Skip to main content
Log in

MYB3R-mediated active repression of cell cycle and growth under salt stress in Arabidopsis thaliana

  • Regular Paper – Genetics/Developmental Biology
  • Published:
Journal of Plant Research Aims and scope Submit manuscript

Abstract

Under environmental stress, plants are believed to actively repress their growth to save resource and alter its allocation to acquire tolerance against the stress. Although a lot of studies have uncovered precise mechanisms for responding to stress and acquiring tolerance, the mechanisms for regulating growth repression under stress are not as well understood. It is especially unclear which particular genes related to cell cycle control are involved in active growth repression. Here, we showed that decreased growth in plants exposed to moderate salt stress is mediated by MYB3R transcription factors that have been known to positively and negatively regulate the transcription of G2/M-specific genes. Our genome-wide gene expression analysis revealed occurrences of general downregulation of G2/M-specific genes in Arabidopsis under salt stress. Importantly, this downregulation is significantly and universally mitigated by the loss of MYB3R repressors by mutations. Accordingly, the growth performance of Arabidopsis plants under salt stress is significantly recovered in mutants lacking MYB3R repressors. This growth recovery involves improved cell proliferation that is possibly due to prolonging and accelerating cell proliferation, which were partly suggested by enlarged root meristem and increased number of cells positive for CYCB1;1-GUS. Our ploidy analysis further suggested that cell cycle progression at the G2 phase was delayed under salt stress, and this delay was recovered by loss of MYB3R repressors. Under salt stress, the changes in expression of MYB3R activators and repressors at both the mRNA and protein levels were not significant. This observation suggests novel mechanisms underlying MYB3R-mediated growth repression under salt stress that are different from the mechanisms operating under other stress conditions such as DNA damage and high temperature.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8

Similar content being viewed by others

Data deposition

RNA-seq data generated in this study has been deposited in the DDBJ Sequence Read Archive (DRA) under Accession Numbers DRA010790.

References

  • Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94

    Article  CAS  PubMed  Google Scholar 

  • Achard P, Gong F, Cheminant S, Alioua M, Hedden P, Genschik P (2008) The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20:2117–2129

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bechtold U, Field B (2018) Molecular mechanisms controlling plant growth during abiotic stress. J Exp Bot 69:2753–2758

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beemster GT, De Veylder L, Vercruysse S, West G, Rombaut D, Van Hummelen P, Galichet A, Gruissem W, Inzé D, Vuylsteke M (2005) Genome-wide analysis of gene expression profiles associated with cell cycle transitions in growing organs of Arabidopsis. Plant Physiol 138:734–743

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bouyer D, Heese M, Chen P, Harashima H, Roudier F, Grüttner C, Schnittger A (2018) Genome-wide identification of RETINOBLASTOMA RELATED 1 binding sites in Arabidopsis reveals novel DNA damage regulators. PLoS Genet 14:e1007797

    Article  PubMed  PubMed Central  Google Scholar 

  • Burssens S, Himanen K, van de Cotte B, Beeckman T, Van Montagu M, Inzé D, Verbruggen N (2000) Expression of cell cycle regulatory genes and morphological alterations in response to salt stress in Arabidopsis thaliana. Planta 211:632–640

    Article  CAS  PubMed  Google Scholar 

  • Campilho A, Garcia B, Toorn HV, Wijk HV, Campilho A, Scheres B (2006) Time-lapse analysis of stem-cell divisions in the Arabidopsis thaliana root meristem. Plant J 48:619–627

    Article  CAS  PubMed  Google Scholar 

  • Chen P, Takatsuka H, Takahashi N, Kurata R, Fukao Y, Kobayashi K, Ito M, Umeda M (2017) Arabidopsis R1R2R3-Myb proteins are essential for inhibiting cell division in response to DNA damage. Nat Commun 8:635

    Article  PubMed  PubMed Central  Google Scholar 

  • Claeys H, Skirycz A, Maleux K, Inzé D (2012) DELLA signaling mediates stress-induced cell differentiation in Arabidopsis leaves through modulation of anaphase-promoting complex/cyclosome activity. Plant Physiol 159:739–747

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217:67–75

    Article  CAS  PubMed  Google Scholar 

  • Colón-Carmona A, You R, Haimovitch-Gal T, Doerner P (1999) Spatio-temporal analysis of mitotic activity with a labile cyclin-GUS fusion protein. Plant J 20:503–508

    Article  PubMed  Google Scholar 

  • Davière JM, Achard P (2016) A pivotal role of DELLAs in regulating multiple hormone signals. Mol Plant 9:10–20

    Article  PubMed  Google Scholar 

  • Dubois M, Skirycz A, Claeys H, Maleux K, Dhondt S, De Bodt S, Vanden Bossche R, De Milde L, Yoshizumi T, Matsui M, Inzé D (2013) Ethylene Response Factor6 acts as a central regulator of leaf growth under water-limiting conditions in Arabidopsis. Plant Physiol 162:319–332

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dubos C, Stracke R, Grotewold E, Weisshaar B, Martin C, Lepiniec L (2010) MYB transcription factors in Arabidopsis. Trends Plant Sci 15:573–581

    Article  CAS  PubMed  Google Scholar 

  • Feng G, Burleigh JG, Braun EL, Mei W, Barbazuk WB (2017) Evolution of the 3R-MYB Gene Family in Plants. Genome Biol Evol 9:1013–1029

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer M, DeCaprio JA (2015) Does Arabidopsis thaliana DREAM of cell cycle control? EMBO J 34:1987–1989

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Geng Y, Wu R, Wee CW, Xie F, Wei X, Chan PM, Tham C, Duan L, Dinneny JR (2013) A spatio-temporal understanding of growth regulation during the salt stress response in Arabidopsis. Plant Cell 25:2132–2154

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Georlette D, Ahn S, MacAlpine DM, Cheung E, Lewis PW, Beall EL, Bell SP, Speed T, Manak JR, Botchan MR (2007) Genomic profiling and expression studies reveal both positive and negative activities for the Drosophila Myb MuvB/dREAM complex in proliferating cells. Genes Dev 21:2880–2896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Golldack D, Li C, Mohan H, Probst N (2014) Tolerance to drought and salt stress in plants: unraveling the signaling networks. Front Plant Sci 5:151

    Article  PubMed  PubMed Central  Google Scholar 

  • Gu F, Bringmann M, Combs JR, Yang J, Bergmann DC, Nielsen E (2016) Arabidopsis CSLD5 functions in cell plate formation in a cell cycle-dependent manner. Plant Cell 28:1722–1737

    CAS  PubMed  PubMed Central  Google Scholar 

  • Haga N, Kato K, Murase M, Araki S, Kubo M, Demura T, Suzuki K, Müller I, Voss U, Jürgens G, Ito M (2007) R1R2R3-Myb proteins positively regulate cytokinesis through activation of KNOLLE transcription in Arabidopsis thaliana. Development 134:1101–1110

    Article  CAS  PubMed  Google Scholar 

  • Haga N, Kobayashi K, Suzuki T, Maeo K, Kubo M, Ohtani M, Mitsuda N, Demura T, Nakamura K, Jürgens G, Ito M (2011) Mutations in MYB3R1 and MYB3R4 cause pleiotropic developmental defects and preferential down-regulation of multiple G2/M-specific genes in Arabidopsis. Plant Physiol 157:706–717

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Heyman J, Veylder L (2012) The anaphase-promoting complex/cyclosome in control of plant development. Mol Plant 5:1182–1194

    Article  CAS  PubMed  Google Scholar 

  • Heyman J, Daele H, den Wit K, Boudolf V, Berckmans B, Verkest A, Kamei C, Jaeger G, Koncz C, Veylder L (2011) Arabidopsis ULTRAVIOLET-B-INSENSITIVE4 maintains cell division activity by temporal inhibition of the anaphase-promoting complex/cyclosome. Plant Cell 23:4394–4410

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ito M (2005) Conservation and diversification of three-repeat Myb transcription factors in plants. J Plant Res 118:61–69

    Article  CAS  PubMed  Google Scholar 

  • Ito M, Iwase M, Kodama H, Lavisse P, Komamine A, Nishihama R, Machida Y, Watanabe A (1998) A novel cis-acting element in promoters of plant B-type cyclin genes activates M phase-specific transcription. Plant Cell 10:331–341

    CAS  PubMed  PubMed Central  Google Scholar 

  • Ito M, Araki S, Matsunaga S, Itoh T, Nishihama R, Machida Y, Doonan JH, Watanabe A (2001) G2/M-phase-specific transcription during the plant cell cycle is mediated by c-Myb-like transcription factors. Plant Cell 13:1891–1905

    CAS  PubMed  PubMed Central  Google Scholar 

  • Itoh H, Ueguchi-Tanaka M, Sato Y, Ashikari M, Matsuoka M (2002) The gibberellin signaling pathway is regulated by the appearance and disappearance of SLENDER RICE1 in nuclei. Plant Cell 14:57–70

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Julkowska MM, Testerink C (2015) Tuning plant signaling and growth to survive salt. Trends Plant Sci 20:586–594

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi K, Suzuki T, Iwata E, Nakamichi N, Suzuki T, Chen P, Ohtani M, Ishida T, Hosoya H, Müller S, Leviczky T, Pettkó-Szandtner A, Darula Z, Iwamoto A, Nomoto M, Tada Y, Higashiyama T, Demura T, Doonan JH, Hauser MT, Sugimoto K, Umeda M, Magyar Z, Bögre L, Ito M (2015a) Transcriptional repression by MYB3R proteins regulates plant organ growth. EMBO J 34:1992–2007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kobayashi K, Suzuki T, Iwata E, Magyar Z, Bögre L, Ito M (2015b) MYB3Rs plant homologs of Myb oncoproteins, control cell cycle-regulated transcription and form DREAM-like complexes. Transcription 6:106–111

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kudo M, Kidokoro S, Yoshida T, Mizoi J, Kojima M, Takebayashi Y, Sakakibara H, Fernie AR, Shinozaki K, Yamaguchi-Shinozaki K (2019) A gene-stacking approach to overcome the trade-off between drought stress tolerance and growth in Arabidopsis. Plant J 97:240–256

    Article  CAS  PubMed  Google Scholar 

  • Kumari A, Jewaria PK, Bergmann DC, Kakimoto T (2014) Arabidopsis reduces growth under osmotic stress by decreasing SPEECHLESS protein. Plant Cell Physiol 55:2037–2046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Langmead B, Trapnell C, Pop M, Salzberg SL (2009) Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 10:R25

    Article  PubMed  PubMed Central  Google Scholar 

  • Lauber MH, Waizenegger I, Steinmann T, Schwarz H, Mayer U, Hwang I, Lukowitz W, Jürgens G (1997) The Arabidopsis KNOLLE protein is a cytokinesis-specific syntaxin. J Cell Biol 139:1485–1493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Litovchick L, Sadasivam S, Florens L, Zhu X, Swanson SK, Velmurugan S, Chen R, Washburn MP, Liu XS, DeCaprio JA (2007) Evolutionarily conserved multisubunit RBL2/p130 and E2F4 protein complex represses human cell cycle-dependent genes in quiescence. Mol Cell 26:539–551

    Article  CAS  PubMed  Google Scholar 

  • MacAlister CA, Ohashi-Ito K, Bergmann DC (2007) Transcription factor control of asymmetric cell divisions that establish the stomatal lineage. Nature 445:537–540

    Article  CAS  PubMed  Google Scholar 

  • Magome H, Yamaguchi S, Hanada A, Kamiya Y, Oda K (2008) The DDF1 transcriptional activator upregulates expression of a gibberellin-deactivating gene, GA2ox7, under high-salinity stress in Arabidopsis. Plant J 56:613–626

    Article  CAS  PubMed  Google Scholar 

  • Magyar Z, Bögre L, Ito M (2016) DREAMs make plant cells to cycle or to become quiescent. Curr Opin Plant Biol 34:100–106

    Article  CAS  PubMed  Google Scholar 

  • Marrocco K, Bergdoll M, Achard P, Criqui MC, Genschik P (2010) Selective proteolysis sets the tempo of the cell cycle. Curr Opin Plant Biol 13:631–639

    Article  CAS  PubMed  Google Scholar 

  • Menges M, de Jager SM, Gruissem W, Murray JA (2005) Global analysis of the core cell cycle regulators of Arabidopsis identifies novel genes, reveals multiple and highly specific profiles of expression and provides a coherent model for plant cell cycle control. Plant J 41:546–566

    Article  CAS  PubMed  Google Scholar 

  • Ning YQ, Liu N, Lan KK, Su YN, Li L, Chen S, He XJ (2020) DREAM complex suppresses DNA methylation maintenance genes and precludes DNA hypermethylation. Nat Plants 6:942–956

    Article  CAS  PubMed  Google Scholar 

  • Robinson MD, McCarthy DJ, Smyth GK (2010) edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26:139–140

    Article  CAS  PubMed  Google Scholar 

  • Sadasivam S, Duan S, DeCaprio JA (2012) The MuvB complex sequentially recruits B-Myb and FoxM1 to promote mitotic gene expression. Genes Dev 26:474–489

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seki M, Kamei A, Yamaguchi-Shinozaki K, Shinozaki K (2003) Molecular responses to drought, salinity and frost: common and different paths for plant protection. Curr Opin Biotechnol 14:194–199

    Article  CAS  PubMed  Google Scholar 

  • Shinozaki K, Yamaguchi-Shinozaki K, Seki M (2003) Regulatory network of gene expression in the drought and cold stress responses. Curr Opin Plant Biol 6:410–417

    Article  CAS  PubMed  Google Scholar 

  • Skirycz A, Claeys H, De Bodt S, Oikawa A, Shinoda S, Andriankaja M, Maleux K, Eloy NB, Coppens F, Yoo SD, Saito K, Inzé D (2011a) Pause-and-stop: the effects of osmotic stress on cell proliferation during early leaf development in Arabidopsis and a role for ethylene signaling in cell cycle arrest. Plant Cell 23:1876–1888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Skirycz A, Vandenbroucke K, Clauw P, Maleux K, De Meyer B, Dhondt S, Pucci A, Gonzalez N, Hoeberichts F, Tognetti VB, Galbiati M, Tonelli C, Van Breusegem F, Vuylsteke M, Inzé D (2011b) Survival and growth of Arabidopsis plants given limited water are not equal. Nat Biotechnol 29:212–214

    Article  CAS  PubMed  Google Scholar 

  • Song L, Huang SC, Wise A, Castanon R, Nery JR, Chen H, Watanabe M, Thomas J, Bar-Joseph Z, Ecker JR (2016) A transcription factor hierarchy defines an environmental stress response network. Science 354:aag1550

    Article  PubMed  PubMed Central  Google Scholar 

  • Strompen G, El Kasmi F, Richter S, Lukowitz W, Assaad FF, Jürgens G, Mayer U (2002) The Arabidopsis HINKEL gene encodes a kinesin-related protein involved in cytokinesis and is expressed in a cell cycle-dependent manner. Curr Biol 12:153–158

    Article  CAS  PubMed  Google Scholar 

  • Takahashi N, Ogita N, Takahashi T, Taniguchi S, Tanaka M, Seki M, Umeda M (2019) A regulatory module controlling stress-induced cell cycle arrest in Arabidopsis. Elife 8:e43944

    Article  PubMed  PubMed Central  Google Scholar 

  • Umezawa T, Fujita M, Fujita Y, Yamaguchi-Shinozaki K, Shinozaki K (2006) Engineering drought tolerance in plants: discovering and tailoring genes to unlock the future. Curr Opin Biotechnol 17:113–122

    Article  CAS  PubMed  Google Scholar 

  • Vandepoele K, Vlieghe K, Florquin K, Hennig L, Beemster GT, Gruissem W, Van de Peer Y, Inzé D, De Veylder L (2005) Genome-wide identification of potential plant E2F target genes. Plant Physiol 139:316–328

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vlieghe K, Boudolf V, Beemster GT, Maes S, Magyar Z, Atanassova A, de Almeida Engler J, De Groodt R, Inzé D, De Veylder L (2005) The DP-E2F-like gene DEL1 controls the endocycle in Arabidopsis thaliana. Curr Biol 15:59–63

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Wang H, Shao H, Tang X (2016) Recent Advances in Utilizing Transcription factors to improve plant abiotic stress tolerance by transgenic technology. Front Plant Sci 7:67

    PubMed  PubMed Central  Google Scholar 

  • West G, Inzé D, Beemster GT (2004) Cell cycle modulation in the response of the primary root of Arabidopsis to salt stress. Plant Physiol 135:1050–1058

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803

    Article  CAS  PubMed  Google Scholar 

  • Zhu JK (2016) Abiotic stress signaling and responses in plants. Cell 167:313–324

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

The authors thank Kyoko Kato, Akiko Nakanishi, Natsuko Ono, Akiko Yamamoto, Chikako Inoue, Nanako Ishibashi, Satoko Nasu, Yuiko Tachikawa, Asako Segawa and Ayumi Yamada for technical assistance. This study was funded by The Japan Society for the Promotion of Science KAKENHI (20H05408 and 17H03696 to M. Ito).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masaki Ito.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic Supplementary Material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Okumura, T., Nomoto, Y., Kobayashi, K. et al. MYB3R-mediated active repression of cell cycle and growth under salt stress in Arabidopsis thaliana. J Plant Res 134, 261–277 (2021). https://doi.org/10.1007/s10265-020-01250-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10265-020-01250-8

Keywords

Navigation