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BAC Library Development and Clone Characterization for Dormancy-Responsive DREB4A, DAM, and FT from Leafy Spurge (Euphorbia esula) Identifies Differential Splicing and Conserved Promoter Motifs

Published online by Cambridge University Press:  20 January 2017

David P. Horvath ,
David Kudrna ,
Jayson Talag ,
James V. Anderson ,
Wun S. Chao ,
Rod Wing ,
Michael E. Foley  and
Münevver Doğramacı
David P. Horvath*
Affiliation:
Sunflower and Plant Biology Research Unit, Red River Valley Agricultural Research Center, U.S. Department of Agriculture–Agricultural Research Service, Fargo, ND 58102
David Kudrna
Affiliation:
Arizona Genomics Institute, School of Plant Sciences, University of Arizona, Tucson, AZ 85721
Jayson Talag
Affiliation:
Arizona Genomics Institute, School of Plant Sciences, University of Arizona, Tucson, AZ 85721
James V. Anderson
Affiliation:
Sunflower and Plant Biology Research Unit, Red River Valley Agricultural Research Center, U.S. Department of Agriculture–Agricultural Research Service, Fargo, ND 58102
Wun S. Chao
Affiliation:
Sunflower and Plant Biology Research Unit, Red River Valley Agricultural Research Center, U.S. Department of Agriculture–Agricultural Research Service, Fargo, ND 58102
Rod Wing
Affiliation:
Arizona Genomics Institute, School of Plant Sciences, University of Arizona, Tucson, AZ 85721
Michael E. Foley
Affiliation:
Sunflower and Plant Biology Research Unit, Red River Valley Agricultural Research Center, U.S. Department of Agriculture–Agricultural Research Service, Fargo, ND 58102
Münevver Doğramacı
Affiliation:
Sunflower and Plant Biology Research Unit, Red River Valley Agricultural Research Center, U.S. Department of Agriculture–Agricultural Research Service, Fargo, ND 58102
*
Corresponding author's E-mail: david.horvath@ars.usda.gov
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Abstract

We developed two leafy spurge bacterial artificial chromosome (BAC) libraries that together represent approximately 5× coverage of the leafy spurge genome. The BAC libraries have an average insert size of approximately 143 kb, and copies of the library and filters for hybridization-based screening are publicly available through the Arizona Genomics Institute. These libraries were used to clone full-length genomic copies of an AP2/ERF transcription factor of the A4 subfamily of DEHYDRATION-RESPONSIVE ELEMENT-BINDING PROTEINS (DREB) known to be differentially expressed in crown buds of leafy spurge during endodormancy, a DORMANCY ASSOCIATED MADS-BOX (DAM) gene, and several FLOWERING LOCUS T (FT) genes. Sequencing of these BAC clones revealed the presence of multiple FT genes in leafy spurge. Sequencing also provided evidence that two different DAM transcripts expressed in crown buds of leafy spurge during endo- and eco-dormancy result from alternate splicing of a single DAM gene. Sequence data from the FT promoters was used to identify several conserved elements previously recognized in Arabidopsis, as well as potential novel transcription factor binding sites that may regulate FT. These leafy spurge BAC libraries represent a new genomics-based tool that complements existing genomics resources for the study of plant growth and development in this model perennial weed. Furthermore, phylogenetic footprinting using genes identified with this resource demonstrate the usefulness of studying weedy species to further our general knowledge of agriculturally important genes.

Keywords

Arabidopsis, Arabidopsis thaliana L. ARATHleafy spurge, Euphorbia esula L. EPHESAlternate splicingfloweringphylogenetic footprintingtranscription factors
Type
Weed Biology and Ecology
Information
Weed Science , Volume 61 , Issue 2 , June 2013 , pp. 303 - 309
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Alabadi, D., Oyama, T., Yanovsky, M. J., Harmon, F. G., Mas, P., and Kay, S. A. 2001. Reciprocal regulation between TOC1 and LHY/CCA1 within the Arabidopsis circadian clock. Science 293: 880–883.Google Scholar
Anderson, J. V. 2008. Emerging technologies: an opportunity for weed biology research. Weed Sci. 56: 281–282.Google Scholar
Anderson, J. V., Horvath, D. P., Chao, W. S., Foley, M. E., Hernandez, A. G., Thimmapuram, J., Liu, L., Gong, G. L., Band, M., Kim, R., and Mikel, M. A. 2007. Characterization of an EST database for the perennial weed leafy spurge: an important resource for weed biology research. Weed Sci. 55: 193–203.Google Scholar
Bailey, T. L. and Elkan, C. 1994. Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Pp 28–36 in Proceedings of the Second International Conference on Intelligent Systems for Molecular Biology. Menlo Park, CA: AAAI Press.Google Scholar
Blanchette, M., Schwikowski, B., and Tompa, M. 2002. Discovery of regulatory elements by a computational method for phylogenetic footprinting. J. Comp. Biol. 9: 211–223.Google Scholar
Bohlenius, H., Huang, T., Charbonnel-Campaa, L., Brunner, A. M., Jansson, S., Strauss, S. H., and Nilsson, O. 2006. CO/FT regulatory module controls timing of flowering and seasonal growth cessation in trees. Science 312: 1040–1043.Google Scholar
Chao, W. S., Foley, M. E., Doğramacı, M., Anderson, J. V., and Horvath, D. P. 2011. Alternating temperature breaks dormancy in leafy spurge seeds and impacts signaling networks associated with HY5. Funct. Integr. Genomics 11: 637–649.Google Scholar
Chao, W. S., Horvath, D. P., Anderson, J. V., and Foley, M. E. 2005. Potential model weeds to study genomics, ecology, and physiology in the 21st century. Weed Sci. 53: 929–937.Google Scholar
Doğramacı, M., Horvath, D. P., Chao, W. S., Foley, M. E., Christoffers, M. J., and Anderson, J. V. 2010. Extended low temperature impacts dormancy status, flowering competence, and transcript profiles in crown buds of leafy spurge. Plant Mol. Biol. 73: 207–226.Google Scholar
Doğramacı, M., Horvath, D. P., Christoffers, M. J., and Anderson, J. V. 2011. Dehydration and vernalization treatments identify overlapping molecular networks impacting endodormancy maintenance in leafy spurge crown buds. Funct. Integr. Genomics 11: 611–626.Google Scholar
Dong, M. A., Farré, E. M., and Thomashow, M. F. 2011. CIRCADIAN CLOCK-ASSOCIATED 1 and LATE ELONGATED HYPOCOTYL regulate expression of the C-REPEAT BINDING FACTOR (CBF) pathway in Arabidopsis. Proc. Nat. Acad. Sci. U. S. A. 108: 7241–7246.Google Scholar
Foley, M. E., Anderson, J. V., Chao, W. S., Doğramacı, M., and Horvath, D. P. 2010. Initial changes in the transcriptome of Euphorbia esula seeds induced to germinate with a combination of constant and diurnal alternating temperatures. Plant Mol. Biol. 73: 131–142.Google Scholar
Henson, J., Tischler, G., and Ning, Z. 2012. Next-generation sequencing and large genome assemblies. Pharmacogenomics 13: 901–915.Google Scholar
Horvath, D. P. 2009a. Genomics for weed science. Curr. Genomics 11: 47–51.Google Scholar
Horvath, D. P. 2009b. Common mechanisms regulate flowering and dormancy. Plant Sci. 177: 523–531.Google Scholar
Horvath, D. P., Chao, W. S., Suttle, J. C., Thimmapuram, J., and Anderson, J. V. 2008. Transcriptome analysis identifies novel responses and potential regulatory genes involved in seasonal dormancy transitions of leafy spurge (Euphorbia esula L.). BMC Genomics. 9: 536.Google Scholar
Horvath, D. P., Sung, S., Kim, D., Chao, W. S., and Anderson, J. V. 2010. Cloning, characterization, and regulation of DORMANCY-ASSOCIATED MADS-BOX genes from leafy spurge. Plant Mol. Biol. 73: 169–179.Google Scholar
Hsu, C.-Y., Adams, J. P., Klim, H., No, K., Ma, C., Strauss, S. H., Drnevich, J., Vandervelde, L., Ellis, J. D., Rice, M. D., Wickett, N., Gunter, L. E., Tuskan, G. A., Brunner, A. M., Page, G. P., Barakat, A., Carlson, J. E., dePamphilis, C. W., Luthe, D. S., and Yuceer, C. 2011. FLOWERING LOCUS T duplication coordinates reproductive and vegetative growth in perennial poplar. Proc. Nat. Acad. Sci. U. S. A. 108: 10756–10761.Google Scholar
Jeffares, D. C., Mourier, T., and Penny, D. 2006. The biology of intron gain and loss. Trends Genet. 22: 16–22.Google Scholar
Kahn, M. S. 2011. The role of DREB transcription factors in abiotic stress tolerance of plants. Agric. Environ. Biotech. 25: 2433–2442.Google Scholar
Koren, S., Schatz, M. C., Walenz, B. P., Martin, J., Howard, J. T., Ganapathy, G., Wang, Z., Rasko, D. A., McCombie, W. R., Jarvis, E. D., and Phillippy, A. M. 2012. Hybrid error correction and de novo assembly of single-molecule sequencing reads. Nat. Biotech. 30: 693–700.Google Scholar
Lescot, M., Déhais, P., Thijs, G., Marchal, K., Moreau, Y., Van de Peer, Y., Rouzé, P., and Rombauts, S. 2002. PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res. 30: 325–327.Google Scholar
Loman, N. J., Misra, R. V., Dallman, T. J., Constantinidou, C., Gharbia, S. E., Wain, J., and Pallen, M. 2012. Performance comparison of benchtop high-throughput sequencing platforms. Nat. Biotech. 30: 434–439.Google Scholar
Luo, M. and Wing, R. 2003. An improved method for plant BAC library construction. Methods Mol. Biol. 236: 3–20.Google Scholar
Nakano, T., Suzuki, K., Fujimura, T., and Shinshi, H. 2006. Genome-wide analysis of the ERF gene family in Arabidopsis and rice. Plant Physiol. 140: 411–432.Google Scholar
Pin, P. A. and Nilsson, O. 2012. The multifaceted roles of FLOWERING LOCUS T in plant development. Plant Cell Environ. 35: 1742–1755.Google Scholar
Rinne, P. L. H., Welling, A., Vahala, J., Ripel, L., Ruonala, R., Kangasjarvi, J., and van der Schoot, C. 2011. Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-beta-glucanases to reopen signal conduits and release dormancy in Populus . Plant Cell 23: 130–146.Google Scholar
Salome, P. A., To, J. P. C., Kieber, J. J., and McClung, C. R. 2006. Arabidopsis response regulators ARR3 and ARR4 play cytokinin-independent roles in the control of circadian period. Plant Cell 18: 55–69.Google Scholar
Schaller, G. E., Mathews, D. E., Gribskov, M., and Walker, J. C. 2002. Two-component signaling elements and histidyl-aspartyl phosphorelays. in Somerville, C. R., and Meyerowitz, E. M., eds. The Arabidopsis Book. Rockville, MD: American Society of Plant Biologists. doi/10.1199/tab.0044. http://www.aspb.org/publications/arabidopsis/. Accessed January 3, 2013.Google Scholar
Schulz-Schaeffer, J. and Gerhardt, S. 1989. Cytotaxonomic analysis of the Euphorbia spp. (leafy spurge) complex. II. Comparative study of the chromosome morphology. Biol. Zentralbl. 108: 64–76.Google Scholar
Stahevitch, A. E., Crompton, C. W., and Wojtas, W. A. 1988. Cytogenetic studies of leafy spurge, Euphorbia esula, and its allies (Euphorbiaceae). Can. J. Bot. 66: 2247–2257.Google Scholar
Stewart, C. N. Jr., Tranel, P. J., Horvath, D. P., Anderson, J. V., Rieseberg, L. H., Westwood, J. H., Mallory-Smith, C. A., Zapiola, M. L., and Dlugosch, K. M. 2009. Evolution of weediness and invasiveness: charting the course for weed genomics. Weed Sci. 57: 451–462.Google Scholar
The Arabidopsis Information Resource (TAIR), http://www.arabidopsis.org/servlets/Search?type=general&search_action=detail&method=1&show_obsolete=F&name=DREB+subfamily+A-4&sub_type=gene&SEARCH_EXACT=4&SEARCH_CONTAINS=1, on 1/3/2013.Google Scholar
Tiwari, S. B., Shen, Y., Chang, H.-C., Hou, Y., Harris, A., Ma, S. F., McPartland, M., Hymus, G. J., Adam, L., Marion, C., Belachew, A., Repetti, P. P., Reuber, T. L., and Ratcliffe, O. J. 2010. The flowering time regulator CONSTANS is recruited to the FLOWERING LOCUS T promoter via a unique cis-element. New Phytol. 187: 57–66.Google Scholar