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Secrets of Palm Oil Biosynthesis Revealed

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Secrets of Palm Oil Biosynthesis Revealed COMMENTARY Secrets of palm oil biosynthesis revealed Toni Voelker1 Monsanto, Davis, CA 95616 lobally, vegetable oils are har- Not only is oil palm by far the most diacylglycerol or phosphatidyl choline to vested from a handful of oil productive oil crop, with annual yields of- TAG. So, how then is the oil palm meso- G crops at an annual rate ex- ten exceeding 4 tons/ha, but during fruit carp cell programmed for the divergence ceeding 100 million tons (1). maturation, its mesocarp cells efficiently of almost all photosynthate to lipid stor- Most oils are used for human or animal convert photosynthate to TAGs, which age, when date palm cells store photosyn- consumption, although a minor fraction is subsequently accumulate to levels as high thate simply as sugars? A priori one would derivatized to oleochemicals. More re- as exceeding 90% of the tissue dry weight predict that there must be an up-regula- cently, an increasing amount of vegetable at maturity. In contrast, in the mesocarp of tion of all of the pertinent components oil is being diverted to the production of date palm, no TAGs are found. Instead, from FA biosynthesis, precursor supply, as biodiesel [i.e., fatty acid (FA) methyl- large amounts of sugars accumulate during well as lipid assembly. However, this is not esters], and is an attractive feedstock for maturation to levels as high as 50% of what Bourgis et al. (9) find. Surprisingly, the so-called “drop-in” biofuels of the fu- dry weight (9). For their study in PNAS, none of the ER enzymes of the so-called ture, further increasing the demand on this Bourgis et al. (9) obtained several million Kennedy pathway, including DGAT or commodity (2). Because of the commer- ESTs from developing fruit tissues of the PDAT, enzymes essential for TAG bio- cial importance of vegetable oils, during two palm species. After gene annotation synthesis, were strongly up-regulated in the past 30 y, the biosynthesis of FAs and using Arabidopsis as a reference genome oil palm. Most transcript levels were found their derived acyl lipids, especially plant (3), expression levels of orthologous tran- to be the same; no or only very subtle triacylglycerols (TAGs), has attracted scripts encoding lipid biosynthesis enzymes increases were found during mesoderm a tremendous amount of scientific interest, found in oil palm and date palm were development. Clearly, the enzymes known resulting in the identification and charac- compared. Sequence identities between for this segment of the pathway appear terization of the functions of most of the the two palm species were generally higher to have an enormous capacity of adjusting fl enzymes involved in their production and than 90%, as expected for members of the to metabolic uxes, possibly 100 times sequestration (3). In addition, researchers same plant family. In a second approach, higher than in a general plant cell. In have attempted to understand the quanti- the authors monitored the levels of lipid contrast, all transcripts encoding the 18 tative regulation of biosynthesis with the plastidial FA biosynthesis enzymes in- ultimate goal of increasing oil production volved in the conversion of pyruvate to in crops. Practically all investigations in Bourgis et al. add a FAs were found significantly up-regulated this field have been conducted in devel- in oil palm, 13 times on average, and oping embryos of oilseeds, most notably new chapter to our the three members of the multisubunit in Arabidopsis. As cDNA sequences of FA synthase between 17 and 44 times. enzymes considered “rate-limiting” be- understanding of plant Somewhat more moderate but significant came available in the mid-1990s, in- oil biosynthesis. up-regulation of the same plastidial FA creasing oil production in plants has enzymes during oil palm mesoderm become the “holy grail” of plant FA bio- development were observed as well, chemistry (4, 5). However, even though enzyme transcripts through oil palm me- corroborating the interspecies compari- there are more than a dozen reports of socarp development including the transi- son. As the plastids of the oil palm meso- marginal increases of seed oil through tion to TAG production. derm produce a large quantity of FA, are genetic manipulation, channeling carbon Plant lipid biosynthesis is compartmen- there any transcriptional signatures for intermediates to TAGs has had very lim- talized differently from that of fungi and photosynthate transport, and how is gly- ited success, and no high-oil engineered animals. De novo FAs biosynthesis occurs colysis affected? Again, most of the action crop is on the market (6, 7). Only very exclusively in the plastids, and TAG as- appears to happen in the plastid; only recently a comprehensive analysis of oil sembly is located in the endoplasmic re- marginal modulations were observed in palm mesoderm during fruit ripening was ticulum (3). In oil palm fruit tissue, TAGs the cytoplasm. Plastidial transporters for published by Tranbarger et al. (8). With accumulate as oil droplets in the cyto- hexose, pentose, triose phosphate, and this investigation, Tranberger et al. step- plasm, as the electron micrographs of phosphoenolpyruvate were strongly up- ped “outside the box” (i.e., the seed) and Bourgis et al. (9) show. This is in contrast regulated in oil palm, indicating increased delivered a first detailed insight into the to the membrane-bordered oil bodies of capacity of carbon flow into the plastid, compositional, hormonal, and transcrip- seeds (10). The compartmentation of the and several plastidial glycolytic enzymes tional changes during the different phases complete biosynthetic pathway neces- were elevated as well. Photosynthate from of oil palm fruit development and com- sitates that the photosynthate, supplied as the leaves arriving as sucrose can be pared their finding to the established sugar from the leaves, not only be im- cleaved by invertase or sucrose synthase, knowledge of oilseed development. While ported into the mesocarp cells but also be and in developing oilseeds, a switch from comparing the transcriptomes and meta- transferred to the plastid lumen to become the former to the latter is observed during bolomes of developing oil accumulating substrate for FA biosynthesis. the transition to oil biosynthesis (11). It mesoderm of oil palm (Elaeis guineensis) is interesting to note that, in oil palm and sugar accumulating mesoderm of Most of the Action Is in the Plastid date palm (Phoenix dactylifera), Bourgis All plant cells are autonomous in respect et al. (9) follow a strategy that enables to acyl lipid biosynthesis, each supplying Author contributions: T.V. wrote the paper. them to differentiate metabolic determi- all their own membrane lipids. In princi- The author declares no conflict of interest. nants of the respective tissues from other ple, only one enzymatic step is needed to See companion article on page 12527. developmental phenomena. convert common membrane lipids like 1E-mail: toni.voelker@monsanto.com. www.pnas.org/cgi/doi/10.1073/pnas.1109296108 PNAS | July 26, 2011 | vol. 108 | no. 30 | 12193–12194 Downloaded by guest on September 24, 2021 mesoderm, 35 times more cell wall in- were found up-regulated during oil palm no obvious orthologues to Arabidopsis vertase than sucrose synthase transcripts maturation and at higher levels than found LEC1, LEC2, and other transcription were detected. Either the increase of su- in date palm. One of these candidates factors known to act on WRI1 in the seed crose synthase in seeds is correlated with encodes a polypeptide with high similarity were found in oil palm mesoderm. Likely, oil biosynthesis but is not causal (12), or in to the Arabidopsis WRINKLED1 tran- WRI1 in palm mesoderm responds to mesoderm, alternative metabolic routes scription factor (WRI1). A mutant of a very different network of transcrip- have evolved. WRI1 had been discovered through an tion factors. In summary, the differential analysis of Arabidopsis low-oil seed selection, which By delivering a comprehensive frame- the two palm mesocarp transcriptomes accumulated only 20% of normal TAG work of carbon partitioning in an oil-pro- revealed the following picture: in oil palm, levels in its seeds (13). The respective gene ducing, nonseed tissue, Bourgis et al. (9), the arriving sucrose is cleaved to hexoses, was identified as encoding an APETALA2- add a new chapter to our understanding of and intermediates are transported to the type transcription factor, and the mutant plant oil biosynthesis. The results demon- plastid, where glycolysis and FA synthesis rendered developing embryos unable to strate some of the principal mechanisms so are massively up-regulated. The large flux efficiently produce FAs (14). WRI1 ap- often observed in evolution, in which, out of de novo FAs is then channeled to the pears to be regulated by LEC1 and LEC2, of established networks of enzymes and endoplasmic reticulum, where “house- key transcriptional regulators of seed transcription factors, through some re- keeping” levels of the Kennedy pathway maturation, and it effects the signal from shuffling of modules, a new system is built. and associated enzymes are sufficient to LEC1, LEC2, and other factors (15) to There are other species with oil-bearing assemble the TAG, which simply accu- the transcriptional up-regulation of at mesocarp, like olive and avocado (17). mulates as oil droplets in the cytoplasm. least 10 FA biosynthesis genes, hence it is Does carbon partitioning to TAGs in these a metabolic pathway “master switch” (16). likely independently evolved high-oil tis- A WRINKLED1 for More Oil? Indeed, ectopic expression of Arabidopsis sues follow the same principles as found in The EST data not only revealed a very WRI1 has been shown to induce FA bio- oil palm? Hopefully, such questions will be clear picture of transcriptional modulation synthesis and TAG accumulation in seed- answered soon. Bourgis et al. (9) signifi- of enzymes, enabling the upscaling of acyl lings of Arabidopsis (14).
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