Despite the essential role of specialized metabolites (SMs) in the interaction of plants with the environment, studying the ability of crop seeds to produce these protective compounds has been neglected. Furthermore, seeds produce a myriad of SMs, providing an interesting model to investigate their diversity and plasticity. Camelina sativa gained a lot of interest in the past few years as a rustic oilseed crop. A characterization of seed SM landscapes in six camelina genotypes grown in the field and harvested during five growing seasons has been undertaken in this work. This allowed a comprehensive annotation of seed SMs combining analyses that cluster SMs based on their chemical structures and co-accumulation patterns. These data showed broad effects of the environment on the stimulation of the seed SM. Among well-annotated compounds, flavonols were identified as the metabolic class characterized by high plasticity, revealing significant variable accumulation according to the year and/or the genotype. Lastly, a deeper characterization of primary metabolites and lipids in two selected genotypes has been performed. We showed that, in addition to flavonols, alkaloids and glucosinolates displayed a higher phenotypic plasticity with respect to most of the primary metabolites, including some sugars and major storage compounds such as fatty acids, proteins and most lipid classes (e.g. diacylglycerols, triacylglycerols), but similar plasticity compared with free amino acids and carboxylic acids. This work highlighted major and unexplored effects of the environment on the seed SM, demonstrating that seeds exhibit a dynamic and plastic metabolism, with an impact on seed quality.

SummarySeeds produce a myriad of Specialized Metabolites (SMs). Nevertheless, despite the essential role of SMs in the interaction of plants with their environment, studying the ability of crop seeds to produce these protective compounds has been neglected. Camelina is an oilseed crop, whose seeds are characterized by high oil content and a unique composition, including broad SM diversity. We characterized SM landscapes in the seeds of six camelina cultivars grown in the open field and harvested during five consecutive growing seasons. We achieved a comprehensive annotation of camelina seed SMs combining molecular and correlation network analyses, which cluster SMs based on their chemical structures and co-accumulation patterns, respectively. Thus, we were able to evaluate the impact of the genotype and environment on the accumulation of these metabolites. Our data showed surprisingly high and unexplored effects of the environment on the stimulation of the seed-specialized metabolome. Moreover, they emphasize that seed SMs display a much higher environmental plasticity than storage compounds (e.g. oil and proteins). Last, we identified flavonols as the most plastic metabolic class, revealing highly variable accumulation according to the environmental conditions and/or the genotype. This work highlights the predominant effect of the environment on the regulation of the seed-specialized metabolome, with a potential impact on the seed quality of camelina and other crop species.Significance statementSeeds produce a myriad of Specialized Metabolites (SMs) with an essential role in the interaction of plants with their environment. We characterized SM landscapes in the seeds of six camelina cultivars grown in the open field and harvested during five consecutive growing seasons. We highlight the predominant effect of the environment on the regulation of the seed-specialized metabolome, with a potential impact on seed quality of camelina and other crop plant species.