Untargeted metabolomic analyses reveal the diversity and plasticity of the specialized metabolome in seeds of different Camelina sativa genotypes

Abstract

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.

Ablation of glucosinolate accumulation in the oil crop Camelina sativa by targeted mutagenesis of genes encoding the transporters GTR1 and GTR2 and regulators of biosynthesis MYB28 and MYB29

“…Besides, impaired growth was observed for broiler chickens when fed with 5% of camelina seed cake (Ryhänen et al ., 2007 ). Camelina seeds exhibit a higher glucosinolate content (13.2–36.2 mmol/kg seed meal, depending on the variety) than canola (7.2 mmol/kg; Boutet et al ., 2022 ; Colombini et al ., 2014 ; Schuster and Friedt, 1998 ). We obtained comparable values for seeds of camelina WT139 (22.4 nmol/mg).…”

“…The glucosinolate content in camelina meal after solvent extraction can be further decreased during post‐processing and can thus meet the regulatory limits (European Food Safety Authority (EFSA), 2008 ; Matthäus and Angelini, 2005 ). On the other hand, the glucosinolate content of the seeds, similar to other specialized metabolites of camelina, show a very high plasticity due to environmental conditions and in different genotypes (Boutet et al ., 2022 ). Therefore, it is desirable to generate new camelina lines showing a stable and reduced glucosinolate content.…”

Recent progress in molecular genetics and omics-driven research in seed biology

“…Despite little information is available, it has been also reported that glucosinolate content decreased in seeds of B. rapa plants subjected to potassium deficiency [169]. More recently, a large environmental induction and plasticity of SMs has been observed in seeds of Camelina sativa cultivated during five consecutive growing seasons [152,153]. This work highlighted major effects of the environment on the stimulation of the seed specialized metabolome.…”

“…In addition to genetic determinism and tissue distribution, the content and nature of storage compounds (including oil and proteins) and SMs are also shaped by the environment, and strongly impact the nutritional, agronomic or industrial quality of seeds (Figure 4). Many biotic and abiotic factors, such as drought or elevated temperatures can affect seed oil and protein composition [152][153][154][155][156], seed germination, and impact seedling vigour [157,158].…”

“…Malgré le peu d'informations disponibles, il a également été rapporté que la teneur en glucosinolates diminue dans les graines de plantes B. rapa soumises à une carence en potassium [169]. Plus récemment, une forte induction environnementale et une plasticité des SMs ont été observées dans des graines de Camelina sativa cultivées pendant cinq saisons consécutives [152,153]. Ce travail a mis en évidence des effets majeurs de l'environnement sur la stimulation du métabolome spécialisé de la graine.…”