Environment Sensing in Spring-dispersed Seeds of a Winter Annual Arabidopsis Influences the Regulation of Dormancy to Align Germination Potential with Seasonal Changes

Overview

Journal New Phytol

Specialty Biology

Date 2014 Jan 22

PMID 24444091

Citations 24

Authors

Steven Footitt

Heather A Clay

Katherine Dent

William E Finch-Savage

Affiliations

Soon will be listed here.

Abstract

Seed dormancy cycling plays a crucial role in the lifecycle timing of many plants. Little is known of how the seeds respond to the soil seed bank environment following dispersal in spring into the short-term seed bank before seedling emergence in autumn. Seeds of the winter annual Arabidopsis ecotype Cvi were buried in field soils in spring and recovered monthly until autumn and their molecular eco-physiological responses were recorded. DOG1 expression is initially low and then increases as dormancy increases. MFT expression is negatively correlated with germination potential. Abscisic acid (ABA) and gibberellin (GA) signalling responds rapidly following burial and adjusts to the seasonal change in soil temperature. Collectively these changes align germination potential with the optimum climate space for seedling emergence. Seeds naturally dispersed to the soil in spring enter a shallow dormancy cycle dominated by spatial sensing that adjusts germination potential to the maximum when soil environment is most favourable for germination and seedling emergence upon soil disturbance. This behaviour differs subtly from that of seeds overwintered in the soil seed bank to spread the period of potential germination in the seed population (existing seed bank and newly dispersed). As soil temperature declines in autumn, deep dormancy is re-imposed as seeds become part of the persistent seed bank.

Citing Articles

Genetic study for seed germination and shattering in in response to different seed treatments.

Istaitieh M, Najafabadi M, Edwards A, Todd J, Van Acker R, Rajcan I Heliyon. 2024; 10(7):e27975.

PMID: 38560240 PMC: 10979140. DOI: 10.1016/j.heliyon.2024.e27975.

Updated role of ABA in seed maturation, dormancy, and germination.

Ali F, Qanmber G, Li F, Wang Z J Adv Res. 2022; 35:199-214.

PMID: 35003801 PMC: 8721241. DOI: 10.1016/j.jare.2021.03.011.

The Arabidopsis circadian clock protein PRR5 interacts with and stimulates ABI5 to modulate abscisic acid signaling during seed germination.

Yang M, Han X, Yang J, Jiang Y, Hu Y Plant Cell. 2021; 33(9):3022-3041.

PMID: 34152411 PMC: 8462813. DOI: 10.1093/plcell/koab168.

Regulation of Seed Dormancy and Germination Mechanisms in a Changing Environment.

Klupczynska E, Pawlowski T Int J Mol Sci. 2021; 22(3).

PMID: 33572974 PMC: 7866424. DOI: 10.3390/ijms22031357.

Ecological, (epi)genetic and physiological aspects of bet-hedging in angiosperms.

Gianella M, Bradford K, Guzzon F Plant Reprod. 2021; 34(1):21-36.

PMID: 33449209 PMC: 7902588. DOI: 10.1007/s00497-020-00402-z.

References

Vaistij F, Gan Y, Penfield S, Gilday A, Dave A, He Z . Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA. Proc Natl Acad Sci U S A. 2013; 110(26):10866-71. PMC: 3696787. DOI: 10.1073/pnas.1301647110. View

Donohue K, Heschel M, Butler C, Barua D, Sharrock R, Whitelam G . Diversification of phytochrome contributions to germination as a function of seed-maturation environment. New Phytol. 2007; 177(2):367-379. DOI: 10.1111/j.1469-8137.2007.02281.x. View

Finch-Savage W, Leubner-Metzger G . Seed dormancy and the control of germination. New Phytol. 2006; 171(3):501-23. DOI: 10.1111/j.1469-8137.2006.01787.x. View

Daviere J, de Lucas M, Prat S . Transcriptional factor interaction: a central step in DELLA function. Curr Opin Genet Dev. 2008; 18(4):295-303. DOI: 10.1016/j.gde.2008.05.004. View

Nakamura S, Abe F, Kawahigashi H, Nakazono K, Tagiri A, Matsumoto T . A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. Plant Cell. 2011; 23(9):3215-29. PMC: 3203438. DOI: 10.1105/tpc.111.088492. View

Donohue K . Completing the cycle: maternal effects as the missing link in plant life histories. Philos Trans R Soc Lond B Biol Sci. 2009; 364(1520):1059-74. PMC: 2666684. DOI: 10.1098/rstb.2008.0291. View

Bassel G, Lan H, Glaab E, Gibbs D, Gerjets T, Krasnogor N . Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc Natl Acad Sci U S A. 2011; 108(23):9709-14. PMC: 3111290. DOI: 10.1073/pnas.1100958108. View

Arc E, Chibani K, Grappin P, Jullien M, Godin B, Cueff G . Cold stratification and exogenous nitrates entail similar functional proteome adjustments during Arabidopsis seed dormancy release. J Proteome Res. 2012; 11(11):5418-32. DOI: 10.1021/pr3006815. View

Alboresi A, Gestin C, Leydecker M, Bedu M, Meyer C, Truong H . Nitrate, a signal relieving seed dormancy in Arabidopsis. Plant Cell Environ. 2005; 28(4):500-12. DOI: 10.1111/j.1365-3040.2005.01292.x. View

10.

Nakabayashi K, Bartsch M, Xiang Y, Miatton E, Pellengahr S, Yano R . The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION1 protein levels in freshly harvested seeds. Plant Cell. 2012; 24(7):2826-38. PMC: 3426117. DOI: 10.1105/tpc.112.100214. View

11.

Cadman C, Toorop P, Hilhorst H, Finch-Savage W . Gene expression profiles of Arabidopsis Cvi seeds during dormancy cycling indicate a common underlying dormancy control mechanism. Plant J. 2006; 46(5):805-22. DOI: 10.1111/j.1365-313X.2006.02738.x. View

12.

Penfield S, Josse E, Kannangara R, Gilday A, Halliday K, Graham I . Cold and light control seed germination through the bHLH transcription factor SPATULA. Curr Biol. 2005; 15(22):1998-2006. DOI: 10.1016/j.cub.2005.11.010. View

13.

Xi W, Liu C, Hou X, Yu H . MOTHER OF FT AND TFL1 regulates seed germination through a negative feedback loop modulating ABA signaling in Arabidopsis. Plant Cell. 2010; 22(6):1733-48. PMC: 2910974. DOI: 10.1105/tpc.109.073072. View

14.

Remans T, Smeets K, Opdenakker K, Mathijsen D, Vangronsveld J, Cuypers A . Normalisation of real-time RT-PCR gene expression measurements in Arabidopsis thaliana exposed to increased metal concentrations. Planta. 2008; 227(6):1343-9. DOI: 10.1007/s00425-008-0706-4. View

15.

Voegele A, Linkies A, Muller K, Leubner-Metzger G . Members of the gibberellin receptor gene family GID1 (GIBBERELLIN INSENSITIVE DWARF1) play distinct roles during Lepidium sativum and Arabidopsis thaliana seed germination. J Exp Bot. 2011; 62(14):5131-47. PMC: 3193015. DOI: 10.1093/jxb/err214. View

16.

Footitt S, Huang Z, Clay H, Mead A, Finch-Savage W . Temperature, light and nitrate sensing coordinate Arabidopsis seed dormancy cycling, resulting in winter and summer annual phenotypes. Plant J. 2013; 74(6):1003-15. PMC: 3764396. DOI: 10.1111/tpj.12186. View

17.

Dekkers B, Willems L, Bassel G, van Bolderen-Veldkamp R, Ligterink W, Hilhorst H . Identification of reference genes for RT-qPCR expression analysis in Arabidopsis and tomato seeds. Plant Cell Physiol. 2011; 53(1):28-37. DOI: 10.1093/pcp/pcr113. View

18.

Dekkers B, Pearce S, van Bolderen-Veldkamp R, Marshall A, Widera P, Gilbert J . Transcriptional dynamics of two seed compartments with opposing roles in Arabidopsis seed germination. Plant Physiol. 2013; 163(1):205-15. PMC: 3762641. DOI: 10.1104/pp.113.223511. View

19.

Bentsink L, Jowett J, Hanhart C, Koornneef M . Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc Natl Acad Sci U S A. 2006; 103(45):17042-7. PMC: 1636575. DOI: 10.1073/pnas.0607877103. View

20.

Footitt S, Douterelo-Soler I, Clay H, Finch-Savage W . Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proc Natl Acad Sci U S A. 2011; 108(50):20236-41. PMC: 3250134. DOI: 10.1073/pnas.1116325108. View