finkina, E.I.; Melnikova, D.N.; Bogdanov, I.V.; Nuzhnaya, T.; Ovchinnikova, T.V.; Veselov, D.S.; Kudoyarova, G.R. Effects of Salinity and Abscisic Acid on Lipid Transfer Protein Accumulation, Suberin Deposition and Hydraulic Conductance in Pea Roots. Membranes 2021, 11, 762. https://doi.org/10.3390/membranes11100762
Akhiyarova GR, Ivanov RS, Ivanov II, Finkina EI, Melnikova DN, Bogdanov IV, Nuzhnaya T, Ovchinnikova TV, Veselov DS, Kudoyarova GR. Effects of Salinity and Abscisic Acid on Lipid Transfer Protein Accumulation, Suberin Deposition and Hydraulic Conductance in Pea Roots. Membranes. 2021; 11(10):762. https://doi.org/10.3390/membranes11100762
Chicago/Turabian StyleAkhiyarova, Guzel R., Ruslan S. Ivanov, Igor I. Ivanov, Ekaterina I. Finkina, Daria N. Melnikova, Ivan V. Bogdanov, Tatyana Nuzhnaya, Tatiana V. Ovchinnikova, Dmitriy S. Veselov, and Guzel R. Kudoyarova. 2021. "Effects of Salinity and Abscisic Acid on Lipid Transfer Protein Accumulation, Suberin Deposition and Hydraulic Conductance in Pea Roots" Membranes 11, no. 10: 762. https://doi.org/10.3390/membranes11100762