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Acta Agronomica Sinica ›› 2020, Vol. 46 ›› Issue (7): 1052-1062.doi: 10.3724/SP.J.1006.2020.94144


Photo-thermal interaction model under different photoperiod-temperature conditions and expression analysis of SiCCT gene in foxtail millet (Setaria italica L.)

JIA Xiao-Ping1,*(),YUAN Xi-Lei1,LI Jian-Feng1,WANG Yong-Fang2,ZHANG Xiao-Mei1,ZHANG Bo1,QUAN Jian-Zhang2,DONG Zhi-Ping2,*()   

  1. 1 College of Agriculture, Henan University of Science and Technology, Luoyang 471023, Henan, China
    2 Institute of Millet, Hebei Academy of Agriculture and Forestry Sciences / National Millet Improvement Center, Shijiazhuang 050035, Hebei, China
  • Received:2019-09-27 Accepted:2020-01-15 Online:2020-07-12 Published:2020-01-24
  • Contact: Xiao-Ping JIA,Zhi-Ping DONG E-mail:jiaxiaoping2007@163.com;dzp001@163.com
  • Supported by:
    National Natural Science Foundation of China(31471569);“Twelfth Five-Year” National Science and Technology Support Program(2011BAD06B01-1)


Photoperiod and temperature are two important environmental factors that affect growth and development, ecological adaptability and yield of crops. Uncovering the effect of interaction between photoperiod and temperature on crop growth and development and the molecular mechanism for this interaction has important influence on breeding practice and theoretical research. In this study, four photo-thermal treatments (long-day and high temperature, long-day and low temperature, short-day and high temperature, short-day and low temperature) were designed to investigate heading stage, plant height, leaf number and panicle length of ‘Huangmaogu’. The photoperiod played a key role on growth of foxtail millet, while changes in temperature had no more effect on delaying reproductive growth by long-day treatment compared with that by short-day treatment. The effect of temperature differed with the difference of photoperiod, high temperature shortened vegetative growth period and low temperature prolonged vegetative growth period under short-day condition, while it was opposite under long-day condition. The effect on reproductive growth was short-day and high temperature treatment > short-day and low temperature treatment > long-day and low temperature treatment > long-day and high temperature treatment. Furthermore, a CCT-motif gene named SiCCT was cloned from leaf of ‘Huangmaogu’ by RT-PCR technology, which encodes 286 aa and belongs to CMF subfamily. Phylogenetic analysis based on aa sequences of CCT-motif genes showed that there existed a close relationship among foxtail millet, sorghum and maize. Real-time PCR analysis showed that the expression level of SiCCT was higher in leaf than in young panicle and leaf sheath. The SiCCT showed a circadian expression pattern under both long-day and short-day conditions. The expression level of SiCCT was the highest at 7-leaf stage, and decreased rapidly at 8-leaf stage (heading) and after heading under short-day condition. The expression of SiCCT maintained high level from 7-leaf stage to 10-leaf stage under long-day condition, during which ‘Huangmaogu’ was at vegetative growth phase. No matter high temperature or low temperature, the expression level of SiCCT at different leaf stages was totally higher in long-day treatment than in short-day treatment, and lower in low temperature than in high temperature under long-day condition. The general expression level of SiCCT was positively correlated with vegetative growth period of ‘Huangmaogu’. In summary, SiCCT is regulated by both photoperiod and temperature, suggesting that SiCCT participates in photoperiod pathway and thermosensory pathway, and regulates the whole vegetative and reproductive growth process of foxtail millet through interaction between the two pathways.

Key words: foxtail millet, photoperiod, thermosensory, photo-thermal interaction, CCT-motif gene

Fig. 1

Effect of different photo-thermal treatments on growth and development of ‘Huangmaogu’ SD: short day; LD: long day."

Fig. 2

Comparison of four traits among different photo-thermal treatments a: heading date; b: plant height; c: panicle length; d: leaf number. SD: short day; LD: long day."

Fig. 3

Electrophoregram of total RNA extracted from leaves of ‘Huangmaogu’ 1, 2: two tubes of RNA extracted."

Fig. 4

Electrophoregram of RT-PCR products of SiCCT gene M: marker DL2000; 1, 2: two tubes of RT-PCR products."

Supplementary Fig. 1

cDNA sequences of SiCCT gene The bolded parts are primer sequences, the underlined parts are initiation codon and termination codon."

Supplementary Fig. 2

The deduced amino acid sequence of SiCCT gene"

Supplementary Fig. 3

Prediction for the conserved domains of SiCCT protein"

Fig. 5

Phylogenetic tree of CCT-motif genes based on protein sequences"

Fig. 6

Relative expression of SiCCT in different tissues"

Fig. 7

Circadian expression of SiCCT gene under different photoperiod conditions a: short-day treatment; b: long-day treatment. Black bars represent dark period, and white bars represent light period."

Fig. 8

Expression level of SiCCT gene at different leaf ages under different photoperiod conditions a: short-day; b: long-day."

Fig. 9

Expression feature of SiCCT gene under different photo-thermal combinations a: high temperature and long-day, high temperature and short-day; b: low temperature and long-day, low temperature and short-day; c: short-day and high temperature, short-day and low temperature; d: long-day and high temperature, long-day and low temperature."

[1] Song Y H, Ito S, Imaizumi T. Flowering time regulation: photoperiod- and temperature-sensing in leaves. Trends Plant Sci, 2013,18:575-583.
doi: 10.1016/j.tplants.2013.05.003 pmid: 23790253
[2] Balasubramanian S, Sureshkumar S, Lempe J, Weigel D. Potent induction of Arabidopsis thaliana flowering by elevated growth temperature. PLoS Genet, 2006,2:e106. doi: 10.1371/journal. pgen.0020106.
doi: 10.1371/journal.pgen.0020106 pmid: 16839183
[3] Hemming M N, Walford S A, Fieg S, Dennis E S, Trevaskis B. Identification of high-temperature-responsive genes in cereals. Plant Physiol, 2012,158:1439-1450.
doi: 10.1104/pp.111.192013
[4] Cober E R, Stewart D W, Voldeng H D. Crop physiology & metabolism: photoperiod and temperature responses in early- maturing, near-isogenic soybean lines. Crop Sci, 2001,41:721-727.
doi: 10.2135/cropsci2001.413721x
[5] 孙洪波. 大豆光温互作新模式的验证及PEBP家族基因的克隆和功能分析. 中国农业科学院博士后出站报告, 北京, 2008.
Sun H B. Verification of A New Light-Temperature Interaction Model and Clone, Function Analysis of PEBP Family Genes in Soybean. Postdoctoral outbound Report of Chinese Academy of Agricultural Sciences, Beijing, China, 2008 (in Chinese with English abstract).
[6] 刘易科. 大豆光温互作新模型的验证和FT家族基因的克隆. 西北农林科技大学硕士学位论文, 陕西杨凌, 2006.
Liu Y K. Verification of A New Light-Temperature Interaction Model and Clone of FT Family Genes in Soybean. MS Thesis of Northwest A&F University, Yangling, Shaanxi, China, 2006 (in Chinese with English abstract).
[7] 张艺能, 周玉萍, 陈琼华, 黄小玲, 田长恩. 拟南芥开花时间调控的分子基础. 植物学报, 2014,49:469-482.
Zhang Y N, Zhou Y P, Chen Q H, Huang X L, Tian C E. Molecular basis of flowering time regulation in Arabidopsis. Acta Bot Sin, 2014,49:469-482(in Chinese with English abstract).
[8] 孔德艳, 陈守俊, 周立国, 高欢, 罗利军, 刘灶长. 水稻开花光周期调控相关基因研究进展. 遗传, 2016,38:532-542.
Kong D Y, Chen S J, Zhou L G, Gao H, Luo L J, Liu Z C. Research progress of photoperiod regulated genes on flowering time in rice. Hereditas, 2016,38:532-542 (in Chinese with English abstract).
[9] Capovilla G, Schmid M, Pose D. Control of flowering by ambient temperature. J Exp Bot, 2015,66:59-69.
doi: 10.1093/jxb/eru416 pmid: 25326628
[10] Kinmonth-Schultz H A, Tong X, Lee J, Song Y H, Ito S, Kim S H, Imaizumi T. Cool night-time temperatures induce the expression of CONSTANS and FLOWERING LOCUS T to regulate flowering in Arabidopsis. New Phytol, 2016,211:208-224.
doi: 10.1111/nph.13883 pmid: 26856528
[11] Cockram J, Jones H, Leigh F J, O’Sullivan D, Powell W, Laurie D A, Greenland A J. Control of flowering time in temperate cereals: genes, domestication, and sustainable productivity. J Exp Bot, 2007,58:1231-1244.
doi: 10.1093/jxb/erm042 pmid: 17420173
[12] Salome P A, McClung C R. PSEUDO-RESPONSE REGULATOR 7 and 9 are partially redundant genes essential for the temperature responsiveness of theArabidopsis circadian clock. Plant Cell, 2005,17:791-803.
doi: 10.1105/tpc.104.029504 pmid: 15705949
[13] 陈华夏, 申国境, 王磊, 邢永忠. 4个物种CCT结构域基因家族的序列进化分析. 华中农业大学学报, 2010,29:669-676.
doi: 1000-2421(2010)06-0669-08
Chen H X, Shen G J, Wang L, Xing Y Z. Sequence evolution analysis of CCT domain gene family in rice, Arabidopsis, maize and sorghum. J Huazhong Agric Univ, 2010,29:669-676 (in Chinese with English abstract).
doi: 1000-2421(2010)06-0669-08
[14] Yano M, Katayose Y, Ashikari M, Yamanouchi U, Monna L, Fuse T, Baba T, Yamamoto K, Umehara Y, Nagamura Y, Sasaki T. Hd1, a major photoperiod sensitivity quantitative trait locus in rice, is closely related to the Arabidopsis flowering time gene CONSTANS. Plant Cell, 2000,12:2473-2483.
doi: 10.1105/tpc.12.12.2473 pmid: 11148291
[15] Hayama R, Yokoi S, Tamaki S, Yano M, Shimamoto K. Adaptation of photoperiodic control pathways produces short-day flowering in rice. Nature, 2003,422:719-722.
doi: 10.1038/nature01549 pmid: 12700762
[16] Campoli C, Drosse B, Searle I, Coupland G, von Korff M. Functional characterization of HvCO1, the barley (Hordeum vulgare) flowering time ortholog of CONSTANS. Plant J, 2012,69:868-880.
doi: 10.1111/j.1365-313X.2011.04839.x
[17] Yang S S, Wers B D, Morishige D T, Mullet J E. CONSTANS is a photoperiod regulated activator of flowering in sorghum. BMC Plant Biol, 2014,14:1-15.
doi: 10.1186/1471-2229-14-1 pmid: 24387633
[18] 薛为亚. 水稻产量相关基因Ghd7的分离与鉴定. 华中农业大学博士学位论文, 湖北武汉, 2008.
Xue W Y. Isolation and Identification of Rice Yield Related Gene Ghd7. PhD Dissertation of Huazhong Agricultural University, Wuhan, Hubei, China, 2008 (in Chinese with English abstract).
[19] 刘海洋. 水稻多效性基因Ghd7.1的克隆与功能分析. 华中农业大学博士学位论文, 湖北武汉, 2016.
Liu H Y. Cloning and Functional Analysis of Rice Multiplexing Gene Ghd7.1. PhD Dissertation of Huazhong Agricultural University, Wuhan, Hubei, China, 2016 (in Chinese with English abstract).
[20] Murphy R L, Morishige D T, Brady J A, Rooney W L, Yang S, Klein P E. Ghd7 (Ma6) represses sorghum flowering in long days: alleles enhance biomass accumulation and grain production. Plant Genome, 2014,7:1-10.
[21] Huang C, Sun H Y, Xu D Y, Chen Q Y, Liang Y M, Wang X F, Xu G H, Tian J G, Wang C L, Li D, Wu L S, Yang X H, Jin W W, Doebley J F, Tian F. ZmCCT9 enhances maize adaptation to higher latitudes. Proc Natl Acad Sci USA, 2018,115:e334-e341.
doi: 10.1073/pnas.1718058115 pmid: 29279404
[22] Li Y P, Tong L X, Deng L L, Liu Q Y, Xing Y X, Wang C, Liu B S, Yang X H, Xu M L. Evaluation ofZmCCT haplotypes for genetic improvement of maize hybrids. Theor Appl Genet, 2017,130:2587-2600.
doi: 10.1007/s00122-017-2978-1 pmid: 28916922
[23] Wu W X, Zheng X M, Lu G W, Zhong Z Z, Gao H, Chen L P, Wu C Y, Wang H J, Wang Q, Zhou K N, Wang J L, Wu F Q, Zhang X, Guo X P, Cheng Z J, Lei C L, Lin Q B, Jiang L, Wang H Y, Ge S, Wan J M. Association of functional nucleotide polymorphisms at DTH2 with the northward expansion of rice cultivation in Asia. Proc Natl Acad Sci USA, 2013,110:2775-2780.
doi: 10.1073/pnas.1213962110 pmid: 23388640
[24] 谭俊杰. 水稻CONSTANS-like基因OsCOL10作用于光周期开花途径的分子遗传与生化分析. 湖南大学博士学位论文, 湖南长沙, 2015.
Tan J J. Molecular Genetic and Biochemical Analysis of the Effect of OsCOL10 on Photoperiod Flowering Pathway in Rice. PhD Dissertation of Hunan University, Changsha, Hunan, China, 2015 (in Chinese with English abstract).
[25] Liu J H, Shen J Q, Xu Y, Li X H, Xiao J H, Xiong L Z. Ghd2, a CONSTANS-like gene, confers drought sensitivity through regulation of senescence in rice. J Exp Bot, 2016,67:5785-5798.
doi: 10.1093/jxb/erw344 pmid: 27638689
[26] Bennetzen J L, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli A C, Estep M, Feng L, Vaughn J N, Grimwood J, Jenkins J, Barry K, Lindquist E, Hellsten U, Deshpande S, Wang X W, Wu X M, Therese Mitros T, Triplett J, Yang X H, Ye C Y, Mauro-Herrera M, Wang L, Li P H, Sharma M, Sharma R, Ronald P C, Panaud O, Kellogg E A, Brutnell T P, Doust A N, Tuskan G A, Rokhsar D, Devos K M. Reference genome sequence of the model plant setaria. Nat Biotechnol, 2012,30:555-564.
doi: 10.1038/nbt.2196 pmid: 22580951
[27] Zhang G Y, Liu X, Quan Z W, Cheng S F, Xu X, Pan S K, Xie M, Zeng P, Yue Z, Wang W L, Tao Y, Bian C, Han C L, Xia Q J, Peng X H, Cao R, Yang X H, Zhan D L, Hu J C, Zhang Y X, Li H N, Li H, Li N, Wang J Y, Wang C C, Wang R Y, Guo T, Cai Y J, Liu C Z, Xiang H T, Shi Q X, Huang P, Chen Q C, Li Y R, Wang J, Zhao Z H, Wang J. Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential. Nat Biotechnol, 2012,30:549-556.
doi: 10.1038/nbt.2195 pmid: 22580950
[28] Brutnell T P, Lin W, Swartwood K, Goldschmidt A, Jackson D, Zhu X G, Kellogg E, Van Eck J. Setaria viridis: a model for C4 photosynthesis. Plant Cell, 2010,22:2537-2544.
doi: 10.1105/tpc.110.075309 pmid: 20693355
[29] Lata C, Gupta S, Prasad M. Foxtail millet: a model crop for genetic and genomic studies in bioenergy grasses. Crit Rev Biotechnol, 2013,33:328-343.
doi: 10.3109/07388551.2012.716809
[30] 贾小平, 全建章, 王永芳, 董志平, 袁玺垒, 张博, 李剑峰. 不同光周期环境对谷子农艺性状的影响. 作物学报, 2019, 45:1119-1127.
doi: 10.3724/SP.J.1006.2019.84128
Jia X P, Quan J Z, Wang Y F, Dong Z P, Yuan X L, Zhang B, Li J F. Effects of different photoperiod conditions on agronomic traits of foxtail millet. Acta Agron Sin, 2019,45:1119-1127 (in Chinese with English abstract).
doi: 10.3724/SP.J.1006.2019.84128
[31] 杨希文, 胡银岗. 谷子DREB转录因子基因的克隆及其在干旱胁迫下的表达模式分析. 干旱地区农业研究, 2011,29(5):69-74.
Yang X W, Hu Y G. Cloning of a DREB gene from foxtail millet (Setaria italica L.) and its expression during drought stress. Agric Res Arid Areas, 2011,29(5):69-74 (in Chinese with English abstract).
[32] Zhang Y, Zhang G, Xiao N, Wang L, Fu Y, Sun Z, Fang R, Chen X. The rice ‘nutrition response and root growth’ (NRR) gene regulates heading date. Mol Plant, 2013,6:585-588.
doi: 10.1093/mp/sss157 pmid: 23253602
[33] Zhang L, Li Q P, Dong H J, He Q, Liang L W, Tan C, Han Z M, Yao W, Li G W, Zhao H, Xie W B, Xing Y Z. Three CCT domain-containing genes were identified to regulate heading date by candidate gene-based association mapping and transformation in rice. Sci Rep, 2015,5:7663.
doi: 10.1038/srep07663 pmid: 25563494
[34] 金敏亮. 玉米泛转录组的构建及玉米开花抑制因子ZmCOL3的功能解析. 华中农业大学博士学位论文, 湖北武汉, 2018.
Jin M L. Maize Pan-transcriptome Construction and Functional Analysis of Maize Flowering Repressor ZmCOL3. PhD Dissertation of Huazhong Agricultural University, Wuhan, Hubei, China, 2018 (in Chinese with English abstract).
[35] 章佳. 水稻CCT家族基因的功能研究和Hd1的重新克隆. 华中农业大学博士学位论文, 湖北武汉, 2017.
Zhang J. The Functional Analysis of Rice CCT Family Genes and the Recloning of Hd1. PhD Dissertation of Huazhong Agricultural University, Wuhan, Hebei, China, 2017 (in Chinese with English abstract).
[36] 宋远丽, 高志超, 栾维江. 温度和光周期对水稻抽穗期调控的交互作用. 中国科学: 生命科学, 2012,42:316-325.
Song Y L, Gao Z C, Luan W J. The interaction of temperature and photoperiod on regulating of heading date in rice. Sci China Life Sci, 2012,42:316-325 (in Chinese with English abstract).
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