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Changes in the Transcriptome of Dry Leafy Spurge (Euphorbia esula) Seeds Imbibed at a Constant and Alternating Temperature

Published online by Cambridge University Press:  20 January 2017

Michael E. Foley ,
Wun S. Chao ,
Münevver Doğramaci ,
David P. Horvath  and
James V. Anderson
Michael E. Foley*
Affiliation:
USDA-Agricultural Research Service, Biosciences Research Lab, Weed Biology Research Unit, 1605 Albrecht Boulevard, Fargo, ND 58102-2765
Wun S. Chao
Affiliation:
USDA-Agricultural Research Service, Biosciences Research Lab, Weed Biology Research Unit, 1605 Albrecht Boulevard, Fargo, ND 58102-2765
Münevver Doğramaci
Affiliation:
USDA-Agricultural Research Service, Biosciences Research Lab, Weed Biology Research Unit, 1605 Albrecht Boulevard, Fargo, ND 58102-2765
David P. Horvath
Affiliation:
USDA-Agricultural Research Service, Biosciences Research Lab, Weed Biology Research Unit, 1605 Albrecht Boulevard, Fargo, ND 58102-2765
James V. Anderson
Affiliation:
USDA-Agricultural Research Service, Biosciences Research Lab, Weed Biology Research Unit, 1605 Albrecht Boulevard, Fargo, ND 58102-2765
*
Corresponding author's E-mail: michael.foley@ars.usda.gov
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Abstract

Leafy spurge seeds are responsive to alternating temperature rather than constant temperature for germination. Transcriptome changes of dry leafy spurge seeds and seeds imbibed for 1 and 3 d at 20 C constant (C) and 20 : 30 C alternating (A) temperature were determined by microarray analysis to examine temperature responsiveness. Principal component analysis revealed differences in the transcriptome of imbibed seeds based on the temperature regime. Computational methods in bioinformatics parsed the data into overrepresented AraCyc pathways and gene regulation subnetworks providing biological context to temperature responses. After 1 d of imbibition, the degradation of starch and sucrose leading to anaerobic respiration were common pathways at both temperature regimes. Several overrepresented pathways unique to 1 d A were associated with generation of energy, reducing power, and carbon substrates; several of these pathways remained overrepresented and up-regulated at 3 d A. At 1 d C, pathways for the phytohormones jasmonic acid and brassinosteroids were uniquely overrepresented. There was little similarity in overrepresented pathways at 1 d C between leafy spurge and arabidopsis seeds, indicating species-specific effects upon imbibition of dry seeds. Overrepresented gene subnetworks at 1 d and 3 d at both temperature regimes related to signaling processes and stress responses. A major overrepresented subnetwork unique to 1 d C related to photomorphogenesis via the E3 ubiquitin ligase COP1. At 1 d A, major overrepresented subnetworks involved circadian rhythm via LHY and TOC1 proteins and expression of stress-related genes such as DREB1A, which is subject to circadian regulation. Collectively, substantial differences were observed in the transcriptome of leafy spurge seeds imbibed under conditions that affect the capacity to germinate.

Keywords

Mouse-ear cress, Arabidopsis thaliana (L.) Heynhleafy spurge, Euphorbia esula L. (EPHES)Gene expressiongerminationimbibitionmicroarrayweed
Type
Weed Biology and Ecology
Information
Weed Science , Volume 60 , Issue 1 , March 2012 , pp. 48 - 56
Copyright
Copyright © Weed Science Society of America 

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References

Literature Cited

Achard, P. and Genschik, P. 2009. Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J. Exp. Bot. 60:1085–1092.Google Scholar
Ali-Rachedi, S., Bouinot, D., Wagner, M-H., Bonnet, M., Sotta, B., Grappin, P., and Jullien, M. 2004. Changes in endogenous abscisic acid levels during dormancy release and maintenance of mature seeds: studies with the Cape Verde Islands ecotype, the dormant model of Arabidopsis thaliana . Planta. 219:479–488.Google Scholar
Anderson, G. L., Prosser, C. W., Wendel, L. E., Delfosse, E. S., and Faust, R. M. 2003. The Ecological Areawide Management (TEAM) of leafy spurge program of the United States Department of Agriculture–Agricultural Research Service. Pest Manag. Sci. 59:609–613.Google Scholar
Anderson, J. V., Horvath, D. P., Chao, W. S., et al. 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
Arc, E., Galland, M., Cueff, G., Godin, B., Lounifi, I., Job, D., and Rajjou, L. 2011. Reboot the system thanks to protein post-translational modifications and proteome diversity: how quiescent seeds restart their metabolism to prepare seedling establishment. Proteomics. 11:1606–1618.Google Scholar
Auge, G. A., Perelman, S., Crocco, C. D., Sánchez, R. A., and Botto, J. F. 2009. Gene expression analysis of light-modulated germination in tomato seeds. New Phytol. 183:301–314.Google Scholar
Baker, H. G. 1974. The evolution of weeds. Ann. Rev. Ecol. Syst. 5:1–24.Google Scholar
Barrero, J. M., Talbot, M. J., White, R. G., Jacobsen, J. V., and Gubler, F. 2009. Anatomical and transcriptomic studies of the coleorhiza reveal the importance of this tissue in regulating dormancy in barley. Plant Physiol. 150:1006–1021.Google Scholar
Baskin, C. C. and Baskin, J. M. 1998. Seeds: Ecology, Biogeography, and Evolution of Dormancy and Germination. San Diego, CA Academic Press. 666 p.Google Scholar
Benech-Arnold, R. L., Sánchez, R. A., Forcella, F., Kruka, B. C., and Ghersa, C. M. 2000. Environmental control of dormancy in weed seed banks in soil. Field Crops Res. 67:105–122.Google Scholar
Brown, E. O. and Porter, R. H. 1942. The viability and germination of seeds of Convolvulus arvensis L. and other perennial weeds. Iowa Agric. Exp. Stn. Res. Bull. 294:475–504.Google Scholar
Browse, J. 2009. Jasmonate passes muster: a receptor and targets for the defense hormone. Annu. Rev. Plant Biol. 60:183–205.Google Scholar
Cadman, C. S. C., Toorop, P. E., Hilhorst, H. W. M., and Finch-Savage, W. E. 2006. Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J. 46:805–822.Google Scholar
Carranco, R. l., Espinosa, J. M., Prieto-Dapena, P., Almoguera, C., and Jordano, J. 2010. Repression by an auxin/indole acetic acid protein connects auxin signaling with heat shock factor-mediated seed longevity. Proc. Natl. Acad. Sci. USA. 107:21908–21913.Google Scholar
Carrera, E., Holman, T., Medhurst, A., Dietrich, D., Footitt, S., Theodoulou, F. L., and Holdsworth, M. J. 2008. Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. Plant J. 53:214–224.Google Scholar
Chao, W. S. 2008. Real-time PCR as a tool to study weed biology. Weed Sci. 56:290–296.Google Scholar
Chiang, G. C. K., Barua, D., Kramer, E. M., Amasino, R. M., and Donohue, K. 2009. Major flowering time gene, FLOWERING LOCUS C, regulates seed germination in Arabidopsis thaliana . Proc. Natl. Acad. Sci. USA. 106:11661–11666.Google Scholar
Churchill, G. A. 2002. Fundamentals of experimental design for cDNA microarrays. Nat. Genet. 32:490–495.Google Scholar
Cutler, S. R., Rodriguez, P. L., Finkelstein, R. R., and Abrams, S. R. 2010. Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61:651–679.Google Scholar
Dave, A., Hernández, M. L., He, Z., Andriotis, V. M. E., Vaistij, F. E., Larson, T. R., and Graham, I. A. 2011. 12-oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis . Plant Cell. 23:583–599.Google Scholar
Debeaujon, I. and Koornneef, M. 2000. Gibberellin requirement for Arabidopsis seed germination is determined both by testa characteristics and embryonic abscisic acid. Plant Physiol. 122:415–424.Google Scholar
de Montaigu, A., Tóth, R., and Coupland, G. 2010. Plant development goes like clockwork. Trends Genet. 26:296–306.Google Scholar
Dietrich, K., Weltmeier, F., Ehlert, A., Weiste, C., Stahl, M., Harter, K., and Dröge-Laser, W. 2011. Heterodimers of the Arabidopsis transcription factors bZIP1 and bZIP53 reprogram amino acid metabolism during low energy stress. Plant Cell. 23:381–395.Google Scholar
Dure, L. and Waters, L. 1965. Long-lived messenger RNA: evidence from cotton seed germination. Science. 147:410–412.Google Scholar
Eisen, M. B., Spellman, P. T., Brown, P. O., and Botstein, D. 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA. 95:14863–14868.Google Scholar
Fatland, B. L., Nikolau, B. J., and Wurtele, E. S. 2005. Reverse genetic characterization of cytosolic acetyl-CoA generation by ATP-citrate lyase in Arabidopsis. Plant Cell. 17:182–203.Google Scholar
Fenner, M. and Thompson, K. 2005. The Ecology of Seeds. Cambridge, UK Cambridge University Press. 260 p.Google Scholar
Fernandez, O., Béthencourt, L., Quero, A., Sangwan, R. S., and Clément, C. 2010. Trehalose and plant stress responses: friend or foe? Trends Plant Sci. 15:409–417.Google Scholar
Finch-Savage, W. E., Cadman, C. S. C., Toorop, P. E., Lynn, J. R., and Hilhorst, H. W. M. 2007. Seed dormancy release in Arabidopsis Cvi by dry after-ripening, low temperature, nitrate and light shows common quantitative patterns of gene expression directed by environmentally specific sensing. Plant J. 51:60–78.Google Scholar
Finch-Savage, W. E. and Leubner-Metzger, G. 2006. Seed dormancy and the control of germination. New Phytol. 171:501–523.Google Scholar
Foley, M. E., Anderson, J. V., Chao, W. S., Doğramaci, 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
Foley, M. E. and Chao, W. S. 2008. Growth regulators and chemicals stimulate germination of leafy spurge (Euphorbia esula) seeds. Weed Sci. 56:516–522.Google Scholar
Fowler, S. G., Cook, D., and Thomashow, M. F. 2005. Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol. 137:961–968.Google Scholar
Gaines, T. A., Zhang, W., Wang, D., et al. 2010. Gene amplification confers glyphosate resistance in Amaranthus palmeri . Proc. Natl. Acad. Sci. USA. 107:1029–1034.Google Scholar
Gaufichon, L., Reisdorf-Cren, M., Rothstein, S. J., Chardon, F., and Suzuki, A. 2010. Biological functions of asparagine synthetase in plants. Plant Sci. 179:141–153.Google Scholar
Geneve, R. L. 2003. Impact of temperature on seed dormancy. Hortscience. 38:336–341.Google Scholar
Guo, J., Wu, J., Ji, Q., Wang, C., Luo, L., Yuan, Y., Wang, Y., and Wang, J. 2008. Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis . J. Genet. Genomics. 35:105–118.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
Howell, K. A., Narsai, R., Carroll, A., Ivanova, A., Lohse, M., Usadel, B., Millar, A. H., and Whelan, J. 2009. Mapping metabolic and transcript temporal switches during germination in rice highlights specific transcription factors and the role of RNA instability in the germination process. Plant Physiol. 149:961–980.Google Scholar
Hsu, S. C., Belmonte, M. F., Harada, J. J., and Inoue, K. 2010. Indispensable roles of plastids in Arabidopsis thaliana embryogenesis. Curr. Genomics. 11:338–349.Google Scholar
Jakoby, M., Weisshaar, B., Dröge-Laser, W., Vicente-Carbajosa, J., Tiedemann, J., Kroj, T., and Parcy, F. 2002. bZIP transcription factors in Arabidopsis . Trends Plant Sci. 7:106–111.Google Scholar
Joshi, A., Olson, D. L., and Carey, D. R. 2009. Overwintering survival of Aphthona beetles (Coleoptera: Chrysomelidae): a biological control agent of leafy spurge released in North Dakota. Environ. Entomol. 38:1539–1545.Google Scholar
Lee, K. P., Piskurewicz, U., Tureĉková, V., Strnad, M., and Lopez-Molina, L. 2010. A seed coat bedding assay shows that RGL2-dependent release of abscisic acid by the endosperm controls embryo growth in Arabidopsis dormant seeds. Proc. Natl. Acad. Sci. USA. 107:19108–19113.Google Scholar
Leivar, P. and Quail, P. H. 2011. PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci. 16:19–28.Google Scholar
Lesica, P. and Hanna, D. 2009. Effect of biological control on leafy spurge (Euphorbia esula) and diversity of associated grasslands over 14 years. Invasive Plant Sci. Manag. 2:151–157.Google Scholar
Lin, R. and Wang, H. 2007. Targeting proteins for degradation by Arabidopsis COP1: teamwork is what matters. J. Integr. Plant Biol. 49:35–42.Google Scholar
Liu, Y., Koornneef, M., and Soppe, W. J. J. 2007. The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell. 19:433–444.Google Scholar
Lopez-Molina, L., Mongrand, S., McLachlin, D. T., Chait, B. T., and Chua, N. H. 2002. ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J. 32:317–328.Google Scholar
Lym, R. G. 2005. Leafy spurge Euphorbia esula L. Pages 99–118 in Duncan, C. L., and Clark, J. K., eds. Invasive Plants of Range and Wildlands and Their Environmental, Economic, and Societal Impacts. Lawrence, KS Weed Science Society of America.Google Scholar
Ma, L., Gao, Y., Qu, L., Chen, Z., Li, J., Zhao, H., and Deng, X. W. 2002. Genomic evidence for COP1 as a repressor of light-regulated gene expression and development in Arabidopsis. Plant Cell. 14:2383–2398.Google Scholar
Mueller, L. A., Zhang, P., and Rhee, S. Y. 2003. AraCyc: a biochemical pathway database for Arabidopsis. Plant Physiol. 132:453–460.Google Scholar
Nakabayashi, K., Okamoto, M., Koshiba, T., Kamiya, Y., and Nambara, E. 2005. Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J. 41:697–709.Google Scholar
Nambara, E., Okamoto, M., Tatematsu, K., Yano, R., Seo, M., and Kamiya, Y. 2010. Abscisic acid and the control of seed dormancy and germination. Seed Sci. Res. 20:55–67.Google Scholar
Novillo, F., Alonso, J. M., Ecker, J. R., and Salinas, J. 2004. CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis . Proc. Natl. Acad. Sci. USA. 101:3985–3990.Google Scholar
Oh, E., Kang, H., Yamaguchi, S., Park, J., Lee, D., Kamiya, Y., and Choi, G. 2009. Genome-wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during seed germination in Arabidopsis . Plant Cell. 21:403–419.Google Scholar
Owen, M. J., Michael, P. J., Renton, M., Steadman, K. J., and Powles, S. B. 2011. Towards large-scale prediction of Lolium rigidum emergence. II. Correlation between dormancy and herbicide resistance levels suggests an impact of cropping systems. Weed. Res. 51:133–141.Google Scholar
Parcy, F., Valon, C., Raynal, M., Gaubiercomella, P., Delseny, M., and Giraudat, J. 1994. Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell. 6:1567–1582.Google Scholar
Penfield, S., Gilday, A. D., Halliday, K. J., and Graham, I. A. 2006. DELLA-mediated cotyledon expansion breaks coat-imposed seed dormancy. Curr. Biol. 16:2366–2370.Google Scholar
Peng, Y., Abercrombie, L. L., Yuan, J. S., Riggins, C. W., Sammons, R. D., Tranel, P. J., and Stewart, C. N. 2010. Characterization of the horseweed (Conyza canadensis) transcriptome using GS-FLX 454 pyrosequencing and its application for expression analysis of candidate non-target herbicide resistance genes. Pest. Manag. Sci. 66:1053–1062.Google Scholar
Pestsova, E., Meinhard, J., Menze, A., Fischer, U., Windhövel, A., and Westhoff, P. 2008. Transcript profiles uncover temporal and stress-induced changes of metabolic pathways in germinating sugar beet seeds. BMC Plant Biol. 8:122.Google Scholar
Preston, J., Tatematsu, K., Kanno, Y., Hobo, T., Kimura, M., Jikumaru, Y., Yano, R., Kamiya, Y., and Nambara, E. 2009. Temporal expression patterns of hormone metabolism genes during imbibition of Arabidopsis thaliana seeds: a comparative study on dormant and non-dormant accessions. Plant Cell Physiol. 50:1786–1800.Google Scholar
Steckel, L. E., Sprague, C. L., Stoller, E. W., and Wax, L. M. 2004. Temperature effects on germination of nine Amaranthus species. Weed Sci. 52:217–221.Google Scholar
Steinbauer, G. P. and Grigsby, B. 1957. Interaction of temperature, light, and moistening agent in the germination of weed seeds. Weeds. 5:175–182.Google Scholar
Stewart, C. N., 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
Subramanian, A., Tamayo, P., and Mootha, V. K. 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA. 102:15545–15550.Google Scholar
Sun, T. 2011. The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr. Biol. 21:R338–R345.Google Scholar
Sweetlove, L. J., Beard, K. F. M., Nunes-Nesi, A., Fernie, A. R., and Ratcliffe, R. G. 2010. Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci. 15:462–470.Google Scholar
Thompson, K. and Grime, J. P. 1983. A comparative study of germination responses to diurnally-fluctuating temperatures. J. Appl. Ecol. 20:141–156.Google Scholar
To, A., Valon, C., Savino, G., Guilleminot, J., Devic, M., Giraudat, J., and Parcy, F. 2006. A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell. 18:1642–1651.Google Scholar
Toh, S., Imamura, A., Watanabe, A., et al. 2008. High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol. 146:1368–1385.Google Scholar
Weller, S. C., Bressan, R. A., Goldsbrough, P. B., Fredenburg, T. B., and Hasegawa, P. M. 2001. The effect of genomics on weed management in the 21st century. Weed. Sci. 49:282–289.Google Scholar
Wilson, I. D., Barker, G. L., Lu, C., Coghill, J. A., Beswick, R. W., Lenton, J. R., and Edwards, K. J. 2005. Alteration of the embryo transcriptome of hexaploid winter wheat (Triticum aestivum cv. Mercia) during maturation and germination. Funct. Integr. Genomics. 5:144–154.Google Scholar
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