Dual Regulations of Cell Cycle Regulator DPa by Auxin in Root Distal Stem Cell Maintenance

Overview

Journal Proc Natl Acad Sci U S A

Specialty Science

Date 2023 May 1

PMID 37126711

Authors

Junxia Wang

Xiaoxuan Li

Xiaolu Chen

Wenxin Tang

Zipeng Yu

Tongda Xu

Huiyu Tian

Zhaojun Ding

Affiliations

Soon will be listed here.

Abstract

The plant hormone auxin plays a key role to maintain root stem cell identity which is essential for root development. However, the molecular mechanism by which auxin regulates root distal stem cell (DSC) identity is not well understood. In this study, we revealed that the cell cycle factor DPa is a vital regulator in the maintenance of root DSC identity through multiple auxin signaling cascades. On the one hand, auxin positively regulates the transcription of via AUXIN RESPONSE FACTOR 7 and ARF19. On the other hand, auxin enhances the protein stability of DPa through MITOGEN-ACTIVATED PROTEIN KINASE 3 (MPK3)/MPK6-mediated phosphorylation. Consistently, mutation of the identified three threonine residues (Thr, Thr, and Thr) of DPa to nonphosphorylated form alanine (DPa) highly decreased the phosphorylation level of DPa, which decreased its protein stability and affected the maintenance of root DSC identity. Taken together, this study provides insight into the molecular mechanism of how auxin regulates root distal stem cell identity through the dual regulations of DPa at both transcriptional and posttranslational levels.

Citing Articles

Behind phyllotaxis, within the meristem: a REM-ARF complex shapes inflorescence in Arabidopsis thaliana.

Caselli F, Ferrario C, Beretta V, Tondepu S, Dumas R, Herrera-Ubaldo H Plant J. 2025; 121(5):e70041.

PMID: 40025809 PMC: 11873677. DOI: 10.1111/tpj.70041.

Overexpression of Wheat Selenium-Binding Protein Gene Enhances Plant Growth and Grain Selenium Accumulation under Spraying Sodium Selenite.

Xiao T, Qiang J, Sun H, Luo F, Li X, Yan Y Int J Mol Sci. 2024; 25(13).

PMID: 39000115 PMC: 11240915. DOI: 10.3390/ijms25137007.

References

Guilfoyle T, Hagen G . Auxin response factors. Curr Opin Plant Biol. 2007; 10(5):453-60. DOI: 10.1016/j.pbi.2007.08.014. View

Lee Y, Lee W, Kim S . Hormonal regulation of stem cell maintenance in roots. J Exp Bot. 2012; 64(5):1153-65. DOI: 10.1093/jxb/ers331. View

Okushima Y, Overvoorde P, Arima K, Alonso J, Chan A, Chang C . Functional genomic analysis of the AUXIN RESPONSE FACTOR gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell. 2005; 17(2):444-63. PMC: 548818. DOI: 10.1105/tpc.104.028316. View

Pitzschke A . Modes of MAPK substrate recognition and control. Trends Plant Sci. 2014; 20(1):49-55. DOI: 10.1016/j.tplants.2014.09.006. View

Truernit E, Bauby H, Dubreucq B, Grandjean O, Runions J, Barthelemy J . High-resolution whole-mount imaging of three-dimensional tissue organization and gene expression enables the study of Phloem development and structure in Arabidopsis. Plant Cell. 2008; 20(6):1494-503. PMC: 2483377. DOI: 10.1105/tpc.107.056069. View

Pi L, Aichinger E, van der Graaff E, Llavata-Peris C, Weijers D, Hennig L . Organizer-Derived WOX5 Signal Maintains Root Columella Stem Cells through Chromatin-Mediated Repression of CDF4 Expression. Dev Cell. 2015; 33(5):576-88. DOI: 10.1016/j.devcel.2015.04.024. View

Jiang K, Feldman L . Regulation of root apical meristem development. Annu Rev Cell Dev Biol. 2005; 21:485-509. DOI: 10.1146/annurev.cellbio.21.122303.114753. View

Perilli S, Di Mambro R, Sabatini S . Growth and development of the root apical meristem. Curr Opin Plant Biol. 2011; 15(1):17-23. DOI: 10.1016/j.pbi.2011.10.006. View

Li H, Ding Y, Shi Y, Zhang X, Zhang S, Gong Z . MPK3- and MPK6-Mediated ICE1 Phosphorylation Negatively Regulates ICE1 Stability and Freezing Tolerance in Arabidopsis. Dev Cell. 2017; 43(5):630-642.e4. DOI: 10.1016/j.devcel.2017.09.025. View

10.

Lv B, Yu Q, Liu J, Wen X, Yan Z, Hu K . Non-canonical AUX/IAA protein IAA33 competes with canonical AUX/IAA repressor IAA5 to negatively regulate auxin signaling. EMBO J. 2019; 39(1):e101515. PMC: 6939196. DOI: 10.15252/embj.2019101515. View

11.

Savina M, Pasternak T, Omelyanchuk N, Novikova D, Palme K, Mironova V . Cell Dynamics in WOX5-Overexpressing Root Tips: The Impact of Local Auxin Biosynthesis. Front Plant Sci. 2020; 11:560169. PMC: 7642516. DOI: 10.3389/fpls.2020.560169. View

12.

Xu J, Xie J, Yan C, Zou X, Ren D, Zhang S . A chemical genetic approach demonstrates that MPK3/MPK6 activation and NADPH oxidase-mediated oxidative burst are two independent signaling events in plant immunity. Plant J. 2013; 77(2):222-34. PMC: 4017028. DOI: 10.1111/tpj.12382. View

13.

Cheng Y, Dai X, Zhao Y . Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell. 2007; 19(8):2430-9. PMC: 2002601. DOI: 10.1105/tpc.107.053009. View

14.

Vandepoele K, Raes J, De Veylder L, Rouze P, Rombauts S, Inze D . Genome-wide analysis of core cell cycle genes in Arabidopsis. Plant Cell. 2002; 14(4):903-16. PMC: 150691. DOI: 10.1105/tpc.010445. View

15.

Chapman E, Estelle M . Mechanism of auxin-regulated gene expression in plants. Annu Rev Genet. 2009; 43:265-85. DOI: 10.1146/annurev-genet-102108-134148. View

16.

Grieneisen V, Xu J, Maree A, Hogeweg P, Scheres B . Auxin transport is sufficient to generate a maximum and gradient guiding root growth. Nature. 2007; 449(7165):1008-13. DOI: 10.1038/nature06215. View

17.

Leyser O . Auxin Signaling. Plant Physiol. 2017; 176(1):465-479. PMC: 5761761. DOI: 10.1104/pp.17.00765. View

18.

Yan D, Wang J, Yuan T, Hong L, Gao X, Lu Y . Perturbation of auxin homeostasis by overexpression of wild-type IAA15 results in impaired stem cell differentiation and gravitropism in roots. PLoS One. 2013; 8(3):e58103. PMC: 3589423. DOI: 10.1371/journal.pone.0058103. View

19.

Liu Y, Lai J, Yu M, Wang F, Zhang J, Jiang J . The Arabidopsis SUMO E3 Ligase AtMMS21 Dissociates the E2Fa/DPa Complex in Cell Cycle Regulation. Plant Cell. 2016; 28(9):2225-2237. PMC: 5059808. DOI: 10.1105/tpc.16.00439. View

20.

Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J . An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell. 1999; 99(5):463-72. DOI: 10.1016/s0092-8674(00)81535-4. View