How plant cells set the tempo of rhythmic shoot construction

Project Information

TEMPO

Grant agreement ID: 101095380

DOI

10.3030/101095380

EC signature date 2 June 2023

Start date 1 January 2024

End date 31 December 2028

Funded under

• European Research Council (ERC)

Total cost

€ 3 378 750,00

EU contribution

€ 3 378 750,00

Coordinated by

CENTRE NATIONAL DE LA RECHERCHE SCIENTIFIQUE CNRS
France

Periodic Reporting for period 1 - TEMPO (How plant cells set the tempo of rhythmic shoot construction)

Reporting period: 2024-01-01 to 2026-06-30

Summary of the context and overall objectives of the project

Time is central to the development of the body plan of multicellular organisms. One prominent developmental timing mechanism is the rhythmic, iterative addition of tissues and organs. While the tempo of rhythmic construction is often set by developmental clocks, plants use a unique mechanism in the shoot, whereby rhythmic organogenesis emerges from dynamic changes in the distribution of the hormone auxin. High auxin levels trigger organogenesis but, contrary to a long-standing theory, the period of shoot organ production - or plastochron - cannot simply be encoded in periodic auxin oscillations, due to noise in these oscillations. In this project, we hypothesize that cells record and use the history of their auxin exposure, in order to robustly set the timing of organogenesis and the period of organogenesis production (the plastochron) at the tissue scale despite noisy auxin temporal information. We are testing whether and how epigenetic tracking of auxin temporal information is used to set a robust plastochron across scales, with the aim to predictively manipulate the timing of organogenesis and the tempo of shoot construction.

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

During the first two years of the project, we made significant progress in demonstrating that manipulating the dynamics of auxin distribution affects the tempo of shoot construction and the robustness of the final shoot architecture. We also found that autophagy is directly regulated by auxin signaling and that involved in setting the timing of organogenesis. We could also analyze auxin information using live-imaging at the single cell scale and showed that auxin target gene activation is better explained by temporally integrated auxin levels than instantaneous levels. We have set the approaches to expand this analysis to the genome-wide scale using single nuclei RNA sequencing. We have also demonstrated that auxin target gene regulation involves a feedback mechanism between the effectors of auxin signaling and DNA cis-elements on which they bind in target gene promoters. This creates a combinatorial code that gives us fundamental knowledge about how auxin information is processed to regulate transcription and tools to explore the regulation of the timing of transcription and how it translates into determining the tempo of organogenesis. We have also identified putative chromatin regulators involved in epigenetic tracking of auxin information and are testing how auxin effectors impact the chromatin state and the timing of transcription. Finally, we have established key elements of a computational framework that will allow us to model auxin-regulated chromatin changes and how it translates into a memory of auxin exposure and impacts the tempo of organogenesis.

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

One of the breakthrough outcomes of this project so far is our results on how auxin signaling effectors and DNA cis-elements creates a combinatorial code controlling auxin-regulated transcription. We demonstrate that this code allows to process the auxin information into a variety of transcriptional patterns that can be radically different from the auxin distribution pattern. This works tells us that cis-elements present in the promoter of target genes will be bound by specific populations of effectors, a property that will likely be determinant for the tracking of auxin information mediated by chromatin modifications.