Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Effect of FLOWERING LOCUS C on seed germination depends on dormancy

Logan Blair A B C , Gabriela Auge A and Kathleen Donohue A
+ Author Affiliations
- Author Affiliations

A Duke University, Department of Biology, Box 90338, Durham, NC 27708, USA.

B Present address: University of California, Davis, 2320 Storer Hall, One Shields Avenue, Davis, CA 95616, USA.

C Corresponding author. Email: lkblair@ucdavis.edu

Functional Plant Biology 44(5) 493-506 https://doi.org/10.1071/FP16368
Submitted: 25 October 2016  Accepted: 28 December 2016   Published: 22 March 2017

Abstract

FLOWERING LOCUS C (FLC) has a major regulatory role in the timing of flowering in Arabidopsis thaliana (L.) Heynh. and has more recently been shown to influence germination. Here, we investigated the conditions under which FLC influences germination, and demonstrated that its effect depends on the level of primary and secondary dormancy and the temperature of seed imbibition. We tested the germination response of genotypes with different degrees of FLC activity over the course of after-ripening and after secondary dormancy induction by hot stratification. Genotypes with high FLC-activity showed higher germination; this response was greatest when seeds exhibited primary dormancy or were induced into secondary dormancy by hot stratification. In this study, which used less dormant seeds, the effect of FLC was more evident at 22°C, the less permissive germination temperature, than at 10°C, in contrast to prior published results that used more dormant seeds. Thus, because effects of FLC variation depend on dormancy, and because the range of temperature that permits germination also depends on dormancy, the temperature at which FLC affects germination can also vary with dormancy. Finally, we document that the effect of FLC can depend on FRIGIDA and that FRIGIDA itself appears to influence germination. Thus, pleiotropy between germination and flowering pathways in A. thaliana extends beyond FLC and involves other genes in the FLC genetic pathway.

Additional keywords: after-ripening, conditional dormancy, dormancy, germination, FRIGIDA, pleiotropy, temperature.


References

Akiyama R, Ågren J (2014) Conflicting selection on the timing of germination in a natural population of Arabidopsis thaliana. Journal of Evolutionary Biology 27, 193–199.
Conflicting selection on the timing of germination in a natural population of Arabidopsis thaliana.CrossRef | 1:STN:280:DC%2BC2c3lvFartA%3D%3D&md5=fd86d4158b681069af0e849d3e0d9cf8CAS |

Alonso-Blanco C, El-Assal SE, Coupland G, Koornneef M (1998) Analysis of natural allelic variation at flowering time loci in the Landsberg erecta and Cape Verde Islands ecotypes of Arabidopsis thaliana. Genetics 149, 749–764.

Atchley WR (1984) Ontogeny, timing of development, and genetic variance-covariance structure. American Naturalist 123, 519–540.
Ontogeny, timing of development, and genetic variance-covariance structure.CrossRef |

Auge G, Edwards B, Blair L, Burghardt L, Coughlan J, Leverett L, Donohue K (2015) Secondary dormancy dynamics depends on primary dormancy status in Arabidopsis thaliana. Seed Science Research 25, 230–246.
Secondary dormancy dynamics depends on primary dormancy status in Arabidopsis thaliana.CrossRef |

Ausin I, Alonso-Blanco C, Martinez-Zapater JM (2005) Environmental regulation of flowering. International Journal of Developmental Biology 49, 689–705.
Environmental regulation of flowering.CrossRef | 1:CAS:528:DC%2BD2MXht1OktLjJ&md5=3fe8e08cd38a2def6603513f994c9e63CAS |

Barton NH (1990) Pleiotropic models of quantitative variation. Genetics 124, 773–782.

Baskin CC, Baskin JM (2014) ‘Seeds: ecology, biogeography and evolution of dormancy and germination.’ (2nd edn) (Academic Press: San Diego, CA, USA)

Bäurle I, Dean C (2006) The timing of developmental transitions in plants. Cell 125, 655–664.
The timing of developmental transitions in plants.CrossRef |

Bewley JD (1997) Seed germination and dormancy. Plant Cell 9, 1055–1066.
Seed germination and dormancy.CrossRef | 1:CAS:528:DyaK2sXlt1ShtLs%3D&md5=420704617a689efaf0a2160e24cb604fCAS |

Brakefield PM (2006) Evo-devo and constraints on selection. Trends in Ecology and Evolution 21, 362–368.
Evo-devo and constraints on selection.CrossRef |

Burghardt L, Metcalf CJE, Wilczek A, Schmitt J, Donohue K (2015) Modeling the influence of genetic and environmental variation on the expression of plant life cycles across landscapes. American Naturalist 185, 212–227.
Modeling the influence of genetic and environmental variation on the expression of plant life cycles across landscapes.CrossRef |

Burghardt L, Edwards B, Kovach K, Donohue K (2016) Multiple paths to similar germination behavior in Arabidopsis thaliana. New Phytologist 209, 1301–1312.
Multiple paths to similar germination behavior in Arabidopsis thaliana.CrossRef |

Caicedo AL, Stinchcombe JR, Olsen KM, Schmitt J, Purugganan MJ (2004) Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait. Proceedings of the National Academy of Sciences of the United States of America 101, 15670–15675.
Epistatic interaction between Arabidopsis FRI and FLC flowering time genes generates a latitudinal cline in a life history trait.CrossRef | 1:CAS:528:DC%2BD2cXhtVWisLvF&md5=cf64e941510aba4adbcabb021b1a5bddCAS |

Chiang GCK, Barua D, Amasino R, Donohue K (2009) A major flowering-time gene, FLOWERING LOCUS C, controls temperature-dependent germination in Arabidopsis thaliana. Proceedings of the National Academy of Sciences of the United States of America 106, 11661–11666.
A major flowering-time gene, FLOWERING LOCUS C, controls temperature-dependent germination in Arabidopsis thaliana.CrossRef | 1:CAS:528:DC%2BD1MXptVSqurY%3D&md5=0544b2fdf609a58fa9221bee444460a4CAS |

Choi J, Hyun Y, Kang MJ, Yun HI, Yun JY, Lister C, Dean C, Amasino RM, Noh B, Noh YS, Choic Y (2009) Resetting and regulation of FLOWERING LOCUS C expression during Arabidopsis reproductive development. The Plant Journal 57, 918–931.
Resetting and regulation of FLOWERING LOCUS C expression during Arabidopsis reproductive development.CrossRef | 1:CAS:528:DC%2BD1MXjslSltr8%3D&md5=8b280bb0ac9ab7e6505c45e3171602ddCAS |

Chouard P (1960) Vernalization and its relations to dormancy. Annual Review of Plant Physiology 11, 191–238.
Vernalization and its relations to dormancy.CrossRef | 1:CAS:528:DyaF3MXntFenug%3D%3D&md5=b2e00a0cc45151d3f6eae78dd0751b57CAS |

Chuine I (2010) Why does phenology drive species distribution? Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 365, 3149–3160.
Why does phenology drive species distribution?CrossRef |

Clarke JH, Dean C (1994) Mapping FRI, a locus controlling flowering time and vernalization response in Arabidopsis thaliana. Molecular & General Genetics 242, 81–89.

Coustham V, Li P, Strange A, Lister C, Song J, Dean C (2012) Quantitative modulation of polycomb silencing underlies natural variation in vernalization. Science 337, 584–587.
Quantitative modulation of polycomb silencing underlies natural variation in vernalization.CrossRef | 1:CAS:528:DC%2BC38XhtFWhsbbN&md5=0916c324a1f2d8188cd4a4fb55ba3fe2CAS |

Crespi BJ (2000) The evolution of maladaptation. Heredity 84, 623–629.
The evolution of maladaptation.CrossRef |

Dennis ES, Peacock WJ (2007) Epigenetic regulation of flowering. Current Opinion in Plant Biology 10, 520–527.
Epigenetic regulation of flowering.CrossRef | 1:CAS:528:DC%2BD2sXhtFekurjE&md5=61cdc8f99cb0fad14d23b52a8567dbdeCAS |

Donohue K, Dorn LA, Griffith C, Schmitt J, Kim ES, Aguilera A (2005) The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing. Evolution 59, 758–770.
The evolutionary ecology of seed germination of Arabidopsis thaliana: variable natural selection on germination timing.CrossRef |

Donohue K, de Casas RR, Burghardt L, Kovach K, Willis CG (2010) Germination, post-germination adaptation, and species ecological ranges. Annual Review of Ecology, Evolution, and Systematics 41, 293–319.
Germination, post-germination adaptation, and species ecological ranges.CrossRef |

Ehrlén J (2015) Selection on flowering time in a life-cycle context. Oikos 124, 92–101.
Selection on flowering time in a life-cycle context.CrossRef |

Finch-Savage WE, Leubner-Metzger G (2006) Seed dormancy and the control of germination. New Phytologist 171, 501–523.
Seed dormancy and the control of germination.CrossRef | 1:CAS:528:DC%2BD28XpsVertbw%3D&md5=2619b3cc9ea63d6fe4285e93c8fc7114CAS |

Fisher RA (1958) ‘The genetical theory of natural selection.’ (2nd edn) (Dover: New York)

Footitt S, Douterelo-Soler I, Clay H, Finch-Savage WE (2011) Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways. Proceedings of the National Academy of Sciences of the United States of America 108, 20236–20241.
Dormancy cycling in Arabidopsis seeds is controlled by seasonally distinct hormone-signaling pathways.CrossRef | 1:CAS:528:DC%2BC3MXhs1yqsbzI&md5=86d68b98f7f826d85b406c690639533aCAS |

Footitt S, Clay HA, Dent K, Finch-Savage WE (2014) Environment sensing in spring-dispersed seeds of a winter annual Arabidopsis influences the regulation of dormancy to align germination potential with seasonal changes. New Phytologist 202, 929–939.
Environment sensing in spring-dispersed seeds of a winter annual Arabidopsis influences the regulation of dormancy to align germination potential with seasonal changes.CrossRef | 1:CAS:528:DC%2BC2cXmt1WmtrY%3D&md5=aef11ce200b8187f1195a1f879f49fc9CAS |

Gazzani S, Gendall AR, Lister C, Dean C (2003) Analysis of the molecular basis of flowering time variation in Arabidopsis accessions. Plant Physiology 132, 1107–1114.
Analysis of the molecular basis of flowering time variation in Arabidopsis accessions.CrossRef | 1:CAS:528:DC%2BD3sXksleruro%3D&md5=9769ed854d990337ecc327b2bc3f2a6dCAS |

Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe WJJ (2012) Molecular mechanisms of seed dormancy. Plant, Cell & Environment 35, 1769–1786.
Molecular mechanisms of seed dormancy.CrossRef | 1:CAS:528:DC%2BC38Xht12itr3K&md5=a3cf7d129bc33c590b9b1a88c49ea9e6CAS |

Griswold CK, Whitlock MJ (2003) The genetics of adaptation: the roles of pleiotropy, stabilizing selection and drift in shaping the distribution of bidirectional fixed mutational effects. Genetics 165, 2181–2192.

Gutterman Y (2000) Maternal effects on seeds during development. In ‘Seeds: the ecology of regeneration in plant communities’. (2nd edn) pp. 59–84. (CABI Publishing: Wallingford, UK)

Holdsworth MJ, Bentsink L, Soppe WJJ (2008a) Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy, and germination. New Phytologist 179, 33–54.
Molecular networks regulating Arabidopsis seed maturation, after-ripening, dormancy, and germination.CrossRef | 1:CAS:528:DC%2BD1cXosFWhsb0%3D&md5=0b622eb69273287c63a4f1af7d987ef6CAS |

Holdsworth MJ, Finch-Savage WE, Grappin P, Job D (2008b) Post-genomics dissection of seed dormancy and germination. Trends in Plant Science 13, 7–13.
Post-genomics dissection of seed dormancy and germination.CrossRef | 1:CAS:528:DC%2BD1cXlsFaiug%3D%3D&md5=ddc5151a579bbd362827d7c07d60d572CAS |

Huang X, Schmitt J, Dorn L, Griffith C, Effgen S, Takao S, Koornneef M, Donohue K (2010) The earliest stages of adaptation in an experimental plant population: strong selection on QTLs for seed dormancy. Molecular Ecology 19, 1335–1351.
The earliest stages of adaptation in an experimental plant population: strong selection on QTLs for seed dormancy.CrossRef |

Johanson U, West J, Lister C, Michaels S, Amasino R, Dean C (2000) Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time. Science 290, 344–347.
Molecular analysis of FRIGIDA, a major determinant of natural variation in Arabidopsis flowering time.CrossRef | 1:CAS:528:DC%2BD3cXnsVGiurw%3D&md5=4b075239ce5901a615d2f90848df670aCAS |

Kalisz S (1986) Variable selection on the timing of germination in Collinsia verna (Scrophulariaceae). Evolution 40, 479–491.
Variable selection on the timing of germination in Collinsia verna (Scrophulariaceae).CrossRef |

Kalisz S, Wardle GM (1994) Life history variation in Campanula americana (Campanulaceae): population differentiation. American Journal of Botany 81, 521–527.
Life history variation in Campanula americana (Campanulaceae): population differentiation.CrossRef |

Kendall S, Penfield S (2012) Maternal and zygotic temperature signalling in the control of seed dormancy and germination. Seed Science Research 22, S23–S29.
Maternal and zygotic temperature signalling in the control of seed dormancy and germination.CrossRef | 1:CAS:528:DC%2BC38XkvF2htw%3D%3D&md5=6ea2c40dc22b5a48f097875f2ad03af8CAS |

Kendall SL, Hellwege A, Marriot P, Whalley C, Graham IA, Penfield S (2011) Induction of dormancy in Arabidopsis summer annuals requires parallel regulation of DOG1 and hormone metabolism by low temperature and CBF transcription factors. The Plant Cell 23, 2568–2580.
Induction of dormancy in Arabidopsis summer annuals requires parallel regulation of DOG1 and hormone metabolism by low temperature and CBF transcription factors.CrossRef | 1:CAS:528:DC%2BC3MXhtFeqsL7I&md5=98c6e5e3271d15bf92a94d774931a056CAS |

Koornneef M, Blankestijn-de Vries H, Hanhart CJ, Soppe WJJ, Peeters T (1994) The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild type. The Plant Journal 6, 911–919.
The phenotype of some late-flowering mutants is enhanced by a locus on chromosome 5 that is not effective in the Landsberg erecta wild type.CrossRef | 1:CAS:528:DyaK2MXjsFyqu7w%3D&md5=9077f16d073ef4ec49bbd4c5ead33956CAS |

Korves TM, Schmid KJ, Caicedo AL, Mays C, Stinchcombe JR, Purugganan MD, Schmitt J (2007) Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field. American Naturalist 169, E141–E157.
Fitness effects associated with the major flowering time gene FRIGIDA in Arabidopsis thaliana in the field.CrossRef |

Kronholm I, Xavier Pico F, Alonso-Blanco C, Goudet J, de Meaux J (2012) Genetic basis of adaptation in Arabidopsis thaliana: local adaptation at the seed dormancy QTL DOG1. Evolution 66, 2287–2302.
Genetic basis of adaptation in Arabidopsis thaliana: local adaptation at the seed dormancy QTL DOG1.CrossRef |

Kucera B, Cohn MA, Leubner-Metzger G (2005) Plant hormone interactions during seed dormancy release and germination. Seed Science Research 15, 281–307.
Plant hormone interactions during seed dormancy release and germination.CrossRef | 1:CAS:528:DC%2BD28XhsFGrtr0%3D&md5=3c78b91e870795275ee5ef2df638be7fCAS |

Le Corre V (2005) Variation at two flowering time genes within and among populations of Arabidopsis thaliana: comparison with markers and traits. Molecular Ecology 14, 4181–4192.
Variation at two flowering time genes within and among populations of Arabidopsis thaliana: comparison with markers and traits.CrossRef | 1:CAS:528:DC%2BD2MXht1OltbfI&md5=31f7c5a1eb8864eb604c10143887fb76CAS |

Le Corre V, Roux F, Reboud X (2002) DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time. Molecular Biology and Evolution 19, 1261–1271.
DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation is consistent with local selection for flowering time.CrossRef | 1:CAS:528:DC%2BD38XmtF2rsr4%3D&md5=856caf528659d5225f092b7a84690476CAS |

Lee I, Amasino RM (1995) Effect of vernalization, photoperiod, and light quality on the flowering phenotype of Arabidopsis plants containing the FRIGIDA gene. Plant Physiology 108, 157–162.
Effect of vernalization, photoperiod, and light quality on the flowering phenotype of Arabidopsis plants containing the FRIGIDA gene.CrossRef | 1:CAS:528:DyaK2MXls1Ohs78%3D&md5=8293ec2dc1f060fa2cfa55f2ea2ec4afCAS |

Lee H, Suh SS, Park E, Cho E, Ahn JH, Kim SG, Lee JS, Kwon YM, Lee I (2000) The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis. Genes & Development 14, 2366–2376.
The AGAMOUS-LIKE 20 MADS domain protein integrates floral inductive pathways in Arabidopsis.CrossRef | 1:CAS:528:DC%2BD3cXntVSksrY%3D&md5=9f552d7c03f79d4250a78aa2592bcdadCAS |

Liu Y, Geyer R, Van Zanten M, Carles A, Li Y, Hörold A, van Nocker S, Soppe WJ (2011) Identification of the Arabidopsis REDUCED DORMANCY 2 gene uncovers a role for the polymerase associated factor 1 complex in seed dormancy. PLoS One 6, e22241
Identification of the Arabidopsis REDUCED DORMANCY 2 gene uncovers a role for the polymerase associated factor 1 complex in seed dormancy.CrossRef | 1:CAS:528:DC%2BC3MXhtVKgtLjF&md5=e09e90318c62b92d0e6aa834317254f6CAS |

Lovell JT, Juenger TE, Michaels SD, Lasky JR, Platt A, Richards JH, Yu X, Easlon HM, Sen S, McKay JK (2013) Pleiotropy of FRIGIDA enhances the potential for multivariate adaptation. Proceedings of the Royal Society of London. Series B, Biological Sciences 280, 20131043
Pleiotropy of FRIGIDA enhances the potential for multivariate adaptation.CrossRef |

MacGregor DR, Kendall SL, Florance H, Fedi F, Moore K, Paszkiewicz K, Smirnoff N, Penfield S (2015) Seed production temperature regulation of primary dormancy occurs through control of seed coat phenylpropanoid metabolism. New Phytologist 205, 642–652.
Seed production temperature regulation of primary dormancy occurs through control of seed coat phenylpropanoid metabolism.CrossRef | 1:CAS:528:DC%2BC2cXitFantr7M&md5=33b3cee3e0d39948cfbf8fc6eec0108fCAS |

Mendiondo GM, Leymarie J, Farrant JM, Corbineau F, Benech-Arnold RL (2010) Differential expression of abscisic acid metabolism and signalling genes induced by seed-covering structures or hypoxia in barley (Hordeum vulgare L.) grains. Seed Science Research 20, 69–77.
Differential expression of abscisic acid metabolism and signalling genes induced by seed-covering structures or hypoxia in barley (Hordeum vulgare L.) grains.CrossRef | 1:CAS:528:DC%2BC3cXltlegtLo%3D&md5=b8e4d9bf4ab1b08c4df18e4ac5e49eb2CAS |

Menzel A, Sparks TH, Estrella N, Roy DB (2006) Altered geographic and temporal variability in phenology in response to climate change. Global Ecology and Biogeography 15, 498–504.
Altered geographic and temporal variability in phenology in response to climate change.CrossRef |

Michaels SD, Amasino RM (1999) FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering. The Plant Cell 11, 949–956.
FLOWERING LOCUS C encodes a novel MADS domain protein that acts as a repressor of flowering.CrossRef | 1:CAS:528:DyaK1MXjvVajsLc%3D&md5=29bfe9217cdea5769d328f8771679948CAS |

Michaels SD, Amasino RM (2001) Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization. The Plant Cell 13, 935–941.
Loss of FLOWERING LOCUS C activity eliminates the late-flowering phenotype of FRIGIDA and autonomous pathway mutations but not responsiveness to vernalization.CrossRef | 1:CAS:528:DC%2BD3MXjtFajsrs%3D&md5=66311b370c1fe458f8fa0910dada2e49CAS |

Michaels SD, He Y, Scortecci KC, Amasino RM (2003) Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 100, 10102–10107.
Attenuation of FLOWERING LOCUS C activity as a mechanism for the evolution of summer-annual flowering behavior in Arabidopsis.CrossRef | 1:CAS:528:DC%2BD3sXmvVeisL8%3D&md5=995afef805d4811602129b9f42b9c88bCAS |

Michaels SD, Bezerra IC, Amasino RM (2004) FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America 101, 3281–3285.
FRIGIDA-related genes are required for the winter-annual habit in Arabidopsis.CrossRef | 1:CAS:528:DC%2BD2cXitlWhurc%3D&md5=89367dc53f27d51cdf6bf8ca80710cc2CAS |

Michaels SD, Himelblau E, Kim SY, Schomburg FM, Amasino RM (2005) Integration of flowering signals in winter-annual Arabidopsis. Plant Physiology 137, 149–156.
Integration of flowering signals in winter-annual Arabidopsis.CrossRef | 1:CAS:528:DC%2BD2MXhtFOmu7w%3D&md5=bf475a7af584b3cca95d53ef9bec26f3CAS |

Montesinos-Navarro A, Xavier Picó F, Tonsor SJ (2012) Clinal variation in seed traits influencing life cycle timing in Arabidopsis thaliana. Evolution 66, 3417–3431.
Clinal variation in seed traits influencing life cycle timing in Arabidopsis thaliana.CrossRef |

Mouradov A, Cremer F, Coupland G (2002) Control of flowering time: interacting pathways as a basis for diversity. The Plant Cell 14, S111–S130.

Munguía-Rosas MA, Ollerton J, Parra-Tabla V, De-Nova JA (2011) Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured. Ecology Letters 14, 511–521.
Meta-analysis of phenotypic selection on flowering phenology suggests that early flowering plants are favoured.CrossRef |

Murphey M, Kovach K, Elnacash T, He H, Bentskink L, Donohue K (2015) DOG1-imposed dormancy mediates germination responses to temperature cues. Environmental and Experimental Botany 112, 33–43.
DOG1-imposed dormancy mediates germination responses to temperature cues.CrossRef | 1:CAS:528:DC%2BC2cXhvF2htb3I&md5=a8a52fbcb1262cbc47fa336e99504848CAS |

Murren CJ (2002) Phenotypic integration in plants. Plant Species Biology 17, 89–99.
Phenotypic integration in plants.CrossRef |

Nakabayashi K, Bartsch M, Xiang Y, Miatton E, Pellengahr S, Yano R, Seo M, Soppe WJ (2012) The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION1 protein levels in freshly harvested seeds. The Plant Cell 24, 2826–2838.
The time required for dormancy release in Arabidopsis is determined by DELAY OF GERMINATION1 protein levels in freshly harvested seeds.CrossRef | 1:CAS:528:DC%2BC38XhtlChsb%2FJ&md5=88b52cce746c4cc236d70b88a5a1ed6bCAS |

Nakamura S, Abe F, Kawahigashi H, Nakazono K, Tagiri A, Matsumoto T, Utsugi S, Ogawa T, Handa H, Ishida H, Mori M (2011) A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination. The Plant Cell 23, 3215–3229.
A wheat homolog of MOTHER OF FT AND TFL1 acts in the regulation of germination.CrossRef | 1:CAS:528:DC%2BC3MXhsVGqtr%2FF&md5=e06162fdc617e4d5b988270136f1922fCAS |

Nordborg M, Bergelson J (1999) The effect of seed and rosette cold treatment on germination and flowering time in some Arabidopsis thaliana (Brassicaceae) ecotypes. American Journal of Botany 86, 470–475.
The effect of seed and rosette cold treatment on germination and flowering time in some Arabidopsis thaliana (Brassicaceae) ecotypes.CrossRef | 1:STN:280:DC%2BC3MnhtVKjsA%3D%3D&md5=be4c47ba1e505edcbfaccbc689af7f8aCAS |

Orr HA (2000) Adaptation and the cost of complexity. Evolution 54, 13–20.
Adaptation and the cost of complexity.CrossRef | 1:STN:280:DC%2BD3cvjsFOmuw%3D%3D&md5=f48de014ac6a4b21245a202368fb17ddCAS |

Parmesan C (2006) Ecological and evolutionary responses to recent climate change. Annual Review of Ecology Evolution and Systematics 37, 637–669.
Ecological and evolutionary responses to recent climate change.CrossRef |

Pigliucci M (2003) Phenotypic integration: studying the ecology and evolution of complex phenotypes. Ecology Letters 6, 265–272.
Phenotypic integration: studying the ecology and evolution of complex phenotypes.CrossRef |

Ream TS, Woods DP, Amasino RM (2012) The molecular basis of vernalization in different plant groups. In ‘Cold Spring Harbor symposia on quantitative biology, vol. 77’. pp. 105–115. (Cold Spring Harbor Laboratory Press).

Rodríguez MV, Mendiondo GM, Maskin L, Gudesblat GE, Iusem ND, Benech-Arnold RL (2009) Expression of ABA signalling genes and ABI5 protein levels in imbibed Sorghum bicolor caryopses with contrasting dormancy and at different developmental stages. Annals of Botany
Expression of ABA signalling genes and ABI5 protein levels in imbibed Sorghum bicolor caryopses with contrasting dormancy and at different developmental stages.CrossRef |

Sánchez-Bermejo E, Méndez-Vigo B, Picó FX, Martínez-Zapater JM, Alonso-Blanco C (2012) Novel natural alleles at FLC and LVR loci account for enhanced vernalization responses in Arabidopsis thaliana. Plant, Cell & Environment 35, 1672–1684.
Novel natural alleles at FLC and LVR loci account for enhanced vernalization responses in Arabidopsis thaliana.CrossRef |

Scarcelli N, Cheverud JM, Schaal BA, Kover PX (2007) Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus. Proceedings of the National Academy of Sciences of the United States of America 104, 16986–16991.
Antagonistic pleiotropic effects reduce the potential adaptive value of the FRIGIDA locus.CrossRef | 1:CAS:528:DC%2BD2sXht1KgtLbO&md5=1f6df2f94bbde8d2af9eec200c076658CAS |

Sheldon CC, Rouse DT, Finnegan EJ, Peacock WJ, Dennis ES (2000) The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC). Proceedings of the National Academy of Sciences of the United States of America 97, 3753–3758.
The molecular basis of vernalization: the central role of FLOWERING LOCUS C (FLC).CrossRef | 1:CAS:528:DC%2BD3cXitlajsrc%3D&md5=d8546fa53fc0b4388c4a2518ad1702b2CAS |

Shindo C, Aranzana MJ, Lister C, Baxter C, Nicholls C, Nordborg M, Dean C (2005) Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis. Plant Physiology 138, 1163–1173.
Role of FRIGIDA and FLOWERING LOCUS C in determining variation in flowering time of Arabidopsis.CrossRef | 1:CAS:528:DC%2BD2MXmtVejsb0%3D&md5=7674cfc858d481bccd781f4852c66944CAS |

Shindo C, Lister C, Crevillen P, Nordborg M, Dean C (2006) Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response. Genes & Development 20, 3079–3083.
Variation in the epigenetic silencing of FLC contributes to natural variation in Arabidopsis vernalization response.CrossRef | 1:CAS:528:DC%2BD28Xht1Gnt77L&md5=92435e9b9a355ff5406ccb6f311053d9CAS |

Simpson GG, Dean C (2002) Arabidopsis: the rosetta stone of flowering time? Science 296, 285–289.
Arabidopsis: the rosetta stone of flowering time?CrossRef | 1:CAS:528:DC%2BD38XjtVWisbo%3D&md5=63b5f4795ed64520bb75cb4624d1e10aCAS |

Springthorpe V, Penfield S (2015) Flowering time and seed dormancy control use external coincidence to generate life history strategy. eLife 4, e05557
Flowering time and seed dormancy control use external coincidence to generate life history strategy.CrossRef |

Stinchcombe JR, Weinig C, Ungerer M, Olsen KM, Mays V, Halldorsdottir SS, Purugganan MD, Schmitt J (2004) A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proceedings of the National Academy of Sciences of the United States of America 101, 4712–4717.
A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA.CrossRef | 1:CAS:528:DC%2BD2cXjtFKisbc%3D&md5=40fac2850d61f09e9891c9f1a7645042CAS |

Stinchcombe JR, Caicedo AL, Hopkins R, Mays C, Boyd EW, Purugganan MD, Schmitt J (2005) Vernalization sensitivity in Arabidopsis thaliana (Brassicaceae): the effects of latitude and FLC variation. American Journal of Botany 92, 1701–1707.
Vernalization sensitivity in Arabidopsis thaliana (Brassicaceae): the effects of latitude and FLC variation.CrossRef | 1:CAS:528:DC%2BD2MXhtFOgs7fE&md5=4f944ad13a3a42c331c0762cbb7fab89CAS |

Strange A, Li P, Lister C, Anderson J, Warthmann N, Shindo C, Irwin J, Nordborg M, Dean C (2011) Major-effect alleles at relatively few loci underlie distinct vernalization and flowering variation in Arabidopsis accessions. PLoS One 6, e19949
Major-effect alleles at relatively few loci underlie distinct vernalization and flowering variation in Arabidopsis accessions.CrossRef | 1:CAS:528:DC%2BC3MXms1Kmtr0%3D&md5=0c0a3a9f572f3ae46470ec107cd6cf01CAS |

Vaistij FE, Gan Y, Penfield S, Gilday AD, Dave A, He Z, Josse EM, Choi G, Halliday KJ, Graham IA (2013) Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA. Proceedings of the National Academy of Sciences of the United States of America 110, 10866–10871.
Differential control of seed primary dormancy in Arabidopsis ecotypes by the transcription factor SPATULA.CrossRef | 1:CAS:528:DC%2BC3sXhtFejs7bN&md5=ff2b8324270330946350ce89b945e16aCAS |

Wagner GP (1988) The influence of variation and of developmental constraints on the rate of multivariate phenotypic evolution. Journal of Evolutionary Biology 1, 45–66.
The influence of variation and of developmental constraints on the rate of multivariate phenotypic evolution.CrossRef |

Wagner GP (1995) Adaptation and the modular design of organisms. In ‘Advances in artificial life’. (Eds F Moran, A Moreno, JJ Merelo, P Chacon) pp. 317–328. (Springer: Berlin)

Wagner GP, Kenney-Hunt JP, Pavlicev M, Peck JR, Waxman D, Cheverud JM (2008) Pleiotropic scaling of gene effects and the ‘cost of complexity’. Nature 452, 470–472.
Pleiotropic scaling of gene effects and the ‘cost of complexity’.CrossRef | 1:CAS:528:DC%2BD1cXjslCnurY%3D&md5=1d1001eaf786f34e61f2d1aecc6a35e6CAS |

Walther GR, Post E, Convey P, Menzel A, Parmesan C, Beebee TJC, Fromentin JM, Hoegh-Guldberg O, Bairlein F (2002) Ecological responses to recent climate change. Nature 416, 389–395.
Ecological responses to recent climate change.CrossRef | 1:CAS:528:DC%2BD38XislantL8%3D&md5=723d9098516acce9f598f0a4fa2e28e0CAS |

Werner JD, Borevitz JO, Uhlenhaut NH, Ecker JR, Chory J, Weigel D (2005) FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions. Genetics 170, 1197–1207.
FRIGIDA-independent variation in flowering time of natural Arabidopsis thaliana accessions.CrossRef | 1:CAS:528:DC%2BD2MXps1Khs7c%3D&md5=d7d1245362a6fac20405ebe6dd6da5daCAS |

Willis CG, Baskin C, Baskin J, Auld JR, Venable DL, Cavender-Bares J, Donohue K, Rubio de Casas R, Group TNGW (2014) Dormancy and diversification: environmentally cued dormancy, evolutionary hubs, and diversification of the seed plants. New Phytologist 203, 300–309.
Dormancy and diversification: environmentally cued dormancy, evolutionary hubs, and diversification of the seed plants.CrossRef |



Rent Article (via Deepdyve) Export Citation Cited By (4)

View Altmetrics