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Acta Agron Sin ›› 2014, Vol. 40 ›› Issue (09): 1585-1594.doi: 10.3724/SP.J.1006.2014.01585

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

Identification, Classification, and Drought Response of F-box Gene Family in Foxtail Millet

HUO Dong-Ying1,2,ZHENG Wei-Jun1,LI Pan-Song1,2,XU Zhao-Shi2,ZHOU Yong-Bin1,2,CHEN Ming2,MA You-Zhi2,MIN Dong-Hong1,2,*,ZHANG Xiao-Hong1,2,*   

  1. 1 State Key Laboratory of Crop Stress Biology for Arid Areas / Northwest Agricultural and Forestry University, Yangling 712100, China; 2 Institute of Crop Science, Chinese Academy of Agricultural Sciences / National Key Facility for Crop Gene Resources and Genetic Improvement / Key Laboratory of Crop Genetics and Breeding, Ministry of Agriculture, Beijing 100081, China?
  • Received:2013-12-01 Revised:2014-06-16 Online:2014-09-12 Published:2014-07-09
  • Contact: 张小红, E-mail: zhxh2493@126.com; 闵东红, E-mail: mdh2493@126.com E-mail:huodongyingyr@126.com

Abstract:

F-box proteins play critical roles in plant growth and development and respond to abiotic stresses, involving in cell-cycle regulation, cell apoptosis and signal transduction. Foxtail millet has a character with drought-tolerance. We identified 19 up-regulated F-box genes from 525 F-box families under stress in foxtail millet based on the transcriptome sequencing and divided them into six subgroups, and the genes in the same subgroup had the same intron-exon structure. These genes were unevenly distributed on eight foxtail millet chromosomes, and there were six genes on chromosome 2, that gene number was more than that contained on other chromosomes. The analysis of conserved domain of 19 genes showed that all the protein sequences had a conserved F-box motif, and several other domain also existed in C-terminal including FBD, WD40, FBA, ZnF, and Kelch LRR. Putative cis-acting elements showed that the number of MYB and MYC was the most, which ranged from 9 to 78. Transcriptome sequencing showed that SiF-box18 was more hypersensitive to the drought stress than other F-box members and response to drought, salt, ABA, GA, SA and JA based on the real time PCR. The transient expression in Arabidopsis protoplasts displayed that SiF-box18 protein was localized in nuclear section. This study provided experimental data for further studying the functions of the SiF-box18 gene.

Key words: Foxtail millet, F-box protein, Subcellular localization, Drought response, Induction mechanism

[1]Verslues P E, Agarwal M, Katiyar A S, Zhu J, Zhu J K. Methods and concepts in quantifying resistance to drought, salt and freezing, abiotic stresses that affect plant water status. Plant J, 2006, 45: 523–539



[2]Sadanandom A, Bailey M, Ewan R, Lee J, Nelis S. The ubiquitin-proteasome system: central modifier of plant signalling. New Phytol, 2012, 196: 13–28



[3]Jackson P K, Eldridge A G, Freed E, Furstenthal L, Hsu J Y, Kaiser B K, Reimann J D. The lore of the RINGs: substrate recognition and catalysis by ubiquitin ligases. Trends Cell Biol, 2000, 10: 429–439



[4]Cardozo T, Pagano M. The SCF ubiquitin ligase: insights into a molecular machine. Nat Rev Mol Cell Biol, 2004, 5: 739–751



[5]Ho M S, Tsai P I, Chien C T. F-box proteins: the key to protein degradation. J Biomed Sci, 2006, 13: 181–191



[6]Bai C, Richman R, Elledge S J. Human cyclin F. EMBO J, 1994, 13: 6087–6098



[7]Levin J Z, Meyerowitz E M. UFO: an Arabidopsis gene involved in both floral meristem and floral organ development. Plant Cell, 1995, 7: 529–548



[8]Hepworth S R, Klenz J E, Haughn G W. UFO in the Arabidopsis inflorescence apex is required for floral-meristem identity and bract suppression. Planta, 2006, 223:769–778



[9]Sasaki K, Yamaguchi H, Aida R, Shikata M, Abe T, Ohtsubo N. Mutation in Torenia fournieri Lind: UFO homolog confers loss of TfLFY interaction and results in a petal to sepal transformation. Plant J, 2012, 71: 1002–1014



[10]Wang Z, Chen J, Weng L, Li X, Cao X, Hu X, Luo D, Yang J. Multiple components are integrated to determine leaf complexity in Lotus japonicus. J Integr Plant Biol, 2013, 55: 419–433



[11]Nelson D C, Lasswell J, Rogg L E, Cohen M A, Bartel B. FKF1, a clock-controlled gene that regulates the transition to flowering in Arabidopsis. Cell, 2000, 101: 331–340



[12]Imaizumi T, Schultz T F, Harmon F G, Ho L A, Kay S A. FKF1F-box protein mediates cyclic degradation of a repressor of CONSTANS in Arabidopsis. Science, 2005, 309: 293–297



[13]Tomoyuki T, Yuuki N, Haruna T, Yasunobu O, Yuji M, Yumiko Y, Tomohiro K. LOV KELCH PROTEIN2 and ZEITLUPE repress Arabidopsis photoperiodic flowering under non-inductive conditions, dependent on FLAVIN-BINDING KELCH REPEAT F-BOX1. Plant J, 2011, 67: 608–621



[14]Suetsugu N, Wada M. Evolution of three LOV blue light receptor families in green plants and photosynthetic stramenopiles: phototropin, ZTL/FKF1/LKP2 and aureochrome. Plant Cell Physiol, 2013, 54: 8–23



[15]Lai Z, Ma W, Han B, Liang L, Zhang Y, Hong G, Xue Y. An F-box gene linked to the self-incompatibility locus of Antirrhinum is expressed specifically in pollen and tapetum. Plant Mol Biol, 2002, 50: 29–42



[16]Ushijima K, Yamane H, Watari A, Kakehi E, Ikeda K, Hauck N R, Iezzoni A F, Tao R. The S haplotype-specific F-box protein gene, SFB, is defective in self-compatible haplotypes of Prunus avium and P. mume. Plant J, 2004, 39: 573–586



[17]Hidenori S, Hiroyuki K, Mai M. Pollen-expressed F-box gene family and mechanism of S-RNase-based gametophytic self-incompatibility (GSI) in Rosaceae. Sex Plant Reprod, 2010, 23: 39–43



[18]Wu J, Li M, Li T. Genetic Features of the Spontaneous Self-Compatible Mutant, ‘Jin Zhui’ (Pyrus bretschneideri Rehd.). PLoS One, 2013, 8, doi: 10.1371



[19]Gray W M, Kepinski S, Rouse D, Leyser O, Estelle M. Auxin regulates SCF(TIR1)-dependent degradation of AUX/IAA proteins. Nature, 2001, 414: 271–276



[20]Kepinski S, Leyser O. The Arabidopsis F-box protein TIR1 is an auxin receptor. Nature, 2005, 435: 446–451



[21]Yu H, Moss B L, Jang S S, Prigge M, Klavins E, Nemhauser J L, Estelle M. Mutations in the TIR1 auxin receptor that increase affinity for auxin/indole-3-acetic acid proteins result in auxin hypersensitivity. Plant Physiol, 2013, 162: 295–303



[22]Tromas A, Paque S, Stierlé V, Quettier A L, Muller P, Lechner E, Genschik P, Perrot-Rechenmann C. Auxin-Binding Protein 1 is a negative regulator of the SCF TIR1/AFB pathway. Nat Commun, 2013, 4: 2496



[23]Guo H, Ecker J R. Plant responses to ethylene gas are mediated by SCF (EBF1/EBF2)-dependent proteolysis of EIN3 transcription factor. 2003, Cell, 115: 667–677



[24]Iqbal N, Trivellini A, Masood A, Ferrante A, Khan N A. Current understanding on ethylene signaling in plants: The influence of nutrient availability. Plant Physiol Biochem, 2013, 73, 128–138



[25]Itoh H, Matsuoka M, Steber C M. A role for the ubiquitin-26Sproteasome pathway in gibberellin signaling. Trends Plant Sci, 2003, 8: 492–497



[26]Ariizumi T, Hauvermale A L, Nelson S K, Hanada A, Yamaguchi S, Steber C M. Lifting DELLA repression of Arabidopsis seed germination by nonproteolytic gibberellin signaling. Plant Physiol, 2013, 162: 2125–2139



[27]Xie D X, Feys B F, James S, Nieto-Rostro M, Turner J G, COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science, 1998, 280: 1091–1094



[28]Devoto A, Ellis C, Magusin A, Chang H S, Chilcott C, Zhu T, Turner J G. Expression profiling reveals COI1 to be a key regulator of genes involved in wound-and methyl jasmonate-induced secondary metabolism, defence, and hormone interactions. Plant Mol Biol, 2005, 58: 497–513



[29]Sasaki-Sekimoto Y, Jikumaru Y, Obayashi T, Saito H, Masuda S, Kamiya Y, Ohta H, Shirasu K. Basic helix-loop-helix transcription factors JASMONATE-ASSOCIATED MYC2-LIKE1 (JAM1), JAM2, and JAM3 are negative regulators of jasmonate responses in Arabidopsis. Plant Physiol, 2013, 163, 291–304



[30]Zhang Y, Xu W, Li Z, Deng X W, Wu W, Xue Y. F-box protein DOR functions as a novel inhibitory factor for abscisic acid-induced stomatal closure under drought stress in Arabidopsis. Plant Physiol, 2008, 148:2121–2133



[31]Bu Q, Lü T, Shen H, Luong P, Wang J, Wang Z, Huang Z, Xiao L, Engineer C, Kim T H, Schroeder J I, Huq E. Regulation of drought tolerance by the F-box protein MAX2 in Arabidopsis. Plant Physiol, 2013, doi: 10.1104



[32]Ren J, Wen L, Gao X, Jin C, Xue Y, Yao X. DOG 1.0: illustrator of protein domain structures cell research. Cell Res, 2009, 19: 271–273



[33]Yang S, Zhang X, Yue J X, Tian D, Chen J Q: Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genom, 2008, 280: 187–198



[34]Liu P, Xu Z S, Pan-Pan L, Hu D, Chen M, Li L C, Ma Y Z. A wheat plasma membrane-localized PI4K gene possessing threonine autophophorylation activity confers tolerance to drought and salt in Arabidopsis. J Exp Bot, 2013, 64: 2915–2927



[35]Jin J, Cardozo T, Lovering R C, Elledge S J, Pagano M, Harper J W. Systematic analysis and nomenclature of mammalian F-box proteins. Genes Dev, 2004, 18: 2573–2580



[36]Gagne J M, Downes B P, Shiu S H, Durski A M, Vierstra R D. The F-box subunit of the SCF E3 complex is encoded by a diverse superfamily of genes in Arabidopsis. Proc Natl Acad Sci USA, 2002, 99: 11519–11524



[37]Kuroda H, Takahashi N, Shimada H, Seki M, Shinozaki K, Matsui M. Classification and expression analysis of Arabidopsis F-box-containing protein genes. Plant Cell Physiol, 2002, 43: 1073–1085



[38]Jain M, Nijhawan A, Arora R, Agarwal P, Ray S, Sharma P, Kapoor S, Tyagi A K, Khurana J P. F-box proteins in rice. Genomewide analysis, classification, temporal and spatial gene expression during panicle and seed development, and regulation by light and abiotic stress. Plant Physiol, 2007, 143: 1467–1483



[39]Jia F, Wu B, Li H, Huang J, Zheng C. Genome-wide identification and characterization of F-box family in maize. Mol Genet Genomics, 2013, 288: 559–577



[40]Andrade M A, Perez-Iratxeta C, Ponting C P. Protein repeats: structures, functions, and evolution. J Struct Biol, 2001, 134: 117–131



[41]Smith T F, Gaitatzes C, Saxena K, Neer E J. The WD repeat: a common architecture for diverse functions. Trends Biochem Sci, 1999, 24: 181–185



[42]Craig K L, Tyers M. The F-box: a new motif for ubiquitin dependent proteolysis in cell cycle regulation and signal transduction. Prog Biophys Mol Biol, 1999, 72: 299–328



[43]Koops P, Pelser S, Ignatz M, Klose C, Marrocco-Selden K, Kretsch T. EDL3 is an F-box protein involved in the regulation of abscisic acid signalling in Arabidopsis thaliana. J Exp Bot, 2011, 62: 5547–5560

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