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Acta Agronomica Sinica ›› 2019, Vol. 45 ›› Issue (4): 499-507.doi: 10.3724/SP.J.1006.2019.83068

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

Identification of indeterminate domain protein family genes associated with flowering time in maize

Yun-Fu LI1,2,Jing-Xian WANG1,Yan-Fang DU1,Hua-Wen ZOU2,Zu-Xin ZHANG1,*()   

  1. 1 National Key Laboratory of Crop Genetic Improvement / Huazhong Agricultural University, Wuhan 430070, Hubei, China
    2 College of Agronomy, Yangtze University, Jingzhou 434000, Hubei, China
  • Received:2018-11-01 Accepted:2019-01-12 Online:2019-04-12 Published:2019-01-31
  • Contact: Zu-Xin ZHANG E-mail:zuxinzhang@mail.hza
  • Supported by:
    This study was supported by the National Natural Science Foundation of China(31871628)

Abstract:

Flowering time is one of the important factors affecting grain yield in maize (Zea mays L.). Indeterminate1 (ID1) is a known gene encoding indeterminate domain (IDD) protein which controls flowering time of maize. However, biological functions of the other IDD family genes are little known. In this study, we identified 37 IDD family genes, referred to as ZmIDDs by searching conserved IDD domains using bioinformatics strategy, and we then isolated these ZmIDDs by amplifying B73 genome using PCR. Diverse expression patterns of these ZmIDDs were revealed in eight tissues using B73 transcriptome data deposited in public database MaizeGDB (www.maizeGDB.org). In addition, we found that 35 ZmIDDs showed abundant genetic diversity with an average of 37.8 polymorphic loci per gene in 172 inbred lines, and seven ZmIDDs including ID1 were significantly associated with three flowering time-traits: days to tassel, days to anthesis and days to silking under multiple environments. We resequenced a 2 kb promoter region and 600 bp coding region of Zm00001d020683, and found 64 variants within 172 inbred lines. Candidate gene association analysis identified that two variants at promoter region were significantly associated with flowering time, and the haplotype composed of 3 bp and 2 bp insertion at the two associated loci showed an effect of shortening flowering time. The results provide a subset of flowering time-related candidate genes for further function assay and genetic improvement of flowering time in maize.

Key words: maize (Zea mays L.), flowering time, indeterminate domain (IDD) protein, association analysis, resequencing

Fig. 1

Gene structures and putative conserved motifs of IDD family genes in maize Gene structures are showed by the GSDS2.0. Putative conserved motifs of IDD family proteins are predicted by the MEME program. Black box: motif 1; gray box: motif 2; white box: motif 3."

Fig. 2

Phylogenetic tree of IDD proteins in Zea mays and Arabidopsis thaliana The phylogenetic tree is constructed by Neighbor-Joining method with 1000 bootstraps based on the amino acid sequence of IDD proteins in Zea mays and Arabidopsis thaliana."

Fig. 3

Expression patterns of 37 maize IDD family genes Color boxes show the expression level of maize IDD family genes. RNA-sequencing is showed by FPKM (fragments per kilobase of exon per million fragments mapped)."

Table 1

Genetic variations of IDD family genes and their associations with flowering time in maize"

基因
Gene
染色体
Chr.
数目
No.
显著性水平Significance level P<0.01 显著性水平Significance level P<0.00075 P<0.00075
环境1 Env1 环境2 Env2 环境2 Env2 BLUP 环境1 Env1 环境2 Env2 环境2 Env2 BLUP
Zm00001d032922 1 18 5/7/5 7/7/7 7/8/8 3/3/3 1/1/1 1/1/1 5/3/5 2/2/1
Zm00001d005566 2 14 7/7/7 7/7/6 6/7/6 1/1//1 6/2/6 4/2/5 5/0/5 0
Zm00001d039467 3 36 7/4/4 6/3/3 6/2/2 2/2/0 6/2/0 5/1/1 0 0
Zm00001d044261 3 25 4/2/2 3/3/3 3/3/3 0 2/2/0 2/2/2 0 0
Zm00001d020683 7 31 4/3/3 3/5/5 7/4/5 3/3/3 2/2/2 3/3/3 1/1/1 1/1/1
Zm00001d011223 8 39 0 2/3/3 4/4/4 0 0 1/1/0 0/1/1 0
Zm00001d023558 10 80 12/11/13 10/9/9 9/9/9 1/1/2 4/4/2 3/4/2 7/2/5 0/1/1

Fig. 4

Association analysis of candidate gene A) Association of variants at Zm00001d020683 with maize flowering time in the association panel, and linkage disequilibrium block among variants at Zm00001d020683. B) Comparison of flowering time between haplotypes. Hap1: 0 + 0 haplotype. Hap3: 3 bp + 0 haplotype. Hap4: 3 bp + 2 bp haplotype. DTT: days to tassel; DTA: days to anthesis; DTA: days to silking. * P < 0.05; **P < 0.01."

[1] Matsuoka Y, Vigouroux Y, Goodman M M, Sanchez G J, Buckler E, Doebley J . A single domestication for maize shown by multilocus microsatellite genotyping. Proc Natl Acad Sci USA, 2002,99:6080-6084.
doi: 10.1073/pnas.052125199 pmid: 11983901
[2] 李玉玲, 李学慧, 董永彬, 牛素贞, 刘艳阳, 王延召 . 利用相同来源F2:3和BC2S1群体定位玉米开花期QTL. 华北农学报, 2007,22:38-43.
Li Y L, Li X H, Dong Y B, Niu S Z, Liu Y L, Wang Y Z . QTL mapping of developmental stages using F2:3 and BC2S1 populations derived from the same cross in maize. Acta Agric Boreali-Sin, 2007,22:38-43 (in Chinese with English abstract).
[3] 兰进好, 李新海, 高树仁 . 不同生态环境下玉米产量性状QTL分析. 作物学报, 2005,31:1253-1259.
Lan J H, Li X H, Gao S R . QTL analysis of yield components in maize under different environments. Acta Agron Sin, 2005,31:1253-1259 (in Chinese with English abstract).
[4] Chardon F, Vklon B, Moreau L, Falque M, Joets J, Decousset L, Murigneux A, Chareosset A . Genetic architecture of flowering time in maize as inferred from quantitative trait loci meta- analysis and synteny conservation with the rice genome. Genetics, 2004,168:2169-2185.
doi: 10.1534/genetics.104.032375 pmid: 15611184
[5] Dong Z, Danilevskaya O, Abadie T, Messina C, Coles N, Cooper M . A gene regulatory network model for floral transition of the shoot apex in maize and its dynamic modeling. PLoS One, 2002,7:e43450.
[6] Meng X, Muszynski M G, Danilevskaya O N . The FT-like ZCN8 gene functions as a floral activator and is involved in photoperiod sensitivity in maize. Plant Cell, 2010,23:942-960.
[7] Danilevskaya O, Meng X, Ananiev E . Concerted modification of flowering time and inflorescence architecture by ectopic expression of TFL1-Like genes in maize. Plant Physiol, 2010,153:238-251.
doi: 10.1104/pp.110.154211
[8] Huang C, Sun H, Xu D, Chen Q, Liang Y, Wang X, Xu G, Tian F . ZmCCT9 enhances maize adaptation to higher latitudes. Proc Natl Acad Sci USA, 2018,115:E334-E341.
[9] Ducrocq S, Giauffret C, Madur D, Combes V, Dumas F, Jouanne S, Coubriche D, Jamin P, Moreau L, Charcosset A . Fine mapping and haplotype structure analysis of a major flowering time quantitative trait locus on maize chromosome 10. Proc Natl Acad Sci USA, 2009,183:1555-63.
doi: 10.1534/genetics.109.106922 pmid: 19822732
[10] Yang Q, Li Z, Li W, Ku L, Wang C, Ye J, Li K, Yang N, Li Y, Zhong T, Li J, Chen Y, Yan J, Yang X, Xu M . CACTA-like transposable element in ZmCCT attenuated photoperiod sensitivity and accelerated the post do mestication spread of maize. Proc Natl Acad Sci USA, 2013,15:16969-16974.
[11] Hung H Y, Shannon L M, Tian F, Bradbury P J, Chen C ,Flint-GarciaS A,McMullen M D,Ware D, Buckler E S, Doebley J F, Holland J B . ZmCCT and the genetic basis of day-length adaptation underlying the postdomestication spread of maize. Proc Natl Acad Sci USA, 2012,109:E1913-1921.
[12] Lawit S J, Wych H M, Xu D, Kundu S, Tomes D T . Maize DELLA proteins dwarf plant8 and dwarf plant9 as modulators of plant development. Plant Cell Physiol, 2010,51:1854-1868.
[13] Thornsberry J, Goodman M, Doebley J, Kresovich S, Nielsen D , Buckler E S 4th. Dwarf8 polymorphisms associate with variation in flowering time. Nat Genet, 2001,28:286-289.
[14] Bolduc N, Hake S . The maize transcription factor KNOTTED1 directly regulates the gibberellin catabolism gene ga2ox1. Plant Cell, 2009,21:1647-1658.
doi: 10.1105/tpc.109.068221
[15] Muszynski M, Dam T, Li B, Shirbroun D, Hou Z, Bruggemann E, Archibald R, Ananiev E V, Danilevskaya O N . delayed flowering1 encodes a basic leucine zipper protein that mediates floral inductive signals at the shoot apex in maize. Plant Physiol, 2006,142:1523-1536.
doi: 10.1104/pp.106.088815 pmid: 17071646
[16] Salvi S, Sponza G, Morgante M, Tomes D, Niu X, Fengler K A, Meeley R, Ananiev E V, Svitashev S, Bruggemann E, Li B, Hainey C F, Radovic S, Zaina G, Rafalski J A, Tingey S V, Miao G H, Phillips R L, Tuberosa R . Conserved noncoding genomic sequences associated with a flowering-time quantitative trait locus in maize. Proc Natl Acad Sci USA, 2007,104:11376-11381.
doi: 10.1073/pnas.0704145104 pmid: 17595297
[17] Castelletti S, Tuberosa R, Pindo M, Salvi S . A MITE transposon insertion is associated with differential methylation at the maize flowering time QTL Vgt1. G3: Genes Genom Genet, 2014,4:805-812.
doi: 10.1534/g3.114.010686 pmid: 4025479
[18] Danilevskaya O, Meng X, Selinger D A, Deschamps S, Hermon P, Vansant G, Gupta R, Ananiev E V, Muszynski M G . Involvement of the MADS-box gene ZMM4 in floral induction and inflorescence development in maize. Plant Physiol, 2008,147:2054-2069.
[19] Alter P, Bircheneder S, Zhou L Z, Schlüter U, Gahrtz M, Sonnewald U, Dresselhaus T . Flowering time-regulated genes in maize include the transcription factor ZmMADS1. Plant Physiol, 2016,172:389-340.
doi: 10.1104/pp.16.00285 pmid: 27457125
[20] Liang Y, Liu Q, Wang X, Huang C, Xu G, Hey S, Lin H Y, Li C, Xu D, Wu L, Wang C, Wu W, Xia J, Han X, Lu S, Lai J, Song W, Schnable P S, Tian F . ZmMADS69 functions as a flowering activator through the ZmRap2.7-ZCN8 regulatory module and contributes to maize flowering time adaptation. New Phytol, 2018, doi: 10.1111/nph.15512.
[21] Buckler E S, Holland J B, Mcmullen M D, Kresovich S, Acharya C, Bradbury P, Brown P, Browne C J, Eller M S, Ersoz E , Flint Garcia S A, Garcia A, Glaubitz J C, Goodman M, Haries C, Guill K E, Kroon D, Larsson S, Lepak N K, Li H, Mitchell S E, Pressoir G, Peiffer J, Oropeza Rosas M, Rocheford T, Romay C, Romero S, Salvo S A, Sanchez Villeda H, Sun Q, Tian F, Upadyayula N, Ware D, Yates H, Yu J, Zhang Z . The genetic architecture of maize flowering time. Science, 2009,325:714-718.
doi: 10.1126/science.1174276 pmid: 19661422
[22] Seo P J, Ryu J, Kang S K, Park C M . Modulation of sugar metabolism by an INDETERMINATE DOMAIN transcription factor contributes to photoperiodic flowering in Arabidopsis. Plant J, 2011,65:418-429.
doi: 10.1111/j.1365-313X.2010.04432.x pmid: 202020202020202020202020202020202020
[23] Wu C, You C, Li C, Long T, Chen G, Byme M E, Zhang Q . RID1, encoding a Cys2/His2-type zinc finger transcription factor, acts as a master switch from vegetative to floral development in rice. Proc Natl Acad Sci USA, 2008,105:12915-12920.
doi: 10.1073/pnas.0806019105
[24] Wong A Y M, Colasanti J . Maize floral regulator protein INDETERMINATE1 is localized to developing leaves and is not altered by light or the sink/source transition. J Exp Bot, 2007,58:403-414.
doi: 10.1093/jxb/erl206 pmid: 17307745
[25] 郭安源, 朱其慧, 陈新, 罗静初 . GSDS: 基因结构显示系统. 遗传, 2007,29:1023-1026.
Guo A Y, Zhu Q H, Chen X, Luo J C . GSDS: a gene structure display server. Hereditas( Beijing), 2007,29:1023-1026 (in Chinese with English abstract).
[26] Li H, Peng Z, Yang X, Wang W, Fu J, Wang J, Han Y, Chai Y, Guo T, Yang N, Liu J, Warburton M L, Cheng Y, Hao X, Zhang P, Zhao J, Liu Y, Wang G, Li J, Yan J . Genome-wide association study dissects the genetic architecture of oil biosynthesis in maize kernels. Nat Genet, 2013,45:43-50.
doi: 10.1038/ng.2484 pmid: 23242369
[27] Yang X H, Gao S B, Xu S T, Zhang Z X, Prasanna B M, Li L, Li J S, Yan J B . Characterization of a global germplasm collection and its potential utilization for analysis of complex quantitative traits in maize. Mol Breed, 2011,28:511-526.
[28] Bland J M, Altman D G . Multiple significance tests: the Bonferroni method. British Med J, 1995,310:170.
pmid: 2548561
[29] Merk H L, Yarnes S C, Van Deynze A . Trait diversity andpotential for selection indices based on variation among regionally adapted processing tomato germplasm. J Am Soc Hortic Sci, 2012,137:427-437.
[30] Takatsuji H . Zinc-finger transcription factors in plants. Cell Mol Life Sci, 1998,54:582-596.
doi: 10.1007/s000180050186 pmid: 9676577
[31] 黄骥, 王建飞, 张红生 . 植物C2H2型锌指蛋白的结构与功能. 遗传, 2004,26:414-418.
Huang J, Wang J F, Zhang H S . Structure and function of plant C2H2 zing finger protein. Hereditas ( Beijing), 2004,26:414-418 (in Chinese with English abstract).
[32] Frankel A D, Pabo C O . Fingering too many proteins. Cell, 1988,56:675.
[33] Park S J, Kim S, Lee S, Je B I, Piao H L, Park S H, Kim C M, Ryu C H, Park S H, Xuan Y H, Colasanti J, An G, Han C D . Rice Indeterminate 1 (OsId1) is necessary for the expression of Ehd1 (Early heading date 1) regardless of photoperiod. Plant J, 2008,56:1018-1029.
[34] Matsubara K, Yamanouchi U, Wang Z X, Minobe Y, Izawa T, Yano M . Ehd2, a rice ortholog of the maize INDETERMINATE1 gene, promotes flowering by up-regulating Ehd1. Plant Physiol, 2008,148:1425-1435.
doi: 10.1104/pp.108.125542 pmid: 18790997
[35] Li D, Wang X F, Zhang X B, Chen Q Y, Xu G G, Xu D Y, Wang C L, Liang Y M, Wu L S, Huang C, Tian J G, Wu Y Y, Tian F . The genetic architecture of leaf number and its genetic relationship to flowering time in maize. New Phytol, 2012,210:256-268.
doi: 10.1111/nph.13765 pmid: 26593156
[36] Welch D, Hassan H, Blilou I, Immink R, Heidstra R . Arabidopsis JACKDAW and MAGPIE zinc finger proteins delimit asymmetric cell division and stabilize tissue boundaries by restricting SHORT-ROOT action. Genes Dev, 2007,21:2196-2204.
[37] Kim J Y, Ryu J Y, Baek K, Park C M . High temperature attenuates the gravitropism of inflorescence stems by inducing SHOOT GRAVITROPISM 5 alternative splicing in Arabidopsis. New Phytol, 2016,209:265-279.
doi: 10.1111/nph.13602 pmid: 26256266
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