The promoter from SlREO, a highly-expressed, root-specific Solanum lycopersicum gene, directs expression to cortex of mature roots
Matthew O. Jones A B C , Kenneth Manning B , John Andrews B , Carole Wright B , Ian B. Taylor A and Andrew J. Thompson BA Plant and Crop Sciences Division, School of Biosciences, University of Nottingham, Sutton Bonington, Loughborough, LE12 5RD, UK.
B Warwick HRI, University of Warwick, Wellesbourne, Warwick, CV35 9EF, UK.
C Corresponding author. Email: matthew.jones@rhul.ac.uk
Functional Plant Biology 35(12) 1224-1233 https://doi.org/10.1071/FP08139
Submitted: 3 May 2008 Accepted: 8 September 2008 Published: 16 December 2008
Abstract
Root-specific promoters are valuable tools for targeting transgene expression, but many of those already described have limitations to their general applicability. We present the expression characteristics of SlREO, a novel gene isolated from tomato (Solanum lycopersicum L.). This gene was highly expressed in roots but had a very low level of expression in aerial plant organs. A 2.4-kb region representing the SlREO promoter sequence was cloned upstream of the uidA GUS reporter gene and shown to direct expression in the root cortex. In mature, glasshouse-grown plants this strict root specificity was maintained. Furthermore, promoter activity was unaffected by dehydration or wounding stress but was somewhat suppressed by exposure to NaCl, salicylic acid and jasmonic acid. The predicted protein sequence of SlREO contains a domain found in enzymes of the 2-oxoglutarate and Fe(II)-dependent dioxygenase superfamily. The novel SlREO promoter has properties ideal for applications requiring strong and specific gene expression in the bulk of tomato root tissue growing in soil, and is also likely to be useful in other Solanaceous crops.
Additional keywords: genetic engineering, over-expression, root expression, Solanaceae, 2-ODD.
Acknowledgements
We thank Carol Evered for assistance in microscopy. We are grateful to Angela Hambidge and Linda Brown for technical assistance. This work was funded by the Department for Environment, Food and Rural Affairs, UK, project HP0218.
Abe M,
Takahashi T, Komeda Y
(2001) Identification of a cis-regulatory element for L1 layer-specific gene expression, which is targeted by an L1-specific homeodomain protein. The Plant Journal 26, 487–494.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bassett CL,
Callahan AM,
Artlip TS,
Scorza R, Srinivasan C
(2007) A minimal peach type II chlorophyll a/b-binding protein promoter retains tissue-specificity and light regulation in tomato. BMC Biotechnology 7, 47.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Benfey PN,
Takatsuji H,
Ren L,
Shah DM, Chua NH
(1990) Sequence requirements of the 5-enolpyruvylshikimate-3-phosphate synthase 5′-upstream region for tissue-specific expression in flowers and seedlings. The Plant Cell 2, 849–856.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bird CR,
Smith CJS,
Ray JA,
Moureau P,
Bevan MW,
Bird AS,
Hughes S,
Morris PC,
Grierson D, Schuch W
(1988) The tomato polygalacturonase gene and ripening-specific expression in transgenic plants. Plant Molecular Biology 11, 651–662.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Bradford M
(1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bucher M,
Schroeer B,
Willmitzer L, Riesmeier JW
(1997) Two genes encoding extensin-like proteins are predominantly expressed in tomato root hair cells. Plant Molecular Biology 35, 497–508.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bucher M,
Brunner S,
Zimmermann P,
Zardi GI,
Amrhein N,
Willmitzer L, Riesmeier JW
(2002) The expression of an extensin-like protein correlates with cellular tip growth in tomato. Plant Physiology 128, 911–923.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Butler ED, Gallagher TF
(2000) Characterization of auxin-induced ARRO-1 expression in the primary root of Malus domestica. Journal of Experimental Botany 51, 1765–1766.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Cardon ZG, Gage DJ
(2006) Resource exchange in the rhizosphere: molecular tools and the microbial perspective. Annual Review of Ecology Evolution and Systematics 37, 459–488.
| Crossref | GoogleScholarGoogle Scholar |
Chan YL,
Prasad V,
Sanjaya
,
Chen KH,
Liu PC,
Chan MT, Cheng CP
(2005) Transgenic tomato plants expressing an Arabidopsis thionin (Thi2.1) driven by fruit-inactive promoter battle against phytopathogenic attack. Planta 221, 386–393.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Chen F,
Ro D-K,
Petri J,
Gershenzon J,
Bohlmann J,
Pichersky E, Tholl D
(2004) Characterization of a root-specific Arabidopsis terpene synthase responsible for the formation of the volatile monoterpene 1,8-cineole. Plant Physiology 135, 1956–1966.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Diatchenko L,
Lau YC,
Campbell AP,
Chenchik A, Moqadam F , et al.
(1996) Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proceedings of the National Academy of Sciences of the United States of America 93, 6025–6030.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Elmayan T, Tepfer M
(1995) Evaluation in tobacco of the organ specificity and strength of the rolD promoter, domain A of the 35S promoter and the 35S2 promoter. Transgenic Research 4, 388–396.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Fester T,
Schmidt D,
Lohse S,
Walter MH,
Giuliano G,
Bramley PM,
Fraser PD,
Hause B, Strack D
(2002) Stimulation of carotenoid metabolism in arbuscular mycorrhizal roots. Planta 216, 148–154.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Garoosi GA,
Salter MG,
Caddick MX, Tomsett AB
(2005) Characterisation of the ethanol-inducible alc gene expression system in tomato. Journal of Experimental Botany 56, 1635–1642.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Giritch A,
Herbik A,
Balzer HJ, Ganal M
(1997) A root-specific iron-regulated gene of tomato encodes a lysyl-tRNA-synthetase-like protein. European Journal of Biochemistry 244, 310–317.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Giritch A,
Ganal M,
Stephan UW, Baumlein H
(1998) Structure, expression and chromosomal localisation of the metallothionein-like gene family of tomato. Plant Molecular Biology 37, 701–714.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Gittins JR,
Hiles ER,
Pellny TK,
Biricolti S, James DJ
(2001) The Brassica napus extA promoter: a novel alternative promoter to CaMV 35S for directing transgene expression to young stem tissues and load bearing regions of transgenic apple trees (Malus pumila Mill). Molecular Breeding 7, 51–62.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Grichko VP, Glick BR
(2001) Flooding tolerance of transgenic tomato plants expressing the bacterial enzyme ACC deaminase controlled by the 35S, rolD or PRB-1b promoter. Plant Physiology and Biochemistry 39, 19–25.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Gubler F, Jacobsen JV
(1992) Gibberellin-responsive elements in the promoter of a barley high pl- α-amylase gene. The Plant Cell 4, 1435–1441.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hagen G, Guilfoyle T
(2002) Auxin-responsive gene expression: genes, promoters and regulatory factors. Plant Molecular Biology 49, 373–385.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hans J,
Hause B,
Strack D, Walter MH
(2004) Cloning, characterization, and immunolocalization of a mycorrhiza-inducible 1-deoxy-d-xylulose 5-phosphate reductoisomerase in arbuscule-containing cells of maize. Plant Physiology 134, 614–624.
| Crossref | d-xylulose 5-phosphate reductoisomerase in arbuscule-containing cells of maize.&journal=Plant Physiology&volume=134&pages=614-624&publication_year=2004&author=MH%20Walter&hl=en&doi=10.1104/pp.103.032342" target="_blank" rel="nofollow noopener noreferrer" class="reftools">GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hausinger RP
(2004) Fe(II)/α-ketoglutarate dependent hydroxylases and related enzymes. Critical Reviews in Biochemistry and Molecular Biology 39, 21–68.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hertig C,
Rebmann G,
Bull J,
Mauch F, Dudler R
(1991) Sequence and tissue-specific expression of a putative peroxidase gene from wheat (Triticum aestivum L.). Plant Molecular Biology 16, 171–174.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Higo K,
Ugawa Y,
Iwamoto M, Korenaga T
(1999) Plant cis-acting regulatory DNA elements (PLACE) database 1999. Nucleic Acids Research 27, 297–300.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hudson ME, Quail PH
(2003) Identification of promoter motifs involved in the network of phytochrome A-regulated gene expression by combined analysis of genomic sequence and microarray data. Plant Physiology 133, 1605–1616.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Itzhaki H,
Maxson JM, Woodson WR
(1994) An ethylene-responsive enhancer element is involved in the senescence-related expression of the carnation glutathione-S-transferase (GST1) gene. Proceedings of the National Academy of Sciences of the United States of America 91, 8925–8929.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Jefferson RA,
Kavanagh TA, Bevan MW
(1987) GUS fusions: β-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO Journal 6, 3901–3907.
|
CAS |
PubMed |
Karimi M,
Inze D, Depicker A
(2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7, 193–195.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Keller B, Baumgartner C
(1991) Vascular-specific expression of the bean grp 1.8 gene is negatively regulated. The Plant Cell 3, 1051–1061.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Klinedinst S,
Pascuzzi P,
Redman J,
Desai M, Arias J
(2000) A xenobiotic-stress-activated transcription factor and its cognate target genes are preferentially expressed in root tip meristems. Plant Molecular Biology 42, 679–688.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Köck M,
Stenzel I, Zimmer A
(2006) Tissue-specific expression of tomato ribonuclease LX during phosphate starvation-induced root growth. Journal of Experimental Botany 57, 3717–3726.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Koyama T,
Ono T,
Shimizu M,
Jinbo T, Mizuno R , et al.
(2005) Promoter of Arabidopsis thaliana phosphate transporter gene drives root-specific expression of transgene in rice. Journal of Bioscience and Bioengineering 99, 38–42.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Krasnyanski SF,
Sandu J,
Domier LL,
Buetow DE, Korbani SS
(2001) Effect of an enhanced CAMV 35S promoter and a fruit-specific promoter on UIDA gene expression in transgenic tomato plants. In Vitro Cellular & Developmental Biology. Plant 37, 427–433.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Liedl BE,
McCormick S, Mutschlerm MA
(1993) A clearing technique for histochemical location of GUS activity in pollen tubes and ovules of Lycopersicon. Plant Molecular Biology Reporter 11, 194–201.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Léon-Kloosterziel KM,
Verhagen BW,
Keurentjes JJ,
Van Pelt JA,
Rep M,
Van Loon LC, Pieterse CM
(2005) Colonization of the Arabidopsis rhizosphere by fluorescent Pseudomonas spp. activates a root-specific, ethylene-responsive PR-5 gene in the vascular bundle. Plant Molecular Biology 57, 731–748.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Liang M,
Haroldsen V,
Cai X, Wu Y
(2006) Expression of a putative laccase gene, ZmLAC1, in maize primary roots under stress. Plant, Cell & Environment 29, 746–753.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Marin E,
Divol F,
Bechtold N,
Vavasseur A,
Nussaume L, Forestier C
(2006) Molecular characterization of three Arabidopsis soluble ABC proteins which expression is induced by sugars. Plant Science 171, 84–90.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Matsuda J,
Okabe S,
Hashimoto T, Yamada Y
(1991) Molecular cloning of hyoscyamine 6 β-hydroxylase, a 2- oxoglutarate- dependent dioxygenase, from cultured roots of Hyoscyamus niger. Journal of Biological Chemistry 266, 9460–9464.
|
CAS |
PubMed |
Mudge SR,
Rae AL,
Diatloff E, Smith FW
(2002) Expression analysis suggests novel roles for members of the Pht1 family of phosphate transporters in Arabidopsis. The Plant Journal 31, 341–353.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Mudge SR,
Smith FW, Richardson AE
(2003) Root-specific and phosphate regulated expression of phytase under the control of a phosphate transporter promoter enables Arabidopsis to grow on phytate as a sole P source. Plant Science 165, 871–878.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Okubara PA, Paulitz TC
(2005) Root defense responses to fungal pathogens: a molecular perspective. Plant and Soil 274, 215–226.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Phillips AL,
Ward DA,
Uknes S,
Appleford N,
Lange T,
Huttly AK,
Gaskin P,
Graebe JE, Hedden P
(1995) Isolation and expression of three gibberellin 20-oxidase cDNA clones from Arabidopsis. Plant Physiology 108, 1049–1057.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Prescott AG, John P
(1996) Dioxygenases: molecular structure and role in plant metabolism. Annual Review of Plant Physiology and Plant Molecular Biology 47, 245–271.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Prescott AG, Lloyd MD
(2000) The iron(II) and 2-oxoacid-dependent dioxygenases and their role in metabolism. Natural Product Reports 17, 367–383.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Radi A,
Dina P, Guy A
(2006) Expression of sarcotoxin IA gene via a root-specific tob promoter enhanced host resistance against parasitic weeds in tomato plants. Plant Cell Reports 25, 297–303.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ro D,
Ehlting J,
Keeling CI,
Lin R,
Mattheus N, Bohlmann J
(2006) Microarray expression profiling and functional characterization of AtTPS genes: duplicated Arabidopsis thaliana sesquiterpene synthase genes At4g13280 and At4g13300 encode root-specific and wound-inducible (Z)-γ-bisabolene synthases. Archives of Biochemistry and Biophysics 448, 104–116.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Saslowsky D, Winkel-Shirley B
(2001) Localisation of flavonoid enzymes in Arabidopsis roots. The Plant Journal 27, 37–48.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Sobeih WY,
Dodd IC,
Bacon MA,
Grierson D, Davies WJ
(2004) Long-distance signals regulating stomatal conductance and leaf growth in tomato (Lycopersicon esculentum) plants subjected to partial root-zone drying. Journal of Experimental Botany 55, 2353–2363.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Subramanian S,
Hu X,
Lu G,
Odelland JT, Yu O
(2004) The promoters of two isoflavone synthase genes respond differentially to nodulation and defence signals in transgenic soybean roots. Plant Molecular Biology 54, 623–639.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Suzuki H,
Fowler TJ, Tierney ML
(1993) Deletion analysis and localization of SbPRP1, a soybean cell wall protein gene, in roots of transgenic tobacco and cowpea. Plant Molecular Biology 21, 109–119.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Tang X,
Wang H,
Brandt AS, Woodson WR
(1993) Organisation and structure of the 1-aminocylcopropane-1-carboxylate oxidase gene family from Petunia hybrida. Plant Molecular Biology 23, 1151–1164.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Thompson AJ, Corlett JE
(1995) mRNA levels of four tomato (Lycopersicon esculentum Mill.L) genes related to fluctuating plant and soil water status. Plant, Cell & Environment 18, 773–780.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Tirajoh A,
Aung TST,
Byun McKay A, Plant AL
(2005) Stress-responsive α-dioxygenase expression in tomato roots. Journal of Experimental Botany 56, 713–723.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Vaughan SP,
James DJ,
Lindsey K, Massiah AJ
(2006) Characterization of FaRB7, a near root-specific gene from strawberry (Fragaria × ananassa Duch.) and promoter activity analysis in homologous and heterologous hosts. Journal of Experimental Botany 57, 3901–3910.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
von Schweinichen C, Büttner M
(2005) Expression of a plant cell wall invertase in roots of Arabidopsis leads to early flowering and an increase in whole plant biomass. Plant Biology 7, 469–475.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
White PJ,
Broadley MR,
Hammond JP, Thompson AJ
(2005) Optimising the potato root system for phosphorous and water acquisition in low-input growing systems. Aspects of Applied Biology 73, 111–118.
Xiao K,
Liu J,
Dewbre G,
Harrison M, Wang ZY
(2006) Isolation and characterization of root-specific phosphate transporter promoters from Medicago truncatula. Plant Biology 8, 439–449.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Xu W,
Purugganan MM,
Polisensky DH,
Antiosiewicz DM,
Fry SC, Braam J
(1995) Arabidopsis TCH4, regulated by hormones and the environment, encodes a xyloglucan endotransglycolase. The Plant Cell 7, 1555–1567.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Yamamoto YT,
Taylor CG,
Acedo GN,
Cheng C, Conkling MA
(1991) Characterization of cis-acting sequences regulating root-specific gene expression in tobacco. The Plant Cell 3, 371–382.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Yoshimoto N,
Takahashi H,
Smith FW,
Yamaya T, Saito K
(2002) Two distinct high-affinity sulfate transporters with different inducibilities mediate uptake of sulfate in Arabidopsis roots. The Plant Journal 29, 465–473.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zhang Z, Gurr SJ
(2000) Walking into the unknown: a ‘step down’ PCR-based technique leading to the direct sequence analysis of flanking genomic DNA. Gene 253, 145–150.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zhang P,
Bohl-Zenger S,
Puonti-Kaerlas J,
Potrykus I, Gruissem W
(2003) Two cassava promoters related to vascular expression and storage root formation. Planta 218, 192–203.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
