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 10C 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.
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