SB1 Encoding RING-Like Zinc-Finger Protein Regulates Branch Development as a Transcription Repressor

doi:10.1016/j.rsci.2021.04.004

Abstract

Abstract:

Inflorescence structure of rice, including the number and length of branches, and the density of the spikelet, can greatly affect the number of grains per panicle, which is one of the key factors in yield compositions. Here we identified five allelic mutants sb1-1/2/3/4/5 that related to branch development of rice. In these mutants, the branch meristem fate was prolonged sharply, resulting in delay of transition from branches to spikelets, and then increased the numbers of branches and spikelets per panicle. SB1 encodes a nuclear RING-like domain protein of SHI/LRP/SRS family and strongly expressed in branch meristems. The results of protein interaction and chromatin immunoprecipitation further suggested that SB1 directly repressed the expression of DEP1, TAW1, MOC1 and IPA1 by interacting with a co-repressor complex to affect acetylation level of histone H3 on target regions. Thus, we proposed that SB1 is a transcription repressor of branch meristem activity by widely and negatively regulating a series of genes that maintain branch meristem fate.

Key words: branch development, grain number per panicle, rice, RING-like zinc-finger, transcription repressor, panicle arthitecture

Xiaoqin Zeng, Hui Zhuang, Qinglan Cheng, Jun Tang, Fayu Yang, Mingjiang Huang, Ziyi Wang, Zhongcheng Li, Honghui Zhu, Rui Chen, Guanghua He, Yunfeng Li. SB1 Encoding RING-Like Zinc-Finger Protein Regulates Branch Development as a Transcription Repressor[J]. Rice Science, 2021, 28(3): 243-256.

Figures/Tables 13

Fig. 1. Phenotypes of panicles in wild type (WT) and sb1-1/2/3/4/5 mutants. A, Panicles of the WT and sb1-1/2/3/4/5 mutants with spikelets on the branches. Bars are 5 cm. B, Panicles of the WT and sb1-1/2/3/4/5 mutants without spikelets on the branches. Bars are 5 cm. C?H, Numbers of primary branches per panicle (C), numbers of secondary branches per panicle (D), numbers of tertiary branches per panicle (E), numbers of spikelets per panicle (F), numbers of grains per panicle (G) and seed-setting rates (H) of WT and sb1-1/2/3/4/5.The wild type plants and sb1-1/2/3/4/5 mutants were grown in standard paddy field under conventional cultivation conditions. Data are Mean ± SD (n = 10). The Student’s t-test was used to generate the P values. **, P < 0.01.

Fig. S1. scanning electron microscopy analysis of young panicles of sb1-1 mutant and wild type. A, Wild type panicles. B, Magnified figure of A. C, sb1-1 panicles. D, Magnified figure of C.E, Expression of LAX1, RCN1, OSH1 and MOC3. bm, branch meristem; sm, spikelet meristem. Bars are 500μm. Data are Mean ± SD (n = 3). The Student’s t-test was used to generate the P values. *, P < 0.05, **, P < 0.01.

Fig. S2. Sequence of motifs predicted by MEME.

Fig. S3. Protein sequence analysis of SHI/LRP/SRS protein family in rice, maize and Arabidopsis thaliana.

Fig. 2. Map-based cloning of SB1. A, Fine mapping of SB1 on chromosome 9. B, Structure of SB1 and mutation sites of sb1-1/2/3/4/5. C, Structure of the SB1-GFP fusion complementary vector. D, Phenotypes of the wild type, sb1-1 and sb1-1-GFP transgenic plant. Bars are 5 cm.ORF, Open reading frame; SB1-comF and SB1-comR, Cloning primers of SB1 for complementary test.

Fig. 3. SB1 encodes a RING-like zinc finger protein.A, Phylogenetic tree analysis. The phylogenetic tree was constructed using the neighbor- joining method based on the Jone-Taylor- Thornton matrix-based model, and bootstrap support values calculated from 1 000 replicates are given at the branch nodes. At, Arabidopisis thaliana; Os, Oryza sativa; Zm, Zea mays. B, Location of conserved domains of the genes in the phylogeny tree.

Fig. S4. Subcellular location of SB1 by observing the GFP signal in SB1P:SB1: GFP transgenic plants. A, GFP signals in cells of branch meristem. B, DAPI signal in nucleus. C, Merged fluorescence signal of GFP and DAPI.Bars are 50 μm.

Fig. 4. Expression pattern of SB1. A, qPCR analysis of SB1 in root, shoot, leaf, sheath, tiller bud and panicles of different length. Panicles 1, 2 and 3 refer to panicles with the lengths of < 0.5, 0.5?1.0 and 1.1?2.0 cm, respectively. OsActin was used as a reference gene. Data are Mean ± SD (n = 3).B?M, GFP signal indicating SB1 expression in complementary transgenic plants harboring the construct SB1P: SB1:GFP. B and C, Panicles at the stage In2; D and E, Panicles at the stage In3; F and G, Panicles at the stage In4; H and I were the magnification figure of a PBM in F and G; J and K, Panicles at the stage In5; L and M were the magnification figure of a PBM in J and K. PBM, Primary branch meristem; SBM, Secondary branch meristem; SM, Spikelet meristem. In2, 3, 4 and 5 refer to the four inflorescence stages of rice during which the branch meristems formed. Bars are 100 μm.

Fig. 5. Interaction of SB1 with corepressors of OsSEU1 and OsLUG1. A, Autoactivation analysis of SB1 protein. PGBKT7-FZP was used as a positive control and PGBKT7-empty as a negative control. B, SB1 interacted with OsSEU1 and OsLUG1 in yeast cells by a yeast two- hybrid assay. C, SB1 interacted with OsSEU1 and OsLUG1 in epidermal cells of Nicotiana benthamiana by a bimolecular fluorescent complimentary (BiFC) assay. YFP, Yellow fluorescent protein; ChlA, Chlorophyll A; DAPI, 4’,6-diamidino-2-phenylindole. Bars are 20 μm.

Table S1. Interacting proteins of SB1 identified by yeast two-hybrid screening.

No.	ID	Description
1	Os09g0552800	No apical meristem protein, putative
2	Os12g0580700	Zinc finger, C3HC4 type domain containing protein
3	Os05g0103500	CHCH domain containing protein
4	Os03g0685600	WD40 repeat-like domain containing protein
5	Os01g0231000	OsIAA3 - Auxin-responsive Aux/IAA gene family member
6	Os02g0757100	Cell cycle gene
7	Os09g0567000	DUF1618 domain containing protein
8	Os02g0170500	Nuclear transcription factor Y subunit C
9	Os02g0261100	Licitor-responsive ubiquitin-conjugating enzyme
10	Os04g0510200	Transcriptional corepressor LEUNIG
11	Os06g0160400	Heading and grain weight regulat gene
12	Os02g0203000	bZIP transcription factor domain containing protein
13	Os04g0548000	Ethylene-responsive element-binding protein, putative
14	Os06g0142600	Heading date gene,
15	Os03g0177400	Elongation factor Tu
16	Os03g0192400	NADH dehydrogenase 1 alpha subcomplex subunit 13
17	Os02g0255500	Pyrabactin resistance-like abscisic acid receptor
18	Os04g0386900	Transcriptional factor B3 family protein
19	Os10g0575900	Expressed protein
20	Os05g0411300	bZIP transcription factor
21	Os04g0550600	Carotenoid cleavage dioxygenase
22	Os04g0615000	Narrow leaf NAL1,
23	Os05g0573500	Nuclear transcription factor Y subunit B
24	Os07g0600400	WD repeat-containing protein 12
25	Os06g0126000	Transcriptional corepressor SEUSS
26	Os02g0170500	Nuclear transcription factor Y subunit C
27	Os09g0369050	Similar to DRE binding factor 2
28	Os03g0775500	Expressed protein
29	Os02g0723700	SWI/SNF-related regulator
30	Os02g0122000	Histone deacetylase complex subunit SAP18
31	Os03g0122100	Helix-loop-helix DNA-binding domain containing protein

Fig. 6. SB1 directly repressed expression of DEP1, TAW1, MOC1 and IPA1. A, Binding peaks of SB1 with DEP1, TAW1, MOC1 and IPA1 by chromatin immunoprecipitation-sequence (ChIP-seq) using an anti-GFP antibody.B, Relative expression of DEP1, TAW1, MOC1 and IPA1 in the wild type (WT) and sb1 panicles, respectively.C, ChIP-qPCR for P1 and P2 sites of DEP1, TAW1, MOC1 and IPA1 with anti-GFP antibody, respectively. ChIP enrichment compared with the input sample was tested by qPCR. D, ChIP-qPCR for several sites of DEP1, TAW1, MOC1 and IPA1 with a H3K9Ac antibody, respectively. ChIP enrichment compared with the IgG sample was tested by qPCR.Pro, Promoter; P1 to P6 represent primers for ChIP-qPCR. Error bars indicated SD of three repeats. The Student’s t-test was used to generate the P values. *, P < 0.05; **, P < 0.01.

Fig. 7. Model of SB1 gene regulating rice panicle architecture. In the wild type plants, SB1 interacts with the corepressors OsSEU1 and OsLUG1 to form the repression complex and repress DEP1, TAW1, MOC1 and IPA1 by downregulating the acetylation levels of histone on chromosome. In the sb1-1/2/3/4/5 mutants, the repression complex cannot work, resulting in the increased acetylation levels and the expression levels of DEP1, TAW1, MOC1 and IPA1, which enables the formation of the increased numbers of branches and spikelets.HDACs, Histone deacetylases; BM, Branch meristem; PB, Primary branch; SB, Secondary branch; TB, Tertiary branch.

Table S2. Primers used in the study.

Purpose	Primer name	Sequence
Mapping	SSR1-F	CAGTGGCGTGGAGAGAAATTTGG
	SSR1-R	CTCACCTGCGACAGCAAGATCG
	SSR2-F	TGAGCACCATGCAATAACTGTCG
	SSR2-R	ACCATCTATCGCCACATCTCACC
	SNP-1-F	CGGGACATTCTTAGCTTTGCTTTGAT
	SNP-1-R	GAAAGTAGTAGTCTCACCATGCTTTGCCAC
	SNP-2-F	CCCACACTGACTGGGACTCACTCG
	SNP-2-R	GATTAGCGTCTCGTCCTCGCAGC
Candidate gene cloning	SB1-F	GCAATGGCACAAGTGACACTACAAGA
	SB1-R	CTCCGATCAGTTCACGCAAAGTCG
Complementation test	SB1-com-F	GTATTTGTCTGTGCTGGATCCGTGTGCGAAGGGATACATGATGAAGC
	SB1-com-R	CGCCCTTGCTCACCATACTAGTCGGCCGCGGGTGGCC
qPCR	Actin-F	TGCTATGTACGTCGCCATCCAG
	Actin-R	AATGAGTAACCACGCTCCGTCA
	RT-SB1-F	AACGCCACTACAATCTCTCACTCGC
	RT-SB1-R	AGTCTAAAGGGTTCGCCTGCCTAA
	RT- MOC1-F	CTGTGGTTGCATGACACAGATGCAC
	RT- MOC1-R	CCTTGGATGGAATGTCTCAGTCCC
	RT- DEP1-F	CCGTTTCTCGTTCTGGAT
	RT- DEP1-R	ATCTGTGCCTCCTTCTCT
	RT-IPA1-F	TCTTCTGTCAACCCAGCCAT
	RT-IPA1-R	GCCATCAAAGCTGGTGGTAG
	RT-TAW1-F	GACTGGAACACGTTCGGGCAGTAC
	RT-TAW1-R	CACCTTGGTCTTGCCGAACTGGT
	RT-LAX1-F	TGACGACGCTGGAGATGGCG
	RT-LAX1-R	GGAGGCAGCTGATGAGCGCC
	RT-RCN11-F	GACAGCAACCTGCTCAAGGTCATCTC
	RT-RCN1-R	GCTGGTCGATTAGCTCCTTCACCC
	RT-OSH1-F	CAGGACCTGGAGCTTCGCCAG
	RT-OSH1-R	GGAGAGCGTGTTGAGCTGCGTCT
	RT-MOC3-F	GGATCAGGCCAACGTCGTCAACT
	RT-MOC3-R	CGACTGGGAAGAGTGGAAGCGTCT
Two-Hybrid System	SB1-BD-F1	ATGGGCAGCGGCGGCGGT
	SB1-BD-R1	GAACATCCCACGGTTTGGAGGTT
	SEU-AD-F1	ATGTCCAACCTCCAAACCGTGGG
	SEU-AD-R1-	CTAAGATCCACAGATGGACATGGAGAG
	LEU-AD-F1	ATGTCGTCGCTCAGCCGGGAG
	LEU-AD-R1	CTATCTTTGGATTTGGTCTGCAGCT
BiFC assay	SB1-YC-F	CAATTACAGGTACCCGGGGATCCATGGCGGGGTTCCCTCTAGGC
	SB1-YC-R	TGCACGCTGCCACCGCCGTCGACCGGCCGCGGGTGGCCGTGGAA
	OsLUG1-YN-F	CATCGAGGACGCCGGCGGATCCATGGCGCAGAGCAACTGGGAAG
	OsLUG1-YN-R	GAACGAAAGCTCTGCAGGTCGACCTTCCACAGCTTGACAGAGTTGTCG
	OsSEU1-YN-F	CATCGAGGACGCCGGCGGATCCATGTCTGGGGCGCCATGCTC
	OsSEU1-YN-R	GAACGAAAGCTCTGCAGGTCGACCATGTTCCATGAGTAGCCACCACCT
ChIP-qPCR	DEP1-P1-F	CGCCCACACACAACACAGCTAG
	DEP1-P1-R	GACCGGGAACACACGTTGTCA
	DEP1-P2-F	AGCTCAACTGAACGCTGGCTG
	DEP1-P2-R	CCACCACTGCTGCTACTGCCTA
	DEP1-P3-F	ACGAAGGATCGGCTTTGCAT
	DEP1-P3-R	CGAGCCTACGTTGGATACGCT
	DEP1-P4-F	GGAGCTACCCGCTACTGCAAG
	DEP1-P4-R	CGTGATTCACCTCCGCCTAGA
	DEP1-P5-F	CCTGCATCATAACGTTCCTAGTGGT
	DEP1-P5-R	CTCAGGACTGTGAGCTGTAATATGG
	DEP1-P6-F	GCTGTAGTCCAGACTGCTGCTCATG
	DEP1-P6-R	GTTGCACTGGGACTTGAAGCATG
	TAW1-P1-F	TGGACCAGTTCGGCAAGACCAAG
	TAW1-P1-R	TGCTCGCGGACCTCGCGGAGGTAG
	TAW1-P2-F	TCGAGTCATGTCAGCACTGTGGC
	TAW1-P2-R	GCATCACTCTCTTAACGCTGCTGC
	TAW1-P3-F	TCTCTCTCTCTCTTGGACCACTGCG
	TAW1-P3-R	CGAACTCCATCGTCGATCTGCAC
	TAW1-P4-F	CGAGCAGGTACGAGTCGCAGAAG
	TAW1-P4-R	CTTGGTCTTGCCGAACTGGTCC
	TAW1-P5-F	ACTCCACTCCACTCCACTCCACTATG
	TAW1-P5-R	TAGTAGACGAGACGACGTGCGAGAG
	TAW1-P6-F	CTCTCTCTCTGCTGCTGCAACAAG
	TAW1-P6-R	CTGCCTGACTGACTGACTCTCTCTG
	MOC1-P1-F	GAGTGGCACTTGCTACTGTGCATG
	MOC1-P1-R	TGATGATGGCCTCCAGATAACTTCC
	MOC1-P2-F	TATGGCACAAACAGTCACAGCTGC
	MOC1-P2-R	TGCTCATTCCTTGATGAGAGAGTGAG
	MOC1-P4-F	GTGGAGAGCCGGAATCAACACTGT
	MOC1-P4-R	GACATATAATGATACTCCGGCCATCTC
	MOC1-P5-F	GCTGGGATTGCACAGTGAAGCTAG
	MOC1-P5-R	GCACGTCCAACATCTGGGCTT
	MOC1-P6-F	TACCTGGCGTTCAACCAGATCG
	MOC1-P6-R	CGTCGAGGTCGAGGATGTGGAC
	IPA1-P1-F	GAGTGGCACTTGCTACTGTGCATG
	IPA1-P1-R	TGATGATGGCCTCCAGATAACTTCC
	IPA1-P2-F	TATGGCACAAACAGTCACAGCTGC
	IPA1-P2-R	TGCTCATTCCTTGATGAGAGAGTGAG
	IPA1-P3-F	CCAGTTACAACCCTCCACCATTCAC
	IPA1-P3-R	TGTGGCAGTGCCCACAGTGTGT
	IPA1-P6-F	GACGTGGCGTGTGGCAATGTAG
	IPA1-P6-R	TACTCCGACGAGCCTCCTTTCTCT

Table S2. Primers used in the study.

Purpose	Primer name	Sequence
Mapping	SSR1-F	CAGTGGCGTGGAGAGAAATTTGG
	SSR1-R	CTCACCTGCGACAGCAAGATCG
	SSR2-F	TGAGCACCATGCAATAACTGTCG
	SSR2-R	ACCATCTATCGCCACATCTCACC
	SNP-1-F	CGGGACATTCTTAGCTTTGCTTTGAT
	SNP-1-R	GAAAGTAGTAGTCTCACCATGCTTTGCCAC
	SNP-2-F	CCCACACTGACTGGGACTCACTCG
	SNP-2-R	GATTAGCGTCTCGTCCTCGCAGC
Candidate gene cloning	SB1-F	GCAATGGCACAAGTGACACTACAAGA
	SB1-R	CTCCGATCAGTTCACGCAAAGTCG
Complementation test	SB1-com-F	GTATTTGTCTGTGCTGGATCCGTGTGCGAAGGGATACATGATGAAGC
	SB1-com-R	CGCCCTTGCTCACCATACTAGTCGGCCGCGGGTGGCC
qPCR	Actin-F	TGCTATGTACGTCGCCATCCAG
	Actin-R	AATGAGTAACCACGCTCCGTCA
	RT-SB1-F	AACGCCACTACAATCTCTCACTCGC
	RT-SB1-R	AGTCTAAAGGGTTCGCCTGCCTAA
	RT- MOC1-F	CTGTGGTTGCATGACACAGATGCAC
	RT- MOC1-R	CCTTGGATGGAATGTCTCAGTCCC
	RT- DEP1-F	CCGTTTCTCGTTCTGGAT
	RT- DEP1-R	ATCTGTGCCTCCTTCTCT
	RT-IPA1-F	TCTTCTGTCAACCCAGCCAT
	RT-IPA1-R	GCCATCAAAGCTGGTGGTAG
	RT-TAW1-F	GACTGGAACACGTTCGGGCAGTAC
	RT-TAW1-R	CACCTTGGTCTTGCCGAACTGGT
	RT-LAX1-F	TGACGACGCTGGAGATGGCG
	RT-LAX1-R	GGAGGCAGCTGATGAGCGCC
	RT-RCN11-F	GACAGCAACCTGCTCAAGGTCATCTC
	RT-RCN1-R	GCTGGTCGATTAGCTCCTTCACCC
	RT-OSH1-F	CAGGACCTGGAGCTTCGCCAG
	RT-OSH1-R	GGAGAGCGTGTTGAGCTGCGTCT
	RT-MOC3-F	GGATCAGGCCAACGTCGTCAACT
	RT-MOC3-R	CGACTGGGAAGAGTGGAAGCGTCT
Two-Hybrid System	SB1-BD-F1	ATGGGCAGCGGCGGCGGT
	SB1-BD-R1	GAACATCCCACGGTTTGGAGGTT
	SEU-AD-F1	ATGTCCAACCTCCAAACCGTGGG
	SEU-AD-R1-	CTAAGATCCACAGATGGACATGGAGAG
	LEU-AD-F1	ATGTCGTCGCTCAGCCGGGAG
	LEU-AD-R1	CTATCTTTGGATTTGGTCTGCAGCT
BiFC assay	SB1-YC-F	CAATTACAGGTACCCGGGGATCCATGGCGGGGTTCCCTCTAGGC
	SB1-YC-R	TGCACGCTGCCACCGCCGTCGACCGGCCGCGGGTGGCCGTGGAA
	OsLUG1-YN-F	CATCGAGGACGCCGGCGGATCCATGGCGCAGAGCAACTGGGAAG
	OsLUG1-YN-R	GAACGAAAGCTCTGCAGGTCGACCTTCCACAGCTTGACAGAGTTGTCG
	OsSEU1-YN-F	CATCGAGGACGCCGGCGGATCCATGTCTGGGGCGCCATGCTC
	OsSEU1-YN-R	GAACGAAAGCTCTGCAGGTCGACCATGTTCCATGAGTAGCCACCACCT
ChIP-qPCR	DEP1-P1-F	CGCCCACACACAACACAGCTAG
	DEP1-P1-R	GACCGGGAACACACGTTGTCA
	DEP1-P2-F	AGCTCAACTGAACGCTGGCTG
	DEP1-P2-R	CCACCACTGCTGCTACTGCCTA
	DEP1-P3-F	ACGAAGGATCGGCTTTGCAT
	DEP1-P3-R	CGAGCCTACGTTGGATACGCT
	DEP1-P4-F	GGAGCTACCCGCTACTGCAAG
	DEP1-P4-R	CGTGATTCACCTCCGCCTAGA
	DEP1-P5-F	CCTGCATCATAACGTTCCTAGTGGT
	DEP1-P5-R	CTCAGGACTGTGAGCTGTAATATGG
	DEP1-P6-F	GCTGTAGTCCAGACTGCTGCTCATG
	DEP1-P6-R	GTTGCACTGGGACTTGAAGCATG
	TAW1-P1-F	TGGACCAGTTCGGCAAGACCAAG
	TAW1-P1-R	TGCTCGCGGACCTCGCGGAGGTAG
	TAW1-P2-F	TCGAGTCATGTCAGCACTGTGGC
	TAW1-P2-R	GCATCACTCTCTTAACGCTGCTGC
	TAW1-P3-F	TCTCTCTCTCTCTTGGACCACTGCG
	TAW1-P3-R	CGAACTCCATCGTCGATCTGCAC
	TAW1-P4-F	CGAGCAGGTACGAGTCGCAGAAG
	TAW1-P4-R	CTTGGTCTTGCCGAACTGGTCC
	TAW1-P5-F	ACTCCACTCCACTCCACTCCACTATG
	TAW1-P5-R	TAGTAGACGAGACGACGTGCGAGAG
	TAW1-P6-F	CTCTCTCTCTGCTGCTGCAACAAG
	TAW1-P6-R	CTGCCTGACTGACTGACTCTCTCTG
	MOC1-P1-F	GAGTGGCACTTGCTACTGTGCATG
	MOC1-P1-R	TGATGATGGCCTCCAGATAACTTCC
	MOC1-P2-F	TATGGCACAAACAGTCACAGCTGC
	MOC1-P2-R	TGCTCATTCCTTGATGAGAGAGTGAG
	MOC1-P4-F	GTGGAGAGCCGGAATCAACACTGT
	MOC1-P4-R	GACATATAATGATACTCCGGCCATCTC
	MOC1-P5-F	GCTGGGATTGCACAGTGAAGCTAG
	MOC1-P5-R	GCACGTCCAACATCTGGGCTT
	MOC1-P6-F	TACCTGGCGTTCAACCAGATCG
	MOC1-P6-R	CGTCGAGGTCGAGGATGTGGAC
	IPA1-P1-F	GAGTGGCACTTGCTACTGTGCATG
	IPA1-P1-R	TGATGATGGCCTCCAGATAACTTCC
	IPA1-P2-F	TATGGCACAAACAGTCACAGCTGC
	IPA1-P2-R	TGCTCATTCCTTGATGAGAGAGTGAG
	IPA1-P3-F	CCAGTTACAACCCTCCACCATTCAC
	IPA1-P3-R	TGTGGCAGTGCCCACAGTGTGT
	IPA1-P6-F	GACGTGGCGTGTGGCAATGTAG
	IPA1-P6-R	TACTCCGACGAGCCTCCTTTCTCT

References 52

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