Participation of nitrate sensor NRT1.1 in the control of cytokinin level and root elongation under normal conditions and nitrogen deficit
Abstract
NRT1.1 nitrate transporter acts as nitrate sensor in some plant responses. We tried to check if it may be involved in the control of cytokinin level in the plants known to be involved in the growth responses to nitrate level. In accordance, we followed the effects of NRT1.1 gene mutation in chl1-5 plants on hormonal and growth responses to nitrogen starvation. Two types of experimental design were used: (1) plants were placed on either Hoagland-Arnon or modified solution, where potassium and calcium nitrates were substituted with their chlorides; (2) Pryanishnikov medium was used, where ammonium nitrate serves as the source of nitrogen, starvation being modeled by its withdrawal from the medium. We were first to show that mutation of the NRT1.1 resulted in a decline in cytokinin level in the roots of chl1-5, while roots of wild type plants were longer in accordance with lower cytokinin content in them, the hormone being known to inhibit root elongation. Cytokinin content decreased in Columbia plants paralleled by acceleration of root elongation in response to both variants of nitrogen starvation, while chl1-5 roots responded in this way only when nitrogen was withdrawn from Pryanishnikov solution, while substitution of nitrates by chlorides in the Hoagland-Arnon solution had no effects on either chl1-5 roots length or cytokinin content in them. The results suggested the involvement of NRT1.1 transceptor in the control of cytokinin level and root elongation rate in the nitrate, but not in ammonium starved plants, confirming the specificity of response.
About the Authors
A. V. KorobovaRussian Federation
Prospekt Oktyabrya 69, 450054, Ufa
G. R. Akhiyarova
Russian Federation
Prospekt Oktyabrya 69, 450054, Ufa
V. V. Fedyaev
Russian Federation
Zaki Validi st. 32, 450076, Ufa
R. G. Farkhutdinov
Russian Federation
Zaki Validi st. 32, 450076, Ufa
S. Yu. Veselov
Russian Federation
Prospekt Oktyabrya 69, 450054, Ufa; Zaki Validi st. 32, 450076, Ufa
G. R. Kudoyarova
Russian Federation
Prospekt Oktyabrya 69, 450054, Ufa
References
1. Sakakibara H., Takei K., Hirose N. Interactions between nitrogen and cytokinin in the regulation of metabolism and development // Trends Plant Sci. 2006. Vol. 11. N. 9. P. 440-448.
2. Kudoyarova G.R., Dodd I.C., Veselov D.S., Rothwell S.A., Veselov S.Y. Common and specific responses to availability of mineral nutrients and water // J. Exp. Bot. 2015. Vol. 66. N. 8. P. 2133-2144.
3. Takei K, Takahashi H, Sugiyama T, Yamaya T, Sakakibara H. Multiple routes communicating nitrogen availability from roots to shoots: a signal transduction pathway mediated by cytokinin // J. Exp. Bot. 2002. Vol. 53. N. 370. P. 971-977.
4. Takei K., Ueda N, Aoki K., Kuromori T, Hirayama T, Shinozaki K, Yamaya T, Sakakibara H. AtIPT3 is a key determinant of nitrate-dependent cytokinin biosynthesis in Arabidopsis // Plant Cell Physiol. 2004. Vol. 45. N 8. P. 1053-1062.
5. Kamada-Nobusada T, Makita N, Kojima M, Sakakibara H. Nitrogen-dependent regulation of de novo cytokinin biosynthesis in rice: the role of glutamine metabolism as an additional signal // Plant Cell Physiol. 2013. Vol. 54. N 11. P. 1881-1893.
6. Salama A., Wareing P.F. Effects of mineral-nutrition on endogenous cytokinins in plants of sunflower (Helianthus annuus) // J. Exp. Bot. 1979. Vol. 30. N. 118. P. 971-981.
7. Korobova A.V., Vysotskaya L.B., Vasinskaya A.N. Kuluev B.R., Veselov S.Yu, Kudoyarova G.R. Dependence of root biomass accumulation on content and metabolism of cytokinins in ethylene-insensitive plants // Russ. J. Plant Physiol. 2016. Vol. 63. N 5. P. 636-643.
8. Ivanov V.B., Filin A.N. Cytokinins regulate root growth through its action on meristematic cell proliferation but not on the transition to differentiation // Funct. Plant Biol. 2017. Vol. 45. N. 2. P. 215-221.
9. Gojon A., Krouk G, Perrine-Walker F, Laugier E. Nitrate transceptor(s) in plants // J. Exp. Bot. 2011. Vol. 62. N. 7. P. 2299-2308.
10. Krouk G, Mirowski P, LeCun Y., Shasha D.E., Coruzzi G.M. Predictive network modeling of the high-resolution dynamic plant transcriptome in response to nitrate // Genome Biol. 2010. Vol. 11: R123.
11. Yu C, Liu Y., Zhang A., Su S., Yan A., Huang L., Ali I., Liu Y., Forde B.G., Gan Y. MADS-box transcription factor OsMADS25 regulates root development through affection of nitrate accumulation in rice // PLoS One. 2015. Vol. 10. N 8: e0135196.
12. Kudoyarova G.R., Korobova A.V., Akhiyarova G.R., Arkhipova T.N., Zaytsev D.Yu, Prinsen E, Egutkin N.L., Medvedev S.S., Veselov S.Yu. Accumulation of cytokinins in roots and their export to the shoots of durum wheat plants treated with the protonophore carbonyl cyanide m-chlorophenylhydrazone (CCCP) // J. Exp. Bot. 2014. Vol. 65. N. 9. P. 2287-2294.
13. Wu S, Baskin T.I., Gallagher K.L. Mechanical fixation techniques for processing and orienting delicate samples, such as the root of Arabidopsis thaliana, for light or electron microscopy // Nat. Protoc. 2012. Vol. 7. N. 6. P. 1113-1124.
14. Akhiyarova G.R., Korobova A.V., Veselov S.Yu., Kudoyarova G.R., Veselov D.S. Effects of root cutting on cytokinin content in the shoot apex cells of Arabidopsis plants // Moscow Univ. Biol. Sci. Bull. 2018. Vol. 73. N 3. P. 172-177.
15. Kiba T, Kudo T, Kojima M, Sakakibara H. Hormonal control of nitrogen acquisition: roles of auxin, abscisic acid, and cytokinin // J. Exp. Bot. 2011. Vol. 62. N. 4. P. 1399-1409.
16. Wang R., XingX., Wang Y., Tran A., Crawford N.M. A genetic screen for nitrate regulatory mutants captures the nitrate transporter gene NRT1.1 // Plant Physiol. 2009. Vol. 151. N. 1. P. 472-478.
17. Motyka V., Vankova R, Capkova V., Petrasek J., Kaminek M, Schmulling T. Cytokinin-induced upregulation of cytokinin oxidase activity in tobacco includes changes in enzyme glycosylation and secretion // Physiol Plant. 2003. Vol. 117. N. 1. P. 11-21.
18. Bai L, Ma X., Zhang G., Song S, Zhou Y., Gao L., Miao Y., Song C.-P. A receptor-like kinase mediates ammonium homeostasis and is important for the polar growth of root hairs in Arabidopsis // Plant Cell. 2014. Vol. 26. N. 4. P. 1497-1511.
19. Roycewicz P. Malamy J.E. Dissecting the effects of nitrate, sucrose and osmotic potential on Arabidopsis root and shoot system growth in laboratory assays // Philos. Trans. R. Soc. London, B. 2012. Vol. 367. N. 1595. P. 1489-1500.
20. Trapeznikov V.K., Ivanov 1.1., Kudoyarova G.R. Effect of heterogeneous distribution of nutrients on root growth, ABA content and drought resistance of wheat plants // Plant Soil. 2003. Vol. 252. N. 2. P. 207-214.
21. Ruffel S., Krouk G., Ristova D., Shasha D., Birnbaum K.D., Coruzzi G.M. Nitrogen economics of root foraging: Transitive closure of the nitrate-cytokinin relay and distinct systemic signalling for N supply vs. demand // Proc. Natl. Acad. Sci. U.S.A. 2011. Vol. 108. N. 45. P. 18524-18529.
Review
For citations:
Korobova A.V., Akhiyarova G.R., Fedyaev V.V., Farkhutdinov R.G., Veselov S.Yu., Kudoyarova G.R. Participation of nitrate sensor NRT1.1 in the control of cytokinin level and root elongation under normal conditions and nitrogen deficit. Vestnik Moskovskogo universiteta. Seriya 16. Biologiya. 2019;74(4):277–283. (In Russ.)