Lipid Composition and Associated Gene Expression Patterns during Pollen Germination and Pollen Tube Growth in Olive (Olea europaea L.)

Abstract

Pollen lipids are essential for sexual reproduction but our current knowledge regarding lipid dynamics in growing pollen tubes is still very scarce. Here, we report unique lipid composition and associated gene expression patterns during olive pollen germination. Up to 376 genes involved in the biosynthesis of all lipid classes, except suberin, cutin and lipopolysaccharides, are expressed in the olive pollen. The fatty acid profile of the olive pollen is markedly different compared with other plant organs. Triacylglycerol, containing mostly C12-C16 saturated fatty acids, constitutes the bulk of olive pollen lipids. These compounds are partially mobilized, and the released fatty acids enter the β-oxidation pathway to yield acetyl-CoA, which is converted into sugars through the glyoxylate cycle in the course of pollen germination. Our data suggest that fatty acids are synthesized de novo and incorporated into glycerolipids by the “eukaryotic pathway” in elongating pollen tubes. Phosphatidic acid is synthesized de novo in the endomembrane system during pollen germination and seems to have a central role in the pollen tube lipid metabolism. The coordinated action of fatty acid desaturases FAD2-3 and FAD3B might explain the increase of linoleic and alpha-linolenic acids observed in the germinating pollen. A continuous synthesis of triacylglycerol by the action of DGAT1 enzyme, but not PDAT, seems also plausible. All these data allow for a better understanding of the lipid metabolism during the olive reproduction process, which can impact in the future in the increase of olive fruit yield and, therefore, olive oil production.

Distinct Physiological Roles of Three Phospholipid:Diacylglycerol Acyltransferase Genes in Olive Fruit with Respect to Oil Accumulation and the Response to Abiotic Stress

“…In summary, all these results suggest that the relative contribution of PDAT and DGAT enzymes to TAG synthesis in olive seems to be tissue-dependent. Supporting this hypothesis, previous studies from our group indicated that PDAT activity may also participate in the TAG biosynthesis in olive callus culture (Hernández et al, 2008), while during pollen germination and pollen tube growth the contribution of DGAT1 but not DGAT2, PDAT1-1 and PDAT1-2 to de novo TAG synthesis has been reported (Hernández et al, 2020a).…”

“…In olive, two DGAT genes ( OeDGAT1 and OeDGAT2 ) have been isolated and characterized, which show overlapping but distinct expression patterns during olive mesocarp growth ( Giannoulia et al, 2000 ; Banilas et al, 2011 ). In contrast, no PDAT genes have been characterized in olive to date, although two genes ( OePDAT1-1 and OePDAT1-2 ) have been identified in the olive pollen ( Hernández et al, 2020a ).…”

Comparative Metabolic Analysis Reveals a Metabolic Switch in Mature, Hydrated, and Germinated Pollen in Arabidopsis thaliana

“…Neutral lipids including TAG in tobacco pollen were reduced during 6 h of pollen germination, similar to lipid bodies in olive pollen after 7 h of pollen germination ( Rodriguez-Garcia et al, 2003 ). Another study detailed changes in neutral and polar lipid fractions over olive pollen germination ( Hernández et al, 2020 ). Interestingly, they found the fatty acid composition from total lipids was significantly altered, although the TAG content remained unchanged during the first 6 h of germination ( Hernández et al, 2020 ).…”

“…Another study detailed changes in neutral and polar lipid fractions over olive pollen germination ( Hernández et al, 2020 ). Interestingly, they found the fatty acid composition from total lipids was significantly altered, although the TAG content remained unchanged during the first 6 h of germination ( Hernández et al, 2020 ). These results indicate lipid dynamic changes are stage- and species-dependent.…”

In Silico Analysis of Fatty Acid Desaturases Structures in Camelina sativa, and Functional Evaluation of Csafad7 and Csafad8 on Seed Oil Formation and Seed Morphology

“…Particularly, ω-3 fatty acid desaturases have been proven to use C18:2 as substrates to produce 18:3 in the plastid, where FAD7 and FAD8 are located, and in the ER where FAD3 are found [5]. In plants, the accumulation of 18:3 under the activity of ω-3 fatty acid desaturases, particularly FAD3 has been demonstrated in several studies, such as in soybean [108,109], in rice [110], in olive [111][112][113], in peanut [114], in flax [115], in walnuts [116], in cowpea [117], in alfalfa [118], in peach aphid [119] and now in C. sativa, according to the current study.…”