Mouse Fat-Specific Protein 27 (FSP27) expressed in plant cells localizes to lipid droplets and promotes lipid droplet accumulation and fusion

Authors: PRICE, ANN - University Of North Texas; DONER, NATHAN - University Of Guelph; GIDDA, SATINDER - University Of Guelph; PURI, VISHWAJETT - Ohio University; JAMES, CHRIS - University Of North Texas; SCHAMI, ALYSSA - University Of North Texas; Yurchenko, Olga; MULLEN, ROBERT - University Of Guelph; Dyer, John; CHAPMAN, KENT - University Of North Texas

Submitted to: Biochimie
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/5/2019
Publication Date: 8/7/2019
Citation: Price, A.M., Doner, N., Gidda, S.K., Puri, V., James, C., Schami, A., Yurchenko, O., Mullen, R.T., Dyer, J.M., Chapman, K.D. 2019. Mouse Fat-Specific Protein 27 (FSP27) expressed in plant cells localizes to lipid droplets and promotes lipid droplet accumulation and fusion. Biochimie. 169:41-53. https://doi.org/10.1016/j.biochi.2019.08.002.
DOI: https://doi.org/10.1016/j.biochi.2019.08.002

Interpretive Summary: Plant oils are important commodities used for a variety of purposes including food, feed, cooking, industrial applications, and biofuels. Given their high value, there is significant interest in finding ways to increase oil content in plants. While much is known about the enzymes that synthesize plant oils, little is known about the proteins involved in “packaging” these oils into subcellular organelles called “lipid droplets”. In recent years, several proteins have been identified that are involved in this process, and surprisingly, manipulation of these proteins has proven to be an effective means to increase oil content in plants. In the current study, scientists at the ARS lab in Maricopa, Arizona, the University of North Texas, the University of Guelph, and Ohio University characterized the function of a mammalian lipid droplet protein called FSP27 when expressed in plant cells. Notably, plants lack any apparent FSP27-like genes, so it was unclear how FSP27 would function when expressed in plants. Like in mammalian cells, FSP27 targeted to lipid droplets in plants, induced their clustering, and ultimately lead to their fusion. The end-result was an increase in both the number and size of lipid droplets in plants, as well as an increase in seed oil content. These results suggest that expression of FSP27 in plants represents a potential strategy for increasing oil content and energy density in bioenergy and/or non-food oilseed crops.

Technical Abstract: Fat-Specific Protein 27 (FSP27) is a member of a small group of proteins found in vertebrates that contains a Cell-death Inducing DNA fragmentation factor-a-like Effector (CIDE)-C domain involved in lipid droplet (LD) accumulation and energy homeostasis. FSP27 is predominantly expressed in white and brown adipose tissues, as well as liver, and plays a key role in mediating LD-LD fusion. No orthologs have been identified in invertebrates or plants. In this study, we tested the functionality of FSP27 in stably-transformed Arabidopsis thaliana leaves and seeds, as well as through transient expression in Nicotiana tabacum suspension-cultured cells and N. benthamiana leaves. Confocal microscopic analysis of cells revealed that 1) FSP27 correctly localized to LDs in plant tissues in a manner similar to localization observed in mammalian cells, 2) accumulated at LD-LD contact sites, and 3) induced fusion of LDs. Furthermore, expression of native or green fluorescent protein-tagged FSP27 in stable transgenic A. thaliana plants increased LD abundance in leaves and altered LD morphology and increased oil content in seeds. Given that plant oils have uses in human and animal nutrition as well as industrial uses such as biofuels and bioplastics, our results suggest that ectopic expression of FSP27 in plants represents a potential strategy for increasing oil content and energy density in bioenergy or oilseed crops.