The phenotypic tails of circadian traits remain largely diverged under lower temperatures
The variation characterized in the first part of this paper was observed at 22°C which was chosen to make the data comparable to several previously published studies of interest. We wanted to test whether the circadian phenotypic diversity we observed at 22°C continued at temperatures of 16°C and 10°C; closer to those found in the natural Swedish environment. To simplify the dataset, we selected 10 accessions to represent each of the six phenotypic tails as highlighted in Figure 1. We wished to investigate whether reduced temperatures would affect the phenotypic tails equally, drive them further apart or lead to a convergence of their phenotypes. Our null hypothesis was that the phenotypic diversity seen at 22℃ would exist consistently at lower temperatures with no differential effect on the phenotypic tail groups.
The results show that decreasing temperature had a massive overall effect on all three circadian outputs, particularly RAE and phase (accession means can be viewed in Supplementary File 3). Overall, the divergence between the tail groups was largely maintained, although the gap reduced at 10°C (Figure 5a-c). For each trait, a general linear model was fitted to the data in order to test the significance of explanatory factors (Supplementary Tables 15-17).
For period, membership to the short or long tail groups was the largest explanatory variable and the group means remained clearly distinct across all temperatures. Temperature also had a large overall effect on period, with rhythms at 16°C running much slower than at 22°C. At 10°C periods were again shorter, accompanied by higher RAE (reduced rhythm robustness) (Supplementary Figure 7). The difference in the period temperature responses of the two groups can be seen by the gradients of the thick colored lines in Figure 5A. There was also significant variation between the temperature response of individual accessions within each tail group, especially in the long period group (see thin grey lines in Figure 5A). Interestingly, Col-0 reacted very differently to the Swedish accessions tested, showing an almost linear decrease in period with increasing temperature (dashed line in 5A).
For RAE, which we equate to rhythm robustness, we found that temperature had an even greater effect than for period, with rhythms at 10C showing a marked decrease in robustness (Figure 5B). The tails converge as the temperature decreases, with lower temperatures having an especially large effect on the low RAE group.
For phase, decreasing temperature to 10°C caused a large shift of approximately 7.4 hours towards dawn accompanied by increased variability for each accession (Figure 5C). The means of the two phase-tail groups remained distinct across the three temperatures and there was no significant difference in their relative change of phase with temperature.
We also conducted an independent experiment with the phase tail accessions to verify the phase estimates from the two seed batches measured at 22°C (Supplementary Figure 9).
Across all traits we observed an increase in the within-accession variability at lower temperatures indicated by larger standard deviations in period, higher RAE scores and a greater number of rhythms being rejected from Biodare2 analysis as arrhythmic.
Discussion
We measured DF rhythms in 191 naturally occurring SwedishArabidopsis accessions and show that circadian phenotypes display considerable variation. This variation does not conform to previously described latitudinal clines in Arabidopsis (Michael et al., 2003), as we find the longest periods in accessions from the South of the country and the shortest periods in the North. In our study, circadian phenotypes are also clustered into geographical groups rather than following a distinct latitudinal cline. We suggest that the period variation we observe in the Swedish population is due largely to founder effects from ancestral migrations of individuals adapted to different selection pressures (Flohr et al., 2013), and may be influenced by serendipitous fixing of alleles through genetic drift (Song et al., 2006).
We found a high level of correlation between circadian period, phase and RAE in these accessions; period was negatively correlated with both RAE and phase. Interestingly, in the study by Michael et al, period, phase and amplitude were reported to vary independently for leaf movement rhythms in a global panel (Michael et al., 2003).
Periods were found to be significantly different between two sub-populations co-existing in the same geographical area in the South. In spite of this, accessions with very long periods (belonging to the long-period phenotypic tail) were found in both of these populations and the minor COR28 SNP was also found in both the PC.A and PC.C sub-groups.
We show that circadian variation assayed by DF is genetically heritable and is associated with several highly significant polymorphisms, two of which (ELF3 and COR28 ) had previously acknowledged circadian functions. COR28 is partially redundant with its partner COR27 and acts both upstream and downstream of the circadian clock (X. Li et al., 2016; Wang et al., 2017). TDNA insertions in these genes have been shown to lengthen periods, extend flowering time and increase freezing tolerance (X. Li et al., 2016; Wang et al., 2017). Natural allelic diversity in COR28 has not previously been described. Here, we show that a set of 16 naturally occurring accessions from southern Sweden have a W58S amino acid substitution which results in a long period comparable to that seen in cor28 TDNA insert mutants. COR28 and COR27 are expressed in a blue-light and temperature dependent manner, plausibly suggesting why this gene could be under selection in the Swedish environment. The mechanism through which W58S affects the function of COR28 remains unclear. COR28 is a small peptide of ~26kDa and so may not require active transport for nuclear localization (Hicks GR, 2013). No DNA binding domains have been identified in the COR28 sequence, however it has been suggested to regulate TOC1 and PRR5 transcription through the formation of protein complexes (X. Li et al., 2016). It is possible that this modification affects the ability of COR28 to form these protein interactions.
We also identified ELF-sha alleles in Northern accessions which were associated with higher RAE ratios. In barley, a mutant ortholog ofELF3 ; eam8 was shown to have been positively selected for growth in high-latitude environments, particularly in Scandinavia (Zakhrabekova et al., 2012). eam8 cultivars are rapid flowering enabling survival under short growing seasons, but also have severally attenuated circadian function (Faure et al., 2012).
Finally, we investigated the effect of temperature on natural circadian variation between accessions with divergent circadian phenotypes. Temperature had a large effect on period and an even greater one on phase and RAE means in both tail groups, indicating a low level of temperature compensation for these outputs. This also shows that the forces governing compensation for period do not act equally on maintaining constant RAE or peak phase. Interestingly, rhythms appeared to be most robust at 22°C, which might not be expected given that the warmest months in Sweden average around 15-17°C. A similar loss of rhythm robustness at lower temperatures has been observed in wheat (Rees et al., 2019).
Period had a non-linear relationship with temperature in these accessions, lengthening from 22°C to 16°C, before shortening again at 10C. This arrow shaped profile likely reflects two interacting forces at work; 1) between 22°C and 27°C the acceleration of rhythms due to increased rate kinetics and 2) between 22°C and 10°C the balancing forces of circadian temperature compensation. Gould et al. found a similar effect of temperature on period using leaf-movement rhythms at 22°C, 17°C and 12°C, and showed that the cold temperature compensation response works through an independent mechanism to the hot temperature compensation response (Gould et al., 2006). The profile suggests that temperature compensation is biased towards correction at colder temperatures in these accessions. It is possible that adaptation to a cold climate has selected for a cold compensation response to overcome excessive deceleration of the clock, although we are unable to explain why the rhythms should be even shorter at 10°C than at 16°C or why the shortening of periods are accompanied by a loss of overall rhythmicity. Although divergence between the phenotypic tails decreased at lower temperatures, the groups remained largely separate, reconfirming that these tail phenotypes are due to heritable genotypic differences. This work demonstrates the utility of using DF imaging to analyse natural variation across genetically diverse populations.
Authors’ contributions:
This project was conceptualized by AH and HR . HR designed and conducted imaging experiments and mutant screening. JKMB and HR carried out statistical analysis and data processing. The GWA analysis was done by RJ and HR. All authors contributed to interpretation of results. The paper was written by HR with assistance from RJ, JKMB and AH. All authors approved the final manuscript.
Alabadi, D., Oyama, T., Yanovsky, M. J., Harmon, F. G., Más, P., & Kay, S. A. (2001). Reciprocal Regulation Between TOC1 and LHY/CCA1 Within the Arabidopsis Circadian Clock. Science , 293 (5531), 880–883. https://doi.org/10.1126/science.1061320
Allemand, R., & David, J. R. (1974). The Circadian Rhythm of Oviposition in Drosophila melanogaster: A Genetic Latitudinal Cline in Wild Populations. In Jap. J. Pharmac (Vol. 33). Princeton Univ. Press. https://link.springer.com/content/pdf/10.1007%2FBF01937401.pdf
Alonso-Blanco, C., Andrade, J., Becker, C., Bemm, F., Bergelson, J., Borgwardt, K. M., Cao, J., Chae, E., Dezwaan, T. M., Ding, W., Ecker, J. R., Exposito-Alonso, M., Farlow, A., Fitz, J., Gan, X., Grimm, D. G., Hancock, A. M., Henz, S. R., Holm, S., … Zhou, X. (2016). 1,135 Genomes Reveal the Global Pattern of Polymorphism in Arabidopsis thaliana. Cell , 166 (2), 481–491. https://doi.org/10.1016/j.cell.2016.05.063
Anwer, M. U., Boikoglou, E., Herrero, E., Hallstein, M., Davis, A. M., Velikkakam James, G., Nagy, F., & Davis, S. J. (2014). Natural variation reveals that intracellular distribution of ELF3 protein is associated with function in the circadian clock. ELife , 3 . https://doi.org/10.7554/eLife.02206
Aschoff, J. (1979). Circadian rhythms: influences of internal and external factors on the period measured in constant conditions.Zeitschrift Fur Tierpsychologie , 49 (3), 225–249. http://www.ncbi.nlm.nih.gov/pubmed/386643
Bastow, R., Mylne, J. S., Lister, C., Lippman, Z., Martienssen, R. A., & Dean, C. (2004). Vernalization requires epigenetic silencing of FLC by histone methylation. Nature , 427 (6970), 164–167. https://doi.org/10.1038/nature02269
Bloomer, R. H., & Dean, C. (2017). Fine-tuning timing: natural variation informs the mechanistic basis of the switch to flowering in Arabidopsis thaliana. Journal of Experimental Botany ,68 (20), 5439–5452. https://doi.org/10.1093/jxb/erx270
Box, M. S., Huang, B. E., Domijan, M., Jaeger, K. E., Khattak, A. K., Yoo, S. J., Sedivy, E. L., Jones, D. M., Hearn, T. J., Webb, A. A. R., Grant, A., Locke, J. C. W., & Wigge, P. A. (2015). ELF3 Controls Thermoresponsive Growth in Arabidopsis. Current Biology ,25 (2), 194–199. https://doi.org/10.1016/J.CUB.2014.10.076
Covington, M. F., Maloof, J. N., Straume, M., Kay, S. A., & Harmer, S. L. (2008). Global transcriptome analysis reveals circadian regulation of key pathways in plant growth and development. Genome Biology ,9 (8), R130. https://doi.org/10.1186/gb-2008-9-8-r130
de Montaigu, A., Giakountis, A., Rubin, M., Tóth, R., Cremer, F., Sokolova, V., Porri, A., Reymond, M., Weinig, C., & Coupland, G. (2015). Natural diversity in daily rhythms of gene expression contributes to phenotypic variation. Proceedings of the National Academy of Sciences of the United States of America , 112 (3), 905–910. https://doi.org/10.1073/pnas.1422242112
Dodd, A. N., Kusakina, J., Hall, A., Gould, P. D., & Hanaoka, M. (2014). The circadian regulation of photosynthesis. Photosynthesis Research , 119 (1–2), 181–190. https://doi.org/10.1007/s11120-013-9811-8
Dodd, A. N., Salathia, N., Hall, A., Kévei, E., Tóth, R., Nagy, F., Hibberd, J. M., Millar, A. J., & Webb, A. a R. (2005). Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science (New York, N.Y.) , 309 (5734), 630–633. https://doi.org/10.1126/science.1115581
Edwards, K. D., Lynn, J. R., Gyula, P., Nagy, F., & Millar, A. J. (2005). Natural allelic variation in the temperature-compensation mechanisms of the Arabidopsis thaliana circadian clock. Genetics ,170 (1), 387–400. https://doi.org/10.1534/genetics.104.035238
Exposito-Alonso, M., Vasseur, F., Ding, W., Wang, G., Burbano, H. A., & Weigel, D. (2018). Genomic basis and evolutionary potential for extreme drought adaptation in Arabidopsis thaliana Europe PMC Funders Group.Nat Ecol Evol , 2 (2), 352–358. https://doi.org/10.1038/s41559-017-0423-0
Faure, S., Turner, A. S., Gruszka, D., Christodoulou, V., Davis, S. J., Von Korff, M., & Laurie, D. A. (2012). Mutation at the circadian clock gene EARLY MATURITY 8 adapts domesticated barley (Hordeum vulgare) to short growing seasons. Proceedings of the National Academy of Sciences of the United States of America . https://doi.org/10.1073/pnas.1120496109
Fisher, N. I., & Lee, A. J. (1992). Regression Models for an Angular Response. Biometrics , 48 (3), 665. https://doi.org/10.2307/2532334
Flohr, R. C. E., Blom, C. J., Rainey, P. B., & Beaumont, H. J. E. (2013). Founder niche constrains evolutionary adaptive radiation.Proceedings of the National Academy of Sciences of the United States of America , 110 (51), 20663–20668. https://doi.org/10.1073/pnas.1310310110
Goltsev V, Zaharieva I, Chernev P, S. R. (2009). Delayed fuorescence in photosynthesis. Photosynth Res. , 101 (2–3), 217–232.
Gould, P. D., Locke, J. C. W., Larue, C., Southern, M. M., Davis, S. J., Hanano, S., Moyle, R., Milich, R., Putterill, J., Millar, A. J., & Hall, A. (2006). The Molecular Basis of Temperature Compensation in the Arabidopsis Circadian Clock. THE PLANT CELL ONLINE , 18 (5), 1177–1187. https://doi.org/10.1105/tpc.105.039990
Gould, Peter D., Diaz, P., Hogben, C., Kusakina, J., Salem, R., Hartwell, J., & Hall, A. (2009). Delayed fluorescence as a universal tool for the measurement of circadian rhythms in higher plants.The Plant Journal , 58 (5), 893–901. https://doi.org/10.1111/j.1365-313X.2009.03819.x
Green, R. M., Tingay, S., Wang, Z.-Y., & Tobin, E. M. (2002). Circadian rhythms confer a higher level of fitness to Arabidopsis plants.Plant Physiology , 129 (2), 576–584. https://doi.org/10.1104/pp.004374
Greenham, K., Lou, P., Puzey, J. R., Kumar, G., Arnevik, C., Farid, H., Willis, J. H., & McClung, C. R. (2017). Geographic Variation of Plant Circadian Clock Function in Natural and Agricultural Settings.Journal of Biological Rhythms , 32 (1), 26–34. https://doi.org/10.1177/0748730416679307
Harmer, S. L., Hogenesch, J. B., Straume, M., Chang, H. S., Han, B., Zhu, T., Wang, X., Kreps, J. A., & Kay, S. A. (2000). Orchestrated transcription of key pathways in Arabidopsis by the circadian clock.Science (New York, N.Y.) , 290 (5499), 2110–2113. https://doi.org/10.1126/SCIENCE.290.5499.2110
Hernando, C. E., Romanowski, A., & Yanovsky, M. J. (2017). Transcriptional and post-transcriptional control of the plant circadian gene regulatory network. Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms , 1860 (1), 84–94. https://doi.org/10.1016/J.BBAGRM.2016.07.001
Hicks GR. (2013). Nuclear Import of Plant Proteins. In Madame Curie Bioscience Database [Internet]. Landes Bioscience.
Horton, M. W., Hancock, A. M., Huang, Y. S., Toomajian, C., Atwell, S., Auton, A., Muliyati, N. W., Platt, A., Sperone, F. G., Vilhjálmsson, B. J., Nordborg, M., Borevitz, J. O., & Bergelson, J. (2012). Genome-wide patterns of genetic variation in worldwide Arabidopsis thaliana accessions from the RegMap panel. Nature Genetics , 44 (2), 212–216. https://doi.org/10.1038/ng.1042
Horton, M. W., Willems, G., Sasaki, E., Koornneef, M., & Nordborg, M. (2016). The genetic architecture of freezing tolerance varies across the range of Arabidopsis thaliana . Plant, Cell & Environment ,39 (11), 2570–2579. https://doi.org/10.1111/pce.12812
Huber, C. D., Nordborg, M., Hermisson, J., & Hellmann, I. (2014). Keeping it local: evidence for positive selection in Swedish Arabidopsis thaliana. Molecular Biology and Evolution , 31 (11), 3026–3039. https://doi.org/10.1093/molbev/msu247
Ingle, R. A., Stoker, C., Stone, W., Adams, N., Smith, R., Grant, M., Carré, I., Roden, L. C., & Denby, K. J. (2015). Jasmonate signalling drives time-of-day differences in susceptibility of Arabidopsis to the fungal pathogen Botrytis cinerea. The Plant Journal : For Cell and Molecular Biology , 84 (5), 937–948. https://doi.org/10.1111/tpj.13050
James, A. B., Syed, N. H., Bordage, S., Marshall, J., Nimmo, G. A., Jenkins, G. I., Herzyk, P., Brown, J. W. S., & Nimmo, H. G. (2012). Alternative splicing mediates responses of the Arabidopsis circadian clock to temperature changes. The Plant Cell , 24 (3), 961–981. https://doi.org/10.1105/tpc.111.093948
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 (New York, N.Y.) , 290 (5490), 344–347. https://doi.org/10.1126/SCIENCE.290.5490.344
Jursinic, P. (1986). Delayed Fluorescence: Current Concepts and Status. In Light Emission by Plants and Bacteria (pp. 292–293). Academic Press.
Kahle, D., & Wickham, H. (2013). ggmap: Spatial Visualization with ggplot2. The R Journal , 5 (1), 144–161. https://journal.r-project.org/archive/2013-1/kahle-wickham.pdf
Kerdaffrec, E., Filiault, D. L., Korte, A., Sasaki, E., Nizhynska, V., Seren, Ü., & Nordborg, M. (2016). Multiple alleles at a single locus control seed dormancy in Swedish Arabidopsis. ELife , 5 . https://doi.org/10.7554/eLife.22502
Kinmonth-Schultz, H. A., Golembeski, G. S., & Imaizumi, T. (2013). Circadian clock-regulated physiological outputs: dynamic responses in nature. Seminars in Cell & Developmental Biology , 24 (5), 407–413. https://doi.org/10.1016/j.semcdb.2013.02.006
Kooke, R., Kruijer, W., Bours, R., Becker, F., Kuhn, A., van de Geest, H., Buntjer, J., Doeswijk, T., Guerra, J., Bouwmeester, H., Vreugdenhil, D., & Keurentjes, J. J. B. (2016). Genome-Wide Association Mapping and Genomic Prediction Elucidate the Genetic Architecture of Morphological Traits in Arabidopsis. Plant Physiology , 170 (4), 2187–2203. https://doi.org/10.1104/pp.15.00997
Kusakina, J., Gould, P. D., & Hall, A. (2014). A fast circadian clock at high temperatures is a conserved feature across Arabidopsis accessions and likely to be important for vegetative yield. Plant, Cell and Environment , 37 (2), 327–340. https://doi.org/10.1111/pce.12152
Lankinen, P. (1986). Comparative a Geographical variation in circadian eclosion rhythm and photoperiodic adult diapause in Drosophila littorMis. In Journal of Sensory (Vol. 159). https://link.springer.com/content/pdf/10.1007%2FBF00612503.pdf
Li, X., Ma, D., Lu, S. X., Hu, X., Huang, R., Liang, T., Xu, T., Tobin, E. M., & Liu, H. (2016). Blue Light- and Low Temperature-Regulated COR27 and COR28 Play Roles in the Arabidopsis Circadian Clock. The Plant Cell , 28 (11), 2755–2769. https://doi.org/10.1105/tpc.16.00354
Li, Y., Huang, Y., Bergelson, J., Nordborg, M., & Borevitz, J. O. (2010). Association mapping of local climate-sensitive quantitative trait loci in Arabidopsis thaliana PLANT BIOLOGY .7 (49), 21199–21204. https://doi.org/10.1073/pnas.1007431107
Lipka, A. E., Tian, F., Wang, Q., Peiffer, J., Li, M., Bradbury, P. J., Gore, M. A., Buckler, E. S., & Zhang, Z. (2012). GAPIT: Genome association and prediction integrated tool. Bioinformatics ,28 (18), 2397–2399. https://doi.org/10.1093/bioinformatics/bts444
Long, Q., Rabanal, F. A., Meng, D., Huber, C. D., Farlow, A., Platzer, A., Zhang, Q., Vilhjálmsson, B. J., Korte, A., Nizhynska, V., Voronin, V., Korte, P., Sedman, L., Mandáková, T., Lysak, M. A., Seren, Ü., Hellmann, I., & Nordborg, M. (2013). Massive genomic variation and strong selection in Arabidopsis thaliana lines from Sweden. Nature Genetics , 45 (8), 884–890. https://doi.org/10.1038/ng.2678
Más, P., Alabadí, D., Yanovsky, M. J., Oyama, T., & Kay, S. A. (2003). Dual role of TOC1 in the control of circadian and photomorphogenic responses in Arabidopsis. The Plant Cell , 15 (1), 223–236. https://doi.org/10.1105/TPC.006734
Michael, T. P., Salomé, P. A., Yu, H. J., Spencer, T. R., Sharp, E. L., McPeek, M. A., Alonso, J. M., Ecker, J. R., & McClung, C. R. (2003). Enhanced Fitness Conferred by Naturally Occurring Variation in the Circadian Clock. Science , 302 (5647), 1049–1053. https://doi.org/10.1126/science.1082971
Müller, N. A., Wijnen, C. L., Srinivasan, A., Ryngajllo, M., Ofner, I., Lin, T., Ranjan, A., West, D., Maloof, J. N., Sinha, N. R., Huang, S., Zamir, D., & Jiménez-Gómez, J. M. (2016). Domestication selected for deceleration of the circadian clock in cultivated tomato. Nature Genetics , 48 (1), 89–93. https://doi.org/10.1038/ng.3447
Nordborg, M., Hu, T. T., Ishino, Y., Jhaveri, J., Toomajian, C., Zheng, H., Bakker, E., Calabrese, P., Gladstone, J., Goyal, R., Jakobsson, M., Kim, S., Morozov, Y., Padhukasahasram, B., Plagnol, V., Rosenberg, N. A., Shah, C., Wall, J. D., Wang, J., … Bergelson, J. (2005). The Pattern of Polymorphism in Arabidopsis thaliana. PLoS Biology ,3 (7), e196. https://doi.org/10.1371/journal.pbio.0030196
Pittendrigh, C. S. (1954). ON TEMPERATURE INDEPENDENCE IN THE CLOCK SYSTEM CONTROLLING EMERGENCE TIME IN DROSOPHILA. Proceedings of the National Academy of Sciences , 40 (10), 1018 LP – 1029. https://doi.org/10.1073/pnas.40.10.1018
Pittendrigh, C. S., & Minis, D. H. (1964). The Entrainment of Circadian Oscillations by Light and Their Role as Photoperiodic Clocks. The American Naturalist , 98 (902), 261–294. https://doi.org/10.1086/282327
Proietti, S., Caarls, L., Coolen, S., Van Pelt, J. A., Van Wees, S. C. M., & Pieterse, C. M. J. (2018). Genome-wide association study reveals novel players in defense hormone crosstalk in Arabidopsis. Plant Cell and Environment , 41 (10), 2342–2356. https://doi.org/10.1111/pce.13357
Rees, H., Duncan, S., Gould, P., Wells, R., Greenwood, M., Brabbs, T., & Hall, A. (2019). A high-throughput delayed fluorescence method reveals underlying differences in the control of circadian rhythms in Triticum aestivum and Brassica napus. Plant Methods ,15 (1), 51. https://doi.org/10.1186/s13007-019-0436-6
Salome, P. A., & McClung, C. R. (2005). PSEUDO-RESPONSE REGULATOR 7 and 9 Are Partially Redundant Genes Essential for the Temperature Responsiveness of the Arabidopsis Circadian Clock. THE PLANT CELL ONLINE , 17 (3), 791–803. https://doi.org/10.1105/tpc.104.029504
Sasaki, E., Zhang, P., Atwell, S., Meng, D., & Nordborg, M. (2015). “Missing” G x E Variation Controls Flowering Time in Arabidopsis thaliana. PLOS Genetics , 11 (10), e1005597. https://doi.org/10.1371/journal.pgen.1005597
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., Tinevez, J.-Y., White, D. J., Hartenstein, V., Eliceiri, K., Tomancak, P., & Cardona, A. (2012). Fiji: an open-source platform for biological-image analysis. Nature Methods , 9 (7), 676–682. https://doi.org/10.1038/nmeth.2019
Seren, Ü. (2018). GWA-Portal: Genome-Wide Association Studies Made Easy (pp. 303–319). Humana Press, New York, NY. https://doi.org/10.1007/978-1-4939-7747-5_22
Shindo, C., Aranzana, M. J., 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 (2), 1163–1173. https://doi.org/10.1104/pp.105.061309
Song, S., Dey, D. K., & Holsinger, K. E. (2006). DIFFERENTIATION AMONG POPULATIONS WITH MIGRATION, MUTATION, AND DRIFT: IMPLICATIONS FOR GENETIC INFERENCE. Evolution , 60 (1), 1. https://doi.org/10.1554/05-315.1
Suárez-López, P., Wheatley, K., Robson, F., Onouchi, H., Valverde, F., & Coupland, G. (2001). CONSTANS mediates between the circadian clock and the control of flowering in Arabidopsis. Nature ,410 (6832), 1116–1120. https://doi.org/10.1038/35074138
Swarup, K., Alonso-Blanco, C., Lynn, J. R., Michaels, S. D., Amasino, R. M., Koornneef, M., & Millar, A. J. (1999). Natural allelic variation identifies new genes in the Arabidopsis circadian system. Plant Journal , 20 (1), 67–77. https://doi.org/10.1046/j.1365-313X.1999.00577.x
Thorsen, S. (1995). timeanddate.com . https://www.timeanddate.com/information/copyright.html
van Rooijen, R., Aarts, M. G. M., & Harbinson, J. (2015). Natural Genetic Variation for Acclimation of Photosynthetic Light Use Efficiency to Growth Irradiance in Arabidopsis. Plant Physiology ,167 (4), 1412–1429. https://doi.org/10.1104/pp.114.252239
Wang, P., Cui, X., Zhao, C., Shi, L., Zhang, G., Sun, F., Cao, X., Yuan, L., Xie, Q., & Xu, X. (2017). COR27 and COR28 encode nighttime repressors integrating Arabidopsis circadian clock and cold response. InJournal of Integrative Plant Biology (Vol. 59, Issue 2, pp. 78–85). https://doi.org/10.1111/jipb.12512
Weigel, D., & Mott, R. (2009). The 1001 Genomes Project for Arabidopsis thaliana. Genome Biology , 10 (5), 107. https://doi.org/10.1186/gb-2009-10-5-107
Yanovsky, M. J., & Kay, S. A. (2002). Molecular basis of seasonal time measurement in Arabidopsis. Nature , 419 (6904), 308–312. https://doi.org/10.1038/nature00996
Zakhrabekova, S., Gough, S. P., Braumann, I., Mul̈ler, A. H., Lundqvist, J., Ahmann, K., Dockter, C., Matyszczak, I., Kurowska, M., Druka, A., Waugh, R., Granerd, A., Stein, N., Steuernagel, B., Lundqvist, U., & Hansson, M. (2012). Induced mutations in circadian clock regulator Mat-a facilitated short-season adaptation and range extension in cultivated barley. Proceedings of the National Academy of Sciences of the United States of America . https://doi.org/10.1073/pnas.1113009109
Zhang, Z., Ersoz, E., Lai, C. Q., Todhunter, R. J., Tiwari, H. K., Gore, M. A., Bradbury, P. J., Yu, J., Arnett, D. K., Ordovas, J. M., & Buckler, E. S. (2010). Mixed linear model approach adapted for genome-wide association studies. Nature Genetics , 42 (4), 355–360. https://doi.org/10.1038/ng.546