NONSTOP GLUMES 1 Encoding a C2H2 Zinc Finger …...1 1 RESEARCH ARTICLE 2 3 NONSTOP GLUMES 1 Encodes a C2H2 Zinc Finger Protein that 4 Regulates Spikelet Development in Rice 5 6 Hui
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RESEARCH ARTICLE 1
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NONSTOP GLUMES 1 Encodes a C2H2 Zinc Finger Protein that 3
lemma like inner rudimentary glume; le-like mrp, lemma like marginal region of palea; 1248
le/mrp-like fi, lemma and/or marginal region of palea like filament; le/mrp like lo, lemma 1249
and/or marginal region of palea like lodicule; le/mrp-like osl, lemma and/or marginal 1250
region of palea like outer sterile lemma; lo, lodicule; mrp-like irg, marginal region of 1251
palea like inner rudimentary glume; mrp, marginal region of palea; osl, outer sterile 1252
lemma. 1253
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Figure 1. Phenotypes of Spikelets in the Wild Type and nsg1-1 Mutant.(A) Spikelets of the wild type. A1–A2, A wild type spikelet; the lemma was removed in (A2). A3–A7, A wild-typespikelet; the lemma was removed in (A3). A4 to A7 show the surface characters of rg, sl, bp, lo and mrp, respectively.A8, Transverse sections of a wild-type spikelet showing a similar phenotype to those in (A1–A7).(B–E) Spikelets of the nsg1-1 mutant. B1–B2, A nsg1-1 spikelet; the lemma was removed in (B2). B3–B7, A nsg1-1spikelet; the lemma was removed in (B3). B4 to B7 show surface characters of the elongated rg, elongated sl, lemma-likesl, and lemma-like mrp, respectively. B8, Transverse sections of a nsg1-1 spikelet showing a similar phenotype to thosein (B1–B7).C1–C2, A nsg1-1 spikelet; the lemma and the lemma-like palea were removed in (C2). C3–C5, A nsg1-1 spikelet; thelemma and the lemma-like palea were removed in (C3). C4 and C5 show the surface characters of the elongated lodiculeand lodicule-like stamen, respectively. C6, Transverse sections of a nsg1-1 spikelet showing a similar phenotype to thosein (C1–C6).D1–D2, A nsg1-1 spikelet; the additional lemma was separated in (D2). D3–D6, A nsg1-1 spikelet; D4 to D6 show thesurface characters of the elongated rg, osl, and isl, respectively. D7, Transverse sections of a nsg1-1 spikelet showing asimilar phenotype to those in (D1–D6).E1–E2, A nsg1-1 spikelet; the lemma and the additional lemma were removed in (E2). E3–E6, A nsg1-1 spikelet. E4 toE6 show the surface characters of the lemma-like rg, osl and isl, respectively. E7, Transverse sections of a nsg1-1spikelet showing a similar phenotype to those in (E1–E6). Red arrowheads indicate a fused organ of lodicule and palea inan incomplete extra floret.(F) Schematic diagrams of wild type (WT) and nsg1-1 spikelet structure in transverse section.(G) Percentage of elongated or lemma-like organs in nsg1-1 spikelets.absence of org, absence of outer rudimentary glume; bp, body of palea; ele, additional lemma; fi, filament; irg, innerrudimentary glume; isl: inner sterile lemma; le, lemma; le-like isl, lemma like inner rudimentary glume; le-like mrp,lemma like marginal region of palea; le/mrp-like fi, lemma and/or marginal region of palea like filament; le/mrp-like irg:lemma and/or marginal region of palea like inner rudimentayu glume; le/mrp like lo: lemma and/or marginal region ofpalea like lodicule; le/mrp-like osl: lemma and/or marginal region of palea like outer sterile lemma; lo: lodicule; lo-likefi: lodicule like filament; mrp: marginal region of palea; org, outer rudimentary glume; osl: outer sterile lemma; pa:palea; pi: pistil; st: stamen.White type indicates the normal organs, and red type indicates the abnormal organs.Bars = 1,000 μm in *1, *2 and *3; 500 μm in A8, B8, C6, and D7; 50 μm in all other images.
Figure 2A2 A4 A5
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Figure 2. Histological and qPCR Analysis of Lateral Organs in Spikelets of the Wild Type and nsg1-1 Mutant.(A) Transverse sections of lateral organs in a wild-type spikelet.(B–D) Transverse sections of lateral organs in nsg1-1 spikelets.A1 shows the rg of the wild type while B1, C1, and D1 show mrp-like rg in nsg1-1 spikelets.A2 shows the osl of the wild type; B2, C2, and D2 show mrp-like and/or lemma-like osl in nsg1-1 spikelets.A3 shows the isl of the wild type; B3, C3, and D3 show mrp-like and/or lemma-like isl in nsg1-1 spikelets.A4 shows the mrp of the wild type; B4, C4, and D4 show lemma-like mrp in nsg1-1 spikelets.A5 shows the lodicule and stamen of the wild type; B5, C5, and D5 show abnormal lodicule, mrp-like lodicule, and mrp-like filament in nsg1-1 spikelets, respectively.(E–G) qPCR analysis of MFO1, DL, and LHS1 expression. ACTIN was used as a control. RNA was isolated fromflower organs of wild type and nsg1-1 spikelets . Error bars indicate SD. At least three replicates were performed, fromwhich the mean value was used to represent the expression level.ele, additional lemma; fi, filament; irg, inner rudimentary glume; isl, inner sterile lemma; le, lemma; lo, lodicule; mrp,marginal region of palea; osl, outer sterile lemma; pa, palea; st, stamen.White type indicates the normal organs, and red type indicates the abnormal organs.Bars = 150 μm.
Figure 3
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Figure 3. Scanning Electron Micrographs of Spikelets of the nsg1-1 Mutant at Early Developmental Stages. (A) Wild-type spikelets.(B) nsg1-1 spikelets with relatively normal palea primordia.(C) nsg1-1 spikelets with additional lemma or lemma-like palea primordia.A1/B1/C1/, A2/B2/C2, A3/B3/C3, and A4/B4/C4 show spikelets at the Sp4, Sp5, Sp6, and Sp8 developmental stages,respectively.ele, additional lemma; elo:elongated lodicule; irg, inner rudimentary glume; isl, inner sterile lemma; le, lemma; osl,outer sterile lemma; org, outer rudimentary glume; pa, palea.White type indicates the normal organs, and red type indicates the abnormal organs.Bars = 100 μm.
Figure 4
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Figure 4. Map-based cloning of NSG1. (A) Schematic illustration of the genomic structure of NSG1. The sites of the mutation in the nsg1-1, nsg1-2, andnsg1-3 mutants are shown.(B) Structure of the NSG:GFP fusion complementary vector and the phenotypes of three independent transgenic lines.(C) Allelic test between the nsg1-1 and nsg1-2 mutants. Three primer pairs were used to detect the distinct site of thensg1-1 and/or nsg1-2 mutation.Bars = 1,000 μm.
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MaXP009381578 EgXP010913843
AcOAY79850 ZmXP 008652751
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TcEOY29371 JcXP012076458
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Figure 5. NSG1 Encodes a Zinc Finger protein with a Single C2H2 Motif.(A) Phylogenetic tree for NSG1-like proteins. The phylogenetic tree was constructed using the neighbor-joining methodbased on the Jones–Taylor–Thornton matrix-based model. Bootstrap support values calculated from 1000 replicates aregiven at the branch nodes. Ac, Ananas comosus; Aet, Aegilops tauschii; Bd, Brachypodium distachyon; Ca, Capsicumannuum; Cc, Cajanus cajan; Cia, Cicer arietinum; Do, Dichanthelium oligosanthes; Eg, Elaeis guineensis; Gh,Gossypium hirsutum; Gm, Glycine max; Jc, Jatropha curcas; Ma, Musa acuminata; Nt, Nicotiana tabacum; Os, Oryzasativa; Pt, Populus trichocarpa; Sb, Sorghum bicolor; Si, Setaria italica; Sl, Solanum lycopersicum; Tc, Theobromacacao; Vr, Vigna radiata; Vv, Vitis vinifera; Zm, Zea mays.(B) Analysis of the subcellular localization of the NSG1 protein. Bars = 50 µm.(C-E) Analysis of the transcriptional activation of NSG1 using the dual luciferase reporter assay system. Transactivationactivity in rice protoplasts transfected with a pUAS-fLUC reporter construct, effector constructs fused with GAL4BD,and a p35S-rLUC normalization construct. (C) Schematic representation of effectors of GAL4BD plus the full-length orvarious truncated visions of NSG1. (D) and (E) Measurement of relative luciferase activity in rice transient assay.VP16, a transcriptional activator, was used as a positive control and GAL4-BD was regarded as a negative control. Barsand asterisks represent SD and significant difference at P < 0.01, Student’s t test.
Figure 6
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Figure 6. Expression Pattern of NSG1. GFP signal indicating NSG1 expression in transgenic complementary plants harboring the construct NSGP1:NSG1:GFP. (A) A whole young panicle (~1 cm length).(B) Several spikelets at developmental stages Sp4 to Sp7.(C) A spikelet at Sp6.(D) A spikelet at Sp7.(E) A primary branch of a panicle (~3.0 cm length).(F) Several spikelets at developmental stages Sp8 and post-Sp8.(G) A spikelet at Sp8.(H) A spikelet at post-Sp8.Bars = 50 μm.
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Figure 7. Expression Pattern of LHS1 gene in Spikelets of the Wild type and the nsg1-1 Mutant.A–D, I and M show expression of LHS1 in wild type spikelets, using in situ hybridization.E-H, J-L and N-P show expression of LHS1 in nsg1-1 spikelets, using in situ hybridization.A and E, B and F, C and G, D and H show longitudinal sections of spikelets at stages Sp5 to Sp8, respectively.I –L and M-P show transverse sections of basal region and middle region of spikelets at stages of Sp8, respectively.irg, inner rudimentary glume; isl, inner sterile lemma; le, lemma; mrp, marginal region of palea; osl, outer sterilelemma; pa, palea; sl, sterile lemma.Black type indicates the normal expression of genes, and red type indicates the ectopic or abnormal expression signalof genes. Bars = 50 μm.
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Figure 8. Direct Regulation of LHS1 Expression by NSG1.(A) Distribution of potential binding sites in the promoter and ORF regions of LHS1. Blue bars indicate the DNAfragments amplified in the ChIP assays. Red bars indicate the DBS-like motifs in the promoter of LHS1.(B) ChIP-qPCR for P1 site of LHS1 with anti-GFP antibody. ChIP enrichment compared with the input samplewas tested by qPCR. Error bars indicate SD of three repeats.(C) NSG1WT represses LHS1 expression in vivo. Tobacco leaves were transformed with p35Sm:LUC,p35Sm:LUC plus 35S:NSGWT, pLHS1P-35Sm:LUC, pLHS1P-35Sm:LUC plus 35S:NSGWT, or pLHS1P-35Sm:LUC plus 35S:NSGnsg1-1. Error bars indicate SD of three repeats.(D) NSG1 interacts with OsTPR1, OsTPR2 and OsTPR3 in yeast cells by a Y2H assay .(E) NSG1 interacts with OsTPR1, OsTPR2 and OsTPR3 in the nuclear of tobacco leave cells by a BiFC assay.(F) ChIP-qPCR for several sites of LHS1 with anti-H3K9ac antibody between WT panicles and nsg1-1 panicles.Error bars indicate SD of three repeats.(G) Model of NSG1 repressing the expression of LHS1 by recruiting TPRs-HDACs.
Figure 9
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Figure 9. Spikelet Phenotypes of the lhs1-z Single Mutants and the nsg1-1+lhs1-z Double Mutant.(A) Spikelets of the lhs1-z mutant. A1–A2, lhs1-z spikelet; the lemma and palea were removed in (A2). A3–A5,lhs1-z spikelet; the lemma and palea were removed in (A3). A4 and A5 show the surface characters of rg and sl,respectively. A6–A8, Transverse sections of lhs1-z spikelet; A7 and A8 show the anatomical structure of osl and isl,respectively.(B) Spikelets of the nsg1-1+lhs1-z mutant. B1–B2, nsg1-1+lhs1-z spikelet; the lemma and palea were removed in(B2).B3–B6, nsg1-1+lhs1-z spikelet. B4 to B6 show surface characters of the elongated irg, osl and isl, respectively. B7–B9, Transverse sections of nsg1-1+lhs1-z spikelet; B8 and B9 show the anatomical structure of irg, osl and isl,respectively.(C) Percentage of elongated or lemma-like organs in nsg1-1 spikelets.(D–F) qPCR analysis of LHS1, DL, and MFO1 expression in spikelets of nsg1-1, lhs1-z, nsg1-1+lhs1-z doublemutant. ACTIN was used as a control. RNA was isolated from rg and sl of nsg1-1, lhs1-z, nsg1-1+lhs1-z spikelets.Error bars indicate SD. At least three replicates were performed, from which the mean value was used to representthe expression level.irg, inner rudimentary glume; isl, inner sterile lemma; org, outer rudimentary glume; osl, outer sterile lemma; rg,rudimentary glume; sl, sterile lemma.Bars = 1,000 μm in *1, *2 and *3; 100 μm in *4, *5, B6; 100 μm in the other images.
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Figure 10. Roles of NSG1 in the Specification of Organ Identity in the Rice Spikelet.(A) In the wild type spikelet, G1, LHS1, DL, and MFO1 play pivotal roles in specification of lateral organ identities (G1for rg and sl; LHS1 for le; DL for le; and MFO1 for mrp and lo). NSG1 acts as a repressor to regulate the specificationof lateral organs, including rg, sl, mrp, lo, and st, by directly repressing LHS1 and DL, as well as MFO1, and indirectlyactivating G1 through LHS1. (1) indicates a study that suggests LHS1 represses G1 (Wang et al., 2017).(B) In the nsg1 spikelet, with the loss-of-function of NSG1, LHS1, DL, and MFO1 were ectopically expressed in the rg,sl, mrp, lo, or st, and G1 expression was under-regulated in the rg and sl, which led to transformation of other lateralorgans into lemma-like organs. In the nsg1-1+lhs1-z mutant, the lemma-like identity were lost completely in the nsg1-1sterile lemmas and rudimentary glumes, suggesting that ectopic LHS1 activation was an key cause of ectopic formationof lemma-like tissue in these organs. The gene symbols in green type show a normal expression domain, those in redtype show an ectopic expression domain, and those in grey type show an under-regulation expression domain.fi, filament; irg, inner rudimentary glume; isl, inner sterile lemma; le, lemma; le-like isl, lemma like inner rudimentaryglume; le-like mrp, lemma like marginal region of palea; le/mrp-like fi, lemma and/or marginal region of palea likefilament; le/mrp like lo, lemma and/or marginal region of palea like lodicule; le/mrp-like osl, lemma and/or marginalregion of palea like outer sterile lemma; lo, lodicule; mrp-like irg, marginal region of palea like inner rudimentaryglume; mrp, marginal region of palea; osl, outer sterile lemma.
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