Motahari Z , Martinez-De Luna RI , Viczian AS , Zuber ME .

R01 EY015748 NEI NIH HHS , R01 EY017964 NEI NIH HHS , R01 EY019517 NEI NIH HHS

	Fig. 1. Tbx3 is sufficient to specify pluripotent cells to a retinal lineage. (A) Schematic illustrating the animal cap transplant (ACT) to eye field assay (ACT→EF; Viczian and Zuber, 2010). (B) Histogram showing the percentage of tadpoles in which transplanted cells formed retina in response to the expression of YFP only, YFP with the indicated EFTF, an EFTF cocktail or Noggin (YFP only, 500 pg; Otx2, 25 pg; Tbx3, 50 pg; Rax, 50 pg; Pax6, 100 pg; Six3, 25 pg; Six6, 25 pg; Nr2e1, 25 pg; EFTF cocktail; Noggin, 2.5 pg). (C-F) Sections of tadpoles receiving transplants expressing (C) YFP and (D) Noggin, (E) Pax6 or (F) Tbx3. XAP-2 (red), DAPI (blue) and YFP (green) detect rod photoreceptors, nuclei and transplanted cells, respectively. Dorsal is up. N=2; n≥40; *P≤0.05. Scale bar: 50 μm.
	Fig. 2. Tbx3 is required for normal eye formation. Design and test of Tbx3 morpholino activity. (A) Comparison of X. laevis tbx3.L and tbx3.S homeologs showing the position of morpholino target sequences. (B) Western blots were used to detect the expression of YFP and β-actin (loading control) in extracts prepared from embryos injected at the 2-cell stage (both blastomeres) with 10 ng of the indicated morpholino and Tbx3.L/.S-YFP RNA. (C-E) Injected side of tadpoles treated with 10 ng CoMO (C), Tbx3MO-S (D) or Tbx3MO-LS (E). (F) Uninjected side of tadpole in E. (G,H) The percentage reduction in eye size was determined by comparing the dorsoventral (D/V) eye diameter on the uninjected and injected sides. Histograms show eye diameter reduction in tadpoles injected with YFP RNA and the indicated morpholino (G) or combination of morpholinos (H). N=2; n≥29; ****P<0.0001; ns, not significant. Scale bar: 200 μm.
	Fig. 3. Tbx3 knockdown inhibits the retinal- and neural-inducing activity of Noggin. (A-F) Retinal sections of tadpoles that received grafts at stage 15 (ACT→EF). (A-C) Donor cells expressed (A) YFP only, or were co-injected with (B) CoMO or (C) Tbx3MO-LS (Tbx3MO). (D-F) Donor cells expressed (D) YFP plus Noggin (Nog) alone, or in combination with (E) CoMO or (F) Tbx3MO. (G) Histogram showing the average percentage of tadpoles in which donor cells formed retina. (H-J′) Retinas of tadpoles receiving donor cells expressing (H,H′) YFP alone, or in combination with (I,I′) Noggin or (J,J′) Noggin with Tbx3MO. Staining marks nuclei (DAPI; blue), donor-derived cells (YFP; green) and neural tissue (Tubb2b; red). Dashed line in J and J′ indicates location of donor cells. Dorsal side up. N=3; n≥40; ***P<0.001, ****P<0.0001. Scale bar: 50 μm.
	Fig. 4. Tbx3 induces neural but not retinal tissue and is required for Noggin to determine pluripotent cells to a neural and retinal fate. (A-O) Donor cells expressing the indicated RNAs and morpholinos were grafted to the flank of stage 15 host embryos (ACT→Flank). Arrowheads (A-E′) indicate location of grafted cells in brightfield (A-E) and YFP fluorescence (A′-E′) images. Dashed boxes in A-E outline magnified regions in A′-E′. Sections are stained for YFP (F-O, green), the neural marker Tubb2b (F-J, orange) and rod photoreceptor marker, XAP-2 (K-O, red). (P,Q) Histograms showing percentage of donor transplants that were YFP+/Tubb2b+ or YFP+/XAP-2+. (R-Z) Donor eye fields expressing YFP only, with CoMO or Tbx3MO were transplanted to the flank of stage 15 host embryos (EF→Flank). R′-T′ show the location of YFP fluorescence in the flank of embryos in R-T. DAPI-labeled tadpole sections were stained for YFP (green) and Tubb2b (U-W, orange) or XAP-2 (X-Z, red). N=2; n≥39; *P≤0.05, **P<0.01, ***P<0.001. Scale bars: 400 μm (E′,T), 50 μm (Z).
	Fig. 5. Tbx3-expressing cells are specified to a spinal cord, not retinal fate when transplanted to the posterior neural plate. (A-L) Ectodermal explants expressing the indicated RNAs were transplanted to the posterior neural plate of stage 15 embryos and grown to tadpoles (ACT→PNP). Arrowheads (A-C) indicate location of YFP donor tissue. (D-L) Donor cells expressing YFP alone (D,G,J) or with Noggin (E,H,K) or Tbx3 (F,I,L). Sections were stained to detect neural (Tubb2b, orange, D-F), retinal (XAP-2, red, G-I) and spinal cord (Sox2, magenta, ventricular zone; Islet-1/2, yellow, Rohon-Beard and motor neuron, J-L) cells. DAPI (blue) and YFP (green) label nuclei and donor cells, respectively. To better visualize cell fate markers, D′-L′ insets show D-L without YFP channel. (M) Histogram showing the percentage of host embryos expressing the indicated markers in mosaic spinal cords. (N) Ectodermal explants isolated from stage 9 embryos injected bilaterally at the 2-cell stage with the indicated RNA were cultured in vitro to stage 21. RT-PCR was used to detect ncam1, tubb2b, t (xbra), actc1 and histone H4 (h4: loading control). Whole embryos processed with (WE) and without (WE-RT) reverse transcriptase served as positive and negative controls, respectively, N=2; n≥32; ns, not significant. Scale bars: 400 μm (C), 100 μm (L).
	Fig. 6. Noggin and Tbx3 repress bmp4 expression in vitro and in vivo. bmp4 expression was detected by in situ hybridization in ectodermal explants and intact embryos. (A-C,G-N) Ectodermal explants were isolated at stage 9 from embryos injected bilaterally at the 2-cell stage with the indicated RNA. Explants were left untreated (A-C,G-J) until stage 22, or treated from stage 15 with dexamethasone (K-N). The percentage of explants with reduced bmp4 expression is indicated, N=4; n≥36. (D-F,O-V) 4-cell stage embryos were injected in one dorsal blastomere with the indicated RNA. Embryos were left untreated (D-F,O-R) until stage 12.5, or treated from stage 9 with dexamethasone (S-V). The percentage with reduced bmp4 expression is indicated, N=3; n≥48. (V) 100% of embryos showed posterior ectopic bmp4 expression (arrow), while 73% showed reduced bmp4 expression anteriorly. RNA injected: 500 pg YFP, 2.5 pg Noggin, 50 pg Tbx3, 100 pg Tbx3-GR, 250 pg DBD-EnR-GR, 5 pg VP16-DBD-GR (doubled for explants). Dorsal view, anterior toward the bottom. Scale bars: 200 μm (N), 400 μm (V).
	Fig. 7. Tbx3 repressor activity is required at eye field stages for normal neural patterning and eye formation. (A-R) In situ hybridization was used to detect changes in rax, pax6, otx2, foxg1 and ag1 transcript levels at stage 15. Eight-cell embryos were injected in one blastomere with β-gal alone (150 pg, A-F), and in combination with DBD-EnR-GR (12.5 pg, G-K; 50 pg, L) or VP16-DBD-GR (5 pg, M-R) RNA. At stage 12.5, embryos were untreated (A,G,M) or treated with dexamethasone (B-F, H-L and N-R). The percentage showing a change in expression is indicated, N=2; n≥41. (S-Z) The repressor activity of Tbx3 is required at eye field stages for normal eye formation. Control (S-V)- and VP16-DBD-GR (W-Z)-injected embryos were untreated (S,W) or treated with dexamethasone starting at the indicated stage. (AA) Histogram shows the percentage of tadpoles with the indicated eye defects, N=2; n≥35. Scale bars: 300 μm (R), 400 μm (Z).
	Fig. 8. Tbx3 knockdown results in retinal progenitor apoptosis and eye defects. Eye field cells isolated from embryos expressing YFP (A-D′), CoMO (E-H′) or Tbx3MO-LS (I-L′) were grafted into the eye field of untreated embryos (EF→EF). TUNEL staining was used to detect cell death of the transplanted (YFP-positive) cells at stage 22 (A,A′,E,E′,I,I′), 25 (B,B′,F,F′,J,J′), 35 (C,C′,G,G′,K,K′), and 39 (D,D′,H,H′,L,L′). Dotted lines indicate the outline of the optic vesicle (stgs 22 and 25), optic cup and lens (stgs 35 and 39). (M) Line graph indicates the number of TUNEL-positive donor (YFP-positive) cells per unit volume of transplanted cells as a function of developmental stage. (N) Number of TUNEL/YFP double-positive cells per unit volume that were detected in the stage 35 retina of tadpoles that received eye field transplants from embryos injected with YFP only, CoMO, Tbx3MO-LS and Tbx3MO-SP at stage 15. Dorsal retina is the top of each panel. Graphs show mean±s.e.m.; N=3, n≥9; **P≤0.01, ***P≤0.001, ****P≤0.0001. Scale bar: 50 μm.
	Fig. 9. Together, Tbx3 and Pax6 are sufficient to determine retina from pluripotent cells. (A-T) Pluripotent cells isolated from embryos injected with the indicated RNAs were transplanted to the flank of stage 15 embryos then grown to tadpoles (ACT→Flank). Arrowheads (A-E) show location of transplant (green fluorescence, A′-E′). (F-T) Sections were stained for a neural marker (Tubb2b, orange), rod photoreceptor marker transducin (Gαt1, magenta) and nuclei (DAPI, blue). (U) Percentage of transplants with YFP+/Tubb2b+ and YFP+/Gαt1+ cells, N=2; n≥29; *P≤0.05, ***P<0.001, ****P≤0.0001. (V) Schematic graphically summarizing results obtained from transplants performed in Figs 1,3-5 and 9; GOI, gene of interest. Scale bars: 400 μm (E), 50 μm (T).
	Fig. 10. Model illustrating the role of Tbx3 during eye field determination. Noggin protein binds BMP4 directly blocking BMP receptor activation in the early neural plate (light blue), which includes the presumptive eye field (dark blue). Tbx3 is required to repress bmp4 transcript levels, resulting in continued BMP inhibition in the eye field. The combined activity of Tbx3 and Pax6 is sufficient to determine the eye field to form retina. Solid and dashed lines indicate direct and possible indirect interactions, respectively.
	Fig. S1. Tbx3 is expressed in a pattern consistent with a role in eye formation. Posterior (A,E) and anterior (B-D) views of intact embryos showing the expression pattern of tbx3 at the indicated developmental stages. (F-H) Stage 15 embryos stained by whole mount in situ hybridization, then cut midsagittal (F,G) and parasagittal (H) to reveal internal tissues expressing tbx3. (I) RT-PCR of isolated eye fields at the indicated stages detecting the expression of transcripts for tbx3.L and tbx3.S homeologs. Abbreviations: dbl, dorsal blastopore lip; anp, anterior neural plate; ef, eye field; cg, cement gland; ef-m, eye field - midline; ef-a, eye field - eye anlagen; bp, blastopore; vim, ventral involuting mesoderm; dm, dorsal mesoderm; arch, archenteron; pp, prechordal plate; sne, sensorial layer of neuroectoderm; ene, epithelial layer of neuroectoderm; vm, ventral mesoderm; 18-RT, stage 18 minus reverse transcriptase control. Scale bar, 200 μm.
	Fig. S2. Tbx3 is required for normal eye formation. (A-B) Schematic of constructs used to test morpholino activity in the whole embryo. (C-H′′) Bright-field (C-H), mCherry fluorescence (C'-H') and YFP fluorescence (C′′-H′′) Development • Supplementary information Development 143: doi:10.1242/dev.130955: Supplementary information images of neurula stage embryos unilaterally injected at the two-cell stage (right side - reader’s perspective) with cRNA for mCherry and Tbx3-L-YFP (C-E′′) or Tbx3-S-YFP (FH′′) as diagrammed above the panels. CoMO (C-C′′, n=54; F-F′′, n=57), Tbx3MO-LS (DD′′, n=60; G-G′′, n=59) and Tbx3MO-S (E-E′′, n=58; H-H′′, n=60) were also injected to determine if translation of the YFP fusion constructs were blocked by each morpholino. Scale bar, 200 μm. (I-J) The percent reduction in eye size was determined by comparing the anteroposterior diameter of the eye on the uninjected side to the injected side. Histograms show eye size differential measured in wild-type animals and tadpoles injected as embryos with YFP and the indicated morpholino or combination of morpholinos. Histograms show mean±s.e.m; N=3; ns, P>0.05; ****P≤0.0001.
	Fig. S3. Splice blocking phenocopies eye defects observed with translation blocking Tbx3 morpholinos. The splice blocking morpholino (Tbx3MO-SP) was designed to the exon 1 splicedonor site of tbx3.L and tbx3.S. An in frame stop codon is located in intron 1 Development • Supplementary information Development 143: doi:10.1242/dev.130955: Supplementary information immediately following the splice-donor site, resulting in truncation of the protein. (A) Schematic of Tbx3 gene structure, location of the splice blocking morpholino, and PCR primers used to confirm altered splicing. (B) Alignment of tbx3.L and tbx3.S target sites with location of Tbx3MO-SP. Uppercase and lowercase nucleotides identify exon and intron regions, respectively. In frame intronic stop codon (tga) is underlined in red. (C) RT-PCR to detect unspliced tbx3.S (FR1) and tbx3.L (FR2) transcripts. An increase in unspliced tbx3.S and tbx3.L transcripts is detected in Tbx3MO-SP (MO-SP) injected embryos relative to YFP and control (CoMO) morpholino injected embryos. (D-F) Eye defects following splice-blocking of Tbx3 transcript. Injected side of tadpoles treated with Tbx3MO-SP (F, n=87) is shown with the CoMO (D) and Tbx3MO-LS (E) injected tadpoles from Fig. 2 for comparison purposes. (G-H) The percent reduction in eye size was determined by comparing the dorsoventral and anteroposterior diameters of the eye on the injected side relative to the uninjected side. Histograms show eye size differential measured in tadpoles injected in one blastomere at the eight-cell stage with the indicated morpholino. Histograms show mean±s.e.m; N=2; ****P≤0.0001; scale bars, 200 μm.
	Fig. S4. Magnified view of Fig. 4 Panels A-E’. (A-E’) Animal cap cells isolated from embryos injected with the indicated RNAs and morpholinos were transplanted to the flank of stage 15 embryos, which were then grown to tadpole stages (ACT→Flank). Arrowheads (A-E) indicate location of YFP positive (A’-E’) transplant on the flank of tadpoles. Scale bar, 400 μm.
	Fig. S5. Tbx3 knockdown generates cement gland in Noggin expressing donor cells. (A-B) Transverse sections of stage 43 embryos with flank (A) and eye field (B) transplants of donor cells expressing mCherry, Noggin and Tbx3MO. Sections were imaged to detect cell nuclei (DAPI; blue), mCherry fluorescence (red) and green fluorescently labeled cement gland marker ECL (5 μg/ml; Fluorescein Erythrina crista-galli Lectin, cat#FL-1141, Vector Laboratories, Inc., Burlingame, CA). Eye in (B) is oriented with dorsal side to the top; N=2, n≥25. Scale bar, 50 μm.
	Fig. S6. Magnified view of Noggin and Tbx3-treated transplanted cells expressing Sox2 or Islet1/2. (A-B) Panels from Fig. 5K,L with a dashed white box showing the area of magnification. Each column of images were taken from the same sample. Ectodermal explants were isolated from embryos injected with YFP and Noggin (A) or YFP and Tbx3 RNA-injected embryos (B), transplanted to the posterior neural plate at stage 15 and the resulting tadpoles were sectioned and stained at stage 43 (ACT→PNP). (C-D’’’) Enlarged images of panel A and B shows Sox2 (white arrows) or Islet1/2 (yellow arrowheads) positive cells co-expressing YFP.
	Fig. S7. Tbx3 is necessary for the ability of Noggin to repress bmp4 expression in ectodermal explants. (A-F) In situ hybridization was used to detect changes in bmp4 expression in ectodermal explants. Ectodermal explants were isolated from embryos injected bilaterally with RNA at the 2-cell stage of the indicated construct and/or morpholino. In situ hybridization for bmp4 expression performed at the equivalent of stage 22. Embryos injected with 500 pg YFP, 2.5 pg Noggin, 20 ng morpholinos (per blastomere); N=3, n≥47. Scale bar, 200 μm.
	Fig. S8. Tbx3 knockdown results in progressive loss of donor eye field cells and their progeny during eye development. (A-R) Donor embryos were injected into 1 dorsal blastomere at the 8-cell stage, then cultured to stage 15, when a portion of the donor eye fields from YFP-only (A-F, 500 pg, n=59,), YFP plus CoMO (G-L, 10 ng, n=54), or YFP plus Tbx3MO (M-R, 10 ng, n=58) injected embryos were grafted into host, stage 15 eye fields (EF→EF). The fate of YFPDevelopment • Supplementary information Development 143: doi:10.1242/dev.130955: Supplementary information positive donor cells was followed using brightfield (A, G, M, insets C’-E’, I’-K’, and O’-Q’) and YFP fluorescence (B-E, H-K, and N-Q) at stages 25, 35, 39 and 43. (F, L, and R) Sections of stage 43 retinas were stained for YFP-positive donor cells (green), the rod marker XAP-2 (red) and nuclei (blue). (S) The percent of live tadpoles with detectable YFP expression. (T) The volume of YFP-positive cells in retinas that received donor eye field transplants from YFP-only, YFP plus CoMO or YFP plus Tbx3MO transplants (YFP n=20, CoMO n=19, Tbx3MO n=20). Dotted lines indicate the boundary of the optic vesicle or cup. Histograms show mean±s.e.m; *P≤0.05, and ****P≤0.0001; scale bar, 50 μm F,L,R, and 200 μm all others.
	Fig. S9. Noggin represses tbx3 expression in vitro, while inducing in vivo tbx3 expression. (A) RT-PCR was used to detect changes in tbx3 expression in vitro at the equivalent of stages 12 and 15 in ectodermal explants isolated at stage 9 from YFP-only and YFP plus Noggin injected embryos. RT-PCR for histone h4 transcript was used to confirm approximately equal amounts of RNA was used in the reverse transcription reactions. (B-C) Whole mount in situ hybridization was used to detect changes in tbx3 expression (violet) at stage 15 in response to injection of ßgal-only (B; red) and ßgal plus Noggin (C). N=3; n≥58. Scale bar, 300 μm.

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