Circadian and environmental signal integration in a natural population of Arabidopsis

Author:

Nishio Haruki12ORCID,Cano-Ramirez Dora L.34,Muranaka Tomoaki15ORCID,de Barros Dantas Luíza Lane6ORCID,Honjo Mie N.1ORCID,Sugisaka Jiro1,Kudoh Hiroshi1ORCID,Dodd Antony N.6ORCID

Affiliation:

1. Center for Ecological Research, Kyoto University, Otsu, Shiga 520-2113, Japan

2. Data Science and AI Innovation Research Promotion Center, Shiga University, Hikone, Shiga 522-8522, Japan

3. The Sainsbury Laboratory, University of Cambridge, Cambridge CB2 1LR, United Kingdom

4. School of Biological Sciences, University of Bristol, Bristol BS8 1TQ, United Kingdom

5. Graduate School of Bioagricultural Sciences, Nagoya University, Nagoya, Aichi 464-0814, Japan

6. Department of Cell and Developmental Biology, John Innes Centre, Norwich NR4 7RU, United Kingdom

Abstract

Plants sense and respond to environmental cues during 24 h fluctuations in their environment. This requires the integration of internal cues such as circadian timing with environmental cues such as light and temperature to elicit cellular responses through signal transduction. However, the integration and transduction of circadian and environmental signals by plants growing in natural environments remains poorly understood. To gain insights into 24 h dynamics of environmental signaling in nature, we performed a field study of signal transduction from the nucleus to chloroplasts in a natural population of Arabidopsis halleri. Using several modeling approaches to interpret the data, we identified that the circadian clock and temperature are key regulators of this pathway under natural conditions. We identified potential time-delay steps between pathway components, and diel fluctuations in the response of the pathway to temperature cues that are reminiscent of the process of circadian gating. We found that our modeling framework can be extended to other signaling pathways that undergo diel oscillations and respond to environmental cues. This approach of combining studies of gene expression in the field with modeling allowed us to identify the dynamic integration and transduction of environmental cues, in plant cells, under naturally fluctuating diel cycles.

Funder

UKRI | Biotechnology and Biological Sciences Research Council

Royal Society

Leverhulme Trust

MEXT | Japan Society for the Promotion of Science

MEXT | JST | Core Research for Evolutional Science and Technology

Publisher

Proceedings of the National Academy of Sciences

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