Skip to main content
Log in

A low-temperature-responsive element involved in the regulation of the Arabidopsis thaliana At1g71850/At1g71860 divergent gene pair

  • Original Article
  • Published:
Plant Cell Reports Aims and scope Submit manuscript

Key message

The bidirectional promoter of the Arabidopsis thaliana gene pair At1g71850/At1g71860 harbors low-temperature-responsive elements, which participate in anti-correlated transcription regulation of the driving genes in response to environmental low temperature.

Abstract

A divergent gene pair is defined as two adjacent genes organized head to head in opposite orientation, sharing a common promoter region. Divergent gene pairs are mainly coexpressed, but some display opposite regulation. The mechanistic basis of such anti-correlated regulation is not well understood. Here, the regulation of the Arabidopsis thaliana gene pair At1g71850/At1g71860 was investigated. Semi-quantitative RT-PCR and Genevestigator analyses showed that while one of the pair was upregulated by exposure to low temperature, the same treatment downregulated the other. Promoter::GUS fusion transgenes were used to show that this behavior was driven by a bidirectional promoter, which harbored an as-1 motif, associated with the low-temperature response; mutation of this sequence produced a significant decrease in cold-responsive expression. With regard to the as-1 motif in the native orientation repressing the promoter’s low-temperature responsiveness, the same as-1 motif introduced in the reverse direction showed a slight enhancement in the promoter’s responsiveness to low-temperature exposure, indicating that the orientation of the motif was important for the promoter’s activity. These findings provide new insights into the complex transcriptional regulation of bidirectional gene pairs as well as plant stress response.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Abbreviations

AVT:

AtGenExpress Visualization Tool

GUS:

β-Glucuronidase

MS:

Murashige and Skoog

X-gluc:

5-Bromo-4-chloro-3-indolyl-β-D-glucuronide

WT:

Wild type

PlantCARE:

Plant Cis-acting regulatory element

PLACE:

Plant Cis-acting regulatory DNA elements

as-1 :

Activation sequence-1

as-2 :

Activation sequence-2

OBP1:

OBF binding protein 1

OBF:

Ocs-Element binding protein

TGA:

TGACG motif binding protein

MJ:

Methyl jasmonate

References

  • Adachi N, Lieber MR (2002) Bidirectional gene organization: a common architectural feature of the human genome. Cell 109:807–809

    Article  CAS  PubMed  Google Scholar 

  • Andriankaja A, Boisson-Dernier A, Frances L, Sauviac L, Jauneau A, Barker DG, de Carvalho-Niebel F (2007) AP2-ERF transcription factors mediate Nod factor dependent Mt ENOD11 activation in root hairs via a novel cis-regulatory motif. Plant Cell 19:2866–2885

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Banerjee J, Sahoo DK, Dey N, Houtz RL, Maiti IB (2013) An intergenic region shared by At4g35985 and At4g35987 in Arabidopsis thaliana is a tissue specific and stress inducible bidirectional promoter analyzed in transgenic arabidopsis and tobacco plants. PLoS One 8:e79622

    Article  PubMed  PubMed Central  Google Scholar 

  • Bartels S, Anderson JC, Gonzalez Besteiro MA, Carreri A, Hirt H, Buchala A, Metraux JP, Peck SC, Ulm R (2009) MAP kinase phosphatase1 and protein tyrosine phosphatase1 are repressors of salicylic acid synthesis and SNC1-mediated responses in Arabidopsis. Plant Cell 21:2884–2897

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beck CF, Warren RA (1988) Divergent promoters, a common form of gene organization. Microbiol Rev 52:318–326

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bondino HG, Valle EM (2009) A small intergenic region drives exclusive tissue-specific expression of the adjacent genes in Arabidopsis thaliana. BMC Mol Biol 10:95

    Article  PubMed  PubMed Central  Google Scholar 

  • Bouchez D, Tokuhisa JG, Llewellyn DJ, Dennis ES, Ellis JG (1989) The ocs-element is a component of the promoters of several T-DNA and plant viral genes. EMBO J 8:4197–4204

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Bubner B, Baldwin IT (2004) Use of real-time PCR for determining copy number and zygosity in transgenic plants. Plant Cell Rep 23:263–271

    Article  CAS  PubMed  Google Scholar 

  • Chang DT, Wu CY, Fan CY (2012) A study on promoter characteristics of head-to-head genes in Saccharomyces cerevisiae. BMC Genom 13(Suppl 1):S11

    Article  CAS  Google Scholar 

  • Chen W, Singh KB (1999) The auxin, hydrogen peroxide and salicylic acid induced expression of the Arabidopsis GST6 promoter is mediated in part by an ocs element. Plant J 19:667–677

    Article  CAS  PubMed  Google Scholar 

  • Chen W, Chao G, Singh KB (1996) The promoter of a H2O2-inducible, Arabidopsis glutathione S-transferase gene contains closely linked OBF- and OBP1-binding sites. Plant J 10:955–966

    Article  CAS  PubMed  Google Scholar 

  • Chen WH, de Meaux J, Lercher MJ (2010) Co-expression of neighbouring genes in Arabidopsis: separating chromatin effects from direct interactions. BMC Genom 11:178

    Article  Google Scholar 

  • Cheng C, Yun KY, Ressom HW, Mohanty B, Bajic VB, Jia Y, Yun SJ, de los Reyes BG (2007) An early response regulatory cluster induced by low temperature and hydrogen peroxide in seedlings of chilling-tolerant japonica rice. BMC Genom 8:175

    Article  Google Scholar 

  • Christoffersen CA, Brickman TJ, Hook-Barnard I, McIntosh MA (2001) Regulatory architecture of the iron-regulated fepD-ybdA bidirectional promoter region in Escherichia coli. J Bacteriol 183:2059–2070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clough SJ, Bent AF (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J 16:735–743

    Article  CAS  PubMed  Google Scholar 

  • De Paolis A, Sabatini S, De Pascalis L, Costantino P, Capone I (1996) A rolB regulatory factor belongs to a new class of single zinc finger plant proteins. Plant J 10:215–223

    Article  PubMed  Google Scholar 

  • Delpy L, Decourt C, Le Bert M, Cogné M (2002) B cell development arrest upon insertion of a neo gene between JH and Eμ: promoter competition results in transcriptional silencing of germline JH and complete V (D) J rearrangements. J Immunol 169:6875–6882

    Article  CAS  PubMed  Google Scholar 

  • Despres C, DeLong C, Glaze S, Liu E, Fobert PR (2000) The Arabidopsis NPR1/NIM1 protein enhances the DNA binding activity of a subgroup of the TGA family of bZIP transcription factors. Plant Cell 12:279–290

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Di Matteo G, Salerno M, Guarguaglini G, Di Fiore B, Palitti F, Lavia P (1998) Interactions with single-stranded and double-stranded DNA-binding factors and alternative promoter conformation upon transcriptional activation of the Htf9-a/RanBP1 and Htf9-c genes. J Biol Chem 273:495–505

    Article  PubMed  Google Scholar 

  • Du H, Zhang Z, Li J (2010) Isolation and functional characterization of a waterlogging-induced promoter from maize. Plant Cell Rep 29:1269–1275

    Article  CAS  PubMed  Google Scholar 

  • Ellis JG, Llewellyn DJ, Walker JC, Dennis ES, Peacock WJ (1987) The ocs element: a 16 base pair palindrome essential for activity of the octopine synthase enhancer. EMBO J 6:3203–3208

    CAS  PubMed  PubMed Central  Google Scholar 

  • Engstrom PG, Suzuki H, Ninomiya N, Akalin A, Sessa L, Lavorgna G, Brozzi A, Luzi L, Tan SL, Yang L, Kunarso G, Ng EL, Batalov S, Wahlestedt C, Kai C, Kawai J, Carninci P, Hayashizaki Y, Wells C, Bajic VB, Orlando V, Reid JF, Lenhard B, Lipovich L (2006) Complex Loci in human and mouse genomes. PLoS Genet 2:e47

    Article  PubMed  PubMed Central  Google Scholar 

  • Foley RC, Sappl PG, Perl-Treves R, Millar AH, Singh KB (2006) Desensitization of GSTF8 induction by a prior chemical treatment is long lasting and operates in a tissue-dependent manner. Plant Physiol 142:245–253

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garreton V, Carpinelli J, Jordana X, Holuigue L (2002) The as-1 promoter element is an oxidative stress-responsive element and salicylic acid activates it via oxidative species. Plant Physiol 130:1516–1526

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ghelis T, Bolbach G, Clodic G, Habricot Y, Miginiac E, Sotta B, Jeannette E (2008) Protein tyrosine kinases and protein tyrosine phosphatases are involved in abscisic acid-dependent processes in Arabidopsis seeds and suspension cells. Plant Physiol 148:1668–1680

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilmartin PM, Sarokin L, Memelink J, Chua NH (1990) Molecular light switches for plant genes. Plant Cell 2:369–378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Guevara-García A, López-Ochoa L, López-Bucio J, Simpson J, Herrera-Estrella L (1998) A 42 bp fragment of the pmas1′ promoter containing an ocs-like element confers a developmental, wound- and chemically inducible expression pattern. Plant Mol Biol 38:743–753

    Article  PubMed  Google Scholar 

  • Gupta R, Luan S (2003) Redox control of protein tyrosine phosphatases and mitogen-activated protein kinases in plants. Plant Physiol 132:1149–1152

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hansen JJ, Bross P, Westergaard M, Nielsen MN, Eiberg H, Borglum AD, Mogensen J, Kristiansen K, Bolund L, Gregersen N (2003) Genomic structure of the human mitochondrial chaperonin genes: HSP60 and HSP10 are localised head to head on chromosome 2 separated by a bidirectional promoter. Hum Genet 112:71–77

    Article  CAS  PubMed  Google Scholar 

  • Herr DR, Harris GL (2004) Close head-to-head juxtaposition of genes favors their coordinate regulation in Drosophila melanogaster. FEBS Lett 572:147–153

    Article  CAS  PubMed  Google Scholar 

  • Hirschman J, Durbin K, Winston F (1988) Genetic evidence for promoter competition in Saccharomyces cerevisiae. Mol Cell Biol 8:4608–4615

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ikeda S, Ayabe H, Mori K, Seki Y, Seki S (2002) Identification of the functional elements in the bidirectional promoter of the mouse O-sialoglycoprotein endopeptidase and APEX nuclease genes. Biochem Biophys Res Commun 296:785–791

    Article  CAS  PubMed  Google Scholar 

  • Jefferson RA, Kavanagh TA, Bevan MW (1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J 6:3901–3907

    CAS  PubMed  PubMed Central  Google Scholar 

  • Keddie JS, Tsiantis M, Piffanelli P, Cella R, Hatzopoulos P, Murphy DJ (1994) A seed-specific Brassica napus oleosin promoter interacts with a G-box-specific protein and may be bi-directional. Plant Mol Biol 24:327–340

    Article  CAS  PubMed  Google Scholar 

  • Kensche PR, Oti M, Dutilh BE, Huynen MA (2008) Conservation of divergent transcription in fungi. Trends Genet 24:207–211

    Article  CAS  PubMed  Google Scholar 

  • Kourmpetli S, Lee K, Hemsley R, Rossignol P, Papageorgiou T, Drea S (2013) Bidirectional promoters in seed development and related hormone/stress responses. BMC Plant Biol 13:187

    Article  PubMed  PubMed Central  Google Scholar 

  • Krom N, Ramakrishna W (2008) Comparative analysis of divergent and convergent gene pairs and their expression patterns in rice, Arabidopsis, and populus. Plant Physiol 147:1763–1773

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lam E, Chua N-H (1989) ASF-2: a factor that binds to the cauliflower mosaic virus 35S promoter and a conserved GATA motif in Cab promoters. Plant Cell 1:1147–1156

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lam E, Lam YK (1995) Binding site requirements and differential representation of TGF factors in nuclear ASF-1 activity. Nucl Acids Res 23:3778–3785

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lam E, Benfey PN, Gilmartin PM, Fang RX, Chua NH (1989) Site-specific mutations alter in vitro factor binding and change promoter expression pattern in transgenic plants. Proc Natl Acad Sci USA 86:7890–7894

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lee SG, Song K (2000) Identification and characterization of a bidirectional promoter from the intergenic region between the human DDX13 and RD genes. Mol Cells 10:47–53

    Article  CAS  PubMed  Google Scholar 

  • Liu SJ, Yue QJ, Zhang W (2015) Structural and functional analysis of an asymmetric bidirectional promoter in Arabidopsis thaliana. J Integr Plant Biol 57:162–170

    Article  CAS  PubMed  Google Scholar 

  • McGarry RC, Ayre BG (2008) A DNA element between At4g28630 and At4g28640 confers companion-cell specific expression following the sink-to-source transition in mature minor vein phloem. Planta 228:839–849

    Article  CAS  PubMed  Google Scholar 

  • Mishra RC, Grover A (2014) Intergenic sequence between Arabidopsis caseinolytic protease B-cytoplasmic/heat shock protein100 and choline kinase genes functions as a heat-inducible bidirectional promoter. Plant Physiol 166:1646–1658

    Article  PubMed  PubMed Central  Google Scholar 

  • Mitra A, Han J, Zhang ZJ, Mitra A (2009) The intergenic region of Arabidopsis thaliana cab1 and cab2 divergent genes functions as a bidirectional promoter. Planta 229:1015–1022

    Article  CAS  PubMed  Google Scholar 

  • Nakayama T, Sakamoto A, Yang P, Minami M, Fujimoto Y, Ito T, Iwabuchi M (1992) Highly conserved hexamer, octamer and nonamer motifs are positive cis-regulatory elements of the wheat histone H3 gene. FEBS Lett 300:167–170

    Article  CAS  PubMed  Google Scholar 

  • Narsai R, Law SR, Carrie C, Xu L, Whelan J (2011) In-depth temporal transcriptome profiling reveals a crucial developmental switch with roles for RNA processing and organelle metabolism that are essential for germination in Arabidopsis. Plant Physiol 157:1342–1362

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nieto C, Puyet A, Espinosa M (2001) MalR-mediated regulation of the Streptococcus pneumoniae malMP operon at promoter PM. Influence of a proximal divergent promoter region and competition between MalR and RNA polymerase proteins. J Biol Chem 276:14946–14954

    Article  CAS  PubMed  Google Scholar 

  • Odell JT, Knowlton S, Lin W, Mauvais CJ (1988) Properties of an isolated transcription stimulating sequence derived from the cauliflower mosaic virus 35S promoter. Plant Mol Biol 10:263–272

    Article  CAS  PubMed  Google Scholar 

  • Ow DW, Jacobs JD, Howell SH (1987) Functional regions of the cauliflower mosaic virus 35S RNA promoter determined by use of the firefly luciferase gene as a reporter of promoter activity. Proc Natl Acad Sci USA 84:4870–4874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pontier D, Privat I, Trifa Y, Zhou JM, Klessig DF, Lam E (2002) Differential regulation of TGA transcription factors by post-transcriptional control. Plant J 32:641–653

    Article  CAS  PubMed  Google Scholar 

  • Qin XF, Holuigue L, Horvath DM, Chua NH (1994) Immediate early transcription activation by salicylic acid via the cauliflower mosaic virus as-1 element. Plant Cell 6:863–874

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sadanandom A, Piffanelli P, Knott T, Robinson C, Sharpe A, Lydiate D, Murphy D, Fairbairn DJ (1996) Identification of a peptide methionine sulphoxide reductase gene in an oleosin promoter from Brassica napus. Plant J 10:235–242

    Article  CAS  PubMed  Google Scholar 

  • Shin R, Kim MJ, Paek KH (2003) The CaTin1 (Capsicum annuum TMV-induced clone 1) and CaTin1-2 genes are linked head-to-head and share a bidirectional promoter. Plant Cell Physiol 44:549–554

    Article  CAS  PubMed  Google Scholar 

  • Silver J, Limjoco T, Feinstone S (1995) Site-specific mutagenesis using the polymerase chain reaction. In: Innis MA, Gelfand DH, Sninsky JJ (eds) PCR Strategies. Academic Press, San Diego, pp 179–188

    Chapter  Google Scholar 

  • Singh K, Tokuhisa JG, Dennis ES, Peacock WJ (1989) Saturation mutagenesis of the octopine synthase enhancer: correlation of mutant phenotypes with binding of a nuclear protein factor. Proc Natl Acad Sci USA 86:3733–3737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Singh A, Sahi C, Grover A (2009) Chymotrypsin protease inhibitor gene family in rice: genomic organization and evidence for the presence of a bidirectional promoter shared between two chymotrypsin protease inhibitor genes. Gene 428:9–19

    Article  CAS  PubMed  Google Scholar 

  • Skirycz A, Radziejwoski A, Busch W, Hannah MA, Czeszejko J, Kwasniewski M, Zanor MI, Lohmann JU, De Veylder L, Witt I, Mueller-Roeber B (2008) The DOF transcription factor OBP1 is involved in cell cycle regulation in Arabidopsis thaliana. Plant J 56:779–792

    Article  CAS  PubMed  Google Scholar 

  • Spitz F, Furlong EE (2012) Transcription factors: from enhancer binding to developmental control. Nat Rev Genet 13:613–626

    Article  CAS  PubMed  Google Scholar 

  • Tokuhisa JG, Singh K, Dennis ES, Peacock WJ (1990) A DNA-binding protein factor recognizes two binding domains within the octopine synthase enhancer element. Plant Cell 2:215–224

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Trinklein ND, Aldred SF, Hartman SJ, Schroeder DI, Otillar RP, Myers RM (2004) An abundance of bidirectional promoters in the human genome. Genome Res 14:62–66

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Truman W, Sreekanta S, Lu Y, Bethke G, Tsuda K, Katagiri F, Glazebrook J (2013) The CALMODULIN-BINDING PROTEIN60 family includes both negative and positive regulators of plant immunity. Plant Physiol 163:1741–1751

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tsai HK, Su CP, Lu MY, Shih CH, Wang D (2007) Co-expression of adjacent genes in yeast cannot be simply attributed to shared regulatory system. BMC Genom 8:352

    Article  Google Scholar 

  • Tsai HK, Huang PY, Kao CY, Wang D (2009) Co-expression of neighboring genes in the zebrafish (Danio rerio) genome. Int J Mol Sci 10:3658–3670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ulmasov T, Hagen G, Guilfoyle T (1994) The ocs element in the soybean GH2/4 promoter is activated by both active and inactive auxin and salicylic acid analogues. Plant Mol Biol 26:1055–1064

    Article  CAS  PubMed  Google Scholar 

  • Wang H, Wang S, Lu Y, Alvarez S, Hicks LM, Ge X, Xia Y (2012) Proteomic analysis of early-responsive redox-sensitive proteins in Arabidopsis. J Proteome Res 11:412–424

    Article  CAS  PubMed  Google Scholar 

  • Xu Q, Fu HH, Gupta R, Luan S (1998) Molecular characterization of a tyrosine-specific protein phosphatase encoded by a stress-responsive gene in Arabidopsis. Plant Cell 10:849–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yanagisawa S (2004) Dof domain proteins: plant-specific transcription factors associated with diverse phenomena unique to plants. Plant Cell Physiol 45:386–391

    Article  CAS  PubMed  Google Scholar 

  • Yang MQ, Elnitski LL (2008) Diversity of core promoter elements comprising human bidirectional promoters. BMC Genom 9(Suppl 2):S3

    Article  Google Scholar 

  • Yin Y, Chen L, Beachy R (1997) Promoter elements required for phloem-specific gene expression from the RTBV promoter in rice. Plant J 12:1179–1188

    Article  CAS  PubMed  Google Scholar 

  • Zhang B, Singh KB (1994) ocs element promoter sequences are activated by auxin and salicylic acid in Arabidopsis. Proc Natl Acad Sci USA 91:2507–2511

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang B, Chen W, Foley RC, Büttner M, Singh KB (1995) Interactions between distinct types of DNA binding proteins enhance binding to ocs element promoter sequences. Plant Cell 7:2241–2252

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Fan W, Kinkema M, Li X, Dong X (1999) Interaction of NPR1 with basic leucine zipper protein transcription factors that bind sequences required for salicylic acid induction of the PR-1 gene. Proc Natl Acad Sci USA 96:6523–6528

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou JM, Trifa Y, Silva H, Pontier D, Lam E, Shah J, Klessig DF (2000) NPR1 differentially interacts with members of the TGA/OBF family of transcription factors that bind an element of the PR-1 gene required for induction by salicylic acid. Mol Plant Microbe Interact 13:191–202

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We sincerely thank Dr. Hewei Du and Prof. Zuxin Zhang for providing the transgenic Arabidopsis lines containing one-copy zmzf-GUS transgene. This research was financially supported by the National Natural Science Foundation of China (31271506 to WZ and 31200196 to SL), Program for New Century Excellent Talents in University (NCET-13-0354), the Shandong Science Fund for Distinguished Young Scholars (2014JQE27047) and the Shandong provincial Natural Science Foundation (ZR2011CQ016).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wei Zhang.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Communicated by Renate Schmidt.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLS 48 kb)

Supplementary material 2 (DOC 2597 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Liu, S., Chen, H., Li, X. et al. A low-temperature-responsive element involved in the regulation of the Arabidopsis thaliana At1g71850/At1g71860 divergent gene pair. Plant Cell Rep 35, 1757–1767 (2016). https://doi.org/10.1007/s00299-016-1994-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00299-016-1994-y

Keywords

Navigation