Chin Bull Bot ›› 2016, Vol. 51 ›› Issue (4): 473-487.doi: 10.11983/CBB15148

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Genome-wide Characterization of bZIP Transcription Factors in Foxtail Millet and Their Expression Profiles in Response to Drought and Salt Stresses

Baoling Liu1, Li Zhang1, Yan Sun2, Jinai Xue1, Changyong Gao1, Lixia Yuan1, Jiping Wang1, Xiaoyun Jia2, Runzhi Li1*   

  1. 1Institute of Molecular Agriculture & Bioenergy, Shanxi Agricultural University, Taigu 030801, China
    2Department of Life Sciences, Shanxi Agricultural University, Taigu 030801, China
  • Received:2015-08-18 Accepted:2016-03-25 Online:2016-08-05 Published:2016-07-01
  • Contact: Li Runzhi E-mail:rli2001@126.com
  • About author:

    # Co-first authors

Abstract:

The bZIP protein family is one of the largest and most conserved transcription factor families regulating multiple physiology processes in plants. Foxtail millet (Setaria italica) is an important C4 cereal crop with increased resistance to drought stress. However, little is known about bZIP family members and their functions in this crop. In the present study, we identified and characterized 73 SibZIP transcription factors in foxtail millet genome by using bioinformatics. These SibZIPs are classified into 9 groups, including A, B, C, D, E, G, H, I and X subfamilies. Compared to the sequenced cereal crops, the foxtail millet bZIP family underwent contraction in evolution. In all, 25 conserved motifs were detected among SibZIPs. RNA-seq and qPCR analysis revealed that a number of SibZIPs are induced to change expression levels in response to drought and salt stresses, which suggests that they have important functions in the foxtail millet response to stress. Moreover, correlation analysis of co-expression of the protein coding genes under various stress conditions demonstrates that a set of 19 SibZIPs may mediate the regulation network controlling stress responses by cooperating with some protein kinases or NPR1-related regulatory protein in foxtail millet. Our results could provide new valuable information for comprehensively understanding SibZIP protein structure and their biological functions, the molecular mechanism of drought response, and stress resistance breeding in foxtail millet and related crops.

Table 1

List of primers used in quantitative real-time PCR analysis of SibZIP genes of Setaria italica"

Gene name Forward primer (5'-3') Reverse primer (5'-3')
18S rRNA CCACAGATTGAAAACCGCATTA ACCTCCCACCAGCAGAACC
SibZIP2 ATGGGACAGATGGCGATGG AAGAGCACGCAGCCGAGA
SibZIP3 ATGAGCTGCATTGGCAACG CTCCTTGAGATGGTTCAGTTCG
SibZIP7 GCCGTCCGACCACAACAG CCTCTTGACACGCTTGGGA
SibZIP8 CCCCAACAATCTCAGGGAAGG GAGCGTGTTGTTCTCGTTCTGG
SibZIP21 CCAGTCCTCCTCCTGCTCC CTCCATCACCAGGTCCTTCTCC
SibZIP24 ACGAGAAGGCCGAGCTGG TGGTGCTGGTGGTGTTGTTG
SibZIP37 TACGCCCGATGGTTAGAAGA ATCGATCAGCCGTCGTTG
SibZIP45 GTAGCCCGAGCCCTGACA AGCTCGCGGTCGAAGGTC
SibZIP51 AATCCCTCGGCTAAAA ACCCACAAAGCATCACAAGG
SibZIP57 GGCATCAGCACAGCCAGT CCTGTCCTGTCGCTACCTTCA
SibZIP60 CTCCAAACCCAGCATTCCA GCTCATCCTCTGCCATCACC
SibZIP73 AGCGTGGGCAGGGTAAATG CAGGAGCACCCCAGTAATCTAC

Table 2

Members of the SibZIPs gene family in Setaria italica"

Gene name Phytozome identifier Chromosome location
(bp)
Protein
length (aa)
Theore-
tical pI
Molecular
weight (Da)
Phylogeny
group
NCBI accession
No.
SibZIP1 Si000955m Chr.5: 42034648-42041849 538 6 58030.2 D XP_004970651
SibZIP2 Si001292m Chr.5: 39537137-39542647 473 6 51362.5 D XP_004970302
SibZIP3 Si001731m Chr.5: 42027056-42028626 399 6 42138.5 A XP_004970655
SibZIP4 Si001929m Chr.5: 31392517-31397217 368 9 39273.7 G XP_004969366
SibZIP5 Si002173m Chr.5: 39683613-39687077 333 9 36026.4 A XP_004970325
SibZIP6 Si002192m Chr.5: 3576665-3581966 330 7 36678.2 D XP_004967673
SibZIP7 Si002311m Chr.5: 13207621-13209504 314 6 34130.9 E XP_004968609
SibZIP8 Si002989m Chr.5: 10278963-10280748 196 10 20861.9 H XP_004968380
SibZIP9 Si003247m Chr.5: 42311957-42314982 147 10 16539.8 A XP_002458823
SibZIP10 Si003289m Chr.5: 246101970-24611764 140 9 15506.5 C XP_004968894
SibZIP11 Si006417m Chr.4: 33420130-33425120 449 9 48149.5 D XP_004965885
SibZIP12 Si006667m Chr.4: 11743965-11745864 379 8 41521.2 D XP_004966886
SibZIP13 Si006889m Chr.4: 6541497-4646365 325 9 35254.3 A XP_004964902
SibZIP14 Si006978m Chr.4: 33015635-33017728 303 5 32514.6 B XP_004965858
SibZIP15 Si007043m Chr.4: 30527846-30530681 285 6 30388.8 C XP_004965642
SibZIP16 Si007412m Chr.4: 39706531-39709069 157 9 17268.5 A XP_004966480
SibZIP17 Si007892m Chr.4: 12607851-12608351 167 9 18839.9 C XP_004965226
SibZIP18 Si010177m Chr.7: 31096934-31105294 427 7 47577 D XP_004976974
SibZIP19 Si010440m Chr.7: 32666098-32669917 359 9 39895 E XP_004977157
SibZIP20 Si010549m Chr.7: 33666577-33670528 335 6 36005.8 I XP_004977320
SibZIP21 Si012481m Chr.7: 34001430-34002276 185 9 19986.3 X XP_004978331
SibZIP22 Si013904m Chr.6: 30497939-30500723 390 6 41467.1 A XP_004973666
SibZIP23 Si013962m Chr.6: 3422261-3424756 367 7 40266.7 D XP_004972733
SibZIP24 Si014433m Chr.6: 31421965-31422818 219 9 23535.9 C XP_004973757
SibZIP25 Si014523m Chr.6: 21075712-21078072 175 9 19443.7 C XP_004973271
SibZIP26 Si014546m Chr.6: 35057931-35059283 169 9 18500.6 A XP_004974151
SibZIP27 Si014861m Chr.6: 34473052-34479032 553 8 60827.5 D XP_004978700
SibZIP28 Si017618m Chr.1: 39059405-39061854 357 6 38234.6 A XP_004954028
SibZIP29 Si017637m Chr.1: 8783667-8786862 354 5 37572.7 G XP_004952026
SibZIP30 Si017778m Chr.1: 6341933-6345399 325 6 34446.2 C XP_004951739
SibZIP31 Si018161m Chr.1: 1679857-1681771 252 6 26940.2 E XP_004951321
SibZIP32 Si018524m Chr.1: 4311195-4313806 167 10 18441.4 H XP_004951525
SibZIP33 Si019099m Chr.1: 5311182-5311658 158 6 18128.3 C XP_008645357
SibZIP34 Si019656m Chr.1: 8856565-8857280 101 12 11586.4 C XP_006362088
SibZIP35 Si019897m Chr.1: 36896832-36897341 169 8 19639.9 C XP_004953778
SibZIP36 Si021442m Chr.3: 20717700-20721220 645 9 68096.2 B XP_004962093
SibZIP37 Si022106m Chr.3: 18527822-18531435 431 6 48135.2 D XP_004961926
SibZIP38 Si022325m Chr.3: 5860297-5865473 384 7 40757.5 G XP_004960729
SibZIP39 Si022331m Chr.3: 48207088-48212169 383 6 41545.1 C XP_004963102
SibZIP40 Si022388m Chr.3: 9871788-9876447 373 9 39693.2 G XP_004961173
SibZIP41 Si022626m Chr.3: 14850120-14852158 331 8 36509.2 D XP_004961656
SibZIP42 Si022639m Chr.3: 15026867-15029429 328 5 35423.8 A XP_004961686
SibZIP43 Si023448m Chr.3: 19115835-19117133 170 9 18373.5 A XP_004961973
SibZIP44 Si023541m Chr.3: 42857978-42859308 149 7 16621.5 C XP_004962768
SibZIP45 Si023562m Chr.3: 3146171-3147458 145 9 15989 C XP_004960384
SibZIP46 Si024325m Chr.3: 50281135-50281679 175 11 19023.7 C XP_004964234
Gene name Phytozome identifier Chromosome location
(bp)
Protein
length (aa)
Theore-
tical pI
Molecular
weight (Da)
Phylogeny
group
NCBI accession
No.
SibZIP47 Si026421m Chr.8: 2241219-2245356 418 6 45444.7 D XP_004978700
SibZIP48 Si026452m Chr.8: 2350696-2353211 403 7 42267.1 X XP_004978712
SibZIP49 Si026561m Chr.8: 12073275-12076909 357 9 39171.5 E XP_004979095
SibZIP50 Si026605m Chr.8: 3317921-3321817 336 7 35850.7 I XP_004978752
SibZIP51 Si029351m Chr.2: 46950969-46953724 571 6 60447.1 B XP_004958502
SibZIP52 Si029606m Chr.2: 35632657-35640776 497 7 55157.1 D XP_004957190
SibZIP53 Si029966m Chr.2: 24028261-24036295 417 8 46056.5 D XP_004956460
SibZIP54 Si029970m Chr.2: 4745736-4748783 416 5 45187.2 C XP_004955660
SibZIP55 Si030114m Chr.2: 33169494-33171523 390 9 41890.8 A XP_004957010
SibZIP56 Si030123m Chr.2: 7037626-7041762 389 7 39918.8 G XP_004955801
SibZIP57 Si030182m Chr.2: 37345091-37349203 378 6 40638.3 I XP_004957354
SibZIP58 Si030224m Chr.2: 48343483-48348262 371 6 39761.6 I XP_004958698
SibZIP59 Si031077m Chr.2: 38684243-38685591 216 9 22457.3 A XP_004957504
SibZIP60 Si031238m Chr.2: 34573960-34574626 181 7 20285.7 C XP_004957101
SibZIP61 Si031353m Chr.2: 25296856-25298971 159 9 17806.8 C XP_004956521
SibZIP62 Si032429m Chr.2: 1879467-1880494 315 10 33579.7 C XP_004958923
SibZIP63 Si032507m Chr.2: 37624846-37627738 482 10 50744.7 I XP_002460540
SibZIP64 Si035062m Chr.9: 3209713-3215709 541 5 56605 C XP_004981429
SibZIP65 Si035841m Chr.9: 57321111-57323641 423 6 45305.5 I XP_004985885
SibZIP66 Si036380m Chr.9: 47061608-47065486 353 6 38129.3 I XP_004984459
SibZIP67 Si036527m Chr.9: 47985071-47991293 335 9 37389.2 D XP_004984573
SibZIP68 Si038381m Chr.9: 47741259-47744465 70 10 8263.2 A XP_004987020
SibZIP69 Si039367m Chr.9: 2420394-2422861 344 6 36158.7 G XP_004981331
SibZIP70 Si039558m Chr.9: 9034726-9035118 131 12 14050 C XP_004986317
SibZIP71 Si039566m Chr.9: 40545110-40547482 375 8 40649.5 I XP_004983840
SibZIP72 Si039895m Chr.9: 48442410-48442913 167 10 18179 C XP_004987029
SibZIP73 Si040286m Chr.9: 51600068-51604903 381 9 40899.1 G XP_004985055

Figure 1

The MEME conserved motifs analysis and phylogenetic tree of 73 SibZIPs protein sequences of Setaria italica"

Figure 2

Expression profiles of 73 SibZIP genes in Setaria italica leaves under drought and salt stresses Blocks with colors indicate upregulated (red) and downregulated (green) transcript accumulation of SibZIPs relative to the control. The expression level changed more than 1.5 folds is considered as significant difference (P<0.05)."

Figure 3

Expression analysis of 12 SibZIP genes in leaves of Setaria italic seedlings using real-time quantitative RT-PCR The different letters indicate significant difference (P<0.05) among samples by Duncan’s test."

Figure 4

Correlation analysis of co-expression of Setaria italica SibZIP genes under stressed conditions The expression data of the protein coding genes in foxtail millet under stressed conditions were derived from Setaria italica v2.1 database. Bioinformatics tools in String Functional Protein Interaction website (http://string-db.org/) were employed for correlation analysis of co-expression of SibZIP genes. Red circle represents SibZIP genes and the related genes involved in regulation network responsible for stress responses. The size of circle indicates the significance of the protein with bigger size having more importance in the related pathway. Blue solid line shows correlation between the related proteins with thinker line meaning stronger correlation. Blue dotted line shows possible interraction between the related proteins. The corresponding SibZIP protein name for each foxtail millet protein (red color circle representive) are list in Table 2. Si036309m: serine/threonine-protein kinase SRK2D-related; Si036283m: SF160-serine/threonine-protein kinase; Si036531m: serine/threonine-protein kinase SAPK3; Si000814m: SF66-regulatory protein NPR1-related; Si000647m: KOG0512-fetal globin-inducing factor"

1 曹红利, 岳川, 王新超, 杨亚军 (2012). bZIP转录因子与植物抗逆性研究进展. 南方农业学报 43, 1094-1100.
2 杨颖, 高世庆, 唐益苗, 冶晓芳, 王永波, 刘美英, 赵昌平 (2009). 植物bZIP转录因子的研究进展. 麦类作物学报 29, 730-737.
3 张水军, 曾千春, 卢秀萍, 李文正 (2010). 植物富含甘氨酸蛋白的研究进展. 中国农学通报 26(4), 54-58.
4 朱芸晔, 薛冰, 王安全, 王文杰, 周昂, 黄胜雄, 刘永胜 (2014). 番茄bZIP转录因子家族的生物信息学分析. 应用与环境生物学报 (5), 767-774.
5 Abe M, Kobayashi Y, Yamamoto S, Daimon Y, Yamaguchi A, Ikeda Y, Ichinoki H, Notaguchi M, Goto K, Araki T (2005). FD, a bZIP protein mediating signals from the floral pathway integrator FT at the shoot apex.Science 309, 1052-1056.
6 Baloglu MC, Eldem V, Hajyzadeh M, Unver T (2014). Genome-wide analysis of the bZIP transcription factors in cucumber.PLoS One 9, e96014.
7 Bennetzen JL, Schmutz J, Wang H, Percifield R, Hawkins J, Pontaroli AC, Estep M, Feng L, Vaughn JN, Grimwood J, Jenkins J, Barry K, Lindquist E, Hellsten U, Deshpande S, Wang X, Wu X, Mitros T, Triplett J, Yang X, Ye CY, Mauro-Herrera M, Wang L, Li P, Sharma M, Sharma R, Ronald PC, Panaud O, Kellogg EA, Brutnell TP, Doust AN, Tuskan GA, Rokhsar D, Devos KM (2012). Reference genome sequence of the model plant Setaria.Nat Biotechnol 30, 555-561.
8 Chuang CF, Running MP, Williams RW, Meyerowitz EM (1999). The PERIANTHIA gene encodes a bZIP protein involved in the determination of floral organ number in Arabidopsis thaliana.Genes Devel 13, 334-344.
9 Corrêa LG, Riaño-Pachón DM, Schrago CG, Dos Santos RV, Mueller-Roeber B, Vincentz M (2008). The role of bZIP transcription factors in green plant evolution: adaptive features emerging from four founder genes.PLoS One 3, e2944.
10 Fujita Y, Fujita M, Satoh R, Maruyama K, Parvez MM, Seki M, Hiratsu K, Ohme-Takagi M, Shinozaki K, Yamaguchi-Shinozaki K (2005). AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis.Plant Cell 17, 3470-3488.
11 Gibalová A, Renák D, Matczuk K, Dupl'áková N, Cháb D, Twell D, Honys D (2009). AtbZIP34 is required for Arabidopsis pollen wall patterning and the control of several metabolic pathways in developing pollen.Plant Mol Biol 70, 581-601.
12 Guiltinan MJ, Marcotte WR Jr, Quatrano RS (1990). A plant leucine zipper protein that recognizes an abscisic acid response element.Science 250, 267-271.
13 Iven T, Strathmann A, Böttner S, Zwafink T, Heinekamp T, Guivarc'h A, Roitsch T, Dröge-Laser W (2010). Homo- and heterodimers of tobacco bZIP proteins counteract as positive or negative regulators of transcription during pollen development.Plant J Cell Mol Biol 63, 155-166.
14 Izawa T, Foster R, Nakajima M, Shimamoto K, Chua NH (1994). The rice bZIP transcriptional activator RITA-1 is highly expressed during seed development.Plant Cell 6, 1277-1287.
15 Jakoby M, Weisshaar B, Dröge-Laser W, Vicente-Carba- josa J, Tiedemann J, Kroj T, Parcy F, BZIPRG (2002). bZIP transcription factors in Arabidopsis.Trends Plant Sci 7, 106-111.
16 Jin Z, Xu W, Liu A (2014). Genomic surveys and expression analysis of bZIP gene family in castor bean (Ricinus communis L.).Planta 239, 299-312.
17 Johnson C, Boden E, Arias J (2003). Salicylic acid and NPR1 induce the recruitment of trans-activating TGA factors to a defense gene promoter in Arabidopsis.Plant Cell 15, 1846-1858.
18 Lee SC, Choi HW, Hwang IS, Choi DS, Hwang BK (2006). Functional roles of the pepper pathogen-induced bZIP transcription factor, CAbZIP1, in enhanced resistance to pathogen infection and environmental stresses.Planta 224, 1209-1225.
19 Liao Y, Zou HF, Wei W, Hao YJ, Tian AG, Huang J, Liu YF, Zhang JS, Chen SY (2008). Soybean GmbZIP44, GmbZIP62 and GmbZIP78 genes function as negative regulator of ABA signaling and confer salt and freezing tolerance in transgenic Arabidopsis.Planta 228, 225-240.
20 Liu J, Chen N, Chen F, Cai B, Dal Santo S, Tornielli GB, Pezzotti M, Cheng ZM (2014). Genome-wide analysis and expression profile of the bZIP transcription factor gene family in grapevine (Vitis vinifera).BMC Genomics 15, 281.
21 Liu JX, Srivastava R, Howell SH (2008). Stress-induced expression of an activated form of AtbZIP17 provides protection from salt stress in Arabidopsis.Plant Cell Environ 31, 1735-1743.
22 Nijhawan A, Jain M, Tyagi AK, Khurana JP (2008). Genomic survey and gene expression analysis of the basic leucine zipper transcription factor family in rice.Plant Physiol 146, 333-350.
23 Pourabed E, Ghane Golmohamadi F, Soleymani Monfared P, Razavi SM, Shobbar ZS (2015). Basic leucine zipper family in barley: genome-wide characterization of members and expression analysis.Mol Biotechnol 57, 12-26.
24 Schultz J, Milpetz F, Bork P, Ponting CP (1998). SMART, a simple modular architecture research tool: identification of signaling domains.Proc Natl Acad Sci USA 95, 5857-5864.
25 Schwechheimer C, Zourelidou M, Bevan MW (1998). Plant transcription factor studies.Annu Rev Plant Physiol Plant Mol Biol 49, 127-150.
26 Singh K, Foley RC, Oñate-Sánchez L (2002). Transcription factors in plant defense and stress responses.Curr Opin Plant Biol 5, 430-436.
27 Stanković B, Vian A, Henry-Vian C, Davies E (2000). Molecular cloning and characterization of a tomato cDNA encoding a systemically wound-inducible bZIP DNA- binding protein.Planta 212, 60-66.
28 Toh S, McCourt P, Tsuchiya Y (2012). HY5 is involved in strigolactone-dependent seed germination in Arabidopsis.Plant Signal Behavior 7, 556-558.
29 Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000). Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid- dependent signal transduction pathway under drought and high-salinity conditions.Proc Natl Acad Sci USA 97, 11632-11637.
30 Wang J, Zhou J, Zhang B, Vanitha J, Ramachandran S, Jiang SY (2011). Genome-wide expansion and expression divergence of the basic leucine zipper transcription factors in higher plants with an emphasis on sorghum.J Integr Plant Biol 53, 212-231.
31 Wei K, Chen J, Wang Y, Chen Y, Chen S, Lin Y, Pan S, Zhong X, Xie D (2012). Genome-wide analysis of bZIP- encoding genes in maize.DNA Res 19, 463-476.
32 Xiang Y, Tang N, Du H, Ye H, Xiong L (2008). Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice.Plant Physiol 148, 1938-1952.
33 Xu J, Li Y, Ma X, Ding J, Wang K, Wang S, Tian Y, Zhang H, Zhu XG (2013). Whole transcriptome analysis using next-generation sequencing of model species Setaria viridis to support C4 photosynthesis research.Plant Mol Biol 83, 77-87.
34 Ying S, Zhang DF, Fu J, Shi YS, Song YC, Wang TY, Li Y (2012). Cloning and characterization of a maize bZIP transcription factor, ZmbZIP72, confers drought and salt tolerance in transgenic Arabidopsis.Planta 235, 253-266.
35 Yoshida T, Fujita Y, Sayama H, Kidokoro S, Maruyama K, Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2010). AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation.Plant J 61, 672-685.
36 Zhang G, Liu X, Quan Z, Cheng S, Xu X, Pan S, Xie M, Zeng P, Yue Z, Wang W, Tao Y, Bian C, Han C, Xia Q, Peng X, Cao R, Yang X, Zhan D, Hu J, Zhang Y, Li H, Li H, Li N, Wang J, Wang C, Wang R, Guo T, Cai Y, Liu C, Xiang H, Shi Q, Huang P, Chen Q, Li Y, Wang J, Zhao Z, Wang J (2012). Genome sequence of foxtail millet (Setaria italica) provides insights into grass evolution and biofuel potential.Nat Biotechnol 30, 549-554.
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