Scientia Agricultura Sinica ›› 2021, Vol. 54 ›› Issue (11): 2273-2286.doi: 10.3864/j.issn.0578-1752.2021.11.003

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Characterizations of Transcriptional and Haplotypic Variations of SiTOC1 in Foxtail Millet

ZHANG LinLin(),ZHI Hui,TANG Sha,ZHANG RenLiang,ZHANG Wei,JIA GuanQing(),DIAO XianMin()   

  1. Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081
  • Received:2020-11-09 Accepted:2020-12-07 Online:2021-06-01 Published:2021-06-09
  • Contact: GuanQing JIA,XianMin DIAO E-mail:657044121@qq.com;jiaguanqing@caas.cn;diaoxianmin@caas.cn

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Abstract:

【Objective】 Identification of allelic variations of heading date adaptation related genes and laying foundation for breeding of wide-adapted varieties in foxtail millet. 【Method】In this trial, a vital regulator of heading time in foxtail millet, SiTOC1, was identified using genome-wide association analysis. Spatio-temporal transcription (multi-omics database for Setaria italica,MDSi), sub-cellular localization and 24 hours rhythm expression pattern of SiTOC1 was analyzed. Sequence variations of both promoter and encoding regions in SiTOC1 and relationships between haplotypic variations and heading date were characterized in 99 foxtail millet accessions. 【Result】A significant GWAS signal (Position: 31 456 761 bp) was detected on Chromosome 1 and only one TOC1 homologue was identified (SiTOC1). SiTOC1 highly expressed in root, stem and leaf, and located into cell nucleus. An elevated expression of SiTOC1 was identified at dusk across whole day transcription survey under short-day environment. Many haplotypic variations of SiTOC1 were identified but REC and CCT domains of SiTOC1 were conserved in foxtail millet accessions, and two main haplotypes including H-2 and H-6 in protein encoding regions combined with two co-segregated haplotypes including Hp-591C and Hp-591A were identified. Nearly 2.5 times higher expression of Hp-591C haplotype combined with 9,11 and 12 days delay of heading time through Hainan, Changzhi and Urumuqi were observed. 【Conclusion】The major haplotype Hp-591A identified at 591 bp in the promoter region of SiTOC1 matures earlier than Hp-591C and could be selected as a main effective locus for molecular breeding of foxtail millet.

Key words: Setaria italica, heading time, genome-wide association study, haplotype, genetic variation, rhythmic expression

Table 1

PCR amplification and sequencing primers for SiTOC1 subcellular localization vector’s construction"

载体
Vector		 引物名称
Primer name		 引物序列
Primer sequence (5′-3′)		 产物长度
Product length (bp)
GFP-N
端载体
GFP-N terminal
vector		 GFPG5-F1 GCTGTACAAGACTAGTATGGTGGGCGGCGGCG 1517
GFPG5-R1 GGGGAAATTCGAGCTCCTACTCTGGAGAAGAAATAATC
PUCGFPN-TestF TACAACTACAACAGCCACAA 2163
PUCGFPN-TestR CCTCTTCGCTATTACGC
GFPG5-F1.1 CCATCATCATGATGTCC
GFPG5-R1.1 TTCAGAGCGACTGCATG
GFP-C端载体
GFP-C terminal
vector		 G5GFP-F1 TAGTGGATCCATCGATATGGTGGGCGGCGGCG 1514
G5GFP-R1 TCCCGGGAGCGGTACCCTCTGGAGAAGAAATAATCTC
PUCGFPC-TestF ACCTCCTCGGATTCCAT 2354
PUCGFPC-TestR TGCCGTTCTTCTGCTTG
G5GFP-F1.1 CAAGATGCTCAAGTACA
G5GFP-R1.1 CGATTTACATACCTCACT
RFP-N端载体
RFP-N terminal
vector		 MYBRFP-F GCTGTACAAGACTAGTATGGACATGGCGCACGAGAG 1022
MYBRFP-R GGGGAAATTCGAGCTCTCACACGGCGGCCTGGGT
PUCRFPN-TestF CTCAAGCTCAAGGACGG 1584
PUCRFPN-TestR CCTCTTCGCTATTACGC

Table 2

Primers for amplication and sequencing of SiTOC1"

产物Product 引物名称 Primer name 引物序列 Primer sequence (5′-3′) 产物长度 Product length (bp)
编码区
Coding region		 G5-F1 GATCCAGCGACAGTCCA 1450
G5-R1 AGACAGGTCGGACTGAAATA
G5-F2 GATGAGTTGCCACAAAGATG 1272
G5-R2 TGTATTGCCTTTCCCAGTAG
启动子区
Promoter region		 G5P-F1 GGCCAAACGAAACCATG 2069
G5P-R1 CCTAATCCGGGAAACCAG
G5P-F1.1 ATTGCGTGCACGAATCT
G5P-R1.1 CAGCAGCAGCCTGCCTCG
SiTOC1互补DNA
SiTOC1 cDNA		 G5Q-F1 GCCGATCAAGCATCATATGTTAAGT 250
G5Q-R1 TTTGGCCTTCATTGCTTCGC
Cullin互补DNA
Cullin cDNA		 Cullin-F TATGGGTCATCAACAGCTTGTC 112
Cullin-R GTAGTCCCTCGTGATGAGATCC

Fig. 1

GWAS analysis of SiTOC1 A: Results of SiTOC1 GWAS; B: Candidate gene in the associated locus range"

Table 3

Annotation of candidate gene"

位点名称 LocusName 拟南芥对应基因 Arabi-symbol 拟南芥基因功能注释 Arabi-defline
Seita.1G235800 N/A 无功能注释N/A
Seita.1G235900 MKM21.12 线粒体核糖体蛋白L27 Mitochondrial ribosomal protein L27
Seita.1G236000 N/A 谷氧还蛋白家族 Glutaredoxin family protein
Seita.1G236100 TOC1 含CCT基序的应答调节蛋白 CCT motif-containing response regulator protein
Seita.1G236200 PAP10 紫色酸性磷酸酶10 Purple acid phosphatase 10
Seita.1G236300 NOP10 核仁RNA结合Nop10p家族蛋白 Nucleolar RNA-binding Nop10p family protein
Seita.1G236400 AtMYB79 含MYB结构域蛋白79 MYB domain protein 79

Fig. 2

Gene structure and homologous protein phylogenetic tree of SiTOC1 A: Gene structure of SiTOC1; B: Homologous protein's phylogenetic tree and gene structure of SiTOC1. GRMZM2G020081_T01: Zea mays; Sobic.004G216700.1: Sorghum bicolor; Sevir.1G241000.1: Setaria viridis; Seita.1G236100.1 (SiTOC1): Setaria italica (L); LOC_Os02g40510.1: Oryza sativa; Traes_6AL_A0A31AA9F.1: Triticum aestivum; AT5G61380.1: Arabidopsis thaliana; Gorial.003G098300.2: Gossypium raimondii; Glyma.06G196200.1: Glycine max; Medtr4g108880.2: Medicago truncatula"

Fig. 3

The expression pattern and subcellular location of SiTOC1 A: Tissue-specific analysis of SiTOC1: a: Plant during one-tip-two-leaf; b: Neck panicle internodes during filling stage; c: Flag leaf during filling stage; d: Flag leaf sheath during filling stage; e: Stem of top second during Filling stage; f: Leaf of top-fourth during filling stage; g: Leaf sneath of top fourth during filling stage; h: Root during filling stage; i: Immature spikelet during early development stage; j: Immature spikelet during late development stage; k: Leaf veins; l: Mesophyll. B: Subcellular localization of SiTOC1, the RFP field shows RFP signals of 35S∷RFP∶OsMYB2, bar=10 μm"

Fig. 4

Rhythm expression pattern of SiTOC1 in short day The white part of top bar frame represents the time of light (7：00-17：00), the black part of top bar frame represents the time of dark(17：00-7：00)"

Fig. 5

Variations detected in SiTOC1 coding region Top of the figure is SiTOC1 gene coding region structure, the boxes represent exons, and the connecting lines between the boxes represent introns, the lower part corresponds to the different haplotype combination information table, the solid line connected to the gene structure diagram of the SiTOC1 coding region above indicates the mutation site, the red connecting line indicates the non-synonymous mutation, the different colored cells in the table represent different bases, the green, yellow, blue and red cells represent G, A, C, T bases, respectively, -: Stands for deletion, +: Stands for insertion, the number after the symbol stands for the number of bases deleted or inserted, the Indel position from left to right is: 330(+6)/+gtgctg, 336(+5)/+ atgct, 353(+1)/+t, 398(+1) /+t, 524(+1)/+t, 661(+1)/+g, 807(+11)/+gtgggttgctt, 1099(+ 1)/+c, 1359(+1)/+t, 1381(+5)/+taatc, 1437(+1)/+t"

Fig. 6

Relationships between SiTOC1 haplotypes detected in coding region SiTOC1 haplotype network diagram of coding region, different solid circles represent different haplotypes, the area of the circle is proportional to the number of species contained in the corresponding haplotype, the black connecting lines represent the mutation steps of different haplotypes, and the red circles on the connecting lines dots represent mutation steps more than once"

Fig. 7

SiTOC1 promoters’s haplotype derivation diagram and transcription analysis A: SiTOC1 haplotype network diagram of promoter; B-C: Relative expression analysis of SiTOC1 promoter haplotypes, P=0.014. *: Reach a significant difference at P<0.05. The same as below"

Fig. 8

Analysis on the significant differences of haplotypes’s heading time of SiTOC1’s coding region and promoter **: Reach a highly significant difference at P<0.01. A: Analysis on the significant differences of haplotype’s heading time of SiTOC1’s coding region, 2010 Sanya P=0.0180, 2016 Changzhi P=0.0290, 2016 Urumuqi P=0.0089; B: Analysis on the significant differences of haplotype’s heading time of SiTOC1’s promoters, 2010 Sanya P=0.0262, 2016 Changzhi P=0.0106, 2016 Urumuqi P=0.0257"

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