The dimorphic diaspore model Aethionema arabicum (Brassicaceae): Distinct molecular and morphological control of responses to parental and germination temperatures

Plants in habitats with unpredictable conditions are often characterized by diversifying their 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 seed and pericarp hormone contents identified a role of the IND pericarp in imposing coat dormancy by generating hypoxia affecting ABA sensitivity. This involved expression of morph-specific transcription factors, hypoxia response and cell wall-remodeling genes, as well as altered abscisic acid (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. IN A NUTSHELL BackgroundHeteromorphic diaspores (fruits and seeds) are an adaptive bet-hedging strategy to ensure survival in spatiotemporally variable environments. The stone cress Aethionema arabicum, an annual plant native to semi-arid habitats in Anatolia (Turkey), one of the worlds hotspots of biodiversity. It is a close relative of Arabidopsis, rapeseed, cabbage and other Brassica crops, but in contrast to these Ae. arabicum disperses two distinct diaspores from the same plant. These dimorphic diaspores are the mucilaginous seeds (dispersed by pod shatter) and indehiscent fruits (dispersed by abscission). The wing-like pericarp (fruit coat) of the single-seeded indehiscent fruit allows wind dispersal over large distances. The amounts and ratios of the dimorphic diaspores are variable and depend on the environmental conditions. The dimorphic diaspores differ in morphology, dormancy and germination properties and thereby make Ae. arabicum an excellent model for the comparative investigation of the underpinning molecular mechanisms. QuestionWe asked how temperature during fruit and seed formation and during seed germination affect dormancy release and germination speed, and how the morphology, hormonal regulation, and the expression of genes differ between the dimorphic diaspores. FindingsLarge-scale comparative transcriptome and hormone analyses of the mucilaginous seeds and the indehiscent fruits, as well as the seeds artificially extracted from indehiscent fruits by pericarp (fruit coat) removal, provided comprehensive datasets for their distinct thermal responses. Material obtained from plants grown at different temperatures during reproduction was imbibed at different temperatures for germination. This altered the abscisic acid (ABA) metabolism and the pericarp biomechanical properties. Diaspore-specific differences in response to distinct imbibition temperatures identified distinct gene expression patterns in seeds, distinct seed and pericarp hormone contents, and a role of the pericarp in generating hypoxia inside the fruit and imposing coat dormancy. This revealed distinct combinations of specific transcription factors, hypoxia responses and cell wall-remodeling genes, as well as altered signaling pathway genes. Next stepsOur large-scale comparative transcriptome datasets are easily and publicly accessible via the Aethionema arabicum web portal (https://plantcode.cup.uni-freiburg.de/aetar_db/index.php). We plan to expand this by future work on seedlings derived from the dimorphic diaspores, by comparing different Ae. arabicum genotypes, and by studying responses to specific stresses. Understanding the molecular basis of this fascinating example of developmental diversity and plasticity and its regulation by temperature is expected to add insight how plants respond to changing environmental conditions.