Skip to main content
×
Home
    • Aa
    • Aa

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

  • Michael E. Foley (a1), Wun S. Chao (a1), Münevver Doğramaci (a1), David P. Horvath (a1) and James V. Anderson (a1)...
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.

Copyright
Corresponding author
Corresponding author's E-mail: michael.foley@ars.usda.gov
Linked references
Hide All

This list contains references from the content that can be linked to their source. For a full set of references and notes please see the PDF or HTML where available.

P. Achard and P. Genschik 2009. Releasing the brakes of plant growth: how GAs shutdown DELLA proteins. J. Exp. Bot. 60:10851092.

S. Ali-Rachedi , D. Bouinot , M-H. Wagner , M. Bonnet , B. Sotta , P. Grappin , and M. Jullien 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. 219:479488.

G. L. Anderson , C. W. Prosser , L. E. Wendel , E. S. Delfosse , and R. M. Faust 2003. The Ecological Areawide Management (TEAM) of leafy spurge program of the United States Department of Agriculture–Agricultural Research Service. Pest Manag. Sci. 59:609613.

E. Arc , M. Galland , G. Cueff , B. Godin , I. Lounifi , D. Job , and L. Rajjou 2011. Reboot the system thanks to protein post-translational modifications and proteome diversity: how quiescent seeds restart their metabolism to prepare seedling establishment. Proteomics. 11:16061618.

G. A. Auge , S. Perelman , C. D. Crocco , R. A. Sánchez , and J. F. Botto 2009. Gene expression analysis of light-modulated germination in tomato seeds. New Phytol. 183:301314.

H. G. Baker 1974. The evolution of weeds. Ann. Rev. Ecol. Syst. 5:124.

J. M. Barrero , M. J. Talbot , R. G. White , J. V. Jacobsen , and F. Gubler 2009. Anatomical and transcriptomic studies of the coleorhiza reveal the importance of this tissue in regulating dormancy in barley. Plant Physiol. 150:10061021.

R. L. Benech-Arnold , R. A. Sánchez , F. Forcella , B. C. Kruka , and C. M. Ghersa 2000. Environmental control of dormancy in weed seed banks in soil. Field Crops Res. 67:105122.

J. Browse 2009. Jasmonate passes muster: a receptor and targets for the defense hormone. Annu. Rev. Plant Biol. 60:183205.

C. S. C. Cadman , P. E. Toorop , H. W. M. Hilhorst , and W. E. Finch-Savage 2006. Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J. 46:805822.

R. l. Carranco , J. M. Espinosa , P. Prieto-Dapena , C. Almoguera , and J. Jordano 2010. Repression by an auxin/indole acetic acid protein connects auxin signaling with heat shock factor-mediated seed longevity. Proc. Natl. Acad. Sci. USA. 107:2190821913.

E. Carrera , T. Holman , A. Medhurst , D. Dietrich , S. Footitt , F. L. Theodoulou , and M. J. Holdsworth 2008. Seed after-ripening is a discrete developmental pathway associated with specific gene networks in Arabidopsis. Plant J. 53:214224.

W. S. Chao 2008. Real-time PCR as a tool to study weed biology. Weed Sci. 56:290296.

G. C. K. Chiang , D. Barua , E. M. Kramer , R. M. Amasino , and K. Donohue 2009. Major flowering time gene, FLOWERING LOCUS C, regulates seed germination in Arabidopsis thaliana . Proc. Natl. Acad. Sci. USA. 106:1166111666.

G. A. Churchill 2002. Fundamentals of experimental design for cDNA microarrays. Nat. Genet. 32:490495.

S. R. Cutler , P. L. Rodriguez , R. R. Finkelstein , and S. R. Abrams 2010. Abscisic acid: emergence of a core signaling network. Annu. Rev. Plant Biol. 61:651679.

A. Dave , M. L. Hernández , Z. He , V. M. E. Andriotis , F. E. Vaistij , T. R. Larson , and I. A. Graham 2011. 12-oxo-phytodienoic acid accumulation during seed development represses seed germination in Arabidopsis . Plant Cell. 23:583599.

I. Debeaujon and M. Koornneef 2000. Gibberellin requirement for Arabidopsis seed germination is determined both by testa characteristics and embryonic abscisic acid. Plant Physiol. 122:415424.

A. de Montaigu , R. Tóth , and G. Coupland 2010. Plant development goes like clockwork. Trends Genet. 26:296306.

K. Dietrich , F. Weltmeier , A. Ehlert , C. Weiste , M. Stahl , K. Harter , and W. Dröge-Laser 2011. Heterodimers of the Arabidopsis transcription factors bZIP1 and bZIP53 reprogram amino acid metabolism during low energy stress. Plant Cell. 23:381395.

L. Dure and L. Waters 1965. Long-lived messenger RNA: evidence from cotton seed germination. Science. 147:410412.

M. B. Eisen , P. T. Spellman , P. O. Brown , and D. Botstein 1998. Cluster analysis and display of genome-wide expression patterns. Proc. Natl. Acad. Sci. USA. 95:1486314868.

B. L. Fatland , B. J. Nikolau , and E. S. Wurtele 2005. Reverse genetic characterization of cytosolic acetyl-CoA generation by ATP-citrate lyase in Arabidopsis. Plant Cell. 17:182203.

O. Fernandez , L. Béthencourt , A. Quero , R. S. Sangwan , and C. Clément 2010. Trehalose and plant stress responses: friend or foe? Trends Plant Sci. 15:409417.

W. E. Finch-Savage , C. S. C. Cadman , P. E. Toorop , J. R. Lynn , and H. W. M. Hilhorst 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. 51:6078.

W. E. Finch-Savage and G. Leubner-Metzger 2006. Seed dormancy and the control of germination. New Phytol. 171:501523.

M. E. Foley , J. V. Anderson , W. S. Chao , M. Doğramaci , and D. P. Horvath 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. 73:131142.

M. E. Foley and W. S. Chao 2008. Growth regulators and chemicals stimulate germination of leafy spurge (Euphorbia esula) seeds. Weed Sci. 56:516522.

S. G. Fowler , D. Cook , and M. F. Thomashow 2005. Low temperature induction of Arabidopsis CBF1, 2, and 3 is gated by the circadian clock. Plant Physiol. 137:961968.

T. A. Gaines , W. Zhang , D. Wang , et al. 2010. Gene amplification confers glyphosate resistance in Amaranthus palmeri . Proc. Natl. Acad. Sci. USA. 107:10291034.

L. Gaufichon , M. Reisdorf-Cren , S. J. Rothstein , F. Chardon , and A. Suzuki 2010. Biological functions of asparagine synthetase in plants. Plant Sci. 179:141153.

J. Guo , J. Wu , Q. Ji , C. Wang , L. Luo , Y. Yuan , Y. Wang , and J. Wang 2008. Genome-wide analysis of heat shock transcription factor families in rice and Arabidopsis . J. Genet. Genomics. 35:105118.

D. P. Horvath , W. S. Chao , J. C. Suttle , J. Thimmapuram , and J. V. Anderson 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.

K. A. Howell , R. Narsai , A. Carroll , A. Ivanova , M. Lohse , B. Usadel , A. H. Millar , and J. Whelan 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. 149:961980.

S. C. Hsu , M. F. Belmonte , J. J. Harada , and K. Inoue 2010. Indispensable roles of plastids in Arabidopsis thaliana embryogenesis. Curr. Genomics. 11:338349.

M. Jakoby , B. Weisshaar , W. Dröge-Laser , J. Vicente-Carbajosa , J. Tiedemann , T. Kroj , and F. Parcy 2002. bZIP transcription factors in Arabidopsis . Trends Plant Sci. 7:106111.

A. Joshi , D. L. Olson , and D. R. Carey 2009. Overwintering survival of Aphthona beetles (Coleoptera: Chrysomelidae): a biological control agent of leafy spurge released in North Dakota. Environ. Entomol. 38:15391545.

K. P. Lee , U. Piskurewicz , V. Tureĉková , M. Strnad , and L. Lopez-Molina 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. 107:1910819113.

P. Leivar and P. H. Quail 2011. PIFs: pivotal components in a cellular signaling hub. Trends Plant Sci. 16:1928.

R. Lin and H. Wang 2007. Targeting proteins for degradation by Arabidopsis COP1: teamwork is what matters. J. Integr. Plant Biol. 49:3542.

Y. Liu , M. Koornneef , and W. J. J. Soppe 2007. The absence of histone H2B monoubiquitination in the Arabidopsis hub1 (rdo4) mutant reveals a role for chromatin remodeling in seed dormancy. Plant Cell. 19:433444.

L. Lopez-Molina , S. Mongrand , D. T. McLachlin , B. T. Chait , and N. H. Chua 2002. ABI5 acts downstream of ABI3 to execute an ABA-dependent growth arrest during germination. Plant J. 32:317328.

L. Ma , Y. Gao , L. Qu , Z. Chen , J. Li , H. Zhao , and X. W. Deng 2002. Genomic evidence for COP1 as a repressor of light-regulated gene expression and development in Arabidopsis. Plant Cell. 14:23832398.

L. A. Mueller , P. Zhang , and S. Y. Rhee 2003. AraCyc: a biochemical pathway database for Arabidopsis. Plant Physiol. 132:453460.

K. Nakabayashi , M. Okamoto , T. Koshiba , Y. Kamiya , and E. Nambara 2005. Genome-wide profiling of stored mRNA in Arabidopsis thaliana seed germination: epigenetic and genetic regulation of transcription in seed. Plant J. 41:697709.

E. Nambara , M. Okamoto , K. Tatematsu , R. Yano , M. Seo , and Y. Kamiya 2010. Abscisic acid and the control of seed dormancy and germination. Seed Sci. Res. 20:5567.

F. Novillo , J. M. Alonso , J. R. Ecker , and J. Salinas 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. 101:39853990.

E. Oh , H. Kang , S. Yamaguchi , J. Park , D. Lee , Y. Kamiya , and G. Choi 2009. Genome-wide analysis of genes targeted by PHYTOCHROME INTERACTING FACTOR 3-LIKE5 during seed germination in Arabidopsis . Plant Cell. 21:403419.

M. J. Owen , P. J. Michael , M. Renton , K. J. Steadman , and S. B. Powles 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. 51:133141.

F. Parcy , C. Valon , M. Raynal , P. Gaubiercomella , M. Delseny , and J. Giraudat 1994. Regulation of gene expression programs during Arabidopsis seed development: roles of the ABI3 locus and of endogenous abscisic acid. Plant Cell. 6:15671582.

S. Penfield , A. D. Gilday , K. J. Halliday , and I. A. Graham 2006. DELLA-mediated cotyledon expansion breaks coat-imposed seed dormancy. Curr. Biol. 16:23662370.

Y. Peng , L. L. Abercrombie , J. S. Yuan , C. W. Riggins , R. D. Sammons , P. J. Tranel , and C. N. Stewart 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. 66:10531062.

E. Pestsova , J. Meinhard , A. Menze , U. Fischer , A. Windhövel , and P. Westhoff 2008. Transcript profiles uncover temporal and stress-induced changes of metabolic pathways in germinating sugar beet seeds. BMC Plant Biol. 8:122.

J. Preston , K. Tatematsu , Y. Kanno , T. Hobo , M. Kimura , Y. Jikumaru , R. Yano , Y. Kamiya , and E. Nambara 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. 50:17861800.

G. P. Steinbauer and B. Grigsby 1957. Interaction of temperature, light, and moistening agent in the germination of weed seeds. Weeds. 5:175182.

C. N. Stewart , P. J. Tranel , D. P. Horvath , J. V. Anderson , L. H. Rieseberg , J. H. Westwood , C. A. Mallory-Smith , M. L. Zapiola , and K. M. Dlugosch 2009. Evolution of weediness and invasiveness: Charting the course for weed genomics. Weed. Sci. 57:451462.

A. Subramanian , P. Tamayo , and V. K. Mootha 2005. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl. Acad. Sci. USA. 102:1554515550.

T. Sun 2011. The molecular mechanism and evolution of the GA-GID1-DELLA signaling module in plants. Curr. Biol. 21:R338R345.

L. J. Sweetlove , K. F. M. Beard , A. Nunes-Nesi , A. R. Fernie , and R. G. Ratcliffe 2010. Not just a circle: flux modes in the plant TCA cycle. Trends Plant Sci. 15:462470.

K. Thompson and J. P. Grime 1983. A comparative study of germination responses to diurnally-fluctuating temperatures. J. Appl. Ecol. 20:141156.

A. To , C. Valon , G. Savino , J. Guilleminot , M. Devic , J. Giraudat , and F. Parcy 2006. A network of local and redundant gene regulation governs Arabidopsis seed maturation. Plant Cell. 18:16421651.

S. Toh , A. Imamura , A. Watanabe , et al. 2008. High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol. 146:13681385.

S. C. Weller , R. A. Bressan , P. B. Goldsbrough , T. B. Fredenburg , and P. M. Hasegawa 2001. The effect of genomics on weed management in the 21st century. Weed. Sci. 49:282289.

I. D. Wilson , G. L. Barker , C. Lu , J. A. Coghill , R. W. Beswick , J. R. Lenton , and K. J. Edwards 2005. Alteration of the embryo transcriptome of hexaploid winter wheat (Triticum aestivum cv. Mercia) during maturation and germination. Funct. Integr. Genomics. 5:144154.

Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Weed Science
  • ISSN: 0043-1745
  • EISSN: 1550-2759
  • URL: /core/journals/weed-science
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Type Description Title
WORD
Supplementary Materials

Foley et al. supplementary material
Figure S1

 Word (115 KB)
115 KB
UNKNOWN
Supplementary Materials

Foley et al. supplementary material
Table S3

 Unknown (833 KB)
833 KB
UNKNOWN
Supplementary Materials

Foley et al. supplementary material
Table S2

 Unknown (28 KB)
28 KB
UNKNOWN
Supplementary Materials

Foley et al. supplementary material
Table S1

 Unknown (20 KB)
20 KB

Metrics

Abstract views

Total abstract views: 17 *
Loading metrics...

* Views captured on Cambridge Core between 20th January 2017 - 23rd June 2017. This data will be updated every 24 hours.