eISSN: 2221-6197 DOI: 10.31301/2221-6197

Localization and synthesis of lipid-transfer proteins in pea plants after treatment by strain of growth-stimulating bacteria and their role in the formation of Casparian bands and the regul

Year: 2023

Pages: 7-18

Number: Volume 15, issue 1

Type: scientific article

Summary:

The presence of PGP bacteria in the rhizosphere has a positive effect on plant growth and increases their productivity both under favorable and stressful conditions. Despite the fact that much attention is paid to the various mechanisms of action of growth-promoting bacteria on plants, the aspect of the effect of bacteria on changes in the formation of apoplastic barriers and their effect on water transport remains almost unexplored. Previously, it was shown that Pseudomonas mandelii IB-Ki14 accelerated the formation of Casparian bands in wheat plants, although the involvement of LTPs (Lipid Transfer Proteins) in this process has not been shown. The aim of this study was to elucidate the effect of bacterial inoculation on LTP synthesis in the roots of the pea (Pisum sativum) and its relation to the formation of apoplastic barriers and hydraulic conductance. We aimed to test the hypothesis that the decrease in hydraulic conductance due to increased formation of apoplastic barriers can be compensated by increased activity of aquaporin water channels. Activation of genes encoding PsLTP and an increase in the amount of lipid-transporting proteins in pea root phloem induced by P. mandelii IB-Ki14 treatment were found. Inoculation was accompanied by an increase in suberin deposition in the Casparian bands, while hydraulic conductivity did not decrease. The use of Fenton's reagent, which is an inhibitor of aquaporins, showed that the hydraulic conductivity of plants treated with bacteria decreased to a greater extent compared to the control group, which indicates an increase in the activity of aquaporins under the influence of bacteria. We conclude that P. mandelii IB-Ki14 stimulates the deposition of suberin, the biosynthesis of which involves lipid-transporting proteins, and increases the activity of aquaporins, which, in turn, prevents a possible decrease in hydraulic conductivity due to the formation of apoplastic barriers in pea roots.

Keywords:

Pisum sativum, Pseudomonas mandelii, lipid transfer proteins, LTP, Casparian bands, aquaporins, hydraulic conductance

References:

1. Akhiyarova G.R., Ivanov R.S., Ivanov I.I., Finkina E.I., Melnikova D.N., Bogdanov I.V., Nuzhnaya T.V., 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. V.11. 762. doi: 10.3390/membranes11100762

3. Aroca R., Porcel R., Ruiz-Lozano J.M. Regulation of root water uptake under abiotic stress conditions. Journal of Experimental Botany. 2012. V.1(63). P.43–57. doi: 10.1093/jxb/err266

4. Backer R., Rokem J.S., Ilangumaran G., Lamont J., Praslickova D., Ricci E., Subramanian S., Smith D.L. Plant growth- promoting rhizobacteria: context, mechanisms of action, and roadmap to commercialization of biostimulants for sustainable agriculture. Frontiers in Plant Science. 2018. V.9. 1473. doi: 10.3389/fpls.2018.01473

5. Benning U.F., Tamot B., Guelette B.S., Hoffmann-Benning S. New aspects of phloemmediated long-distance lipid signaling in plants. Frontiers in Plant Science. 2012. V.3 P.53. doi: 10.3389/fpls.2012.00053

6. Boursiac Y., Protto V., Rishmawi L., Maurel C. Experimental and conceptual approaches to root water transport. Plant and Soil. 2022. V.478(1-2). P.349-370. 10.1007/s11104-022-05427-z

7. Bunce J.A., Ziska L.H. Decreased hydraulic conductance in plants at elevated carbon dioxide. Plant Cell Environ. 1998. V.21. P.121–126. doi: 10.1046/j.1365-3040.1998.00256.x

8. Cui B., Liu R., Flowers T.J., Song J. Casparian bands and suberin lamellae: Key targets for breeding salt tolerant crops? Environmental and Experimental Botany. 2021. V.191. 104600. doi: 10.1016/j.envexpbot.2021.104600

9. 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. V.59. P.1374–1380. doi: 10.1194/jlr.R083139

10. 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 Physiology. 2007. V.145(3). P.853–862. doi: 10.1104/pp.107.104851

11. 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 Naturae. 2016. V.8. P.47–61. doi: 10.32607/20758251-2016-8-2-47-61

12. Flexas J., Carriqui M., Nadal M. Gas exchange and hydraulics during drought in crops: who drives whom? Journal of Experimental Botany. 2018. V.69(16). P.3791–3795. doi: 10.1093/jxb/ery235

13. Fonseca-Garcia C., Solis-Miranda J., Pacheco R., Quinto C. Non-specific lipid transfer proteins in9.2008.00701.x legumes and their participation during root-nodule symbiosis. Frontiers in Agronomy. 2021. V.3. 660100. doi: 10.3389/fagro.2021.660100

14. Gao S., Guo W., Feng W., Liu L., Song X., Chen J., Hou W., Zhu H., Tang S., Hu J. LTP3 contributes to
disease susceptibility in Arabidopsis by enhancing  abscisic acid (ABA) biosynthesis. Molecular Plant Pathology. 2016. V.17. P.412–426. doi: 10.1111/mpp.12290

15. Gao H., Ma K., Ji G., Pan L., Zhou Q. Lipid transfer proteins involved in plant–pathogen interactions and their molecular mechanisms. Molecular Plant Pathology. 2022. V.23. P.1815-1829. doi: 10.1111/mpp.13264

16. Gonzalez-Klein Z.; Cuevas-Zuviria B.; Wangorsch A., Hernandez-Ramirez G., Pazos-Castro D., Oeo-Santos C., Romero-Sahagun A., Pacios L.F., Tome-Amat J., Scheurer S., Diaz-Perales A., GarridoArandia M. The key to the allergenicity of lipid transfer protein (LTP) ligands: A structural characterization. Biochimica et Biophysica Acta (BBA) - Molecular and Cell Biology of Lipids. 2021. V.1866. 158928. doi: 10.1016/j.bbalip.2021.158928

17. Henzler T.Ye., Steudle Q.E. Oxidative gating of water channels (aquaporins) in Chara by hydroxyl radicals. Plant, Cell and Environment. 2004. V.27(9). P.1184-1195. doi: 10.1111/j.1365-3040.2004.01226.x

18. Kaluarachchi M., Boulange C.L., Karaman I., Lindon J.C., Ebbels T.M.D., Elliott P., Tracy R.P., Olson N.C. A comparison of human serum and plasma metabolites using untargeted 1H NMR spectroscopy and UPLC-MS. Metabolomics. 2018. V.14(3). P.32. doi: 10.1007/s11306-018-1332-1

19. Kudoyarova G., Arkhipova T., Korshunova T., Bakaeva M., Loginov O., Dodd I.C. Phytohormone mediation of interactions between plants and nonsymbiotic growth promoting bacteria under edaphic stresses. Frontiers in Plant Science. 2019. V.10. 1368. doi: 10.3389/fpls.2019.01368

20. Lawson T., Vialet-Chabrand S. Speedy stomata, photosynthesis and plant water use efficiency. New Phytologist. 2019. V.221. P.93-98. doi: 10.1111/nph.15330  

21. Lee S.B., Go Y.S., Bae H.J., Park J.H., Cho S.H., Cho H.J., Lee D.S., Park O.K., Hwang I., Suh M.C. Disruption of glycosylphosphatidylinositol-anchored lipid transfer protein gene altered cuticular lipid composition, increased plastoglobules, and enhanced susceptibility to infection by the fungal pathogen Alternaria brassicicola. Plant Physiology. 2009. V.150(1). P.42–54. doi: 10.1104/pp.109.137745

22. Lee M.-H., Jeon H.S., Kim S.H., Chung J.H., Roppolo D., Lee H.-J., Cho H.J., Tobimatsu Y., Ralph J., Park O.K. Lignin based barrier restricts pathogens to the infection site and confers resistance in plants. The EMBO Journal. 2019. V.38. e101948. doi: 10.15252/embj.2019101948

23. Li L., Pan S., Melzer R., Fricke W. Apoplastic barriers, aquaporin gene expression and root and cell hydraulic conductivity in phosphate-limited sheepgrass plants. Physiologia Plantarum. 2020. V.168. P.118-132. doi: 10.1111/ppl.12981

24. Martynenko E., Arkhipova T., Safronova V., Seldimirova O., Galin I., Akhtyamova Z., Veselov D., Ivanov R., Kudoyarova G. Effects of phytohormoneproducing rhizobacteria on casparian band formation, ion homeostasis and salt tolerance of durum wheat. Biomolecules. 2022. V.12. 230. doi: 10.3390/biom12020230

25. Megeressa M., Siraj B., Zarina S., Ahmed A. Structural characterization and in vitro lipid binding studies of non-specific lipid transfer protein 1 (nsLTP1) from fennel (Foeniculum vulgare) seeds. Scientific Reports. 2020. V.10. 21243. doi: 10.1038/s41598-020-77278-6

26. Missaoui K., Gonzalez-Klein Z., Pazos-Castro D., Hernandez-Ramirez G., Garrido-Arandia M., Brini F., Perales A.D., Tome-Amat J. Plant non-specific lipid transfer proteins. Plant Physiology and Biochemistry. 2022. V.171. P.115-127. doi: 10.1016/j.plaphy.2021.12.026

27. Moshelion M., Halperin O., Wallach R., Oren R., Way D.A. Role of aquaporins in determining transpiration and photosynthesis in water-stressed plants: crop water-use efficiency, growth and yield. Plant, Cell and Environment. 2015. V.38. P.1785-1793. doi: 10.1111/pce.1241010.1111/pce.12410

28. Olaetxea M., Mora V., Bacaico E., Garnic M., Fuentes M., Casanova E., Zamarreсo A.M., Iriarte J.C., Etayo D., Ederra I., Gonzalo R.. Baigorri R., GarciaMina J.M. Abscisic acid regulation of root hydraulic conductivity and aquaporin gene expression is crucial to the plant shoot growth enhancement caused by rhizosphere humic acids. Plant Physiology. 2015. V.169. P.2587-2596. doi: 10.1104/pp.15.00596

29. Petrillo C., Vitale E., Ambrosino P., Arena C., Isticato R. Plant growth-promoting bacterial consortia as a strategy to alleviate drought stress in Spinacia oleracea. Microorganisms. 2022. V.10. 1798. doi: 10.3390/microorganisms10091798

30. Ruzzi M., Aroca R. Plant growth-promoting rhizobacteria act as biostimulants in horticulture. Scientia Horticulturae. 2015. V.196. P.124–134. doi: 10.1016/j.scienta.2015.08.042

31. Scheurer S., Van Ree R., Vieths S. The role of lipid transfer proteins as food and pollen allergens outside the mediterranean area. Current Allergy and Asthma Reports. 2021. V.21. 7. doi: 10.1007/s11882-020-00982-w

32. Sharipova G., Veselov D., Kudoyarova 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. Annals of Botany. 2016. V.118(4). P.777-785. doi: 10.1093/aob/mcw117

33. Shiono K., Yoshikawa M., Kreszies T., Yamada S., Hojo Y., Matsuura T., Mori I.C., Schreiber L., Yoshioka T. Abscisic acid is required for exodermal suberization to form a barrier to radial oxygen loss in the adventitious roots of rice (Oryza sativa). New Phytologist. 2022. V.233. P.655-669. doi: 10.1111/nph.17751

34. Sorrentino G., Haworth M., Wahbi S.; Mahmood T., Zuomin S., Centritto M. Abscisic acid induces rapid reductions in mesophyll conductance to carbon dioxide. PLoS One 2016. V.11(2). e0148554. doi: 10.1371/journal.pone.0148554

35. Wang C., Wang H., Li P., Li H., Xu C., Cohen H., Aharoni A., Wu S. Developmental programs interact with abscisic acid to coordinate root suberization in Arabidopsis. The Plant Journal. 2020. V.104. P.241-251. doi: 10.1111/tpj.14920

36. Woolfson K.N., Esfandiari M., Bernards M.A. Suberin biosynthesis, assembly and regulation. Plants. 2022. V.11(4). P.555. doi: 10.3390/plants11040555

37. 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. Scientific Reports. 2018. V.8. P.1–14. doi: 10.1038/s41598-018-27274-8

38. Zhao M., Tan H.-T., Scharwies J., Levin K., Evans J.R., Tyerman S.D. Association between water and carbon dioxide transport in leaf plasma membranes: assessing the role of aquaporins. Plant, Cell and Environment. 2017. V.40. P.789–801. doi: 10.1111/pce.12830 

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eISSN: 2221-6197 DOI: 10.31301/2221-6197