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To accept how and whether stem-cell-ubiquitous genes accord to corpuscle identity, maintenance, and/or division, we performed gene announcement assay of the arbor beef in the Arabidopsis root, as this offers a acquiescent arrangement accustomed its 3-dimensional adorable agreement and banausic advice encoded forth its longitudinal axis. To this end, seven basis arbor corpuscle markers (Fig. 1a), as able-bodied as a non-stem corpuscle ascendancy (i.e., a citizenry of beef from the basis meristem excluding best of the arbor cells), were acclimated to analyze arbor cell-enriched genes, and amid those, stem-cell-ubiquitous and stem-cell-specific genes, as it has been apparent that there is a alternation amid announcement levels and functionality in specific corpuscle types1,14 (Supplementary Fig. 1, see Methods). Notably, we begin that the announcement profiles of our markers calm with accepted arbor corpuscle genes accede with their accepted announcement domains, acknowledging that our transcriptional profiles are specific to anniversary arbor corpuscle citizenry (Supplementary Fig. 1). To admeasurement transcriptional differences amid the arbor beef and the non-stem cells, we abutting performed a Arch Basic Assay (PCA). Looking at the top three arch apparatus (50.6% of the aberration in the data), the PCA shows that the non-stem corpuscle samples (red) are abroad from all of the arbor corpuscle populations, suggesting that the arbor beef accept a altered transcriptional signature than the non-stem beef (Fig. 1b). Accordingly, back we performed cogwheel announcement assay on these data, we begin that 9266 (28% of genes) are decidedly accomplished (q < 0.06 and fold-change > 2) in at atomic one arbor corpuscle citizenry compared to the non-stem beef and advised these genes the arbor cell-enriched genes (see Methods and Supplementary Data 1). Thus, this access accustomed us to analyze bulk arbor corpuscle genes, as functionally important genes are generally accomplished in the specific corpuscle populations they control1,14.
While the PCA gives us a accepted abstraction of how abounding genes are cell-specific vs cell-ubiquitous, it reduces the ambit of the botheration to the three bigger apparatus of variance. Consequently, we would apprehend some genes are differentially accomplished beyond all of the arbor corpuscle populations. Indeed, back we performed cogwheel announcement assay on the 9266 arbor cell-enriched genes (see Methods), we begin that 2018 genes (21.8% of the arbor cell-enriched genes, hereinafter referred to as the stem-cell-ubiquitous genes) are accomplished in at atomic four of the six altered arbor corpuscle types, with 569 of these 2018 (6.1% of the arbor cell-enriched genes) accomplished in bristles or six corpuscle types (Fig. 1c). Moreover, as anniversary arbor corpuscle citizenry clusters apart from the others in the PCA, we articular 7248 genes (78.2% of the arbor cell-enriched genes), hereinafter referred to as the stem-cell-specific genes, accomplished in three or beneath arbor corpuscle types, with 4331 of those 7248 genes (46.7% of the arbor cell-enriched genes) accomplished in alone one arbor corpuscle type. This suggests that anniversary specific arbor corpuscle blazon has its own, altered transcriptional signature.
Given the break amid stem-cell-ubiquitous genes and stem-cell-specific genes, we abutting capital to apperceive if these two groups of genes accept acutely afar functions or, for example, if stem-cell-ubiquitous genes attune stem-cell-specific gene announcement to arrange accommodating processes amid altered corpuscle types. To assay the closing hypothesis, in which stem-cell-specific genes are important for acclimation cell-type-specific aspects (e.g., corpuscle identity), but are adapted by stem-cell-ubiquitous genes so that arbor corpuscle aliment and capacity are deeply coordinated, we acclimated Gene Authoritative Arrangement (GRN) inference and predicted the relationships amid all 9266 genes accomplished in the arbor cells. We developed a machine-learning, corruption tree-based access to infer activating networks from abiding state, carbon abstracts (see Methods). Our accepted GRN begin regulations amid 2982 (32.2%) of the arbor cell-enriched genes and predicted that the stem-cell-ubiquitous (red) genes are amid in the centermost of the network, which represents the alpha of the authoritative cascade, and are awful affiliated to anniversary added (Fig. 2a). Meanwhile, the cell-specific (blue) genes mostly adapt anniversary added aural the aforementioned corpuscle blazon and are amid on the alfresco of the network, afterwards of the cell-ubiquitous genes (Fig. 2a). This suggests that the cell-ubiquitous genes are potentially circuitous in analogous processes amid altered arbor beef through the adjustment of cell-specific genes.
Gene authoritative arrangement (GRN) of the arbor cell-enriched genes. a Accepted GRN of 2982 out of the 9266 arbor cell-enriched genes. Genes are black based on the cardinal of genes in which they are enriched, with red genes (>3 accomplished cells) advised stem-cell-ubiquitous and dejected genes (≤3 accomplished cells) advised stem-cell-specific. Black outlines represent hub genes which accept a arrangement burden account (NMS) > 0. b First-neighbor GRN of TCX2. Gene admeasurement represents the NMS score. Red borders represent the genes which accept a accepted arbor corpuscle (SC) phenotype. Bend colors represent the corpuscle in which the adjustment is inferred. Blue—CEI; Pink—Protophlo; Green—Epi/LRC; Purple—CSCs; Orange—Xyl; Yellow—QC. c Outdegree (top plot) and indegree (bottom plot) vs NMS account of the genes with the top 10 NMS array in a. TCX2 is accent in orange.
We abutting capital to analyze if the best biologically important genes in the arrangement were stem-cell-specific, stem-cell-ubiquitous, or both, as best after-effects in animals accept that bulk TFs charge be bidding in a cell-specific manner1. To adumbrate biological significance, we developed a Arrangement Burden Account (NMS) to quantify the cardinal of times anniversary gene appears in assertive arrangement motifs, such a acknowledgment and feed-forward loops (see Methods). These motifs were called as they were decidedly accomplished in our biological arrangement against a accidental arrangement of the aforementioned admeasurement and accept been apparent to generally accommodate genes that accept important biological functions15,16,17 (Supplementary Fig. 2). In our accepted GRN, we begin that 737 (24.7%) of the 2982 genes accept an NMS > 0, acceptation they arise in at atomic one of the arrangement motifs. To validate the NMS, we begin that 22 accepted arbor corpuscle regulators had array in the top 50% of genes, with 10 of those 22 (45.5%) in the top 25% of genes, acknowledging that aerial NMS array are activated with arbor corpuscle action (Supplementary Data 2). Further, 510 (69.2%) and 217 (31.8%) of these genes are stem-cell-ubiquitous (four or added accomplished arbor cells, red) and stem-cell-specific (three or beneath accomplished arbor cells, blue), appropriately (Fig. 2a). Accustomed that added cell-ubiquitous genes accept college accent array in our dataset, we focused our afterwards assay on anecdotic a stem-cell-ubiquitous gene with characteristics of a functionally important regulator.
When we began to appraise the stem-cell-ubiquitous regulators, we begin that TESMIN-LIKE CXC 2 (TCX2, additionally accepted as SOL2), a accepted homologue of the LIN54 DNA-binding basic of the beastly DREAM complex, which regulates the corpuscle aeon and the alteration from corpuscle cessation to proliferation13,18,19, had the ninth accomplished NMS (top 1.2% of genes). This suggests that TCX2 could accept an important role beyond all of the arbor cells. To added abutment the biological acceptation of TCX2, we advised the subnetwork of its aboriginal neighbors (i.e., genes predicted to be either anon upstream or afterwards of TCX2). We begin that TCX2 is accomplished in bristles out of the six arbor corpuscle types and predicted to adapt at atomic one gene in all of those corpuscle types, acknowledging that TCX2 could be a stem-cell-ubiquitous regulator that controls stem-cell-specific bulk genes (Fig. 2b). In addition, back compared to the genes with the top 10 NMS, TCX2 has the accomplished outdegree (number of edges activity out) and almost low indegree (number of edges advancing in), suggesting that TCX2 could arrange accommodating arbor corpuscle assay as appropriate by the action of its beastly homologue13,18,19.
If TCX2 is absolutely a key regulator for arbor corpuscle aliment and division, we would apprehend that a change in its announcement would account a adorning phenotype accompanying to these aspects. To assay this hypothesis, we acquired two altercation (tcx2-1, tcx2-2) and one knockout (tcx2-3) abnormal of TCX2, which all appearance agnate phenotypes (Fig. 3a, Supplementary Fig. 3). Importantly, we empiric in tcx2-3 an all-embracing chaos of the arbor cells, including abnormal capacity in the Quiescent Centermost (QC), columella, endodermis, pericycle, and xylem beef (Fig. 3a). Additionally, tcx2-3 mutants showed best roots due to a college cardinal of meristematic cells, suggesting college corpuscle admeasurement (Fig. 3a, Supplementary Fig. 3). Notably, agnate phenotypes accompanying to corpuscle capacity accept been empiric additionally in the stomatal birth of tcx2 sol1 bifold mutants13. To added investigate TCX2’s role in arbor corpuscle division, we beyond the corpuscle assay (G2/M phase) brand CYCB1;1:CYCB1;1-GFP20,21 into the tcx2 abnormal and performed banausic tracking of the GFP arresting over time. We aboriginal begin that boilerplate CYCB1;1 announcement was college in the tcx2 abnormal compared to WT. Second, we afar beef cogent CYCB1;1 into three categories: low, intermediate, and aerial expression. We begin that decidedly added beef in the tcx2 abnormal accept aerial CYCB1;1 expression, while decidedly beneath beef accept low CYCB1;1 expression. Finally, we affected the cardinal of afterwards timepoints anniversary corpuscle showed CYCB1;1 expression. We begin that decidedly beneath beef in the tcx2 abnormal had two afterwards timepoints with CYCB1;1 announcement (Supplementary Fig. 4). All of these alterations in CYCB1;1 announcement in the tcx2 abnormal advance that abridgement of TCX2 announcement correlates with added actively adding cells. Taken together, these after-effects advance that TCX2, as a stem-cell-ubiquitous gene, regulates arbor corpuscle capacity beyond altered arbor corpuscle populations.
TCX2 controls arbor corpuscle assay through cell-specific regulators and targets. a (Left) Centermost longitudinal (left) and adorable (right) sections of 5-day-old WT (top) and tcx2-mutant (bottom) plants. In centermost longitudinal sections, asterisk labels QC beef and numbers denote columella corpuscle files. In adorable sections, white numbers denote xylem cells, chicken pericycle, and dejected endodermis. Scale bar = 20 µm. (Middle) Length of 7-day-old WT (blue, n = 18) and tcx2 mutant (orange, n = 18) roots. Centermost band represents median; box bound represent 25th and 75th percentiles; bristles represent minimum and best values. Black X represents the mean. (Right) Quantification of arbor corpuscle phenotypes (top plot) and cardinal of corpuscle files (bottom plot) in 5-day old WT (n = 21) and tcx2 abnormal (n = 17) roots. In top plot, blooming denotes the percent of roots that showed a phenotype, while gray denotes the percent of roots that did not appearance a phenotype. LRC, Col (Columella), QC refers to a corpuscle chaos phenotype in those cells. Asterisk denotes p < 0.1, Bifold asterisks denote p < 0.05, Wilcoxon test. b (Left) Centermost longitudinal sections of 5-day-old WOX5:GFP (left), CYCD6:GFP (second from left), FEZ:FEZ-GFP (third from left), and TMO5:3xGFP (right) in WT (top) and tcx2-mutant (bottom) plants. For TMO5:3xGFP, a adorable breadth (middle) was taken at the breadth of the white, abject line. (Right) Quantification of GFP in WT (blue, n = 35, n = 8, n = 5 for CYCD6, FEZ, TMO5) and tcx2-mutant (orange, n = 25, n = 6, n = 10 for CYCD6, FEZ, TMO5) plants. Centermost band represents median; box bound represent 25th and 75th percentiles; bristles represent minimum and best excluding outliers. Black dots represent outliers. Black dots represent alone abstracts points. Asterisk denotes p < 0.1, bifold asterisks denote p < 0.05, Wilcoxon test. c (Left) Predicted absolute targets of TCX2 and (right) predicted upstream regulators of TCX2 with arbor corpuscle (SC) phenotypes. Gene admeasurement represents the NMS score. Red borders represent the genes that accept a accepted SC phenotype. Arrows represent predicted activation, confined repression, and circles no predicted sign. Thick edges were accurate application qPCR/RNA-Seq. Black edges were predicted in the actual corpuscle blazon but did not accept a predicted sign. Dejected edges accept the actual corpuscle blazon and actual sign, while orange edges accept the actual corpuscle blazon but the incorrect sign. Arrows with chevrons are DAPSeq validated. Source abstracts are provided as a Source Abstracts file.
We accepted that TCX2 controls arbor corpuscle assay by acclimation important, stem-cell-type-specific genes. Notably, all of our arbor corpuscle markers, in accession to actuality bidding in alone one arbor corpuscle type, are accepted to accept functions in arbor corpuscle regulation22,23,24,25,26. Thus, we beyond the brand curve for the Quiescent Centermost (QC; WOX5:GFP), Case Endodermis Initials (CEI; CYCD6:GFP), Epidermis/Lateral Basis Cap Initials (Epi/LRC; FEZ:FEZ-GFP), and Xylem Initials (Xyl; TMO5:3xGFP) (Fig. 1a) into the tcx2-2 and tcx2-3-mutant alleles (Fig. 3b). Compared to WT, in a tcx2 abnormal the announcement arrangement of these markers is expanded. Specifically, the QC brand expands into the CEI, the CEI brand expands into the endodermis and case layers, the Epi/LRC brand expands into the Columella Arbor Beef (CSCs), and the Xyl brand expands into the procambial beef (Fig. 3b). This suggests that, in the absence of TCX2, allocation of arbor corpuscle assay and character is misregulated through an alien mechanism.
When we advised the predicted upstream regulators and afterwards targets of TCX2, we begin that 75% are predicted to be cell-specific (expressed in ≤3 arbor corpuscle types), suggesting that TCX2 could be adapted and itself adapt targets in a corpuscle type-specific manner. (Supplementary Data 3). Thus, to analyze added cell-specific regulators as able-bodied as targets of TCX2, we acquired mutants of the archetype factors (TFs) predicted to be TCX2’s aboriginal neighbors (i.e., anon upstream or downstream) that additionally had aerial NMS array (Fig. 3c, Supplementary Data 3). Two of the genes, SHORTROOT (SHR), and SOMBRERO (SMB) accept phenotypes in the arbor beef of their loss-of-function mutants, while the loss-of-function abnormal of STERILE APETALA (SAP) is homozygous sterile23,25,27,28,29. Additionally, a quadruple abnormal of REVOLUTA (REV) calm with three added xylem regulators after-effects in missing xylem layers30. Further, we acquired loss-of-function mutants of GATA TRANSCRIPTION FACTOR 9 (GATA9), AT1G75710, ORIGIN OF REPLICATION COMPLEX 1B (ORC1B), ANTHOCYANINLESS 2 (ANL2), and REPRODUCTIVE MERISTEM 28 (REM28), which showed basis arbor corpuscle phenotypes (Fig. 3c, Supplementary Fig. 5). We were able to validate that TCX2 was differentially bidding in gata9, at1g75710, rev, orc1b, and anl2 mutants application qPCR as able-bodied as in the SHR overexpression line23. Further, we performed FACS accompanying with RNA-Seq on the 4 brand curve (WOX5:GFP, CYCD6:GFP, FEZ:FEZ-GFP, and TMO5:3xGFP) that we beyond into the tcx2 abnormal to actuate the aftereffect of TCX2 on its predicted afterwards stem-cell-specific targets. In addition, we performed RNA-Seq on tissue from the arbor corpuscle breadth of the tcx2 abnormal (Supplementary Data 5). Application these data, we were able to validate that 77.8% of the predicted absolute targets of TCX2 are differentially bidding in the tcx2-mutant arbor cells. Further, 41.5% of these edges are predicted in the actual corpuscle type, and of those edges predicted in the actual corpuscle blazon that had a predicted sign, 58.3% of the bend signs are accurately predicted (slightly bigger than about allotment bend signs, which would accept a 50% bulk of success). To validate some of the absolute interactions amid TCX2 and its afterwards targets, we mined a appear DAP-Seq dataset from Arabidopsis leaves31 and were able to affirm that TCX2 can anon bind 15.1% of its predicted absolute targets (Fig. 3c, Supplementary Data 4). Overall, these after-effects advance TCX2 orchestrates accommodating arbor corpuscle capacity through stem-cell-specific authoritative cascades.
Given that best of the accurate upstream regulators of TCX2 are stem-cell-type-specific (Supplementary Data 3), we adduce that these stem-cell-specific regulators attune the dynamics of TCX2 announcement in alone corpuscle types. In turn, changes in TCX2 dynamics associate with changes in announcement of its afterwards targets (Fig. 3c, d). Thus, we accepted that altered dynamics of TCX2 in specific arbor cells, as able-bodied as changes in TCX2 expression, could be acclimated to adumbrate back anniversary arbor corpuscle citizenry divides.
If TCX2 announcement is dynamically alteration over time in a cell-specific manner, we would adumbrate that the TCX2 GRN additionally changes temporally. Specifically, we could apprehend that TCX2 differentially regulates its targets in specific corpuscle types at assertive times depending on its announcement levels. Thus, to actuate if the TCX2 authoritative arrangement changes over time, we aboriginal called 176 genes of absorption that were differentially bidding in the tcx2 basis tip sample (Supplementary Data 5) as able-bodied as accomplished in the arbor cells, as these are best acceptable to be afterwards of TCX2 beyond altered arbor corpuscle populations. We accepted GRNs application a time advance of the basis meristem that is stem-cell-enriched (hereinafter referred to as the arbor corpuscle time course, see Methods) to adumbrate one arrangement per time point (every 8 h from 4 to 6 days). We begin that genes in the first-neighbor arrangement of TCX2 accept altered predicted regulations depending on the time point. Specifically, best of the regulations to and from TCX2 are predicted to action amid 4 canicule (4D) and 5 canicule (5D), which is the adorning time at which abounding arbor corpuscle capacity booty place23 (Supplementary Fig. 6). Thus, back our gene announcement abstracts advance that accident of TCX2 action correlates with an access in arbor corpuscle division, we accepted that best of the TCX2-regulated arbor corpuscle assay is occurring amid 4D 16H and 5D back the bigger abatement in TCX2 announcement occurs (Supplementary Fig. 6).
To assay how these time- and cell-specific GRNs affect TCX2 announcement and accordingly corpuscle division, we congenital a mechanistic archetypal of the GRNs predicted every 8 h from 4D to 5D (see Methods and Supplementary Information). We acclimated our arbor corpuscle time advance to actuate the stem-cell-specific networks at anniversary time point and complete equations for anniversary gene in the arrangement (Fig. 4a, Supplementary Fig. 7). Unlike our GRN, which alone predicts the regulations in anniversary corpuscle at anniversary time point, our Ordinary Cogwheel Equation (ODE) archetypal converts the arrangement anticipation into a quantitative archetypal of gene expression. Thus, this archetypal accustomed us to quantify how TCX2 dynamics change over time and to associate cogent changes in announcement with corpuscle division. Our archetypal included the achievability of some of the proteins affective amid corpuscle types, as this is a accepted bounded signaling/cell-to-cell advice mechanism28,32. Specifically, we acclimated scanning Fluorescence Alternation Spectroscopy (Scanning FCS) and empiric that TCX2 does not move amid cells, appropriately suggesting a cell-autonomous function, while empiric movement of WOX533 and CRF2/TMO3 amid beef is in band with a non-cell-autonomous action (Supplementary Fig. 8). As our acuteness assay predicted that the oligomeric accompaniment of TCX2 in the Xyl, circulation accessory of WOX5 from the CEI to the QC, and circulation accessory of WOX5 from the QC to the Xyl were three of the best important ambit in the model, we experimentally bent these ambit (Supplementary Fig. 8, Supplementary Data 6). Accustomed that our arrangement and time advance abstracts adumbrate that TCX2-mediated corpuscle assay is deeply accommodating and controlled amid 4D 16H and 5D, we capital to ensure that we accurately abstinent TCX2 dynamics in this time aeon to aftermath the best predictive archetypal of arbor corpuscle division. To this end, we quantified the announcement of the TCX2:TCX2-YFP brand in altered arbor beef every 2 h from 4D 18H to 4D 22H (hereinafter referred to as the YFP tracking data) (Fig. 4b, see Methods). We again acclimated the boilerplate announcement of TCX2 in anniversary corpuscle at anniversary time point to appraisal ambit in our archetypal (Supplementary Data 7). The aftereffect of this archetypal is appropriately a spatiotemporal map of the announcement dynamics of TCX2 and its predicted aboriginal neighbors. Accustomed that TCX2 announcement has ahead been apparent to abandon 1–2 h afore stomatal division13, we articular that we could use our archetypal of TCX2 announcement to adumbrate back arbor corpuscle assay occurs in the root.
Mathematical clay of TCX2 arrangement predicts timing of corpuscle division. a TCX2 first-neighbor TF networks predicted application RTP-STAR on the arbor corpuscle time advance for 4 day (4D) to 4 canicule 8 h (4D 8H) (top), 4D 8H to 4D 16H (middle), and 4D 16H to 5D (bottom). Networks are afar based on the corpuscle blazon the genes are bidding in: QC (yellow), CEI (blue), CSCs (purple), Epi/LRC (green), Xyl (orange). Arrows represent predicted activation, confined accepted repression, and circles no accepted sign. b (left) Representative angel of TCX2:TCX2-YFP at 4D 16H. White box represents the arbor corpuscle alcove were beef were tracked over time. Scale bar = 20 µm. (right, top) YFP-positive beef tracked every 2 h from 4D 16H (left) to 4D 20H (right). Arbor beef that were tracked are apparent in dejected (CEI), blooming (Epi/LRC), and orange (Xyl). Two Xyl beef were tracked, #1 and #2. All of these four arbor beef had no assessable YFP announcement at 4D 22H. (right,bottom) Quantification of YFP announcement in tracked cells. c ODE archetypal anticipation of cell-specific TCX2 announcement from 4D to 5D. FPKM: bits per kilobase per actor mapped reads.
Our archetypal predicts that there is a cogent (fold-change >1.5) access in TCX2 announcement accurately in the QC and Xyl amid 4D 8H and 4D 16H. Afterwards this time, our archetypal predicts that the announcement of TCX2 in the QC does not decidedly abatement and is decidedly college than in all of the actively adding arbor beef (Fig. 4c, Supplementary Data 8). Accustomed that the QC is almost mitotically inactive, this suggests that aerial levels of TCX2 associate with a abridgement of QC division. This anticipation is accurate by our YFP tracking data, which shows that bisected of the QC corpuscle clusters accept either almost connected or added TCX2 announcement amid 4D 16H an 5D (Supplementary Fig. 9). Meanwhile, TCX2 announcement is predicted to decidedly abatement amid 4D 16H and 5D in both the Xyl and CSCs, suggesting that these beef bisect during this time. This anticipation is additionally accurate by our YFP tracking abstracts assuming that the majority of Xyl and CSCs beef accept low TCX2 announcement afterwards 4D 20H (Supplementary Fig. 9). In contrast, the CEI and Epi/LRC appearance alone a bashful abatement in TCX2 announcement amid 4D 16H and 5D. This could be due to alone some of these beef adding at that time, as our YFP tracking abstracts appearance a ample bulk of aberration in TCX2 announcement in these corpuscle populations (Supplementary Fig. 9). Taken together, our archetypal and beginning abstracts both advance that TCX2 not alone initiates the assay of the actively adding arbor cells, but it additionally inhibits the assay of the QC during the aforementioned timeframe, through an alien mechanism. Further, our after-effects acquiesce us to attenuated the timing of TCX2-induced arbor corpuscle assay to a 4-hour window, amid 4D 20H and 5D.
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