Developmental function and state transitions of a gene expression oscillator in
            <i>Caenorhabditis elegans</i>

Meeuse, Milou W.M.; Hauser, Yannick P; Moya, Lucas J Morales; Hendriks, Gert‐Jan; Eglinger, Jan; Bogaarts, Guy; Tsiairis, Charisios D.; Großhans, Helge

doi:10.15252/msb.209975

Cited by 37 publications

(122 citation statements)

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“…In addition, the seam cells V1-V4 and V6 undergo an additional symmetric division in the L2 larval stage, doubling their number. Oscillatory gene expression is a pervasive phenomenon in C. elegans, with thousands of gene transcripts oscillating during development with a periodicity corresponding to that of the molting cycle[12-14]. Here, we focused on the oscillatory gene wrt-2, a hedgehog-like protein expressed in seam cells, that peaks in expression once every larval stage[12, 21] (Fig.…”

Section: Resultsmentioning

confidence: 99%

“…On the molecular level, developmental timing is thought to be controlled either by oscillators or ‘hourglass’ mechanisms. In C. elegans, even though there is now evidence both for hourglass mechanisms[16, 17] and oscillators[11, 14] in regulating timing of larval development, we still do not understand how the exact time at which cell-level events are initiated is determined on the molecular level. Both hourglass and oscillator mechanisms do not exhibit temporal scaling of their decay time or period, respectively, without alterations to their basic mechanism.…”

Section: Discussionmentioning

confidence: 99%

“…There is a clear periodic aspect to C. elegans development, with molts occurring every 8-10 hours at 25°C. Moreover, larval stages are accompanied by genome-wide oscillatory expression of a multitude of genes, with peaks occurring once per larval stage[12-14].…”

Section: Introductionmentioning

confidence: 99%

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Temporal scaling inC. eleganslarval development

Filina

Haagmans

2020

Preprint

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It is essential that correct temporal order of cellular events is maintained during animal development. During post-embryonic development, the duration of development depends on external conditions, such as food availability, diet and temperature. How timing of cellular events is impacted when the rate of development is changed is not known. We used a novel time-lapse microscopy approach to simultaneously measure the timing of oscillatory gene expression, seam cell divisions and cuticle shedding in individual animals during C. elegans larval development. We then studied how timing of these events was impacted by changes in temperature or diet, and in lin-42/Period mutants that show strongly perturbed and heterogeneous timing of larval development. We uncovered significant variability in timing between individuals under the same conditions. However, we found that changes in timing between individuals were fully explained by temporal scaling, meaning that each event occurred at the same relative time, when rescaled by the total duration of development in each individual. Upon changing conditions, we found that larval development separated into distinct epochs that differed in developmental rate. Changes in timing of individual events were fully captured by temporal scaling for events occurring within each epoch, but not for events from different epochs. Overall, our results reveal a surprisingly simple structure that governs changes in timing of development in response to environmental conditions. The unexpected observation of continued development and accurate temporal scaling in growth-arrested lin-42 mutants rules out a mechanism that explains temporal scaling by linking developmental timing to body size.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

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Temporal scaling inC. eleganslarval development

Filina

Haagmans

2020

Preprint

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“…To measure the growth rate and the body size of individuals of C. elegans , we used agarose-based microchambers 22,23 to track individual animals at high temporal resolution throughout post-embryonic development by live imaging. We used a strain ubiquitously expressing gfp under control of the eft-3 promoter from a single-copy transgene 23 , providing high contrast images for robust and precise segmentation of the outline of animals (Fig. 1b).…”

Section: Resultsmentioning

confidence: 99%

“…For example, the phase-shifted oscillatory expression of different cuticular collagens ensures their timely during synthesis prior to moulting 27 . Hence, development and oscillations are tightly linked 23 : conditions that change the duration of development also change the frequency of oscillations, and vice versa 27 .…”

Section: Introductionmentioning

confidence: 99%

A folder mechanism ensures size uniformity amongC. elegansindividuals by coupling growth and development

Großhans

2021

Preprint

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Animals increase by orders of magnitude in their volume during development. Hence, even small differences in the growth rates between individuals could generate large differences in their adult body size. Yet, such volume divergence among individuals is usually not observed in nature.We combined theory and experiment to understand the mechanisms of body size uniformity. Using live imaging, we measured the volume growth of hundreds of individuals of C. elegans over the entire span of their postembryonic development. We find that C. elegans grows exponentially in volume with a coefficient of variation of the growth rate of ∼7%, but that individuals diverge much less in volume than expected from this heterogeneity. The mechanism counteracting size divergence does not involve size thresholds for developmental milestones. Instead, an inverse coupling of the growth rate and the duration of development produces a constant volume fold change per larval stage.The duration of larval stages of C. elegans is determined by the period of a developmental oscillator. Using mathematical modelling, we show that an anti-correlation between the growth rate and the oscillatory period emerges as an intrinsic property of a genetic oscillator. We propose that the robustness of body volume fold change is a hard-wired characteristic of the oscillatory circuit and does not require elaborate mechanisms of size control by cellular signalling. Indeed, the coupling of growth and development was unaltered by mutation of canonical pathways of growth control. This novel concept of size homeostasis may broadly apply to other multicellular systems controlled by genetic oscillators.

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