A nested reciprocal experimental design to map the genetic architecture of transgenerational phenotypic plasticity

Abstract

Extensive studies have revealed the ecological and evolutionary significance of phenotypic plasticity, but little is known about how it is inherited between generations and the genetic architecture of its transgenerational inheritance. To address these issues, we design a mapping study by growing Arabidopsis thaliana RILs in high- and low-light environments and further growing their offspring RILs from each maternal light environment in the same contrasting environments. This tree-like design of the controlled ecological experiment provides a framework for analysing the genetic regulation of phenotypic plasticity and its non-genetic inheritance. We implement the computational approach of functional mapping to identify specific QTLs for transgenerational phenotypic plasticity. By estimating and comparing the plastic response of leaf-number growth trajectories to light environment between generations, we find that the maternal environment affects phenotypic plasticity, whereas transgenerational plasticity is shaped by the offspring environment. The genetic architecture underlying the light-induced change of leaf number not only changes from parental to offspring generations, but also depends on the maternal environment the parental generation experienced and the offspring environment the offspring generation is experiencing. Most plasticity QTLs are annotated to the genomic regions of candidate genes for specific biological functions. Our computational-experimental design provides a unique insight into dissecting the non-genetic and genetic mechanisms of phenotypic plasticity shaping plant adaptation and evolution in various forms.

Acknowledgements

We thank many members at Beijing Forestry University Center for Computational Biology for their contribution to the maintenance and cultivation of Arabidopsis RILs and data collection. This work is partially supported by special grants of Beijing Forestry University.

Author contributions

J.C. analysed data and wrote the draft. Y.W., A.D., and S.W. participated in data analysis. Y.C. performed the experiment and data collection. R.W. conceived of the idea, supervised the project, and extensively revised the manuscript.

3 Data availability statement

All data and codes used throughout this study have been made open source and are available on https://github.com/CCBBeijing/TPP.

Conflict of interests

All authors disclosed no conflict of interest.

Supplementary data

Supplementary data is available at Horticulture Research online.

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