Eukaryotic lipid metabolic pathway is essential for functional chloroplasts and CO ₂ and light responses in Arabidopsis guard cells

Abstract

SignificanceGuard cells have photosynthetically active chloroplasts in most plant species. However, the significance of their existence in guard cells or their developmental mechanisms is unknown. Here, through a forward-genetic approach, we have identified a key feature and a function of guard cell chloroplasts. We observed that a mutation that impaired chloroplast biogenesis in guard cells also disrupted the regulation of stomatal movements by CO2 and light. We demonstrated that guard cell chloroplasts, compared with those in mesophyll cells, display a unique lipid metabolism, in which the prokaryotic pathway is diminished and the eukaryotic pathway gains control. Our findings highlight the importance of the eukaryotic pathway for developing functional chloroplasts in guard cells.

CRISPR-TSKO: A Technique for Efficient Mutagenesis in Specific Cell Types, Tissues, or Organs in Arabidopsis

“…The function of chloroplasts in guard cells has been the subject of debate (Lawson, 2009). Recently, the discovery of the Arabidopsis green less stomata 1 mutant further supports the hypothesis that functional chloroplasts in guard cells are important for stomatal responses to CO 2 and light, resulting in stomatal opening (Negi et al, 2018). CRISPR-TSKO plants with mutated PDS3, or other genes required for chloroplast development and/or function, specifically in the stomatal lineage can be powerful tools to test these and other hypothesized functions of chloroplasts in guard cells.…”

Lipids Composition in Plant Membranes

“…Moreover, 16:3 plants are those which produce up to half of the MGDG in the plastidial pathway [111]. The eukaryotic pathway is involved in the glycerolipid synthesis in all plants, but mostly in 18:3 plants (which means 18 acyl carbons and 3 double bonds) in the sn-2 position of MGDG molecule [110]. Irregardless pathway type, biosynthesis of membrane lipids starts from the formation of PAs, which are utilized to produce plastidic lipids or phospholipids.…”

“…Irregardless pathway type, biosynthesis of membrane lipids starts from the formation of PAs, which are utilized to produce plastidic lipids or phospholipids. Phosphatidic acid produced in the chloroplasts can be converted to diacylglycerol (DAG), which then serves as a precursor for plastidic lipid synthesis [45,110,112,113]. PA is an intermediate molecule in the lipid synthesis and can be converted to and from PC and DAG because of the low energy requirements to remove them from membranes.…”

“…3 Division of lipids based on the type of the lipid phase produced in aqueous systems Fig. 4 Prokaryotic and eukaryotic pathways [45,110,113] synthesized de novo with fatty acids, then removed from other lipids or derived from TAG turnover [111]. The prokaryotic pathway synthesizes four classes of glycerolipids: three glycolipid classes, i.e., MGDG, DGDG, trigalactosyldiacylglycerol (TGDG), and one sulfolipid class, SQDG.…”

“…The eukaryotic pathway of 16:0/18:0 DAG moieties can produce around 20% of total DGDG. During the life cycle of plants, an active lipid exchange between the chloroplast and ER occurs via the import of the DAG moiety of PCs from the ER to the chloroplast envelope where it contributes to the DAG pool used to synthesize plastidic lipids [45,110,112,113].…”