DELAY of GERMINATION1 (DOG1) regulates both Seed dormancy and flowering time through microRNA pathways

Proceedings of the National Academy of Sciences of the United States of America

Volumn 113, Issue 15, 2016, Pages E2199-E2206

  Huo, Heqiang ^a   Wei, Shouhui ^b   Bradford, Kent J ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b INSTITUTE OF PLANT PROTECTION   (China)

Author keywords

DOG1; Flowering; Lettuce; MiRNA; Seed dormancy

Indexed keywords

DELAY OF GERMINATION 1 PROTEIN; MICRORNA; MIRNA 156; MIRNA 172; UNCLASSIFIED DRUG; VEGETABLE PROTEIN; ARABIDOPSIS PROTEIN; DOG1 PROTEIN, ARABIDOPSIS; MIRN156 MICRORNA, ARABIDOPSIS; MIRN172 MICRORNA, ARABIDOPSIS;

ARABIDOPSIS; ARTICLE; FLOWERING; GENETIC ASSOCIATION; LETTUCE; LOSS OF FUNCTION MUTATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REGULATORY MECHANISM; RNA PROCESSING; SEED DORMANCY; BIOSYNTHESIS; DORMANCY; FLOWER; GENE EXPRESSION REGULATION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; FLOWERS; GENE EXPRESSION REGULATION, PLANT; LETTUCE; MICRORNAS; MUTATION; PLANT DORMANCY; TRANSCRIPTION, GENETIC;

EID: 84963770510     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1600558113     Document Type: Article

References (69)

1. Huijser P, Schmid M (2011) The control of developmental phase transitions in plants. Development 138(19):4117-4129.
2. Footitt S, Huang Z, Clay HA, Mead A, Finch-Savage WE (2013) Temperature, light and nitrate sensing coordinate Arabidopsis seed dormancy cycling, resulting in winter and summer annual phenotypes. Plant J 74(6):1003-1015.
3. Chiang GCK, et al. (2011) DOG1 expression is predicted by the seed-maturation environment and contributes to geographical variation in germination in Arabidopsis thaliana. Mol Ecol 20(16):3336-3349.
4. Batlla D, Benech-Arnold R (2015) A framework for the interpretation of temperature effects on dormancy and germination in seed populations showing dormancy. Seed Sci Res 25:147-158.
5. Murphey M, et al. (2015) DOG1-imposed dormancy mediates germination responses to temperature cues. Environ Exp Bot 112:33-43.
6. Andrés F, Coupland G (2012) The genetic basis of flowering responses to seasonal cues. Nat Rev Genet 13(9):627-639.
7. Amasino R (2010) Seasonal and developmental timing of flowering. Plant J 61(6):1001-1013.
8. Alonso-Blanco C, Blankestijn-de Vries H, Hanhart CJ, Koornneef M (1999) Natural allelic variation at seed size loci in relation to other life history traits of Arabidopsis thaliana. Proc Natl Acad Sci USA 96(8):4710-4717.
9. Toorop PE, et al. (2012) Co-adaptation of seed dormancy and flowering time in the arable weed Capsella bursa-pastoris (shepherd's purse). Ann Bot (Lond) 109(2):481-489.
10. Lou P, et al. (2007) Quantitative trait loci for flowering time and morphological traits in multiple populations of Brassica rapa. J Exp Bot 58(14):4005-4016.
11. Debieu M, et al. (2013) Co-variation between seed dormancy, growth rate and flowering time changes with latitude in Arabidopsis thaliana. PLoS One 8(5):e61075.
12. Bewley JD, Bradford KJ, Hilhorst HWM, Nonogaki H (2013) Seeds: Physiology of Development, Germination and Dormancy (Springer, New York), 3rd Ed.
13. Chen M, et al. (2014) Maternal temperature history activates Flowering Locus T in fruits to control progeny dormancy according to time of year. Proc Natl Acad Sci USA 111(52):18787-18792.
14. Bassel GW, et al. (2011) Genome-wide network model capturing seed germination reveals coordinated regulation of plant cellular phase transitions. Proc Natl Acad Sci USA 108(23):9709-9714.
15. Chiang GC, Barua D, Kramer EM, Amasino RM, Donohue K (2009) Major flowering time gene, flowering locus C, regulates seed germination in Arabidopsis thaliana. Proc Natl Acad Sci USA 106(28):11661-11666.
16. Burghardt LT, Edwards BR, Donohue K (2016) Multiple paths to similar germination behavior in Arabidopsis thaliana. New Phytol 209(3):1301-1312. 10.1111/nph.13685.
17. Kendall SL, et al. (2011) Induction of dormancy in Arabidopsis summer annuals requires parallel regulation of DOG1 and hormone metabolism by low temperature and CBF transcription factors. Plant Cell 23(7):2568-2580.
18. Nakabayashi K, et al. (2012) The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION1 protein levels in freshly harvested seeds. Plant Cell 24(7):2826-2838.
19. Bentsink L, Jowett J, Hanhart CJ, Koornneef M (2006) Cloning of DOG1, a quantitative trait locus controlling seed dormancy in Arabidopsis. Proc Natl Acad Sci USA 103(45):17042-17047.
20. Graeber K, et al. (2014) DELAY OF GERMINATION 1 mediates a conserved coat-dormancy mechanism for the temperature-and gibberellin-dependent control of seed germination. Proc Natl Acad Sci USA 111(34):E3571-E3580.
21. Zhao M, Yang S, Liu X, Wu K (2015) Arabidopsis histone demethylases LDL1 and LDL2 control primary seed dormancy by regulating DELAY OF GERMINATION 1 and ABA signaling-related genes. Front Plant Sci 6:159.
22. Atwell S, et al. (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature 465(7298):627-631.
23. Brachi B, et al. (2010) Linkage and association mapping of Arabidopsis thaliana flowering time in nature. PLoS Genet 6(5):e1000940.
24. Huo H, Dahal P, Kunusoth K, McCallum CM, Bradford KJ (2013) Expression of 9-cis-EPOXYCAROTENOID DIOXYGENASE4 is essential for thermoinhibition of lettuce seed germination but not for seed development or stress tolerance. Plant Cell 25(3):884-900.
25. Argyris J, Dahal P, Hayashi E, Still DW, Bradford KJ (2008) Genetic variation for lettuce seed thermoinhibition is associated with temperature-sensitive expression of abscisic acid, gibberellin, and ethylene biosynthesis, metabolism, and response genes. Plant Physiol 148(2):926-947.
26. Cantliffe D, Sung Y, Nascimento W (2000) Lettuce seed germination. Hortic Rev (Am Soc Hortic Sci) 224:229-275.
27. Argyris J, et al. (2011) A gene encoding an abscisic acid biosynthetic enzyme (LsNCED4) collocates with the high temperature germination locus Htg6.1 in lettuce (Lactuca sp.). Theor Appl Genet 122(1):95-108.
28. Toh S, et al. (2008) High temperature-induced abscisic acid biosynthesis and its role in the inhibition of gibberellin action in Arabidopsis seeds. Plant Physiol 146(3):1368-1385.
29. Huo H, Bradford KJ (2015) Molecular and hormonal regulation of thermoinhibition of seed germination. Advances in Plant Dormancy, ed Anderson JV (Springer, New York), pp 3-33.
30. Wu G, et al. (2009) The sequential action of miR156 and miR172 regulates developmental timing in Arabidopsis. Cell 138(4):750-759.
31. Wang JW, Czech B, Weigel D (2009) miR156-regulated SPL transcription factors define an endogenous flowering pathway in Arabidopsis thaliana. Cell 138(4):738-749.
32. Huang D, Koh C, Feurtado JA, Tsang EW, Cutler AJ (2013) MicroRNAs and their putative targets in Brassica napus seed maturation. BMC Genomics 14:140.
33. Nonogaki H (2010) MicroRNA gene regulation cascades during early stages of plant development. Plant Cell Physiol 51(11):1840-1846.
34. Yoong FY, et al. (2016) Genetic variation for thermotolerance in lettuce seed germination is associated with temperature-sensitive regulation of ETHYLENE RESPONSE FACTOR1(ERF1). Plant Physiol 170(1):472-488.
35. Ashikawa I, Mori M, Nakamura S, Abe F (2014) A transgenic approach to controlling wheat seed dormancy level by using TriticeaeDOG1-like genes. Transgenic Res 23(4):621-629.
36. Yu S, et al. (2012) Gibberellin regulates the Arabidopsis floral transition through miR156-targeted SQUAMOSA PROMOTER BINDING-LIKE transcription factors. Plant Cell 24(8):3320-3332.
37. Daxinger L, et al. (2008) Unexpected silencing effects from T-DNA tags in Arabidopsis. Trends Plant Sci 13(1):4-6.
38. Wu G, Poethig RS (2006) Temporal regulation of shoot development in Arabidopsis thaliana by miR156 and its target SPL3. Development 133(18):3539-3547.
39. Cyrek M, et al. (2016) Seed dormancy in Arabidopsis thaliana is controlled by alternative polyadenylation of DOG1. Plant Physiol 170(2):947-955.
40. Wang Y, et al. (2013) The inhibitory effect of ABA on floral transition is mediated by ABI5 in Arabidopsis. J Exp Bot 64(2):675-684.
41. Xie M, Zhang S, Yu B (2015) microRNA biogenesis, degradation and activity in plants. Cell Mol Life Sci 72(1):87-99.
42. Zhang S, Xie M, Ren G, Yu B (2013) CDC5, a DNA binding protein, positively regulates posttranscriptional processing and/or transcription of primary microRNA transcripts. Proc Natl Acad Sci USA 110(43):17588-17593.
43. Huang Z, Liu S, Bradford KJ, Huxman TE, Venable DL (2016) The contribution of germination functional traits to population dynamics of a desert plant community. Ecology 97(1):250-261.
44. Donohue K, Burghardt LT, Runcie D, Bradford KJ, Schmitt J (2015) Applying developmental threshold models to evolutionary ecology. Trends Ecol Evol 30(2):66-77.
45. He H, et al. (2014) Interaction between parental environment and genotype affects plant and seed performance in Arabidopsis. J Exp Bot 65(22):6603-6615.
46. Postma FM, Ågren J (2015) Maternal environment affects the genetic basis of seed dormancy in Arabidopsis thaliana. Mol Ecol 24(4):785-797.
47. Graeber K, et al. (2010) Cross-species approaches to seed dormancy and germination: Conservation and biodiversity of ABA-regulated mechanisms and the Brassicaceae DOG1 genes. Plant Mol Biol 73(1-2):67-87.
48. Chiang GC, et al. (2013) Pleiotropy in the wild: The dormancy gene DOG1 exerts cascading control on life cycles. Evolution 67(3):883-893.
49. de Casas RR, et al. (2012) Seed after-ripening and dormancy determine adult life history independently of germination timing. New Phytol 194(3):868-879.
50. Burghardt LT, Metcalf CJ, Wilczek AM, Schmitt J, Donohue K (2015) Modeling the influence of genetic and environmental variation on the expression of plant life cycles across landscapes. Am Nat 185(2):212-227.
51. Liu Y, Koornneef M, Soppe WJJ (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(2):433-444.
52. Tamura N, et al. (2006) Isolation and characterization of high temperature-resistant germination mutants of Arabidopsis thaliana. Plant Cell Physiol 47(8):1081-1094.
53. Cao Y, Dai Y, Cui S, Ma L (2008) Histone H2B monoubiquitination in the chromatin of FLOWERING LOCUS C regulates flowering time in Arabidopsis. Plant Cell 20(10):2586-2602.
54. Lu C, Fedoroff N (2000) A mutation in the Arabidopsis HYL1 gene encoding a dsRNA binding protein affects responses to abscisic acid, auxin, and cytokinin. Plant Cell 12(12):2351-2366.
55. Bezerra IC, Michaels SD, Schomburg FM, Amasino RM (2004) Lesions in the mRNA capbinding gene ABA HYPERSENSITIVE 1 suppress FRIGIDA-mediated delayed flowering in Arabidopsis. Plant J 40(1):112-119.
56. Tsuzuki M, Takeda A, Watanabe Y (2014) Recovery of dicer-like 1-late flowering phenotype by miR172 expressed by the noncanonical DCL4-dependent biogenesis pathway. RNA 20(8):1320-1327.
57. Clarke JH, Tack D, Findlay K, Van Montagu M, Van Lijsebettens M (1999) The SERRATE locus controls the formation of the early juvenile leaves and phase length in Arabidopsis. Plant J 20(4):493-501.
58. Li S, Yang X, Wu F, He Y (2012) HYL1 controls the miR156-mediated juvenile phase of vegetative growth. J Exp Bot 63(7):2787-2798.
59. Martin RC, et al. (2010) The microRNA156 and microRNA172 gene regulation cascades at post-germinative stages in Arabidopsis. Seed Sci Res 20(2):79-87.
60. Nodine MD, Bartel DP (2010) MicroRNAs prevent precocious gene expression and enable pattern formation during plant embryogenesis. Genes Dev 24(23):2678-2692.
61. Willmann MR, Mehalick AJ, Packer RL, Jenik PD (2011) MicroRNAs regulate the timing of embryo maturation in Arabidopsis. Plant Physiol 155(4):1871-1884.
62. Laubinger S, et al. (2008) Dual roles of the nuclear cap-binding complex and SERRATE in pre-mRNA splicing and microRNA processing in Arabidopsis thaliana. Proc Natl Acad Sci USA 105(25):8795-8800.
63. Ren G, et al. (2012) Regulation of miRNA abundance by RNA binding protein TOUGH in Arabidopsis. Proc Natl Acad Sci USA 109(31):12817-12821.
64. Li D, et al. (2013) Deep sequencing of maize small RNAs reveals a diverse set of microRNA in dry and imbibed seeds. PLoS One 8(1):e55107.
65. Nonogaki H (2014) Seed dormancy and germination-emerging mechanisms and new hypotheses. Front Plant Sci 5:233.
66. Crevillén P, et al. (2014) Epigenetic reprogramming that prevents transgenerational inheritance of the vernalized state. Nature 515(7528):587-590.
67. Choi J, et al. (2009) Resetting and regulation of FLOWERING LOCUS C expression during Arabidopsis reproductive development. Plant J 57(5):918-931.
68. Sheldon CC, et al. (2008) Resetting of FLOWERING LOCUS C expression after epigenetic repression by vernalization. Proc Natl Acad Sci USA 105(6):2214-2219.
69. Bazin J, et al. (2011) Targeted mRNA oxidation regulates sunflower seed dormancy alleviation during dry after-ripening. Plant Cell 23(6):2196-2208.