The Membrane Nanodomain Flot1 Protein Participates in Formation of the Early Endosomes in the Root Cells of Arabidopsis thaliana

Cover Page

Cite item

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Plants are subjected to various stress factors within their lifespan. In this respect, the plasma membrane
is a principal cell compartment responsible for plant adaptations to stresses. It is capable of remodeling
its protein composition by means of endocytosis. In the plants, the main mode of this process is a clathrinmediated
endocytosis. Several clathrin-independent pathways are also known; these alternative mechanisms
involve Flot1 protein. In the present research, the role of Flot1 in the endocytosis process was examined in
seedling roots of a wild type and an Atflot1ko knockout mutant of Arabidopsis thaliana (L.) Heynh. Light
microscopy with an FM4-64 lipophilic probe and transmission electron microscopy were used. It was found
that endocytosis was arrested in the root cells of the wild type after a simultaneous treatment of the roots with
an inhibitor of clathrin-mediated endocytosis (1-naphthylacetic acid) and the agent depleting the plasma
membrane of sterols (methyl-β-cyclodextrin). In this case, such morphological change as reduction in cytoplasm
vesiculation (including the early endosomes, the small vesicles originated from the agranular ER, the
microvacuoles from its fragments, and the clathrin vesicles) was observed. The vesiculation was diminished
in both the control and the stressed plants (exposed to 100 mM NaCl). In the Atflot1ko mutant, the cisterns
of the Golgi complex closed up to a ring, and the process of formation of the early endosomes was completely
abolished under these conditions. It is suggested that, in the roots of A. thaliana exposed to the inhibitors, the
microdomain-associated Flot1 protein of the plasma membrane conserves the structure of the Golgi complex
and its capacity to build early endosomes on the trans-side. In addition, the protein appears to participate in
formation of the early endosomes from the trans-Golgi network.

About the authors

L. A. Khalilova

Timiryazev Institute of Plant Physiology, Russian Academy of Sciences

Email: lhalilova@mail.ru
Moscow

A. S. Voronkov

Timiryazev Institute of Plant Physiology, Russian Academy of Sciences

Author for correspondence.
Email: lhalilova@mail.ru
Moscow

References

  1. Rodas-Junco B.A., Racagni-Di-Palma G.E., Canul-Chan M., Usorach J., Hernández-Sotomayor S.M.T. Link between lipid second messengers and osmotic stress in plants // IJMS. 2021. V. 22. P. 2658. https://doi.org/10.3390/ijms22052658
  2. López-Hernández T., Haucke V., Maritzen T. Endocytosis in the adaptation to cellular stress // Cell Stress. 2020. V. 4. P. 230. https://doi.org/10.15698/cst2020.10.232
  3. Ivanov R., Vert G. Endocytosis in plants: Peculiarities and roles in the regulated trafficking of plant metal transporters // Biol. Cell. 2021. V. 113. P. 1. https://doi.org/10.1111/boc.202000118
  4. Paez Valencia J., Goodman K., Otegui M.S. Endocytosis and Endosomal Trafficking in Plants. Ann. Rev. Plant Biol. 2016. V. 67. P. 309. https://doi.org/10.1146/annurev-arplant-043015-112242
  5. Fan L., Li R., Pan J., Ding Z., Lin J. Endocytosis and its regulation in plants // Trends Plant Sci. 2015. V. 20. P. 388. https://doi.org/10.1016/j.tplants.2015.03.014
  6. Kaksonen M., Roux A. Mechanisms of clathrin-mediated endocytosis // Nat. Rev. Mol. Cell Biol. 2018. V. 19. P. 313. https://doi.org/10.1038/nrm.2017.132
  7. Reynolds G.D., Wang C., Pan J., Bednarek S.Y. Inroads into Internalization: five years of endocytic exploration // Plant Physiol. 2018. V. 176. P. 208. https://doi.org/10.1104/pp.17.01117
  8. Jelínková A., Malínská K., Simon S., Kleine-Vehn J., Pařezová M., Pejchar P., Kubeš M., Martinec J., Friml J., Zažímalová E., Petrášek J. Probing plant membranes with FM dyes: tracking, dragging or blocking? // Plant J. 2010. V. 61. P. 883. https://doi.org/10.1111/j.1365-313X.2009.04102.x
  9. Gadeyne A., Sánchez-Rodríguez C., Vanneste S., Di Rubbo S., Zauber H., Vanneste K., Van Leene J., De Winne N., Eeckhout D., Persiau G., Van De Slijke E., Cannoot B., Vercruysse L., Mayers J.R., Adamowski M., et al. The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants // Cell. 2014. V. 156. P. 691. https://doi.org/10.1016/j.cell.2014.01.039
  10. Estevez J.M. Plant cell expansion. Methods and protocols // MIMB. 2015. V. 1242. P. 59. https://doi.org/10.1007/978-1-4939-1902-4
  11. Dhonukshe P., Aniento F., Hwang I., Robinson D.G., Mravec J., Stierhof Y.-D., Friml J. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis // Curr. Biol. 2007. V. 17. P. 520. https://doi.org/10.1016/j.cub.2007.01.052
  12. Baral A., Irani N.G., Fujimoto M., Nakano A., Mayor S., Mathew M.K. Salt-induced remodeling of spatially restricted clathrin-independent endocytic pathways in Arabidopsis root // Plant Cell. 2015. V. 27. P. 1297. https://doi.org/10.1105/tpc.15.00154
  13. Boutte Y., Jonsson K., McFarlane H.E., Johnson E., Gendre D., Swarup R., Friml J., Samuels L., Robert S., Bhalerao R.P. ECHIDNA-mediated post-Golgi trafficking of auxin carriers for differential cell elongation // Proc. Nat. Acad. Sci. 2013. V. 110. P. 16259.
  14. Ortiz-Zapater E., Soriano-Ortega E., Marcote M.J., Ortiz-Masiá D., Aniento F. Trafficking of the human transferrin receptor in plant cells: effects of tyrphostin A23 and brefeldin A // Plant J. 2006. V. 48. P. 757. https://doi.org/10.1111/j.1365-313X.2006.02909.x
  15. Paciorek T., Zažímalová E., Ruthardt N., Petrášek J., Stierhof Y.D., Kleine-Vehn J., Morris D.A., Emans N., Jürgens G., Geldner N., Friml J. Auxin inhibits endocytosis and promotes its own efflux from cells // Nature. 2005. V. 435. P. 1251. https://doi.org/10.1038/nature03633
  16. Robert S., Kleine-Vehn J., Barbez E., Sauer M., Paciorek T., Baster P., Vanneste S., Zhang J., Simon S., Čovanová M., Hayashi K., Dhonukshe P., Yang Z., Bednarek S.Y., Jones A.M., et al. ABP1 mediates auxin inhibition of clathrin-dependent endocytosis in Arabidopsis // Cell. 2010. V. 143. P. 111. https://doi.org/10.1016/j.cell.2010.09.027
  17. Abas L., Benjamins R., Malenica N., Paciorek T., Wisniewska J., Moulinier-Anzola J.C., Sieberer T., Friml J., Luschnig C. Intracellular trafficking and proteolysis of the Arabidopsis auxin-efflux facilitator PIN2 are involved in root gravitropism // Nat. Cell Biol. 2006. V. 8. P. 249.
  18. Kitakura S., Vanneste S., Robert S., Löfke C., Teichmann T., Tanaka H., Friml J. Clathrin mediates endocytosis and polar distribution of PIN auxin transporters in Arabidopsis // Plant Cell. 2011. V. 23. P. 1920.
  19. Li X., Wang X., Yang Y., Li R., He Q., Fang X., Luu D.T., Maurel C., Lin J. Single-molecule analysis of PIP2;1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation // Plant Cell. 2011. V. 23. P. 3780. https://doi.org/10.1105/tpc.111.091454
  20. Glebov O.O., Bright N.A., Nichols B.J. Flotillin-1 defines a clathrin-independent endocytic pathway in mammalian cells // Nat. Cell. Biol. 2006. V. 8. P. 46.
  21. Li R., Liu P., Wan Y., Chen T., Wang Q., Mettbach U., Baluška F., Šamaj J., Fang X., Lucas W.J., Lin J. A membrane microdomain-associated protein, Arabidopsis Flot1, is involved in a clathrin-independent endocytic pathway and is required for seedling development // Plant Cell. 2012. V. 24. P. 2105. https://doi.org/10.1105/tpc.112.095695
  22. Zhang L., Xing J., Lin J. At the intersection of exocytosis and endocytosis in plants // New Phytol. 2019. V. 224. P. 1479. https://doi.org/10.1111/nph.16018
  23. Cao Y., He Q., Qi Z., Zhang Y., Lu L., Xue J., Li J., Li R. Dynamics and endocytosis of Flot1 in Arabidopsis require CPI1 function // IJMS. 2020. V. 21. P. 1552. https://doi.org/10.3390/ijms21051552
  24. Khalilova L.A., Sergienko O.V., Orlova Y.V., Myasoedov N.A., Karpichev I.V., Balnokin Y.V. Arabidopsis thaliana mutant with t-DNA insertion in the Flot1 (At5g25250) gene promotor possesses increased resistance to NaCl // Russ. J. Plant Physiol. 2020. V. 67. P. 275. https://doi.org/10.1134/S1021443720020077
  25. Saslowsky D.E., Cho J.A., Chinnapen H., Massol R.H., Chinnapen D.J., Wagner J.S., De Luca H.E., Kam W., Paw B.H., Lencer W.I. Intoxication of zebra fish and mammalian cells by cholera toxin depends on the flotillin/reggie proteins but not Derlin-1 or -2 // J. Clin. Invest. 2010. V. 120. P. 4399.
  26. Chadda R., Howes M.T., Plowman S.J., Hancock J.F., Parton R.G., Mayor S. Cholesterol-sensitive cdc42 activation regulates actin polymerization for endocytosis via the GEEC pathway // Traffic. 2007. V. 8. P. 702. https://doi.org/10.1111/j.1600-0854.2007.00565.x
  27. Roche Y., Gerbeau-Pissot P., Buhot B., Thomas D., Bonneau L., Gresti J., Mongrand S., Perrier-Cornet J., Simon-Plas F. Depletion of phytosterols from the plant plasma membrane provides evidence for disruption of lipid rafts // FASEB J. 2008. V. 22. P. 3980. https://doi.org/10.1096/fj.08-111070
  28. Xue Y., Xing J., Wan Y., Lv X., Fan L., Zhang Y., Song K., Wang L., Wang X., Deng X., Baluška F., Christie J.M., Lin J. Arabidopsis blue light receptor phototropin 1 undergoes blue light-induced activation in membrane microdomains // Mol. Plant. 2018. V. 11. P. 846. https://doi.org/10.1016/j.molp.2018.04.003
  29. Khalilova L.A., Lobreva O.V., Nedelyaeva O.I., Karpichev I.V., Balnokin Y.V. Involvement of the membrane nanodomain protein, AtFlot1, in vesicular transport of plasma membrane H+-ATPase in Arabidopsis thaliana under salt stress // IJMS. 2023. V. 24. P. 1251. https://doi.org/10.3390/ijms24021251
  30. Bolte S., Talbot C., Boutte Y., Catrice O., Read N.D., Satiat-Jeunemaitre B. FM-dyes as experimental probes for dissecting vesicle trafficking in living plant cells // J. Microsc. 2004. V. 214. P. 159.
  31. Mayor S., Parton R.G., Donaldson J.G. Clathrin-independent pathways of endocytosis // Cold Spring Harb. Perspect. Biol. 2014. V. 6. a016758. https://doi.org/10.1101/cshperspect.a016758
  32. Šamaj J., Read N.D., Volkmann D., Menzel D., Baluška F. The endocytic network in plants // Trends Cell Biol. 2005. V. 15. P. 425. https://doi.org/10.1016/j.tcb.2005.06.006
  33. Lam S.K., Tse Y.C., Jiang L., Oliviusson P., Heinzerling O., Robinson D.G. Plant prevacuolar compartments and endocytosis // Plant Cell Monographs. 2005. P. 37. https://doi.org/10.1007/7089_004
  34. Narasimhan M., Gallei M., Tan S., Johnson A., Verstraeten I., Li L., Rodriguez L., Han H., Himschoot E., Wang R., Vanneste S., Sánchez-Simarro J., Aniento F., Adamowski M., Friml J. Systematic analysis of specific and nonspecific auxin effects on endocytosis and trafficking // Plant Physiol. 2021. V. 186. P. 1122. https://doi.org/10.1093/plphys/kiab134.
  35. Martinière A., Fiche J.B., Smokvarska M., Mari S., Alcon C., Dumont X., Hematy K., Jaillais Y., Nollmann M., Maurel C. Osmotic stress activates two reactive oxygen species pathways with distinct effects on protein nanodomains and diffusion // Plant Physiol. 2019. V. 179. P. 1581. https://doi.org/10.1104/pp.18.01065
  36. Feraru E., Friml J. PIN polar targeting // Plant Physiol. 2008. V. 147. P. 1553.
  37. Danielsen E.M., Hansen G.H. Lipid rafts in epithelial brush borders: atypical membrane microdomains with specialized functions // Biochim. Biophys. Acta Biomembr. 2003. V. 1617. P. 1.
  38. dos Santos S.M., Weber C.C., Franke C., Muller W.E., Eckert G.P. Cholesterol: coupling between membrane microenvironment and ABC transporter activity // Biochem. BioPhys. Res. Commun. 2007. V. 354. P. 216.

Supplementary files

Supplementary Files
Action
1. JATS XML
Download
2.

Download (175KB)
Indexing metadata
3.

Download (4MB)
Indexing metadata
4.

Download (4MB)
Indexing metadata

Copyright (c) 2023 Л.А. Халилова, А.С. Воронков

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies