LDIP cooperates with SEIPIN and LDAP to facilitate lipid droplet biogenesis in Arabidopsis

Authors: PYC, MICHAL - University Of Guelph; GIDDA, SATINDER - University Of Guelph; Seay, Damien; ESNAY, NICOLAS - University Of North Texas; KRETZSCHMAR, FRANZISKA - University Of Gottingen; CAI, YINGQI - Brookhaven National Laboratory; DONER, NATHAN - University Of Guelph; GREER, MICHAEL - University Of North Texas; Hull, Joe; COULON, DENIS - University Of Bordeaux; BREHELIN, CLAIRE - University Of Bordeaux; YURCHENKO, OLGA - Former ARS Employee; DE VRIES, JAN - Gottingen University; VALERIUS, OLIVER - Goettingen University; BRAUS, GERHARD - Goettingen University; ISCHEBECK, TILL - Goettingen University; CHAPMAN, KENT - University Of North Texas; Dyer, John; MULLEN, ROBERT - University Of Guelph

Submitted to: The Plant Cell
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 6/26/2021
Publication Date: 6/9/2021
Citation: Pyc, M., Gidda, S.K., Seay, D., Esnay, N., Kretzschmar, F.K., Cai, Y., Doner, N.M., Greer, M.S., Hull, J.J., Coulon, D., Brehelin, C., Yurchenko, O., De Vries, J., Valerius, O., Braus, G.H., Ischebeck, T., Chapman, K.D., Dyer, J.M., Mullen, R.T. 2021. LDIP cooperates with SEIPIN and LDAP to facilitate lipid droplet biogenesis in Arabidopsis. The Plant Cell. 33(9):3076-3101. https://doi.org/10.1093/plcell/koab179.
DOI: https://doi.org/10.1093/plcell/koab179

Interpretive Summary: The seed oils of plants represent an energy-dense source of lipids that are important for post-germinative seedling growth, and also have practical end-uses including food, feed, fuel, and feedstocks for industry. While much is known about how oil is synthesized in plant cells, little is known about how the lipids are “packaged” and stored in the aqueous environment of the cell. This study provides significant insight to the molecular mechanisms involved in this process by defining the functional relationships between three different proteins. The results describe a step-wise process where oil is first synthesized in one organelle, then these 3 proteins work together to transfer the lipids into circular storage organelles called “lipid droplets,” which accumulate as an emulsion in the cell interior. These findings represent a significant advancement in our understanding of oil production in plants and will be of greatest interest to scientists interested in the molecular mechanisms of oil synthesis, and utilizing this information for increasing oil content in oilseed and bioenergy crops.

Technical Abstract: Cytoplasmic lipid droplets (LDs) are evolutionarily-conserved organelles that store neutral lipids and play critical roles in plant growth, development and stress responses. However, the molecular mechanisms underlying their biogenesis at the endoplasmic reticulum (ER) remain obscure. Here we show that a recently identified hydrophobic protein termed LDIP (LD-Associated Protein [LDAP]-Interacting Protein) works together with both endoplasmic reticulum-localized SEIPIN and the LD-coat protein LDAP to facilitate the process of LD formation in plants. Heterologous expression in insect cells demonstrated that LDAP is required for the targeting of LDIP to the LD surface, and both proteins were required for the production of normal numbers and sizes of LDs in plant cells. LDIP also interacted and functioned together with SEIPIN to modulate LD numbers and sizes in plants, and co-expression of both proteins was required to restore normal LD production in seipin-deficient yeast cells. These data, combined with the analogous function of LDIP to a recently identified protein in mammalian cells called LDAF1 (LD Assembly Factor 1), are discussed in the context of a new model for LD biogenesis in plant cells with evolutionary connections to LD biogenesis in other eukaryotes.