Quantitative modelling of biological response dynamics reveals novel patterns in plant volatile signalling

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Abstract

Biological responses to environmental stimuli are inherently dynamic. Recent technological advances enable detailed time-resolved measurements of such responses. However, a unifying model for the quantitative characterisation of dynamic response curves is lacking, thus limiting biological insights and comparisons. We developed an unbiased mathematical modelling approach that allows for the quantitative characterisation of biological response curves without a priori knowledge of underlying biochemical mechanisms. Using stress-induced plant volatile emissions, we show that the model performs well across a wide range of datasets, including incomplete induction curves, curves with low sampling resolution and complex multi-modal responses that result from overlapping stimuli. Using the model, we uncover a range of previously unrecognised patterns in volatile induction curves, including i) a strong light-independent impact of the time of day of wounding on the onset, duration and shape of the volatile induction responses, ii) an accentuation of volatile-specific induction curve shapes by herbivory-associated molecular patterns (HAMPs) and iii) independent regulation of the strength and duration of volatile induction across genotypes. We conclude that our model allows for the quantitative analysis of dynamic response curves and can identify new biological response patterns. The presented approach will pave the way to characterising dynamic organismal responses across the tree of life.

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