Temporal changes in metabolism late in seed development affect biomass composition

Authors: KAMBHAMPATI, SHRIKAAR - Danforth Plant Science Center; AZNAR-MORENO, JOSE - Kansas State University; Bailey, Sally; ARP, JENNIFER - Danforth Plant Science Center; CHU, KEVIN - Danforth Plant Science Center; Bilyeu, Kristin; DURRETT, TIMOTHY - Kansas State University; Allen, Douglas - Doug

Submitted to: Plant Physiology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 2/13/2021
Publication Date: 3/9/2021
Citation: Kambhampati, S., Aznar-Moreno, J.A., Bailey, S.R., Arp, J.J., Chu, K., Bilyeu, K.D., Durrett, T.P., Allen, D.K. 2021. Temporal changes in metabolism late in seed development affect biomass composition. Plant Physiology. 186(2):874-890. https://doi.org/10.1093/plphys/kiab116.
DOI: https://doi.org/10.1093/plphys/kiab116

Interpretive Summary: Soybeans are valued for their composition that is high in protein and lipid; however during the course of development seed composition transitions through maximum levels of lipid such that at maturity the total amount of lipid is less. The reduced amount of lipid at maturity implies that seed value is decreased during the final dessication stages of seed metabolism. We performed a series of biochemical analyses including measurements of metabolite levels and labeling of isotopes during development to assess the metabolism within the seed. Our results suggest that some of the carbon from lipids that are turned over late in development may be important to help sustain other activities in the seed including the production of oligosaccharides which are an indigestible form of carbohydrates that do not contribute to seed value. The results from the studies have implications for improving soybean composition for food, feed, fuel and renewable needs that are beneficial.

Technical Abstract: The negative association between protein and oil production in soybean (Glycine max) seed is well-documented. However, this inverse relationship is based primarily on the composition of mature seed, which reflects the cumulative result of events over the course of soybean seed development and therefore does not convey information specific to metabolic fluctuations during developmental growth regimes. In this study, we assessed maternal nutrient supply via measurement of seed coat exudates and metabolite levels within the cotyledon throughout development to identify trends in the accumulation of central carbon and nitrogen metabolic intermediates. Active metabolic activity during late seed development was probed through transient labeling with C substrates. The results indicated: (1) a drop in lipid contents during seed maturation with a concomitant increase in carbohydrates, (2) a transition from seed filling to maturation phases characterized by quantitatively balanced changes in carbon use and CO2 release, (3) changes in measured carbon and nitrogen resources supplied maternally throughout development, (4) C metabolite production through gluconeogenic steps for sustained carbohydrate accumulation as the maternal nutrient supply diminishes, and (5) oligosaccharide biosynthesis within the seed coat during the maturation phase. These results highlight temporal engineering targets for altering final biomass composition to increase the value of soybeans and a path to breaking the inverse correlation between seed protein and oil content.