Plants in habitats with unpredictable conditions often have diversified bet-hedging strategies that ensure fitness over a wider range of variable environmental factors. A striking example is the diaspore (seed and fruit) heteromorphism that evolved to maximize species survival in Aethionema arabicum (Brassicaceae) in which external and endogenous triggers allow the production of two distinct diaspores on the same plant. Using this dimorphic diaspore model, we identified contrasting molecular, biophysical, and ecophysiological mechanisms in the germination responses to different temperatures of the mucilaginous seeds (M+ seed morphs), the dispersed indehiscent fruits (IND fruit morphs), and the bare non-mucilaginous M- seeds obtained by pericarp (fruit coat) removal from IND fruits. Large-scale comparative transcriptome and hormone analyses of M+ seeds, IND fruits, and M- seeds provided comprehensive datasets for their distinct thermal responses. Morph-specific differences in co-expressed gene modules in seeds, as well as in seed and pericarp hormone contents, identified a role of the IND pericarp in imposing coat dormancy by generating hypoxia affecting abscisic acid (ABA) sensitivity. This involved expression of morph-specific transcription factors, hypoxia response, and cell wall remodeling genes, as well as altered ABA metabolism, transport, and signaling. Parental temperature affected ABA contents and ABA-related gene expression and altered IND pericarp biomechanical properties. Elucidating the molecular framework underlying the diaspore heteromorphism can provide insight into developmental responses to globally changing temperatures.

Biosystematics Group Wageningen University PB Wageningen 6708 The Netherlands

Centre for Biological Signalling Studies University of Freiburg Freiburg 79104 Germany

Department of Biological Sciences Royal Holloway University of London Egham Surrey TW20 0EX UK

Department of Biology Botany University of Osnabrück Osnabrück 49076 Germany

Gregor Mendel Institute of Molecular Plant Biology Austrian Academy of Sciences Vienna Biocenter Vienna 1030 Austria

Institute for Mediterranean and Subtropical Horticulture La Mayora Málaga 29010 Spain

Laboratory of Growth Regulators Faculty of Science Palacký University and Institute of Experimental Botany Czech Academy of Sciences Olomouc 78371 Czech Republic

Matthias Schleiden Institute Department of Genetics Friedrich Schiller University Jena Jena 07743 Germany

Plant Cell Biology Faculty of Biology University of Marburg Marburg 35043 Germany

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Aethionema arabicum dimorphic seed trait resetting during transition to seedlings