Transposon-based activation tagging in cereals
M. A. Ayliffe A B and A. J. Pryor AA CSIRO Plant Industry, Box 1600, Clunies Ross Street, Canberra, ACT 2601, Australia.
B Corresponding author. Email: michael.ayliffe@csiro.au
This paper originates from a presentation at the 1st International Plant Phenomics Symposium, Canberra, Australia, April 2009.
Functional Plant Biology 36(11) 915-921 https://doi.org/10.1071/FP09130
Submitted: 3 June 2009 Accepted: 14 August 2009 Published: 5 November 2009
Abstract
Advances in DNA sequencing technologies have produced an ever increasing number of sequenced genomes. However, many of the genes identified in these sequencing efforts have unknown functions or functions inferred based upon sequence homology, highlighting the necessity for functional gene analysis. Mutagenesis combined with phenotypic analyses remains a key mechanism for identifying and establishing gene function. Activation tagging is a mutagenic process that uses altered gene expression, usually gene overexpression, to generate mutant phenotypes. We have developed an activation tagging system in barley (Hordeum vulgare L.) based upon a maize (Zea mays L.) transposable element that carries two highly expressed cereal promoters. Insertion of this mobile genetic element in the genome can lead to insertional gene inactivation, gene overexpression and gene silencing through the production of antisense transcripts. This transposable element system has also been introduced into both wheat (Triticum aestivum L.) and maize and transposon mobility observed.
Additional keywords: barley, mutation, transgenic, transposon, wheat.
Acknowledgements
We thank the Grains Research and Development Corporation for financial assistance.
Alonso JM,
Stepanova AN,
Leisse TJ,
Kim CJ, Chen H ,
et al
.
(2003) Genome-wide insertional mutagenesis of Arabidopsis thaliana. Science 301, 653–657.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
An S,
Park S,
Jeong DH,
Lee DY, Kang HG ,
et al
.
(2003) Generation and analysis of end sequence database for T-DNA tagging lines in rice. Plant Physiology 133, 2040–2047.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ayliffe MA, Pryor AJ
(2007) Activation tagging in plants – generation of novel, gain-of-function mutations. Australian Journal of Agricultural Research 58, 490–497.
| Crossref | GoogleScholarGoogle Scholar |
Ayliffe MA,
Pallotta M,
Langridge P, Pryor AJ
(2007) A barley activation tagging system. Plant Molecular Biology 64, 329–347.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ayliffe MA,
Agostino A,
Clarke BC,
Furbank R,
von Caemmerer S, Pryor AJ
(2009) Suppression of the barley uroporphyrinogen III synthase gene by a Ds activation tagging element generates developmental photosensitivity. The Plant Cell 21, 814–831.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Bouché N, Bouchez D
(2001)
Arabidopsis gene knockout: phenotypes wanted. Current Opinion in Plant Biology 4, 111–117.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Chen S,
Jin W,
Wang M,
Zhang F,
Zhou J,
Jia Q,
Wu Y,
Liu F, Wu P
(2003) Distribution and characterization of over 1000 T-DNA tags in rice genome. The Plant Journal 36, 105–113.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Chern CG,
Fan MJ,
Yu SM,
Hour AL, Lu PC ,
et al
.
(2007) A rice phenomics study – phenotype scoring and seed propagation of a T-DNA insertion-induced rice mutant population. Plant Molecular Biology 65, 427–438.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Cooper LD,
Marquez-Cedillo L,
Singh J,
Sturbaum AK, Zhang S ,
et al
.
(2004) Mapping Ds insertions in barley using a sequence-based approach. Molecular Genetics and Genomics 272, 181–193.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Fridborg I,
Kuusk S,
Moritz T, Sundberg E
(1999) The Arabidopsis dwarf mutant shi exhibits reduced gibberellin responses conferred by overexpression of a new putative zinc finger protein. The Plant Cell 11, 1019–1031.
|
CAS |
Crossref |
PubMed |
Hirochika H
(2001) Contribution of the Tos17 retrotransposon to rice functional genomics. Current Opinion in Plant Biology 4, 118–122.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Hsing YI,
Chern CG,
Fan MJ,
Lu PC, Chen KT ,
et al
.
(2007) A rice gene activation/knockout mutant resource for high throughput functional genomics. Plant Molecular Biology 63, 351–364.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Ito Y,
Eiguchi M, Kurata N
(2004) Establishment of an enhancer trap system with Ds and GUS for functional genomics in rice. Molecular Genetics and Genomics 271, 639–650.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Izawa T,
Ohnishi T,
Nakano T,
Ishida N, Enoki H ,
et al
.
(1997) Transposon tagging in rice. Plant Molecular Biology 35, 219–229.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Jeon J-S,
Lee S,
Jung K-H,
Jun S-H, Jeong D-H ,
et al
.
(2000) T-DNA insertional mutagenesis for functional genomics in rice. The Plant Journal 22, 561–570.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Jeong D-H,
An S,
Kang H-G,
Moon S,
Han J-J,
Park S,
Lee HS,
An K, An G
(2002) T-DNA insertional mutagenesis for activation tagging in rice. Plant Physiology 130, 1636–1644.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Jeong D-H,
An S,
Park S,
Kang H-G, Park G-G ,
et al
.
(2006) Generation of a flanking sequence-tag database for activation-tagging lines in japonica rice. The Plant Journal 45, 123–132.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Jung K-H,
An G, Ronald PC
(2008) Towards a better bowl of rice: assigning function to tens of thousands of rice genes. Nature Reviews Genetics 9, 91–101.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kakimoto T
(1996) CKI1, a histidine kinase homolog implicated in cytokinin signal transduction. Science 274, 982–985.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kim CM,
Piao HL,
Park SJ,
Chon NS, Je BI ,
et al
.
(2004) Rapid, large-scale generation of Ds transposant lines and analyis of the Ds insertion sites in rice. The Plant Journal 39, 252–263.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Kolesnik T,
Szeverenyi I,
Bachmann D,
Kumar CS,
Jiang S,
Ramamoorthy R,
Cai M,
Ma ZG,
Sundaresan V, Ramachandran S
(2004) Establishing an efficient Ac/Ds tagging system in rice: large-scale analysis of Ds flanking sequences. The Plant Journal 37, 301–314.
|
CAS |
PubMed |
Koprek T,
McElroy D,
Louwerse J,
Williams-Carrier R, Lemaux PG
(2000) An efficient method for dispersing Ds elements in the barley genome as a tool for determining gene function. The Plant Journal 24, 253–263.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Koprek T,
Rangel S,
McElroy D,
Louwerse JD,
Williams-Carrier RE, Lemaux PG
(2001) Transposon-mediated single-copy gene delivery leads to increased transgene expression stability in barley. Plant Physiology 125, 1354–1362.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Krattinger SG,
Lagudah ES,
Spielmeyer W,
Singh RP,
Huerta-Espino J,
McFadden H,
Bossolini E,
Selter LL, Keller B
(2009) A putative ABC transporter confers durable resistance to multiple fungal pathogens in wheat. Science 323, 1360–1363.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Larmande P,
Gay C,
Lorieux M,
Périn C, Bouniol M ,
et al
.
(2008)
Oryza Tag Line, a phenotypic mutant database for the Génoplante rice insertion line library. Nucleic Acids Research 36, D1022–D1027.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Mao C,
Ding W,
Wu Y,
Yu J,
He X,
Shou H, Wu P
(2007) Overexpression of a NAC-domain protein promotes shoot branching in rice. New Phytologist 176, 288–298.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Marsch-Martinez N,
Greco R,
van Arkel G,
Herrera-Estrella L, Pereira A
(2002) Activation tagging using the En-I maize transposon system in Arabidopsis. Plant Physiology 129, 1544–1556.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Mori M,
Tomita C,
Sugimoto K,
Hasegawa M,
Hayashi N,
Dubouzet JG,
Ochiai H,
Sekimoto H,
Hirochika H, Kikuchi S
(2007) Isolation and molecular characterisation of a Spotted leaf 18 mutant by modified activation tagging in rice. Plant Molecular Biology 63, 847–860.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Parinov S,
Sevugan M,
Ye D,
Yang WC,
Kumaran M, Sundaresan V
(1999) Analysis of flanking sequences from dissociation insertion lines: a database for reverse genetics in Arabidopsis. The Plant Cell 11, 2263–2270.
|
CAS |
Crossref |
PubMed |
Rorth P
(1996) A modular misexpression screen in Drosophilia detecting tissue specific phenotypes. Proceedings of the National Academy of Sciences of the United States of America 93, 12418–12422.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Rorth P,
Szabo K,
Bailey A,
Laverty T, Rehm J ,
et al
.
(1998) Systematic gain-of-function genetics in Drosophila. Development 125, 1049–1057.
|
CAS |
PubMed |
Ryu CH,
You JH,
Kang HG,
Hur J,
Kim YH,
Han MJ,
An K,
Chung BC,
Lee CH, An G
(2004) Generation of T-DNA tagging lines with a bidirectional gene trap vector and the establishment of an insertion-site database. Plant Molecular Biology 54, 489–502.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Sallaud C,
Gay C,
Larmande P,
Bès M, Piffanelli P ,
et al
.
(2004) High throughput T-DNA insertion mutagenesis in rice: a first step towards in silico reverse genetics. The Plant Journal 39, 450–464.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Schaffer R,
Ramsay N,
Samach A,
Corden S,
Putterill J,
Carre IA, Coupland G
(1998) The late elongated hypocotyl mutation of Arabidopsis disrupts circadian rhythms and the photoperiodic control of flowering. Cell 93, 1219–1229.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Schneider A,
Kirch T,
Gigolashvili T,
Mock H-P,
Sonnewald U,
Simon R,
Flugge U-I, Werr W
(2005) A transposon-based activation tagging population in Arabidopsis thaliana (TAMARA) and its application in the identification of dominant developmental and metabolic mutations. FEBS Letters 579, 4622–4628.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Scholz S,
Lorz H, Lutticke S
(2001) Transposition of the maize Ac transposable element Ac in barley (Hordeum vulgare L.). Molecular Genetics and Genomics 264, 653–661.
|
CAS |
Singh J,
Zhang S,
Chen C,
Cooper L,
Bregitzer P,
Sturbaum A,
Hayes PM, Lemaux PG
(2006) High frequency Ds remobilization over multiple generations in barley facilitates tagging in large genome cereals. Plant Molecular Biology 62, 937–950.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Springer PS
(2000) Gene traps: tools for plant development and genomics. The Plant Cell 12, 1007–1020.
|
CAS |
Crossref |
PubMed |
Suzuki Y,
Uemura S,
Saito Y,
Murofushi N,
Schmitz G,
Theres K, Yamaguchi I
(2001) A novel transposon tagging element for obtaining gain-of-function mutants based on a self-stabilizing Ac derivative. Plant Molecular Biology 45, 123–131.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Tani H,
Chen X,
Nurmberg P,
Grant JJ,
SantaMaria M,
Chini A,
Gilroy E,
Birch PR, Loake GJ
(2004) Activation tagging in plants: a tool for gene discovery. Functional & Integrative Genomics 4, 258–266.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Theres N,
Scheele T, Starlinger P
(1987) Cloning of the Bz2 locus of Zea mays using the transposable element Ds as a gene tag. Molecular & General Genetics 209, 193–197.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Uauy C,
Distelfeld A,
Fahima T,
Blechl A, Dubcovsky J
(2006) A NAC Gene regulating senescence improves grain protein, zinc, and iron content in wheat. Science 314, 1298–1301.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Upadhyaya NM,
Zhou X-R,
Zhu Q-H,
Ramm K, Eamens A ,
et al
.
(2002) An iAc/Ds gene and enhancer trapping system for insertional mutagenesis in rice. Functional Plant Biology 29, 547–559.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Vaucheret H,
Nussaume L,
Palauqui J-C,
Quillere I, Elmayan T
(1997) A transcriptionally active state is required for post-transcriptional silencing (cosuppression) of nitrate reductase host genes and transgenes. The Plant Cell 9, 1495–1504.
|
CAS |
Crossref |
PubMed |
Wan S,
Wu J,
Zhang Z,
Sun X, Lv Y ,
et al
.
(2009) Activation tagging, an efficient tool for functional analysis of the rice genome. Plant Molecular Biology 69, 69–80.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Weigel D,
Ahn JH,
Blazquez MA,
Borevitz JO, Christensen SK ,
et al
.
(2000) Activation tagging in Arabidopsis. Plant Physiology 122, 1003–1014.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Weil CF
(2009) TILLING in grass species. Plant Physiology 149, 158–164.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Wilson K,
Long D,
Swinburne J, Coupland G
(1996) A dissociation insertion causes a semidominant mutation that increases expression of TINY, an Arabidopsis gene related to APETALA2. The Plant Cell 8, 659–671.
|
CAS |
Crossref |
PubMed |
Wu C,
Li X,
Yuan W,
Chen G, Kilian A ,
et al
.
(2003) Development of enhancer trap lines for functional analysis of the rice genome. The Plant Journal 35, 418–427.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Yahiaoui N,
Srichumpa P,
Dudler R, Keller B
(2004) Genome analysis at different ploidy levels allows cloning of the powdery mildew resistance gene Pm3b from hexaploid wheat. The Plant Journal 37, 528–538.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Yan L,
Loukoianov A,
Tranquilli G,
Helguera M,
Fahima T, Dubcovsky J
(2003) Positional cloning of the wheat vernalization gene VRN1. Proceedings of the National Academy of Sciences of the United States of America 100, 6263–6268.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zhang J,
Li C,
Wu C,
Xiong L,
Chen G,
Zhang Q, Wang S
(2006) RMD: a rice mutant database for functional analysis of the rice genome. Nucleic Acids Research 34, D745–D748.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zhang J,
Guo D,
Chang Y,
You C, Li X ,
et al
.
(2007) Non-random distribution of T-DNA insertions at various levels of the genome hierarchy as revealed by analysing 13 804 T-DNA flanking sequences from as enhancer-trap mutant library. The Plant Journal 49, 947–959.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Zhao T,
Palotta M,
Langridge P,
Prasad M,
Graner A,
Schulze-Lefert P, Koprek T
(2006) Mapped Ds/T-DNA launch pads for functional genomics in barley. The Plant Journal 47, 811–826.
| Crossref | GoogleScholarGoogle Scholar | PubMed |