Skip to main content
Log in

The Crosstalk between Cytokinin and Auxin Signaling Pathways in the Control of Natural Senescence of Arabidopsis thaliana Leaves

  • RESEARCH PAPERS
  • Published:
Russian Journal of Plant Physiology Aims and scope Submit manuscript

Abstract

Natural senescence of leaves is a regular physiological process subjected to a certain genetic program and controlled by various phytohormones. Cytokinins (CKs) play a crucial role in the leaf-senescence control being negative regulators of this process. We previously reported on the prolonged vegetative growth and the development of a double knockout ahk2ahk3 mutant of Arabidopsis thaliana Heynh. (L.) for the genes encoding CK receptors. According to the data of the transcriptomic analysis and real-time RT‑PCR of selected genes performed in this study, the delay of leaf senescence in ahk2ahk3 mutants is accompanied by enhanced (4–281-fold) expression of the group of SAUR (small auxin-up RNA) genes encoding auxin response proteins and by upregulation of the SSPP (senescence-suppressed protein phosphatase) gene, whose expression level significantly (137-fold) exceeded that in a wild-type transcriptome. Thus, it is quite possible that under significant inhibition of the CK signaling leaf senescence in Arabidopsis plants regulated via a compensatory mechanism connected with changes in the expression of the SAUR gene family and a certain pool of genes related to the auxin transport and signaling.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1.
Fig. 2.
Fig. 3.

Similar content being viewed by others

REFERENCES

  1. Nooden, L.D., Senescence and Aging in Plants, Amsterdam: Elsevier, 1998.

    Google Scholar 

  2. Buchanan-Wollaston, V., Earl, S., Harrison, E., Mathas, E., Navabpour, S., Page, T., and Pink, D., The molecular analysis of leaf senescence—a genomics approach, Plant Biotechnol. J., 2003, vol. 1, p. 3.

    Article  CAS  Google Scholar 

  3. El-Showk, S., Ruonala, R., and Helariutta, Y., Crossing paths: cytokinin signaling and crosstalk, Development, 2013, vol. 140, p. 1373. https://doi.org/10.1242/dev.086371

    Article  CAS  PubMed  Google Scholar 

  4. Miller, C.O., Skoog, F., von Saltza, N.M., Strong, F.M., Kinetin, a cell division factor from deoxyribonucleic acid, J. Am. Chem. Soc., 1955, vol. 77, p. 1329.

    Google Scholar 

  5. Schaller, G.E., Bishopp, A., and Kieber, J.J., The yin-yang of hormones: cytokinin and auxin interactions in plant development, Plant Cell, 2015, vol. 27, p. 44. https://doi.org/10.1105/tpc.114.133595

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Brenner, W.G., Romanov, G.A., Köllmer, I., Bürkle, L., and Schmülling, T., Immediate-early and delayed cytokinin response genes of Arabidopsis thaliana identified by genome-wide expression profiling reveal novel cytokinin-sensitive processes and suggest cytokinin action through transcriptional cascades, Plant J., 2005, vol. 44, p. 314.

    Article  CAS  Google Scholar 

  7. Riefler, M., Novak, O., Strnad, M., and Schmülling, T., Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development and cytokinin metabolism, Plant Cell, 2006, vol. 18, p. 40.

    Article  CAS  Google Scholar 

  8. Higuchi, M., Pischke, M.S., Mahonen, A.P., Miyawaki, K., Hashimoto, Y., Seki, M., Kobayashi, M., Shinozaki, K., Kato, T., Tabata, S., Helariutta, Y., Sussman, M.R., and Kakimoto, T., In planta functions of the Arabidopsis cytokinin receptor family, Proc. Natl. Acad. Sci. U.S.A., 2004, vol. 101, p. 8821.

    Article  CAS  Google Scholar 

  9. Romanov, G.A., How do cytokinins affect the cell? Russ. J. Plant Physiol., 2009, vol. 56, no. 2, p. 268.

    Article  CAS  Google Scholar 

  10. Kieber, J.J. and Schaller, G.E., Cytokinin signaling in plant development, Development, 2018, vol. 145, art. ID dev149344. https://doi.org/10.1242/dev.149344

    Article  CAS  PubMed  Google Scholar 

  11. Kim, H.J., Ryu, H., Hong, S.H., Woo, H.R., Lim, P.O., Lee, I.C., Sheen, J., Nam, H.G., and Hwang, I., Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis, Proc. Natl. Acad. Sci. U.S.A., 2006, vol. 103, p. 814.

    Article  CAS  Google Scholar 

  12. Danilova, M.N., Kudryakova, N.V., Doroshenko, A.S., Zabrodin, D.A., Rakhmankulova, Z.F., Oelmüller, R., and Kusnetsov, V.V., Opposite roles of the Arabidopsis cytokinin receptors AHK2 and AHK3 in the expression of plastid genes and genes for the plastid transcriptional machinery during senescence, Plant Mol. Biol., 2017, vol. 93, p. 533. https://doi.org/10.1007/s11103-016-0580-6

    Article  CAS  PubMed  Google Scholar 

  13. Lichtenthaler, H.K., Chlorophylls and carotenoids: pigments of photosynthetic biomembranes, Methods Enzymol., 1987, vol. 148, p. 350.

    Article  CAS  Google Scholar 

  14. Igarashi, D., Izumi, Y., Dokiya, Y., Totsuka, K., Fukusaki, E., and Ohsumi, C., Reproductive organs regulate leaf nitrogen metabolism mediated by cytokinin signal, Planta, 2009, vol. 229, p. 633. https://doi.org/10.1007/s00425-008-0858-2

    Article  CAS  PubMed  Google Scholar 

  15. van der Graaff, E., Schwacke, R., Schneider, A., Desimone, M., Flügge, U.I., and Kunze, R., Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence, Plant Physiol., 2006, vol. 141, p. 776.

    Article  CAS  Google Scholar 

  16. Buchanan-Wollaston, V., Page, T., Harrison, E., Breeze, E., Lim, P.O., Nam, H.G., Lin, J.F., Wu, S.H., Swidzinski, J., Ishizaki, K., and Leaver, C.J., Comparative transcriptome analysis reveals significant differences in gene expression and signaling pathways between developmental and dark/starvation-induced senescence in Arabidopsis,Plant J., 2005, vol. 42, p. 567.

    Article  CAS  Google Scholar 

  17. Bürkle, L., Cedzich, A., Döpke, C., Stransky, H., Okumoto, S., Gillissen, B., Kühn, C., and Frommer, W.B., Transport of cytokinins mediated by purine transporters of the PUP family expressed in phloem, hydathodes, and pollen of Arabidopsis,Plant J., 2003, vol. 34, p. 13.

    Article  Google Scholar 

  18. Hou, B., Lim, E.K., Higgins, G.S., and Bowles, D.J., N-glucosylation of cytokinins by glycosyltransferases of Arabidopsis thaliana,J. Biol. Chem., 2004, vol. 46, p. 47822.

    Article  Google Scholar 

  19. Xiao, D., Cui, Y., Xu, F., Xu, X., Gao, G., Wang, Y., Guo, Z., Wang, D., and Wang, N.N., SENESCENCE-SUPPRESSED PROTEIN PHOSPHATASE directly interacts with the cytoplasmic domain of SENESCENCE-ASSOCIATED RECEPTOR-LIKE KINASE and negatively regulates leaf senescence in Arabidopsis,Plant Physiol., 2015, vol. 169, p. 1275. https://doi.org/10.1104/pp.15.01112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Hagen, G. and Guilfoyle, T., Auxin-responsive gene expression: genes, promoters and regulatory factors, Plant Mol. Biol., 2002, vol. 49, p. 373.

    Article  CAS  Google Scholar 

  21. van Mourik, H., van Dijk, A.D.J., Stortenbeker, N., Angenent, G.C., and Bemer, M., Divergent regulation of Arabidopsis SAUR genes: a focus on the SAUR10-clade, BMC Plant Biol., 2017, vol. 17, p. 245. https://doi.org/10.1186/s12870-017-1210-4

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Hellsberg, E., Montanari, F., and Ecker, G.F., The ABC of phytohormone translocation, Planta Med., 2015, vol. 6, p. 474. https://doi.org/10.1055/s-0035-1545880

    Article  CAS  Google Scholar 

  23. Xu, F., Meng, T., Li, P., Yu, Y., Cui, Y., Wang, Y., Gong, Q., and Wang, N.N., A soybean dual-specificity kinase, GmSARK, and its Arabidopsis homolog, AtSARK, regulate leaf senescence through synergistic actions of auxin and ethylene, Plant Physiol., 2011, vol. 157, p. 2131.

    Article  CAS  Google Scholar 

  24. Wang, Y., Zhang, X., Cui, Y., Li, L., Wang, D., Mei, Y., and Wang, N.N., AHK3-mediated cytokinin signaling is required for the delayed leaf senescence induced by SSPP, Int. J. Mol. Sci., 2019, vol. 20, p. e2043. https://doi.org/10.3390/ijms20082043

    Article  CAS  PubMed  Google Scholar 

  25. Wen, Z., Mei, Y., Zhou, J., Cui, Y., Wang, D., and Wang, N.N., SAUR49 can positively regulate leaf senescence by suppressing SSPP in Arabidopsis,Plant Cell Physiol., 2019, vol. 61, p. 644. https://doi.org/10.1093/pcp/pcz231

    Article  CAS  Google Scholar 

  26. Hou, K., Wu, W., and Gan, S.S., SAUR36, a small auxin up RNA gene, is involved in the promotion of leaf senescence in Arabidopsis,Plant Physiol., 2013, vol. 161, p. 1002. https://doi.org/10.1104/pp.112.212787

    Article  CAS  PubMed  Google Scholar 

  27. Ren, H. and Gray, W.M., SAUR Proteins as effectors of hormonal and environmental signals in plant growth, Mol. Plant., 2015, vol. 8, p. 1153. https://doi.org/10.1016/j.molp.2015.05.003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Bartrina, I., Jensen, H., Novák, O., Strnad, M., Werner, T., and Schmülling, T., Gain-of-function mutants of the cytokinin receptors AHK2 and AHK3 regulate plant organ size, flowering time and plant longevity, Plant Physiol., 2017, vol. 173, p. 1783. https://doi.org/10.1104/pp.16.01903

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Skulachev, V.P., Aging is a specific biological function rather than the result of a disorder in complex living systems: biochemical evidence in support of Weismann’s hypothesis, Biochemistry (Moscow), 1997, vol. 62, no. 11, p. 1191.

    CAS  PubMed  Google Scholar 

  30. Cortleven, A., Marg, I., Yamburenko, M.V., Schlicke, H., Hill, K., Grimm, B., Schaller, G.E., and Schmülling, T., Cytokinin regulates the etioplast-chloroplast transition through the two-component signaling system and activation of chloroplast-related genes, Plant Physiol., 2016, vol. 172, p. 464. https://doi.org/10.1104/pp.16.00640

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

ACKNOWLEDGMENTS

We thank Dr. M.D. Logacheva, Head of the Genomics Core Facility of the Skolkovo Institute of Science and Technology, for assistance in this study.

Funding

The study was supported by the Russian Science Foundation (project no. 18-74-00135). The sequencing and bioinformatic analysis were performed at the Genomics Core Facility of the Skolkovo Institute of Science and Technology.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to M. N. Danilova.

Ethics declarations

COMPLIANCE WITH ETHICAL STANDARDS

This article does not contain any studies involving animals or human participants performed by any of the authors.

CONFLICT OF INTEREST

The authors declare that they have no conflict of interest.

Additional information

Translated by N. Statsyuk

Abbreviations: CK—cytokinins; real-time RT-PCR—real-time reverse transcription polymerase chain reaction; AHK—Arabidopsis histidine kinase.

Supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Danilova, M.N., Doroshenko, A.S., Kudryakova, N.V. et al. The Crosstalk between Cytokinin and Auxin Signaling Pathways in the Control of Natural Senescence of Arabidopsis thaliana Leaves. Russ J Plant Physiol 67, 1028–1035 (2020). https://doi.org/10.1134/S1021443720060035

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1021443720060035

Keywords:

Navigation