Spatiotemporal transcriptomics and metabolic profiling provide insights into gene regulatory networks during lentil seed development

Abstract

SUMMARY Lentil (Lens culinaris Medik.) is a nutritious legume with seeds rich in protein, minerals and an array of diverse specialized metabolites. The formation of a seed requires regulation and tight coordination of developmental programs to form the embryo, endosperm and seed coat compartments, which determines the structure and composition of mature seed and thus its end‐use quality. Understanding the molecular and cellular events and metabolic processes of seed development is essential for improving lentil yield and seed nutritional value. However, such information remains largely unknown, especially at the seed compartment level. In this study, we generated high‐resolution spatiotemporal gene expression profiles in lentil embryo, seed coat and whole seeds from fertilization through maturation. Apart from anatomic differences between the embryo and seed coat, comparative transcriptomics and weighted gene co‐expression network analysis revealed embryo‐ and seed coat‐specific genes and gene modules predominant in specific tissues and stages, which highlights distinct genetic programming. Furthermore, we investigated the dynamic profiles of flavonoid, isoflavone, phytic acid and saponin in seed compartments across seed development. Coupled with transcriptome data, we identified sets of candidate genes involved in the biosynthesis of these metabolites. The global view of the transcriptional and metabolic changes of lentil seed tissues throughout development provides a valuable resource for dissecting the genetic control of secondary metabolism and development of molecular tools for improving seed nutritional quality.

The Effect of Phosphorus Fertilization on Transcriptome Expression Profile during Lentil Pod and Seed Development

“…The pattern of the P influence, though, is not consistent among the P treatments, which may suggest the existence of additional factors regulating the expression of F3H. Yu et al reported that two genes in the FLS family, FLS1 and FLS2, are highly expressed in the early stages of seed development, while another gene in the FLS family, FLS3, is highly expressed in the later stages of seed development, suggesting that the FLS genes may play different roles in regulating seed development [30]. In the study conducted by Jia et al in tobacco leaves, it was observed that in higher P treatment there was a reduction in the transcript levels of NtCHS (chalcone synthase), NtCHI (chalcone isomerase), NtF3H (flavanone 3-hydroxylase), NtF30H (flavanone 30-hydroxylase) and NtFLS (flavonol synthase), while NtFLS transcript levels were increased in both juvenile and mature leaves in the lower P treatment.…”

“…These findings suggest that the control of seed size in lentils operates through the regulation of cell division, involving both cell expansion and the overall seed growth [29]. In a recent transcriptomic analysis of lentil embryos, seed coats and whole seeds, specific genes and co-expressed gene sets were found to be prevalent in distinct tissues and developmental stages, distinguishing the expression patterns of the embryo from those of the seed coat [30].The availability of the current lentil's genome assemblies that include the cultivated lentil (Lens culinaris) and the wild relative (Lens ervoides) has facilitated the potential to gain knowledge regarding mechanisms regulating even complex traits [22].…”

Applying a non-GMO breeding approach with an identified natural variation to reduce food allergen Len c3 in Lens culinaris seeds

“…Lentils ( Lens culinaris ) have nutritional, economical, and environmental advantages as an excellent source of protein-based human diet ( Kumar et al., 2016 ). Lentils have twice the level of proteins than cereals and are rich in minerals, polyphenols, and vitamins ( Yu et al., 2023 ). Lentil proteins have been a source of novel food formulations in milk substitute, curd-like products, meat products, extruded products, and baked goods ( Boye et al., 2010 ).…”

“…A major challenge is to identify and utilize the advantageous traits in a breeding program ( Gur and Zamir, 2004 ). Molecular tools for lentil breeding such as genome sequencing and transcriptome profiling are being developed rapidly ( Fedoruk et al., 2013 ; Haile et al., 2020 ; Song et al., 2022 ; Yu et al., 2023 ), which have rendered this relatively facile for identifying the target genes. In this study, we identified the LTP gene that encodes Len c3 in lentil and performed genetic screening via gene sequencing for LTP mutation from a collection of natural lentil accessions.…”