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• W2787678085 abstract "•Prohibitin proteins act as common stem cell regulators in mammals and plants•ERF115, ERF114, and ERF109 are ROS-responsive factors that maintain root SCN identity•PHB3 restricts the spatial expression patterns of ERF115, ERF114, and ERF109 in roots The root stem cell niche, which is composed of four mitotically inactive quiescent center (QC) cells and the surrounding actively divided stem cells in Arabidopsis, is critical for growth and root development. Here, we demonstrate that the Arabidopsis prohibitin protein PHB3 is required for the maintenance of root stem cell niche identity by both inhibiting proliferative processes in the QC and stimulating cell division in the proximal meristem (PM). PHB3 coordinates cell division and differentiation in the root apical meristem by restricting the spatial expression of ethylene response factor (ERF) transcription factors 115, 114, and 109. ERF115, ERF114, and ERF109 mediate ROS signaling, in a PLT-independent manner, to control root stem cell niche maintenance and root growth through phytosulfokine (PSK) peptide hormones in Arabidopsis. The root stem cell niche, which is composed of four mitotically inactive quiescent center (QC) cells and the surrounding actively divided stem cells in Arabidopsis, is critical for growth and root development. Here, we demonstrate that the Arabidopsis prohibitin protein PHB3 is required for the maintenance of root stem cell niche identity by both inhibiting proliferative processes in the QC and stimulating cell division in the proximal meristem (PM). PHB3 coordinates cell division and differentiation in the root apical meristem by restricting the spatial expression of ethylene response factor (ERF) transcription factors 115, 114, and 109. ERF115, ERF114, and ERF109 mediate ROS signaling, in a PLT-independent manner, to control root stem cell niche maintenance and root growth through phytosulfokine (PSK) peptide hormones in Arabidopsis. The development of the root relies on the continuous provision of new cells by the stem cell niche (SCN), which is located within the root apical meristem (RAM) (Aichinger et al., 2012Aichinger E. Kornet N. Friedrich T. Laux T. Plant stem cell niches.Annu. Rev. Plant Biol. 2012; 63: 615-636Crossref PubMed Scopus (229) Google Scholar, Yang et al., 2015Yang S. Li C. Zhao L. Gao S. Lu J. Zhao M. Chen C.Y. Liu X. Luo M. Cui Y. et al.The Arabidopsis SWI2/SNF2 chromatin remodeling ATPase BRAHMA targets directly to PINs and is required for root stem cell niche maintenance.Plant Cell. 2015; 27: 1670-1680Crossref PubMed Scopus (66) Google Scholar). In RAM, coordinated balance between cell division and differentiation determines meristem size. In the Arabidopsis thaliana root, a small group of mitotically hypoactive cells, referred to as the quiescent center (QC), separates the population of stem cells into two distinct domains and prevents any differentiation of the surrounding stem cells (van den Berg et al., 1997van den Berg C. Willemsen V. Hendriks G. Weisbeek P. Scheres B. Short-range control of cell differentiation in the Arabidopsis root meristem.Nature. 1997; 390: 287-289Crossref PubMed Scopus (525) Google Scholar, Heyman et al., 2014Heyman J. Kumpf R.P. De Veylder L. A quiescent path to plant longevity.Trends Cell Biol. 2014; 24: 443-448Abstract Full Text Full Text PDF PubMed Scopus (50) Google Scholar). Maintenance of the root SCN in A. thaliana requires the activity of the homeobox transcription factor WOX5, which is specifically transcribed in the QC and maintains the identity of both the QC and the distal stem cells (DSCs) (Sarkar et al., 2007Sarkar A.K. Luijten M. Miyashima S. Lenhard M. Hashimoto T. Nakajima K. Scheres B. Heidstra R. Laux T. Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers.Nature. 2007; 446: 811-814Crossref PubMed Scopus (753) Google Scholar, Kong et al., 2015Kong X. Lu S. Tian H. Ding Z. WOX5 is shining in the root stem cell niche.Trends Plant Sci. 2015; 20: 601-603Abstract Full Text Full Text PDF PubMed Scopus (35) Google Scholar). WOX5 inhibits cell division in the QC by suppressing CYCD3;3, and it moves from the QC into the DSCs (Forzani et al., 2014Forzani C. Aichinger E. Sornay E. Willemsen V. Laux T. Dewitte W. Murray J.A. WOX5 suppresses CYCLIN D activity to establish quiescence at the center of the root stem cell niche.Curr. Biol. 2014; 24: 1939-1944Abstract Full Text Full Text PDF PubMed Scopus (128) Google Scholar) where it represses the differentiation factor CDF4 to inhibit root DSC differentiation via recruiting TPL/TPR co-repressors and the histone deacetylase HDA19 (Pi et al., 2015Pi L. Aichinger E. van der Graaff E. Llavata-Peris C.I. Weijers D. Hennig L. Groot E. Laux T. Organizer-derived WOX5 signal maintains root Columella stem cells through chromatin-cediated repression of CDF4 expression.Dev. Cell. 2015; 33: 576-588Abstract Full Text Full Text PDF PubMed Scopus (212) Google Scholar). Auxin signaling and REPRESSOR OF WUSCHEL1 (ROW1) regulate DSC differentiation and proximal meristem (PM) differentiation by acting on WOX5, respectively (Ding and Friml, 2010Ding Z. Friml J. Auxin regulates distal stem cell differentiation in Arabidopsis roots.Proc. Natl. Acad. Sci. USA. 2010; 107: 12046-12051Crossref PubMed Scopus (261) Google Scholar, Zhang et al., 2015Zhang Y. Jiao Y. Liu Z. Zhu Y.X. ROW1 maintains quiescent centre identity by confining WOX5 expression to specific cells.Nat. Commun. 2015; 6: 6003Crossref PubMed Scopus (69) Google Scholar). A number of root SCN-defining factors have been identified; these include the two AP2-type transcription factors PLT1 and PLT2, as well as the GRAS transcription factors SCR/SHR (Aichinger et al., 2012Aichinger E. Kornet N. Friedrich T. Laux T. Plant stem cell niches.Annu. Rev. Plant Biol. 2012; 63: 615-636Crossref PubMed Scopus (229) Google Scholar). The loss of either PLT1/PLT2 or SHR/SCR disrupts the maintenance of root SCN identity, with mutants displaying a higher frequency of cell division in the QC and a higher frequency of stem cell differentiation (Nakajima et al., 2001Nakajima K. Sena G. Nawy T. Benfey P.N. Intercellular movement of the putative transcription factor SHR in root patterning.Nature. 2001; 413: 307-311Crossref PubMed Scopus (631) Google Scholar, Sabatini et al., 2003Sabatini S. Heidstra R. Wildwater M. Scheres B. SCARECROW is involved in positioning the stem cell niche in the Arabidopsis root meristem.Genes Dev. 2003; 17: 354-358Crossref PubMed Scopus (558) Google Scholar, Aida et al., 2004Aida M. Beis D. Heidstra R. Willemsen V. Blilou I. Galinha C. Nussaume L. Noh Y.S. Amasino R. Scheres B. The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche.Cell. 2004; 119: 109-120Abstract Full Text Full Text PDF PubMed Scopus (843) Google Scholar, Gallagher et al., 2004Gallagher K.L. Paquette A.J. Nakajima K. Benfey P.N. Mechanisms regulating SHORT-ROOT intercellular movement.Curr. Biol. 2004; 14: 1847-1851Abstract Full Text Full Text PDF PubMed Scopus (165) Google Scholar, Galinha et al., 2007Galinha C. Hofhuis H. Luijten M. Willemsen V. Blilou I. Heidstra R. Scheres B. PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development.Nature. 2007; 449: 1053-1057Crossref PubMed Scopus (594) Google Scholar, Yu et al., 2010Yu N.I. Lee S.A. Lee M.H. Heo J.O. Chang K.S. Lim J. Characterization of SHORT-ROOT function in the Arabidopsis root vascular system.Mol. Cells. 2010; 30: 113-119Crossref PubMed Scopus (27) Google Scholar). SCR has been found to either physically interact with RETINOBLASTOMA-RELATED (RBR) (Cruz-Ramírez et al., 2013Cruz-Ramírez A. Díaz-Triviño S. Wachsman G. Du Y. Arteága-Vázquez M. Zhang H. Benjamins R. Blilou I. Neef A.B. Chandler V. Scheres B. A SCARECROW-RETINOBLASTOMA protein network controls protective quiescence in the Arabidopsis root stem cell organizer.PLoS Biol. 2013; 11: e1001724Crossref PubMed Scopus (111) Google Scholar) or to repress the cytokinin-response transcription factor ARR1 (Moubayidin et al., 2013Moubayidin L. Di Mambro R. Sozzani R. Pacifici E. Salvi E. Terpstra I. Bao D. van Dijken A. Dello Ioio R. Perilli S. et al.Spatial coordination between stem cell activity and cell differentiation in the root meristem.Dev. Cell. 2013; 26: 405-415Abstract Full Text Full Text PDF PubMed Scopus (96) Google Scholar). Other regulators, such as the zinc-finger transcription factors NTT, WIP4, WIP5, and ERF115, also participate in the process of maintaining root SCN identity; NTT, WIP4, and WIP5 all mediate auxin signaling (and thus control root DSC fate) (Crawford et al., 2015Crawford B.C. Sewell J. Golembeski G. Roshan C. Long J.A. Yanofsky M.F. Plant development. Genetic control of distal stem cell fate within root and embryonic meristems.Science. 2015; 347: 655-659Crossref PubMed Scopus (64) Google Scholar), while ERF115 acts as a transcriptional activator of the phytosulfokine PSK5 peptide hormone to function as a rate-limiting factor of QC cell division (Heyman et al., 2013Heyman J. Cools T. Vandenbussche F. Heyndrickx K.S. Van Leene J. Vercauteren I. Vanderauwera S. Vandepoele K. De Jaeger G. Van Der Straeten D. De Veylder L. ERF115 controls root quiescent center cell division and stem cell replenishment.Science. 2013; 342: 860-863Crossref PubMed Scopus (200) Google Scholar). Reactive oxygen species (ROS) are a by-product of aerobic metabolism (Moller, 2001Moller I.M. Plant mitochondria and oxidative stress: Electron transport, NADPH turnover, and metabolism of reactive oxygen species.Annu. Rev. Plant Physiol. Plant Mol. Biol. 2001; 52: 561-591Crossref PubMed Scopus (1321) Google Scholar). Imposing a brake on the over-production of ROS is important for the control of cell division and cell differentiation (Wang et al., 2013Wang K. Zhang T. Dong Q. Nice E.C. Huang C. Wei Y. Redox homeostasis: the linchpin in stem cell self-renewal and differentiation.Cell Death Dis. 2013; 4: e537Crossref PubMed Scopus (201) Google Scholar). Redox homeostasis is essential for the continued renewal and differentiation of animal stem cells, which are sensitive to ROS (Wang et al., 2013Wang K. Zhang T. Dong Q. Nice E.C. Huang C. Wei Y. Redox homeostasis: the linchpin in stem cell self-renewal and differentiation.Cell Death Dis. 2013; 4: e537Crossref PubMed Scopus (201) Google Scholar, Zhou et al., 2014Zhou D. Shao L. Spitz D.R. Reactive oxygen species in normal and tumor stem cells.Adv. Cancer Res. 2014; 122: 1-67Crossref PubMed Scopus (235) Google Scholar). However, our knowledge about the role of ROS function in plant stem cell maintenance is quite limited. In maize, a highly oxidized status is important for maintaining a low level of mitotic activity in the QC (Jiang et al., 2003Jiang K. Meng Y.L. Feldman L.J. Quiescent center formation in maize roots is associated with an auxin-regulated oxidizing environment.Development. 2003; 130: 1429-1438Crossref PubMed Scopus (162) Google Scholar). More recently, Yu et al., 2016Yu Q. Tian H. Yue K. Liu J. Zhang B. Li X. Ding Z. A P-Loop NTPase regulates quiescent center cell division and distal stem cell identity through the regulation of ROS homeostasis in Arabidopsis root.PLoS Genet. 2016; 12: e1006175Crossref PubMed Scopus (63) Google Scholar reported that loss of APP1, which shows a reduction in ROS level, causes terminal differentiation of DSC and increased QC cell division. In rml1 mutants, the post-embryonic root meristem does not form because of the defects of glutathione (GSH) biosynthesis and depletion of an important antioxidant GSH (Vernoux et al., 2000Vernoux T. Wilson R.C. Seeley K.A. Reichheld J.P. Muroy S. Brown S. Maughan S.C. Cobbett C.S. Van Montagu M. Inzé D. et al.The ROOT MERISTEMLESS1/CADMIUM SENSITIVE2 gene defines a glutathione-dependent pathway involved in initiation and maintenance of cell division during postembryonic root development.Plant Cell. 2000; 12: 97-110Crossref PubMed Google Scholar). The basic helix-loop-helix transcriptional factor UPB1 controls the transition from cell proliferation to differentiation and, thus, the root meristem size through the regulation of ROS gradient in the root meristem (Tsukagoshi et al., 2010Tsukagoshi H. Busch W. Benfey P.N. Transcriptional regulation of ROS controls transition from proliferation to differentiation in the root.Cell. 2010; 143: 606-616Abstract Full Text Full Text PDF PubMed Scopus (712) Google Scholar). All these results highlighted the importance of ROS in the root stem cell maintenance in planta. However, the nature of the downstream signaling of ROS involved in the maintenance of QC identity and stem cell activity in planta is still far from clear at the moment. Prohibitins (PHBs) were identified as potential tumor suppressors with anti-proliferative activity through interacting and inhibiting members of the E2F family of transcription factors (Wang et al., 1999Wang S. Nath N. Adlam M. Chellappan S. Prohibitin, a potential tumor suppressor, interacts with RB and regulates E2F function.Oncogene. 1999; 18: 3501-3510Crossref PubMed Scopus (205) Google Scholar). All PHB members shared conserved motifs throughout prokaryotic and eukaryotic evolution, inferring that PHB might present in a common unicellular ancestor and may have conserved functions (Ahn et al., 2006Ahn C.S. Lee J.H. Reum Hwang A. Kim W.T. Pai H.S. Prohibitin is involved in mitochondrial biogenesis in plants.Plant J. 2006; 46: 658-667Crossref PubMed Scopus (92) Google Scholar, Artal-Sanz and Tavernarakis, 2009Artal-Sanz M. Tavernarakis N. Prohibitin and mitochondrial biology.Trends Endocrinol. Metab. 2009; 20: 394-401Abstract Full Text Full Text PDF PubMed Scopus (215) Google Scholar). It was also recently reported that PHB2, an inner mitochondrial membrane protein that is important for mitochondrial homeostasis, is critically required for mitophagic responses in C. elegans (Wei et al., 2017Wei Y. Chiang W.C. Sumpter Jr., R. Mishra P. Levine B. Prohibitin 2 is an inner mitochondrial membrane mitophagy receptor.Cell. 2017; 168: 224-238.e10Abstract Full Text Full Text PDF PubMed Scopus (436) Google Scholar). The Arabidopsis genome has seven conserved PHB genes (Van Aken et al., 2007Van Aken O. Pecenková T. van de Cotte B. De Rycke R. Eeckhout D. Fromm H. De Jaeger G. Witters E. Beemster G.T. Inzé D. Van Breusegem F. Mitochondrial type-I prohibitins of Arabidopsis thaliana are required for supporting proficient meristem development.Plant J. 2007; 52: 850-864Crossref PubMed Scopus (106) Google Scholar). Although PHB3 has been linked to cell division control in the root tip (Van Aken et al., 2007Van Aken O. Pecenková T. van de Cotte B. De Rycke R. Eeckhout D. Fromm H. De Jaeger G. Witters E. Beemster G.T. Inzé D. Van Breusegem F. Mitochondrial type-I prohibitins of Arabidopsis thaliana are required for supporting proficient meristem development.Plant J. 2007; 52: 850-864Crossref PubMed Scopus (106) Google Scholar, Wang et al., 2010Wang Y. Ries A. Wu K. Yang A. Crawford N.M. The Arabidopsis prohibitin gene PHB3 functions in nitric oxide-mediated responses and in hydrogen peroxide-induced nitric oxide accumulation.Plant Cell. 2010; 22: 249-259Crossref PubMed Scopus (90) Google Scholar), the molecular mechanisms by which PHB3 controls root growth remain largely unknown. Here it is shown that mutations of PHB3 led to defective root SCN maintenance. PHB3 coordinates cell division and differentiation in RAM through restricting the spatial expression of ethylene response factor (ERF) transcription factors 115, 114, and 109. The phb3 mutant has been shown to display a short-root phenotype (Van Aken et al., 2007Van Aken O. Pecenková T. van de Cotte B. De Rycke R. Eeckhout D. Fromm H. De Jaeger G. Witters E. Beemster G.T. Inzé D. Van Breusegem F. Mitochondrial type-I prohibitins of Arabidopsis thaliana are required for supporting proficient meristem development.Plant J. 2007; 52: 850-864Crossref PubMed Scopus (106) Google Scholar). Consistent with the reduced root meristem size (Van Aken et al., 2007Van Aken O. Pecenková T. van de Cotte B. De Rycke R. Eeckhout D. Fromm H. De Jaeger G. Witters E. Beemster G.T. Inzé D. Van Breusegem F. Mitochondrial type-I prohibitins of Arabidopsis thaliana are required for supporting proficient meristem development.Plant J. 2007; 52: 850-864Crossref PubMed Scopus (106) Google Scholar), we observed that the abundance of RBR transcript, which encodes a retinoblastoma protein to inhibit cell cycle (Cruz-Ramírez et al., 2013Cruz-Ramírez A. Díaz-Triviño S. Wachsman G. Du Y. Arteága-Vázquez M. Zhang H. Benjamins R. Blilou I. Neef A.B. Chandler V. Scheres B. A SCARECROW-RETINOBLASTOMA protein network controls protective quiescence in the Arabidopsis root stem cell organizer.PLoS Biol. 2013; 11: e1001724Crossref PubMed Scopus (111) Google Scholar), was much higher in the phb3 mutant root (Figures S1A and S1D). On the contrary, the expressions of KNOLLE and CYCB1;1, two cell cycle markers, were both downregulated in phb3 (Figures S1B, S1C, S1E, and S1F). All these results indicate that PHB3 is required for maintaining the cell division activity of the root meristem. The observation that PHB3 is crucial for maintaining root meristem size prompted us to investigate its possible effects on the cellular organization of the QC and surrounding stem cells. From Lugol staining, the phb3 mutant (salk_020707) enhanced root DSC differentiation and increased mitotic activity in root QC (Figures 1A and 1B ). Consistently, PHB3 overexpression lines (PHB3 OE) displayed additional cell layers in its root DSCs (Figures 1A and 1C). In the wild-type (WT) root, QC cells were maintained at the G1/S cell cycle checkpoint and divided infrequently (∼5%) (Figures 1A and 1B). However, the phb3 mutant seedlings showed a highly increased QC cell division (>80%) (Figures 1A and 1B). Furthermore, the differentiation in the root DSC in phb3 was almost complete (>90%), in contrast to the low proportion in the WT root DSCs (∼5%) (Figure 1C). This phenotype was confirmed through analysis of another phb3 mutant allele (salk_022842) (Figures S2A and S2B). The F1 hybrid of these two alleles had a similar root SCN-defective phenotype as that in phb3 (Figure S2B). Furthermore, both the QC-specific transcription factor WOX5 (Figure 1D) and the QC-specific marker QC184 (Figure 1E) were strongly downregulated in the phb3 mutant. In addition, the root SCN-defining transcription factors, such as PLT1, PLT2, and SCR, were all strongly downregulated in phb3 (Figure 2), which is consistent with the root-defective phenotypes. However, the transcription of SHR was not affected in phb3 (Figures 2G–2I). Only PLT1 was strongly downregulated in PHB3 OE lines (Figure S3). These results indicate that PHB3 is essential to maintain root QC and DSC identity.Figure 2PLT1, PTL2, and SCR Transcription Is Reduced in the phb3 MutantShow full caption(A and C) pPLT1::PLT1-YFP (A) and pPLT2::PLT2-YFP (C) transcription in the 5-day-old seedling roots. Scale bars, 50 μm.(B and D) Quantification of the pPLT1::PLT1-YFP (B) and pPLT2::PLT2-YFP (D) fluorescence intensity in the 5-day-old WT and phb3 mutant seedlings. The data are shown as mean ± SD (n = 15) with one-way ANOVA and Tukey’s test. Different letters indicate significant differences (p < 0.01).(E and G) pSCR::SCR-GFP (E) and pSHR::SHR-GFP (G) transcription in the 5-day-old seedling roots. Scale bars, 50 μm.(F and H) Quantification of the pSCR::SCR-GFP (F) and pSHR::SHR-GFP (H) fluorescence intensity in the 5-day-old WT and phb3 mutant seedlings. The data are shown as mean ± SD (n = 15) with one-way ANOVA and Tukey’s test. Different letters indicate significant differences (p < 0.01).(I) Abundance of PLT1, PTL2, SCR, and SHR transcript in 5-day-old WT and phb3 mutant roots. At least 100 seedlings were examined for each biological repeat. Error bars represent SE from triplicate experiments. Asterisks indicate means differing significantly from the WT (p < 0.01).See also Figure S3.View Large Image Figure ViewerDownload Hi-res image Download (PPT) (A and C) pPLT1::PLT1-YFP (A) and pPLT2::PLT2-YFP (C) transcription in the 5-day-old seedling roots. Scale bars, 50 μm. (B and D) Quantification of the pPLT1::PLT1-YFP (B) and pPLT2::PLT2-YFP (D) fluorescence intensity in the 5-day-old WT and phb3 mutant seedlings. The data are shown as mean ± SD (n = 15) with one-way ANOVA and Tukey’s test. Different letters indicate significant differences (p < 0.01). (E and G) pSCR::SCR-GFP (E) and pSHR::SHR-GFP (G) transcription in the 5-day-old seedling roots. Scale bars, 50 μm. (F and H) Quantification of the pSCR::SCR-GFP (F) and pSHR::SHR-GFP (H) fluorescence intensity in the 5-day-old WT and phb3 mutant seedlings. The data are shown as mean ± SD (n = 15) with one-way ANOVA and Tukey’s test. Different letters indicate significant differences (p < 0.01). (I) Abundance of PLT1, PTL2, SCR, and SHR transcript in 5-day-old WT and phb3 mutant roots. At least 100 seedlings were examined for each biological repeat. Error bars represent SE from triplicate experiments. Asterisks indicate means differing significantly from the WT (p < 0.01). See also Figure S3. We next examined if the mitochodria-localized PHB3 (Van Aken et al., 2007Van Aken O. Pecenková T. van de Cotte B. De Rycke R. Eeckhout D. Fromm H. De Jaeger G. Witters E. Beemster G.T. Inzé D. Van Breusegem F. Mitochondrial type-I prohibitins of Arabidopsis thaliana are required for supporting proficient meristem development.Plant J. 2007; 52: 850-864Crossref PubMed Scopus (106) Google Scholar) is involved in ROS homeostasis regulation and, thus, root development. Compared to WT root tips, both peroxide (H2O2) and superoxide (O2−) were overaccumulated in the phb3 mutant root meristem (Figures 3A and 3B ). When probed with Mito-cpYFP, a mitochondrial matrix-targeted O2− indicator (He et al., 2012He J. Duan Y. Hua D. Fan G. Wang L. Liu Y. Chen Z. Han L. Qu L.J. Gong Z. DEXH box RNA helicase-mediated mitochondrial reactive oxygen species production in Arabidopsis mediates crosstalk between abscisic acid and auxin signaling.Plant Cell. 2012; 24: 1815-1833Crossref PubMed Scopus (217) Google Scholar), a greater signal was obtained from the phb3 mutant roots than from the WT controls (Figure S4A). The abundance of AOX1a, AOX1c, NDA1, NDB2, NDB3, and NDB4 transcript was several folds greater in phb3 than in the WT control (Figure 3C; Data S1). The increased NADH dehydrogenase activity was also consistent with the higher ROS levels in phb3 (Figure 3D). The results indicated that PHB3 is involved in the regulation of ROS homeostasis. To determine whether the overaccumulated ROS contribute to the root-defective phenotypes in phb3, WT and the phb3 mutant seedlings were treated with diphenyleneiodonium (DPI, an inhibitor of both NADPH oxidase and complex I), which caused reduced ROS accumulation in both WT and phb3 mutant roots (Figure S4B). Though the DPI treatment caused a significant promotion of cell division in the QC and root DSC differentiation in WT seedlings, the same treatment strongly rescued the promoted QC cell division and root DSC differentiation in phb3 (Figure 3E). Consistently, DPI treatment also partially rescued the downregulated QC-specific marker (QC184 and WOX5) expression (Figures 3F and 3G) and SCN-defining transcription factor (PLT1 and PLT2) expression (Figures 3H–3J) in phb3 mutant. In addition, a low concentration (0.1 μM) of DPI treatment, which had no discernible inhibitory effect on WT seedling roots, promoted root growth in phb3 (Figure 3K). A higher dosage of DPI treatment inhibited root growth in phb3 but to a much less extent than that in WT seedlings (Figure 3K). To address how PHB3 regulated ROS signaling affects root development, RNA sequencing (RNA-seq) analysis was applied to compare the root transcriptomes of WT and the phb3 mutant. A total of 1,445 genes was found to be upregulated and 1,479 downregulated in the phb3 mutant roots compared to the WT control (Figure S5A; Data S1). Many of these genes were classified, using gene ontology (GO) analysis, as antioxidant or catalytic protein-encoding genes (Figure S5B), consistent with the changed ROS homeostasis in phb3 (Figure 3). Another set of differentially transcribed genes were transcription factor-encoding genes; among those that were significantly upregulated in the phb3 mutant were the AP2/ERF factors (Figure S5C). qRT-PCR analysis of four genes belonging to catalytic activity and another four ERF genes belonging to transcription factor activity verified the RNA-seq data (Figure S5D). Among the upregulated ERFs in phb3, ERF109, ERF114, and ERF115 were highly upregulated in phb3, which were confirmed by qRT-PCR analysis (Figure 4A). The upregulated ERF109, ERF114, and ERF115 expression was further confirmed by the highly increased expression of pERF109::GUS, pERF114::GUS, and pERF115::GUS in the phb3 mutant roots (Figures 4B–4D). DPI treatment partially rescued the upregulated ERF109, ERF114, and ERF115 expression in phb3 mutant (Figures 4E–4G). Consistently, similar to the phb3 mutant, ERF109 OE (a transgenic plant overexpressing ERF109) (Cai et al., 2014Cai X.T. Xu P. Zhao P.X. Liu R. Yu L.H. Xiang C.B. Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation.Nat. Commun. 2014; 5: 5833Crossref PubMed Scopus (175) Google Scholar), ERF114 OE, and ERF115 OE (Heyman et al., 2013Heyman J. Cools T. Vandenbussche F. Heyndrickx K.S. Van Leene J. Vercauteren I. Vanderauwera S. Vandepoele K. De Jaeger G. Van Der Straeten D. De Veylder L. ERF115 controls root quiescent center cell division and stem cell replenishment.Science. 2013; 342: 860-863Crossref PubMed Scopus (200) Google Scholar) showed a highly promoted QC cell division (Figure 4H). Furthermore, ERF114 OE and ERF115 OE also displayed a higher rate of root DSC differentiation, which was observed in phb3 (Figure 4H). In addition, similar to ERF109 OE and ERF115 OE, ERF114 OE also showed short-root phenotypes (Cai et al., 2014Cai X.T. Xu P. Zhao P.X. Liu R. Yu L.H. Xiang C.B. Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation.Nat. Commun. 2014; 5: 5833Crossref PubMed Scopus (175) Google Scholar, Heyman et al., 2016Heyman J. Cools T. Canher B. Shavialenka S. Traas J. Vercauteren I. Van den Daele H. Persiau G. De Jaeger G. Sugimoto K. De Veylder L. The heterodimeric transcription factor complex ERF115-PAT1 grants regeneration competence.Nat. Plants. 2016; 2: 16165Crossref PubMed Scopus (75) Google Scholar; Figure S6), which were also consistent with the short-root phenotype in the phb3 mutant. We further examined the root SCN phenotype of erf109 mutant and the dominant-negative constructs ERF114SRDX and ERF115SRDX. The results showed that erf109, ERF114SRDX, and ERF115SRDX displayed normal QC identity (Figure 4I), while ERF115SRDX still displayed a higher rate of root DSC differentiation (Figure 4I). To confirm if the upregulated ERF expression contributes to the root defects in phb3, we introduced the erf109 allele and the dominant-negative ERF114SRDX and ERF115SRDX genes into the phb3 mutant, and we examined the root phenotypes. The results showed that disruption of ERF115 partially rescued the promoted QC cell division and short-root phenotypes in phb3 (Figures 4I–4K), while disruption of ERF114 in the ERF114SRDX line partially rescued both root SCN defects and the short-root phenotype in phb3 (Figures 4I–4K). However, the erf109 allele only partially rescued the short-root phenotype in phb3 (Figures 4I–4K). These results indicate that ERF109, ERF114, and ERF115, which are all highly upregulated in phb3, have both redundant and differential roles in the regulation of root SCN identity and root growth. As mentioned above, the phb3 mutant accumulated more ROS, and ERF109, ERF114, and ERF115 were all strongly upregulated in phb3. To address if ERF109, ERF114, and ERF115 are ROS-responsive genes, we examined the expression profiles of ERF109, ERF114, and ERF115 in response to H2O2. The results showed that ERF109, ERF114, and ERF115 are highly induced by H2O2, which was shown by both qRT-PCR analysis and GUS-staining analysis using the transcriptional reporter lines (pERF109::GUS, pERF114::GUS, and pERF115::GUS) (Figures 5A–5D). In the presence of 500 μM H2O2 treatment, we could observe a strong induction of ERF109, ERF114, and ERF115 within 30 min (Figure 5A). Previous study showed that cell death can induce ERF115 activity (Heyman et al., 2013Heyman J. Cools T. Vandenbussche F. Heyndrickx K.S. Van Leene J. Vercauteren I. Vanderauwera S. Vandepoele K. De Jaeger G. Van Der Straeten D. De Veylder L. ERF115 controls root quiescent center cell division and stem cell replenishment.Science. 2013; 342: 860-863Crossref PubMed Scopus (200) Google Scholar), and we used the propidium iodide (PI) staining to detect cell death after different concentrations (0, 50, 100, 250, 500, and 1,000 μM) of H2O2 treatment for 2 hr. Lower concentrations of H2O2 did not induce a significant cell death in root PM under our experimental conditions (Figure S7), however, it could clearly induce the expression of ERF109, ERF114, and ERF115 (Figures 5A–5D). These results suggest that H2O2-induced ERF109, ERF114, and ERF115 expression are independent of cell death signaling. To determine whether ERF109, ERF114, and ERF115 were involved in ROS-regulated root SCN identity, ERF114SRDX, ERF115SRDX, and erf109 mutant seedlings were analyzed under H2O2 treatment. The H2O2 treatment caused a significant promotion of cell division in the QC and root DSC differentiation in Col roots (Figure 5E), but this stimula" @default.
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• W2787678085 title "PHB3 Maintains Root Stem Cell Niche Identity through ROS-Responsive AP2/ERF Transcription Factors in Arabidopsis" @default.
• W2787678085 cites W1505270625 @default.
• W2787678085 cites W1663820305 @default.
• W2787678085 cites W1976122920 @default.
• W2787678085 cites W1981797401 @default.
• W2787678085 cites W1989619407 @default.
• W2787678085 cites W1992162879 @default.
• W2787678085 cites W1993773504 @default.
• W2787678085 cites W2002426440 @default.
• W2787678085 cites W2004838336 @default.
• W2787678085 cites W2012526077 @default.
• W2787678085 cites W2017140905 @default.
• W2787678085 cites W2019092505 @default.
• W2787678085 cites W2022785470 @default.
• W2787678085 cites W2024233959 @default.
• W2787678085 cites W2024343928 @default.
• W2787678085 cites W2032152188 @default.
• W2787678085 cites W2032265315 @default.
• W2787678085 cites W2033580760 @default.
• W2787678085 cites W2050102962 @default.
• W2787678085 cites W2056996163 @default.
• W2787678085 cites W2059448855 @default.
• W2787678085 cites W2066098222 @default.
• W2787678085 cites W2073640257 @default.
• W2787678085 cites W2077518395 @default.
• W2787678085 cites W2100541085 @default.
• W2787678085 cites W2102338029 @default.
• W2787678085 cites W2103744954 @default.
• W2787678085 cites W2109324504 @default.
• W2787678085 cites W2110711379 @default.
• W2787678085 cites W2112289953 @default.
• W2787678085 cites W2119931973 @default.
• W2787678085 cites W2129108452 @default.
• W2787678085 cites W2135087570 @default.
• W2787678085 cites W2138684277 @default.
• W2787678085 cites W214449776 @default.
• W2787678085 cites W2146516445 @default.
• W2787678085 cites W2151970414 @default.
• W2787678085 cites W2152294605 @default.
• W2787678085 cites W2161558261 @default.
• W2787678085 cites W2162289402 @default.
• W2787678085 cites W2169794803 @default.
• W2787678085 cites W2305661414 @default.
• W2787678085 cites W2346009861 @default.
• W2787678085 cites W2513153996 @default.
• W2787678085 cites W2514374159 @default.
• W2787678085 cites W2544684770 @default.
• W2787678085 cites W2560487446 @default.
• W2787678085 cites W2562998505 @default.
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