Skip to main content
SpringerLink
Log in

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

  • Published:
Plant Molecular Biology Aims and scope Submit manuscript

Abstract

Key message

Cytokinin membrane receptors of the Arabidopsis thaliana AHK2 and AHK3 play opposite roles in the expression of plastid genes and genes for the plastid transcriptional machinery during leaf senescence

Abstract

Loss-of-function mutants of Arabidopsis thaliana were used to study the role of cytokinin receptors in the expression of chloroplast genes during leaf senescence. Accumulation of transcripts of several plastid-encoded genes is dependent on the АНК2/АНК3 receptor combination. АНК2 is particularly important at the final stage of plant development and, unlike АНК3, a positive regulator of leaf senescence. Cytokinin-dependent up-regulation of the nuclear encoded genes for chloroplast RNA polymerases RPOTp and RPOTmp suggests that the hormone controls plastid gene expression, at least in part, via the expression of nuclear genes for the plastid transcription machinery. This is further supported by cytokinin dependent regulation of genes for the nuclear encoded plastid σ-factors, SIG1-6, which code for components of the transcriptional apparatus in chloroplasts.

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

Access this article

Log in via an institution

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
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

References

  • Baumgartner BJ, Rapp JC, Mullet JE (1989) Plastid transcription activity and DNA copy number increase early in barley chloroplast development. Plant Physiol 89:1011–1018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bock R (2007) Structure, function and inheritance of plastid genomes. Topics in current genetic V.19. In: Bock R (ed) Cell and molecular biology of plastids. Springer, Berlin, pp 29–63

    Chapter  Google Scholar 

  • Boffey SA, Leech RM (1982) Chloroplast DNA levels and the control of chloroplast division in light-grown wheat leaves. Plant Physiol 69:1387–1391

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Börner T, Aleynikova AY, Zubo YO, Kusnetsov VV (2015) Chloroplast RNA polymerases: role in chloroplast biogenesis. Biochim Biophys Acta 1847:761–769

    Article  PubMed  Google Scholar 

  • Borsellino L (2011) Influence of light and cytokinin on organellar phage-type RNA polymerase transcript levels and transcription of organellar genes in Arabidopsis thaliana. PhD thesis HumboltUniversitätzu, Berlin

  • Brenner WG, Romanov GA, Köllmer I, Bürkle L, Schmülling T (2005) 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 44:314–333

    Article  CAS  PubMed  Google Scholar 

  • Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim PO, Nam HG, Lin JF, Wu SH, Swidzinski J, Ishizaki K, Leaver CJ (2005) Comparative transcriptome analysis reveals significant differences in gene expression and signalling pathways between developmental and dark/starvation-induced senescence in Arabidopsis. Plant J 42:567–585

    Article  CAS  PubMed  Google Scholar 

  • Cortleven A, Schmülling T (2015) Regulation of chloroplast development and function by cytolkinin. J Exp Bot 66:4999–5013

    Article  CAS  PubMed  Google Scholar 

  • Danilova MN, Kudryakova NV, Oelmüller R, Kusnetsov VV, Kulaeva ON (2012) Participation of membrane cytokinin receptors in regulation of transcription of chloroplast genes. Bulletin of Russian Peoples’ Friendship University. Series: agronomy and animal husbandry 4:23–33

  • Danilova MN, Kudryakova NV, Voronin PY, Kuznetsov VV, Kulaeva ON (2014) Membrane receptors of cytokinin and their regulatory role in Arabidopsis thaliana plant response to photooxidative stress under conditions of water deficit. Russ J Plant Physiol 61(4):466–475

    Article  Google Scholar 

  • Danilova MN, Doroshenko AS, Kudryakova NV, Kusnetsov VV (2015) Nuclear encoded genes for plastid transcription regulate cytokinin-dependent transcription of the chloroplast genome. Proceedings of the all-Russian conference with international participation and school for young scientists “Fundamental and Applied Problems of Modern Experimental Plant Biology” dedicated to 125th anniversary of Timiryazev Institute of Plant Physiology, 23–27 November 2015, Moscow 200–204

  • Danilova MN, Kudryakova NV, Doroshenko AS, Zabrodin DA, Vinogradov NS, Kusnetsov VV (2016) Molecular and physiological responses of Arabidopsis thaliana plants deficient in the genes responsible for ABA and cytokinin reception and metabolism to heat shock. Russ J Plant Physiol 63:308–318

    Article  CAS  Google Scholar 

  • Dortay H, Gruhn N, Pfeifer A, Schwerdtner M, Schmülling T, Heyl A (2008) Toward an interaction map of the two-component signaling pathway of Arabidopsis thaliana. J Proteome Res 7:3649–3660

    Article  CAS  PubMed  Google Scholar 

  • Emanuel C, Groll U, Mṻller M, Börner T, Weihe A (2006) Development- and tissue-specific expression of the RpoT gene family of Arabidopsis encoding mitochondrial and plastid RNA polymerases. Planta 223:998–1009

    Article  CAS  PubMed  Google Scholar 

  • Ferreira FJ, Kieber JJ (2005) Cytokinin signaling. Curr Opin Plant Biol 8:518–525

    Article  CAS  PubMed  Google Scholar 

  • Goentoro L, Shoval O, Kirshner MV, Alon U (2009) The incoherent feedforward loop can provide fold-change detection in gene regulation. Mol Cell 36:894–899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregersen PL, Holm PB (2007) Transcriptome analysis of senescence in the flag leaf of wheat (Triticumaestivum L.). Plant Biotechnol J 5:192–206

    Article  CAS  PubMed  Google Scholar 

  • Hajdukiewicz PT, Allison LA, Maliga P (1997) The two RNA polymerases encoded by the nuclear and the plastid compartments transcribe distinct groups of genes in tobacco plastids. EMBO J 16:4041–4048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Higuchi M, Pischke MS, Mähönen AP, Miyawaki K, Hashimoto Y, Seki M, Kobayashi M, Shinozaki K, Kato T, Tabata S, Helariutta Y, Sussman MR, Kakimoto T (2004) In planta functions of the Arabidopsis cytokinin receptor family. Proc Natl Acad Sci USA 101:8821–8826

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hwang I, Sheen J, Müller B (2012) Cytokinin signaling networks. Ann Rev Plant Biol 63:353–380

    Article  CAS  Google Scholar 

  • Igarashi D, Izumi Y, Dokiya Y, Totsuka K, Fukusaki E, OhsumiCh (2009) Reproductive organs regulate leaf nitrogen metabolism mediated by cytokinin signal. Planta 229:633–644

    Article  CAS  PubMed  Google Scholar 

  • Isono K, Niwa Y, Satoh K, Kobayashi H (1997) Evidence for transcriptional regulation of plastid photosynthesis genes in Arabidopsis thaliana roots. Plant Physiol 114:623–630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Keech O, Pesquet E, Ahad A, Askne A, Nordvall D, Vodnala SM, Tuominen H, Harry V, Dizengremel P, Gardenstrom P (2007) The different fates of mitochondria and chloroplasts during dark-induced senescence in Arabidopsis leaves. Plant cell Environ 30:1523–1534

    Article  CAS  PubMed  Google Scholar 

  • Kim HJ, Ryu H, Hong SH, Woo HR, Lim PO, Lee IC, Sheen J, NamHG, Hwang I (2006) Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc Natl Acad Sci USA 103:814–819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kmiecik P, Leonardelli M, Teige M (2016) Novel connections in plant organellar signalling link different stress responses and signalling pathways. J Exp Bot 67:3793–3807

    Article  CAS  PubMed  Google Scholar 

  • Krause K, Falk J, Humbeck K, Krupinsky R (1998) Responses of the transcriptional apparatus of barley chloroplasts to a prolonged dark period and to subsequent reillumination. Physiol Plant 104:143–152

    Article  CAS  Google Scholar 

  • Krupinska K, Melonek J, Krause K (2013) New insights into plastid nucleoid structure and functionality. Planta 237:653–664

    Article  CAS  PubMed  Google Scholar 

  • Lamppa GK, Bendich AJ (1979) Changes in chloroplast DNA levels during development of pea (Pisum sativum). Plant Physiol 64:126–130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lerbs-Mache S (2011) Function of plastid sigma factors in higher plants: regulation of gene expression or just preservation of constitutive transcription? Plant Mol Biol 76:235–249

    Article  CAS  PubMed  Google Scholar 

  • Li W, Ruf S, Bock R (2006) Constancy of organellar genome copy numbers during leaf development and senescence in higher plants. Mol Genet Genomics 275:185–192

    Article  CAS  PubMed  Google Scholar 

  • Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Methods Enzymol 148:350–382

    Article  CAS  Google Scholar 

  • Liere K, Börner T (2007) Transcription of plastid genes. In: Grasser KD (ed) Regulation of transcription in plants. Oxford, Blackwell, pp 184–224

    Chapter  Google Scholar 

  • Liere K, Börner T (2013) Development dependent changes in the amount and structure of plastid DNA. In: Biswal B, Krupinska K, Biswal UC (eds) Chloroplast development during leaf growth and senescence. Springer, Dordrecht, pp 215–223

    Chapter  Google Scholar 

  • Lim PO, Kim HJ, Nam HG (2007) Leaf senescence. Annu Rev Plant Biol 58:115–136

    Article  CAS  PubMed  Google Scholar 

  • Lysenko EA (2007) Plant sigma factors and their role in plastid transcription. Plant Cell Rep 26:845–859

    Article  CAS  PubMed  Google Scholar 

  • Miyamura S, Nagata T, Kuroiwa T (1986) Quantitative fluorescence microscopy on dynamic changes of plastid nucleoids during wheat development. Protoplasma 133:66–72

    Article  CAS  Google Scholar 

  • Mothes K, Engelbrecht L, Kulajewa O (1959) Uber die Wirkung des Kinitins auf Stickstoffverteilung und Eiweissynthese in isolierten Blattern. Flora 147:446–464

    Google Scholar 

  • Müller B, Sheen J (2007) Advances in cytokinin signaling. Science 318(5847):68–69

    Article  PubMed  Google Scholar 

  • Nagashima A, Hanaoka M, Shikanai T, Fujiwara M, Kanamaru K, Takahashi H, Tanaka K (2004) The multiple-stress responsive plastid sigma factor, SIG5, directs activation of the psbD blue light-responsive promoter (BLRP) in Arabidopsis thaliana. Plant Cell Physiol 45:357–368

    Article  CAS  PubMed  Google Scholar 

  • Nakabayashi K, Ito M, Kiyosue T, Shinozaki K, Wanatabe A (1999) Identification of clp genes expressed in senescing Arabidopsis leaves. Plant Cell Physiol 40:504–514

    Article  CAS  PubMed  Google Scholar 

  • Pfannschmidt T, Blanvillain R, Merendino L, Courtois F, Chevalier F, Liebers M, Grübler B, Hommel E, Lerbs-Mache S (2015) Plastid RNA polymerases: orchestration of enzymes with different evolutionary origins controls chloroplast biogenesis during the plant life cycle. J Exp Bot 66:6957–6973

    Article  CAS  PubMed  Google Scholar 

  • Powikrowska M, Oetke S, Jensen PE, Krupinska K (2014) Dynamic composition, shaping and organization of plastid nucleoids. Front Plant Sci 5:article 424. doi:10.3389/fpls.2014.00424

  • Raines T, Shanks C, Cheng CY, McPherson D, Argueso CT, Kim HJ, Franco-Zorrilla JM, López-Vidriero I, Solano R, Vankova R, Schaller GE, Kieber JJ (2016) The cytokinin response factors modulate root and shoot growth and promote leaf senescence in Arabidopsis. Plant J 85:134–147

    Article  CAS  PubMed  Google Scholar 

  • Riefler M, Novak O, Strnad M, Schmülling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development and cytokinin metabolism. Plant Cell 18:40–54

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schweer J, Türkeri H, Link B, Link G (2010) AtSIG6, a plastid sigma factor from Arabidopsis, reveals functional impact of cpCK2 phosphorylation. Plant J 62:192–202

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Steiner S, Schröter Y, Pfalz J, Pfannschmidt Th (2011) Identification of essential subunits in the plastid-encoded RNA polymerase complex reveals building blocks for proper plastid development. Plant Physiol 157:1043–1055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sugliani M, Abdelkefi H, Ke H, Bouveret E, Robaglia CH, Caffarri S, Field B (2016) An ancient bacterial signaling pathway regulates chloroplast function to influence growth and development in Arabidopsis. Plant Cell 28:661–679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van der Graaf E, Schwacke R, Schneider A, Desimone M, Flṻgge U, Kunze R (2006) Transcription analysis of Arabidopsis membrane transporters and hormone pathways during developmental and induced leaf senescence. Plant Physiol 141: 776–792

    Article  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3:34–45

    Article  Google Scholar 

  • Woo HR, Kim HJ, Nam HG, Lim PO (2013) Plant leaf senescence and death-regulation by multiple layers of control and implications for aging in general. J Cell Sci 126:4823–4833

    Article  CAS  PubMed  Google Scholar 

  • Yamburenko MV, Zubo YO, Börner T (2015) Abscisic acid affects transcription of chloroplast genes via protein phosphatase 2C-dependent activation of nuclear genes: repression by guanosine-3′-5′-bisdiphosphate and activation by sigma factor 5. Plant J 82:1030–1041

    Article  CAS  PubMed  Google Scholar 

  • Yu OB, Huang C, Yang ZN (2014) Nuclear-encoded factors associated with the chloroplast transcription machinery of higher plants. Front Plant Sci 5:316

    PubMed  PubMed Central  Google Scholar 

  • Zhelyazkova P, Sharma CM, Förstner KU, Liere K, Vogel J, Börner T (2012) The primary transcriptome of barley chloroplasts: numerous noncoding RNAs and the dominating role of the plastid-encoded RNA polymerase. Plant Cell 24:123–136

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zoschke R, Liere K, Börner T (2007) From seedling to mature plant: Arabidopsis plastidial genome copy number, RNA accumulation and transcription are differentially regulated during leaf development. Plant J 50:710–722

    Article  CAS  PubMed  Google Scholar 

  • Zubo YO, Yamburenko VN, Selivankina SYu, Shakirova FM, Avalbaev AM, Kudryakova NV, Zubkova NK, Liere K, Kulaeva ON, Kusnetsov VV, Borner Th. (2008) Cytokinins stimulate chloroplast transcription in detached barley leaves. Plant Physiol 148:1082–1093

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zwack PJ, Robinson BR, Risley MG, Rashotte AM (2013) Cytokinin response factor 6 negatively regulates leaf senescence and is induced in response to cytokinin and numerous abiotic stresses. Plant Cell Physiol 54:971–981

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the grant from the Russian Science Foundation (No. 14-14-00584). We thank Dr. Tatsuo Kakimoto from Osaka University, Japan for cre1-12, ahk2-2, ahk3-3, ahk2-2 ahk3-3, ahk2-2 cre1-12, ahk3-3 cre1-12 mutants.

Author contributions

MND designed and conducted the experiments, analyzed the data, and accomplished pictures for the manuscript. ACD, DAZ, ZFR performed the experiments and analyzed the data. NVK contributed in design of the experiments, analyzed the data and wrote the manuscript. RO analyzed the data, and finalized the manuscript. VVK conceived and designed the experiments, analyzed the data, and finalized the manuscript. All authors read and approved the final manuscript.

Author information

Authors and Affiliations

  1. Timiryazev Institute of Plant Physiology, Russian Academy of Sciences, Botanicheskaya 35, Moscow, 127276, Russia

    Maria N. Danilova, Natalia V. Kudryakova, Anastasia S. Doroshenko, Dmitry A. Zabrodin, Zulfira F. Rakhmankulova & Victor V. Kusnetsov

  2. Institute of General Botany and Plant Physiology, Friedrich-Schiller University Jena, 07743, Jena, Germany

    Ralf Oelmüller

Authors
  1. Maria N. Danilova
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Natalia V. Kudryakova
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Anastasia S. Doroshenko
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Dmitry A. Zabrodin
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Zulfira F. Rakhmankulova
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Ralf Oelmüller
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Victor V. Kusnetsov
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Natalia V. Kudryakova.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Electronic 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., Kudryakova, N.V., Doroshenko, A.S. et al. 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 93, 533–546 (2017). https://doi.org/10.1007/s11103-016-0580-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11103-016-0580-6

Keywords

Search

Navigation