Biophysical mechanisms of intracellular signaling (transduction) in higher plants
https://doi.org/10.29235/1029-8940-2023-68-1-75-88
Abstract
Three fundamental processes running in plant organisms under influence of environment (light, gravity) and key importance were considered. In the light case these are phytоchrome regulation and phototropism considering process is gravitropism. Phytochrome is responsible for regulatory reaction at the inhibition of which the plants cannot be normally developed. The plants do not need phototropism and gravitropism. They were elaborated by evolution as protective reactions to optimize the plant vitality. All these processes are realized according to one and the same logical scheme: stimulus reception, signaling processes in plant cell (transduction) and proper biological effect. According to this scheme the three reactions were considered. As the result the data adout the reception stages are principally different because receptor nature. Signaling processes proceed with participation of many low molecular and high molecular mediators to participate and biophysical, biochemical and genetic reactions. One fact attracts attention that the same mediators are involved to signaling ending by principally different final biological effect.This allows to suggest the existance in plant cell no separate chains for each stimulus but regulatory network formed by lateral and horizontal transduction chains.
About the Authors
I. D. VolotovskiBelarus
Igor D. Volotovski – Academician, D. Sc. (Biol.), Professor, Сhief Researcher
27, Akademicheskaya Str., 220072, Minsk
S. V. Sukhaveyeva
Belarus
Sviatlana V. Sukhaveyeva – Researcher
27, Akademicheskaya Str., 220072, Minsk
E. M. Kabachevskaya
Belarus
Elena M. Kabachevskaya – Ph. D. (Biol.), Неad of the Laboratory
27, Akademicheskaya Str., 220072, Minsk
References
1. Rockwell N. C., Su Y.-S., Lagarias J. C. Phytochrome structure and signaling mechanisms. Annual Review of Plant Biology, 2006, vol. 57, pp. 837–858. https://doi.org/10.1146/annurev.arplant.56.032604.144208
2. Legris M., Ince Y. Ç., Fankhauser C. Molecular mechanisms underlying phytochrome-controlled morphogenesis in plants. Nature Communications, 2019, vol. 10, no. 1, p. 5219. https://doi.org/10.1038/s41467-019-13045-0
3. Klose C., Viczián S., Kircher E., Schäfer F., Nagy F. Molecular mechanisms for mediating light-dependent nucleo/cytoplasmic partitioning of phytochrome photoreceptors. New Phytologist, 2015, vol. 206, no. 3, pp. 965–971. https://doi.org/10.1111/nph.13207
4. Bossen M. E., Dassen H. H., Kendrick R. E., Vredenberg W. J. The role of Ca2+ in pnytochrome-controlling swelling of etiolated weat protoplasts. Planta, 1988, vol. 74, no. 1, pp. 94–100. https://doi.org/10.1007/BF00394879
5. Sokolovskii S. G., Yatsevich O. V., Volotovski I. D. Participation of universal messengers in the regulation of phytochrome regulation of Ca2+ accumulation by protoplasts. Fiziologiya rastenii = Russian Journal of Plant Physiology, 1996, vol. 43, no. 6, pp. 883–886 (in Russian).
6. Volotovski I. D., Sokolovsky S. G., Molchan O. V., Knight M. R. Second messenger mediate increases in cytosolic calcium in tobacoo protoplasts. Plant Physiology, 1998, vol. 117, no. 3, pp. 1023–1030. https://doi.org/10.1104/pp.117.3.1023
7. Schäfer Е., Bowler C. Phytochrome-mediated photoperception and signal transduction in higher plants. EMBO Reports, 2002, vol. 3, no. 11, pp. 1042–1048. https://doi.org/10.1093/embo-reports/kvf222
8. Chen M., Chory J. Phytochrome signaling mechanisms and the control of plant development. Trends in Cell Biology, 2007, vol. 21, no. 11, pp. 664–671. https://doi.org/10.1016/j.tcb.2011.07.002
9. Liscum E., Askinosie S. K., Leuchtman D. L., Morrow J., Willenburg K. T., Coats D. R. Phototropism: Growing towards an understanding of plant movement. Plant Cell, 2014, vol. 26, no. 1, pp. 38–55. https://doi.org/10.1105/tpc.113.119727
10. Suetsugu N., Wada M. Evolution of three LOV blue light receptor families in green plants and photosynthetic stramenopiles: phototropin, ZTL/FKF1/LKP2 and aureochrome. Plant and Cell Physiology, 2013, vol. 54, no. 1, pp. 8–23. https:// doi.org/10.1093/pcp/pcs165
11. Holland J. J., Roberts D., Liscum E. Understanding phototropism: From Darwin to today. Journal of Experimental Botany, 2009, vol. 60, no. 7, pp. 1969–1978. https://doi.org/10.1093/jxb/erp113
12. Zhao X., Wang Y.-L., Qiao X.-R., Wang J., Wang L.-D., Xu C.-S., Zhang X. Phototropins function in high-intensity blue light-induced hypocotyl phototropism in Arabidopsis by altering cytosolic calcium. Plant Physiology, 2013, vol. 162, no. 3, pp. 1539–1551. https://doi.org/10.1104/pp.113.216556
13. Christie J. M., Murphy A. S. Shoot phototropism in higher plants: New light through old concepts. American Journal of Botany, 2013, vol. 100, no. 1, pp. 35–46. https://doi.org/10.3732/ajb.1200340
14. Calderón-Villalobos L. I., Lee S., De Oliveira C., Ivetac A., Brandt W., Armitage L. [et al.]. A combinatorial TIR1/ AFB-Aux/IAA co-receptor system for differential sensing of auxin. Nature Chemical Biology, 2012, vol. 8, no. 5, pp. 477– 485. https://doi.org/10.1038/nchembio.926
15. Esmon C. A., Tinsley A. G., Ljung K., Sandberg G., Hearne L. B., Liscum E. A gradient of auxin and auxin-dependent transcription precedes tropic growth responses. Proceedings of the National Academy of Sciences of the United States of America, 2006, vol. 103, no. 1, pp. 236–241. https://doi.org/10.1073/pnas.0507127103
16. Su S.-H., Keith M. A., Masson P. H. Gravity signaling in flowering plant roots. Plants (Basel), 2020, vol. 9, no. 10, art. 1290. https://doi.org/10.3390/plants9101290
17. Baldwin K. L., Strohm A. K., Masson P. H. Gravity sensing and signal transduction in vascular plant primary roots. American Journal of Botany, 2013, vol. 100, no. 1, pp. 126–142. https://doi.org/10.3732/ajb.1200318
18. Sato E. M., Hijazi H., Bennett M. J., Vissenberg K., Swarup R. New insights into root gravitropic signalling. Journal of Experimental Botany, 2015, vol. 66, no. 8, pp. 2155–2165. https://doi.org/10.1093/jxb/eru515
19. Lopez D., Tocquard K., Venisse J.-S., Legué V., Roeckel-Drevet P. Gravity sensing, a largely misunderstood trigger of plant orientated growth. Frontiers in Plant Science, 2014, vol. 5, art. 610. https://doi.org/10.3389/fpls.2014.00610
20. Toyota M., Furuichi T., Tatsumi H., Sokabe M. Critical consideration on the relationship between auxin transport and calcium transients in gravity perception of Arabidopsis seedlings. Plant Signaling and Behavior, vol. 3, no. 8, pp. 521–524. https://doi.org/10.4161/psb.3.8.6339
21. Kolesnikov Y. S., Kretynin S. V., Volotovsky I. D., Kordyum E. L., Ruelland E., Kravets V. S. Molecular mechanisms of gravity perception and signal transduction in plants. Protoplasma, 2016, vol. 253, no. 4, pp. 987–1004. https://doi.org/10.1007/s00709-015-0859-5
22. Bennett M. J., Marchant A., Green H. G., May S. T., Ward S. P., Millner P. A., Walker A. R., Schulz B., Feldmann K. A. Arabidopsis AUX1 gene: A permease-like regulator of root gravitropism. Science, 1996, vol. 273, no. 5277, pp. 948–950. https://doi.org/10.1126/science.273.5277.948
23. Su S.-H., Gibbs N. M., Jancewicz A. L., Masson P. H. Molecular mechanisms of root gravitropism. Current Biology, 2017, vol. 27, no. 17, pp. R964–R972. https://doi.org/10.1016/j.cub.2017.07.015
24. Guan C., Rosen E. S., Boonsirichai K., Poff K. L., Masson P. H. The ARG1-LIKE2 (ARL2) gene of Arabidopsis thaliana functions in a gravity signal transduction pathway that is genetically distinct from the PGM path-way. Plant Physiology, 2003, vol. 133, no. 1, pp. 100–112. https://doi.org/10.1104/pp.103.023358
25. Stanga J. P., Boonsirichai K., Sedbrook J. C., Otegui M. S., Masson P. H. A role for the TOC complex in Arabidopsis root gravitropism. Plant Physiology, 2009, vol. 149, no. 4, pp. 1896–1905. https://doi.org/10.1104/pp.109.135301
26. Strohm A. K., Barrett-Wilt G. A., Masson P. H. A functional TOC complex contributes to gravitty signal transduction in Arabidopsis. Frontiers in Plant Science, 2014, vol. 5, art. 148. https://doi.org/10.3389/fpls.2014.00148
27. Furutani M., Hirano Y., Nishimura T., Nakamura M., Taniguchi M., Suzuki K. [et al.]. Polar recruitment of RLD by LAZY1-like protein during gravity signaling in root branch angle control. Nature Communications, 2020, vol. 11, art. 76. https://doi.org/10.1038/s41467-019-13729-7
28. Retzer K., Akhmanova M., Konstantinova N., Malínská K., Leitner J., Petrášek J., Luschnig C. Brassinosteroid signaling delimits root gravitropism via sorting of the Arabidopsis PIN2 auxin transporter. Nature Communications, 2019, vol. 10, art. 5516. https://doi.org/10.1038/s41467-019-13543-1
29. Sukhoveeva S. V., Kabachevskaya E. M., Volotovskii I. D. Gravimetric analysis of tomato stems in the perception of a gravitational signals. Doklady Natsional’noi akademii nauk Belarusi = Doklady of the National Academy of Sciences of Belarus, 2022, vol. 66, no. 3, рр. 310–320 (in Russian).
30. Sukhoveeva S. V., Kabachevskaya E. M., Kuznetsova T. E., Volotovski I. D. Comparative analysis of the structurefunction changes in the endodermal cells of tomato leaf petioles after gravity stimulation and phytohor mone action. Doklady Natsional’noi a kademii n auk B elarusi = D oklady o f t he N ational A cademy o f S ciences o f B elarus, 2022, vol. 66, no. 4, рр. 425–432 (in Russian).