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• W4313334553 abstract "•DA3 regulates lateral root initiation by modulating auxin signaling in roots•DA3 interacts with SHY2 to synergistically regulate lateral root initiation•DA3 and SHY2 interact with ARF7 and ARF19 and affect their mRNA and protein levels•DA3 and SHY2 suppress LBD16 expression in the pericycle via ARF7 and ARF19 Lateral root (LR) initiation is controlled by the pericycle and the neighboring endodermis in Arabidopsis. Here, we demonstrate that UBIQUITIN-SPECIFIC PROTEASE14/DA3 regulates LR initiation by modulating auxin signaling in the pericycle and endodermis. DA3 negatively affects the mRNA and protein levels of AUXIN RESPONSE FACTOR7 (ARF7) and ARF19 in the pericycle and endodermis but positively regulates the protein stability of SHORT HYPOCOTYL 2 (SHY2/IAA3), an auxin signaling repressor, in the endodermis. We show that DA3 interacts with ARF7 and ARF19, inhibiting their binding to the locus of LATERAL ORGAN BOUNDARY DOMAIN16 (LBD16) to repress its expression in the pericycle. SHY2 also interacts with ARF7 and ARF19 in the endodermis and enhances the DA3 repressive effect on ARF7 and ARF19, thus modulating LBD16 expression in the pericycle. Overall, our findings show that DA3 acts with SHY2, ARF7, and ARF19 to coordinate auxin signaling in the pericycle and endodermis to control LR initiation in Arabidopsis. Lateral root (LR) initiation is controlled by the pericycle and the neighboring endodermis in Arabidopsis. Here, we demonstrate that UBIQUITIN-SPECIFIC PROTEASE14/DA3 regulates LR initiation by modulating auxin signaling in the pericycle and endodermis. DA3 negatively affects the mRNA and protein levels of AUXIN RESPONSE FACTOR7 (ARF7) and ARF19 in the pericycle and endodermis but positively regulates the protein stability of SHORT HYPOCOTYL 2 (SHY2/IAA3), an auxin signaling repressor, in the endodermis. We show that DA3 interacts with ARF7 and ARF19, inhibiting their binding to the locus of LATERAL ORGAN BOUNDARY DOMAIN16 (LBD16) to repress its expression in the pericycle. SHY2 also interacts with ARF7 and ARF19 in the endodermis and enhances the DA3 repressive effect on ARF7 and ARF19, thus modulating LBD16 expression in the pericycle. Overall, our findings show that DA3 acts with SHY2, ARF7, and ARF19 to coordinate auxin signaling in the pericycle and endodermis to control LR initiation in Arabidopsis. Lateral roots (LRs) largely determine root system architecture, which plays a fundamental role in water and nutrient uptake and providing anchorage for plants. LRs initiate from pericycle cells adjacent to xylem poles, but only pericycle cells in root pre-branching sites can be specified as LR founder cells.1Justamante M.S. Ibáñez S. Peidró A. Pérez-Pérez J.M. A genome-wide association study identifies new loci involved in wound-induced lateral root formation in Arabidopsis thaliana.Front. Plant Sci. 2019; 10: 311https://doi.org/10.3389/fpls.2019.00311Crossref PubMed Scopus (3) Google Scholar,2Xuan W. Audenaert D. Parizot B. Möller B.K. Njo M.F. De Rybel B. De Rop G. Van Isterdael G. Mähönen A.P. Vanneste S. Beeckman T. Root cap-derived auxin pre-patterns the longitudinal axis of the Arabidopsis root.Curr. Biol. 2015; 25: 1381-1388https://doi.org/10.1016/j.cub.2015.03.046Abstract Full Text Full Text PDF PubMed Scopus (129) Google Scholar,3Ötvös K. Benková E. Spatiotemporal mechanisms of root branching.Curr. Opin. Genet. Dev. 2017; 45: 82-89https://doi.org/10.1016/j.gde.2017.03.010Crossref PubMed Scopus (10) Google Scholar After oriented cell division and expansion, these founder cells develop into LR primordia (LRPs), which then pass through endodermal, cortical, and epidermal cell layers and finally grow into emerged LRs.4Du Y. Scheres B. Lateral root formation and the multiple roles of auxin.J. Exp. Bot. 2018; 69: 155-167https://doi.org/10.1093/jxb/erx223Crossref PubMed Scopus (200) Google Scholar,5Stoeckle D. Thellmann M. Vermeer J.E. Breakout-lateral root emergence in Arabidopsis thaliana.Curr. Opin. Plant Biol. 2018; 41: 67-72https://doi.org/10.1016/j.pbi.2017.09.005Crossref PubMed Scopus (54) Google Scholar,6Lv B. Wei K. Hu K. Tian T. Zhang F. Yu Z. Zhang D. Su Y. Sang Y. Zhang X. Ding Z. MPK14-mediated auxin signaling controls lateral root development via ERF13-regulated very-long-chain fatty acid biosynthesis.Mol. 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LBD16 and LBD18 acting downstream of ARF7 and ARF19 are involved in adventitious root formation in Arabidopsis.BMC Plant Biol. 2019; 19: 46https://doi.org/10.1186/s12870-019-1659-4Crossref PubMed Scopus (60) Google Scholar,10Liu Y. von Wirén N. Integration of nutrient and water availabilities via auxin into the root developmental program.Curr. Opin. Plant Biol. 2022; 65: 102117https://doi.org/10.1016/j.pbi.2021.102117Crossref PubMed Scopus (20) Google Scholar,11Zhang F. Tao W. Sun R. Wang J. Li C. Kong X. Tian H. Ding Z. PRH1 mediates ARF7-LBD dependent auxin signaling to regulate lateral root development in Arabidopsis thaliana.PLoS Genet. 2020; 16: e1008044https://doi.org/10.1371/journal.pgen.1008044Crossref PubMed Scopus (29) Google Scholar Among these factors, AUXIN RESPONSE FACTOR7 (ARF7) and ARF19 play major roles in LR initiation.11Zhang F. Tao W. Sun R. Wang J. Li C. Kong X. Tian H. Ding Z. PRH1 mediates ARF7-LBD dependent auxin signaling to regulate lateral root development in Arabidopsis thaliana.PLoS Genet. 2020; 16: e1008044https://doi.org/10.1371/journal.pgen.1008044Crossref PubMed Scopus (29) Google Scholar,12Chen Q. Liu Y. Maere S. Lee E. Van Isterdael G. Xie Z. Xuan W. Lucas J. Vassileva V. Kitakura S. et al.A coherent transcriptional feed-forward motif model for mediating auxin-sensitive PIN3 expression during lateral root development.Nat. Commun. 2015; 6: 8821https://doi.org/10.1038/ncomms9821Crossref PubMed Scopus (63) Google Scholar Their loss-of-function mutant arf7-1 arf19-1 shows dramatically inhibited LR initiation and suppressed expression of the genes related to LR initiation.13Yuan T.T. Xu H.H. Li J. Lu Y.T. Auxin abolishes SHI-RELATED SEQUENCE5-mediated inhibition of lateral root development in Arabidopsis.New Phytol. 2020; 225: 297-309https://doi.org/10.1111/nph.16115Crossref PubMed Scopus (15) Google Scholar,14Xun Q. Wu Y. Li H. Chang J. Ou Y. He K. 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Kitakura S. et al.A coherent transcriptional feed-forward motif model for mediating auxin-sensitive PIN3 expression during lateral root development.Nat. Commun. 2015; 6: 8821https://doi.org/10.1038/ncomms9821Crossref PubMed Scopus (63) Google Scholar,16Uehara T. Okushima Y. Mimura T. Tasaka M. Fukaki H. Domain II mutations in CRANE/IAA18 suppress lateral root formation and affect shoot development in Arabidopsis thaliana.Plant Cell Physiol. 2008; 49: 1025-1038https://doi.org/10.1093/pcp/pcn079Crossref PubMed Scopus (101) Google Scholar IAA14 inhibits RNA polymerase II progression at the genes regulated by ARF7 and ARF19 by forming a complex with the CDK8 kinase module (CKM) of Mediator.17Ito J. Fukaki H. Onoda M. Li L. Li C. Tasaka M. Furutani M. Auxin-dependent compositional change in mediator in ARF7- and ARF19-mediated transcription.Proc. Natl. Acad. Sci. USA. 2016; 113: 6562-6567https://doi.org/10.1073/pnas.1600739113Crossref PubMed Scopus (70) Google Scholar PHYB also forms a complex with ARF7, ARF19, and IAA14, which increases the stability of IAA14, suppressing the function of ARF7 and ARF19 in activating genes involved in adventitious root formation.18Li Q.Q. Zhang Z. Wang Y.L. Zhong L.Y. Chao Z.F. Gao Y.Q. Han M.L. Xu L. Chao D.Y. Phytochrome B inhibits darkness-induced hypocotyl adventitious root formation by stabilizing IAA14 and suppressing ARF7 and ARF19.Plant J. 2021; 105: 1689-1702https://doi.org/10.1111/tpj.15142Crossref PubMed Scopus (11) Google Scholar Like IAA14, the other two important IAA proteins, IAA15 and CRANE/IAA18, associate with ARF7 and ARF19 and negatively regulate LR formation by suppressing ARF7 and ARF19 activities.19Kim S.H. Bahk S. An J. Hussain S. Nguyen N.T. Do H.L. Kim J.Y. Hong J.C. Chung W.S. 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Our findings provide a so far unknown molecular framework where LR formation is coordinately regulated by DA3 and its interacting proteins in the pericycle and endodermis. In our previous study, we found that DA3 modulated the cell cycle and slightly affected root length40Xu Y. Jin W. Li N. Zhang W. Liu C. Li C. Li Y. UBIQUITIN-SPECIFIC PROTEASE14 interacts with ULTRAVIOLET-B INSENSITIVE4 to regulate endoreduplication and cell and organ growth in Arabidopsis.Plant Cell. 2016; 28: 1200-1214https://doi.org/10.1105/tpc.16.00007Crossref PubMed Scopus (30) Google Scholar (Figures 1A and 1B ). Given that several cell cycle genes have been reported to be involved in LR formation,41Berckmans B. Vassileva V. Schmid S.P.C. Maes S. Parizot B. Naramoto S. Magyar Z. Alvim Kamei C.L. Koncz C. 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USA. 2009; 106: 22528-22533https://doi.org/10.1073/pnas.0906354106Crossref PubMed Scopus (57) Google Scholar we proceeded to examine whether DA3 was also involved in regulation of LR formation, and found that the density of emerged LRs was significantly reduced in the da3-1 loss-of-function mutants40Xu Y. Jin W. Li N. Zhang W. Liu C. Li C. Li Y. UBIQUITIN-SPECIFIC PROTEASE14 interacts with ULTRAVIOLET-B INSENSITIVE4 to regulate endoreduplication and cell and organ growth in Arabidopsis.Plant Cell. 2016; 28: 1200-1214https://doi.org/10.1105/tpc.16.00007Crossref PubMed Scopus (30) Google Scholar compared with wild-type (WT; Col-0) plants (Figures 1A and 1C), indicating that the da3-1 mutation severely disrupts LR emergence. Because the decrease in LR emergence could result from inhibition of LR initiation or suppression of LR emergence,12Chen Q. Liu Y. Maere S. Lee E. Van Isterdael G. Xie Z. Xuan W. Lucas J. Vassileva V. Kitakura S. et al.A coherent transcriptional feed-forward motif model for mediating auxin-sensitive PIN3 expression during lateral root development.Nat. Commun. 2015; 6: 8821https://doi.org/10.1038/ncomms9821Crossref PubMed Scopus (63) Google Scholar,38Swarup K. Benková E. Swarup R. Casimiro I. Péret B. Yang Y. Parry G. Nielsen E. De Smet I. Vanneste S. et al.The auxin influx carrier LAX3 promotes lateral root emergence.Nat. Cell Biol. 2008; 10: 946-954https://doi.org/10.1038/ncb1754Crossref PubMed Scopus (588) Google Scholar we characterized the developmental stages of LRPs in WT and da3-1 plants based on the previously defined eight stages during the developmental progression of LRs.44Malamy J.E. Benfey P.N. Organization and cell differentiation in lateral roots of Arabidopsis thaliana.Development. 1997; 124: 33-44https://doi.org/10.1242/dev.124.1.33Crossref PubMed Google Scholar The densities of LRPs at stages I and II were significantly higher in da3-1 than in WT plants, whereas their densities were comparable at subsequent stages (Figure 1D), implying that a reduction of emerged LRs in da3-1 could result from suppression of LR emergence rather than inhibition of LRP formation. These observations indicate that increased LR initiation and reduced LR emergence could contribute to increased accumulation of early-stage LRPs in da3-1 (Figures 1C and 1D). Because expression of pPLT7:TNI-amiR or pPLT7:TNIintron in transgenic plants led to downregulation of DA3 or disruption of DA3 function in LRPs, respectively,45Majumdar P. Karidas P. Siddiqi I. Nath U. The ubiquitin-specific protease TNI/UBP14 functions in ubiquitin recycling and affects auxin response.Plant Physiol. 2020; 184: 1499-1513https://doi.org/10.1104/pp.20.00689Crossref PubMed Scopus (5) Google Scholar we created the same constructs and the resulting transgenic lines where DA3 expression was downregulated in pPLT7:TNI-amiR (Figure S1A) or disrupting DA3 transcripts were produced in pPLT7:TNIintron (Figure S1B). Similarly, LR emergence was reduced in pPLT7:TNI-amiR or pPLT7:TNIintron plants, but accumulation of LRPs was obviously increased in these plants (Figures S1C–S1E), demonstrating that downregulation of DA3 and disruption of its function show similar phenotypes in LR development. The defective LR phenotype of da3-1 was rescued by the genomic construct gDA3 containing a 7.06-kb DA3 genomic fragment including the 1.72-kb upstream sequence and the entire coding region40Xu Y. Jin W. Li N. Zhang W. Liu C. Li C. Li Y. UBIQUITIN-SPECIFIC PROTEASE14 interacts with ULTRAVIOLET-B INSENSITIVE4 to regulate endoreduplication and cell and organ growth in Arabidopsis.Plant Cell. 2016; 28: 1200-1214https://doi.org/10.1105/tpc.16.00007Crossref PubMed Scopus (30) Google Scholar (Figures S1F–S1I). These observations support the hypothesis that DA3 affects LR development. We examined an established gDA3-GFP transgenic plant40Xu Y. Jin W. Li N. Zhang W. Liu C. Li C. Li Y. UBIQUITIN-SPECIFIC PROTEASE14 interacts with ULTRAVIOLET-B INSENSITIVE4 to regulate endoreduplication and cell and organ growth in Arabidopsis.Plant Cell. 2016; 28: 1200-1214https://doi.org/10.1105/tpc.16.00007Crossref PubMed Scopus (30) Google Scholar to analyze the expression pattern of DA3. The green fluorescent protein (GFP) signals were detectable in all root tissues, including the stele, endodermis, cortex, and epidermis, as well as different cell layers of developing LRs (Figure 1E). DA3-GFP signals were continuously detectable in LRPs from stage I to emergence of LRs (Figure 1E), which suggests that DA3 contributes to LR initiation and emergence via its expression in different root tissues. To test whether DA3 functions in mediating LR initiation via specific cell layers in roots, we examined LR phenotypes of da3-1 plants expressing DA3-GFP under the control of different cell-layer-specific promoters. The pericycle-expressed DA3-GFP under control of the GATA23 promoter partially rescued the defective LR phenotype of da3-1 (Figures S2A–S2D). Similarly, the endodermis-expressed DA3-GFP under control of the SCARECROW (SCR) promoter also partially rescued the da3-1 LR phenotype, although its complementary effect was weaker than that exhibited by the GATA23 promoter (Figures S2A–S2D). In contrast, the stele-expressed DA3-GFP driven by the CRE1 promoter failed to rescue the da3-1 LR phenotype (Figures S2A–S2D). We found that the DA3-GFP signal was barely expressed in pericycle cells versus other stele cells in pCRE1:DA3-GFP da3-1 roots (Figure S2A), suggesting that tissue-specific expression of DA3 in pericycle cells rather than other stele cells is important for DA3 function in LR initiation. These results substantiate that DA3 mainly functions in the pericycle and endodermis to regulate LR initiation, which is consistent with a previous study showing control of LR initiation by the pericycle and the neighboring endodermis.32Vermeer J.E.M. von Wangenheim D. Barberon M. Lee Y. Stelzer E.H.K. Maizel A. Geldner N. A spatial accommodation by neighboring cells is required for organ initiation in Arabidopsis.Science. 2014; 343: 178-183https://doi.org/10.1126/science.1245871Crossref PubMed Scopus (199) Google Scholar Because auxin is a central plant hormone for LR development and controls almost the whole proc" @default.
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