MALE FERN (DRYOPTERIS FILIX-MAS) SPORES GERMINATION UNDER TREATMENT OF HEXANOYL HOMOSERINE LACTONE
DOI: 10.17721/1728.2748.2024.98.42-46
Keywords:
Dryopteris filix-mas, spore germination, gametophyte, acyl homoserine lactones, quorum sensing, AHL-signalingAbstract
Background. Plants exist in close interaction with microorganisms. Bacteria use a special intercellular communication system called "quorum sensing" (QS). This system depends on the density of the bacterial population and coordinates the formation of responses to changing environmental conditions. QS systems play a key role in regulating the bacterial cell's metabolic and physiological processes. Bacterial signaling is perceived by eukaryotes that form a symbiosis with microbial communities. A plant's growth and development, nutrient assimilation, and stress resistance are largely determined by the nature of such interactions. The key group of QS interactions in the population of gram-negative bacteria is acyl homoserine lactones (AHLs), which affect plant growth and development. The effect of AHLs on Angiosperms has been extensively studied. There is also data on the impact of AHLs on moss gametophytes. However, there is no information on the impact of AHLs on Ferns gametophytes and sporophytes. We present here the first study on the effect of hexanoyl homoserine lactone (C6-HHL), a bacterial signaling molecule of the AHLs class, on spore germination and the initial stages of gametophyte development of the homosporous fern Dryopteris filix-mas.
Methods. The dynamic of spore germination was determined on a liquid Knop medium containing 1 μM, 0.1 μM, 0.01 μM and 0.001 μM C6-HHL. Germination was kept and checked on by light microscopy. (Zeiss Axiocam MRc 5, Carl Zeiss).
Results. A moderate stimulating effect (increasing by 6 %) of low C6-HHL concentrations (0.01 μM and 0.001 μM) and an inhibitory effect (decrease by 5.7 %) of higher C6-HHL concentrations (1 μM, 0.1 μM) on spore germination and gametophyte development were established.
Conclusions. The results indicate the sensitivity of Dryopteris filix-mas gametophyte to the influence of bacterial AHL.
References
Babenko, L.M., Futorna, O.A., Romanenko, К.O., Smirnov, O.E., Rogalsky, S.P., Kosakivska, I.V., Skwarek, E., & Wisniewska, M. (2024). Exogenous N-hexanoyl-L-homoserine lactone mitigates acid rain stress effects through modulation of structural and functional changes in Triticum aestivum leaf. Applied Soil Ecology, 193, 105151. https://doi.org/10.1016/j.apsoil.2023.105151
Babenko, L.M., Kosakivska, I.V., Romanenko, К.О. (2022). Molecular mechanisms of N‐acyl homoserine lactone signals perception by plants. Cell Biology International, 46:523-534. https://doi.org/10.1002/cbin.11749
Ding, L., Cao, J., Duan, Y., Li, J., Yang, Y., Yang, G., & Zhou, Y. (2016). Proteomic and physiological responses of Arabidopsis thaliana exposed to salinity stress and N-acyl-homoserine lactone. Physiol Plantar, 158: 414-434. doi:10.1111/ppl.12476
Dytham, C. (2011). Choosing and Using Statistics: A Biologist's Guide. Wiley-Blackwell. – 3nd ed.
Hartmann, A. & Schikora, A. (2012). Quorum Sensing of Bacteria and Trans-Kingdom Interactions of N-Acyl Homoserine Lactones with Eukaryotes. J. Chem. Ecol., 38, 704–713. https://doi.org/10.1007/s10886-012-0141-7
Hornschuh, M., Grotha, R., & Kutschera, U. (2002). Epiphytic bacteria associated with the bryophyte Funaria hygrometrica: Effects of Methylobacterium strains on protonema development. Plant Biol., 4, 682–687. https://doi.org/10.1016/j.apsoil.2023.105151
Joint, I., Tait, K., & Wheeler, G. (2007). Cross-kingdom signalling: Exploitation of bacterial quorum sensing molecules by the green seaweed Ulva. Philos. Trans. R. Soc. B. Biol. Sci., 362, 1223–1233. doi: 10.1098/rstb.2007.2047
Kosakivska, I.V., Babenko, L.M., Vasyuk, V.A., Voytenko, L.V., Shcherbatiuk, M.M. (2024). Natural growth regulators as inducers of resistance in cereal plants against extreme environmental factors. In: Yastreb T.O., Kolupaev Y.E., Yemets A.I., Blume Y.B. (eds.). Regulation of Adaptive Responses in Plants. New York: Nova Science Publishers, Inc.. P. 33-81.
Kutschera U. Plant-associated methylobacteria as co-evolved phytosymbionts: A hypothesis. (2007). Plant Signal. Behav, 2, 74–78. doi: 10.4161/psb.2.2.4073.
Liu, F., Bian, Z., Jia, Z., Zhao, Q., & Song, S. (2012). The GCR1 and GPA1 participate in promotion of Arabidopsis primary root elongation induced by N-acyl homoserine lactones, the bacterial quorum-sensing signals. Mol Plant-Microbe Interact. 25(5): 677-683. http://doi.org/10.1094/MPMI-10-11-0274.
Mathesius, U., Mulders, S., Gao, M., Teplitski, M., Caetano-Anolles, G., Rolfe, B.G., & Bauer, W.D. (2003). Extensive and specific responses of a eukaryote to bacterial quorum-sensing signals. Proc. Natl. Acad. Sci USA, 100, No. 3, 1444-1449. https://doi.org/10.1073/pnas.262672599
Miao, C., Liu, F., Zhao, Q., Jia, Z., & Song, S. (2012). A proteomic analysis of Arabidopsis thaliana seedling responses to 3-oxo-octanoyl-homoserine lactone, a bacterial quorum-sensing signal. Biochem Biophys Res Commun. 427: 293-298. https://doi.org/10.1016/j.bbrc.2012.09.044
Moshynets, O.V., Babenko, L.M., Rogalsky, S.P., Iungin, O.S., Foster, J., Kosakivska, I.V., Potters, G., & Spiers A.J. (2019) Priming winter wheat seeds with the bacterial quorum sensing signal N-hexanoyl-L-homoserine lactone (C6-HSL) shows potential to improve plant growth and seed yield. PLOS ONE, 14(2), e0209460. https://doi.org/10.1371/journal.pone.0209460
Ortiz-Castro, R.A, Martinez-Trujillo, M.I., Lуpez-Bucio, J.O. (2008). N-acyl-L-homoserine lactones: a class of bacterial quorum-sensing signals alter post-embryonic root development in Arabidopsis thaliana. Plant Cell Environ. 31(10): 1497-1509. https://doi.org/ 10.1111/j.1365-3040.2008.01863.x
Prigge, M.J., & Bezanilla, M. (2010). Evolutionary crossroads in developmental biology: Physcomitrella patens. Development, 137, 3535–3543. doi: 10.1242/dev.049023
von Rad, U., Klein, I., Dobrev, P.I., Kottova, J., Zazimalova, E., Fekete, A., Hartmann, A., Schmitt-Kopplin, P., & Durner, J. (2008). Response of Arabidopsis thaliana to N-hexanoyl-DL-homoserine-lactone, a bacterial quorum sensing molecule produced in the rhizosphere. Planta, 229(1): 73-85. https://doi.org/10.1007/s00425-008-0811-4
Schikora, A., Schenk, S.T., & Hartmann, A. (2016). Beneficial effects of bacteria-plant communication based on quorum sensing molecules of the N-acyl homoserine lactone group. Plant Mol. Biol., 90, 605–612. doi: 10.1007/s11103-016-0457-8
Shrestha, A., Grimm, M., Ojiro, I., Krumwiede, J., & Schikora, A. (2020). Impact of Quorum Sensing Molecules on Plant Growth and Immune System. Frontiers in microbiology, 11, 1545. https://doi.org/10.3389/fmicb.2020.01545
Singh, R.P., Baghel, R.S., Reddy, C.R.K., & Jha, B. (2015) Effect of quorum sensing signals produced by seaweed-associated bacteria on carpospore liberation from Gracilaria dura. Front. Plant Sci., 6, 117. doi: 10.3389/fpls.2015.00117. eCollection 2015
Song, S., Jia, Z., Xu, J., Zhang, Z., & Bian, Z. (2011) N-butyryl-homoserine lactone, a bacterial quorum-sensing signaling molecule, induces intracellular calcium elevation in Arabidopsis root cells. Biochem Biophys Res Commun., 414(2): 355-360. https://doi.org/10.1016/j.bbrc.2011.09.076
Twigg, M.S., Tait, K., Williams, P., Atkinson, S., & Cámara, M. (2014) Interference with the germination and growth of Ulva zoospores by quorum-sensing molecules from Ulva-associated epiphytic bacteria. Environ. Microbiol. 16, 445–453.
Vesty, E.F., Whitbread, A.L., & Needs, S. (2020). Cross-kingdom signalling regulates spore germination in the moss Physcomitrella patens. Sci Rep. 10, 2614. https://doi.org/10.1038/s41598-020-59467-5
Wheeler, G.L., Tait, K., Taylor, A., Brownlee, C., & Joint, I. (2006) Acyl-homoserine lactones modulate the settlement rate of zoospores of the marine alga Ulva intestinalis via a novel chemokinetic mechanism. Plant, Cell Environ., 29, 608–618. doi: 10.1111/j.1365-3040.2005.01440.x
