A Small Phospholipase A2-α from Castor Catalyzes the Removal of Hydroxy Fatty Acids from Phosphatidylcholine in Transgenic Arabidopsis Seeds

Bayon, Shen; Chen, Guanqun; Weselake, Randall J.; Browse, John

doi:10.1104/pp.114.253641

Cited by 50 publications

(39 citation statements)

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“…For example, germination rates of fae1 RcFAH12 seeds show considerable variation, the exact mechanism of which is not clear. Lu et al (2006) observed a normal germination rate, whereas Bayon et al (2015) reported a 24% germination rate of fae1 RcFAH12 seeds. In our experiments, we observed germination rates from 30% to 98% between different batches of seeds.…”

Section: Discussionmentioning

confidence: 86%

WRINKLED1 Rescues Feedback Inhibition of Fatty Acid Synthesis in Hydroxylase-Expressing Seeds

2016

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Previous attempts at engineering Arabidopsis (Arabidopsis thaliana) to produce seed oils containing hydroxy fatty acids (HFA) have resulted in low yields of HFA compared with the native castor (Ricinus communis) plant and caused undesirable effects, including reduced total oil content. Recent studies have led to an understanding of problems involved in the accumulation of HFA in oils of transgenic plants, which include metabolic bottlenecks and a decrease in the rate of fatty acid synthesis. Focusing on engineering the triacylglycerol assembly mechanisms led to modest increases in the HFA content of seed oil, but much room for improvement still remains. We hypothesized that engineering fatty acid synthesis in the plastids to increase flux would facilitate enhanced total incorporation of fatty acids, including HFA, into seed oil. The transcription factor WRINKLED1 (WRI1) positively regulates the expression of genes involved in fatty acid synthesis and controls seed oil levels. We overexpressed Arabidopsis WRI1 in seeds of a transgenic line expressing the castor fatty acid hydroxylase. The proportion of HFA in the oil, the total HFA per seed, and the total oil content of seeds increased to an average of 20.9%, 1.26 µg, and 32.2%, respectively, across five independent lines, compared with 17.6%, 0.83 µg, and 27.9%, respectively, for isogenic segregants. WRI1 and WRI1-regulated genes involved in fatty acid synthesis were up-regulated, providing for a corresponding increase in the rate of fatty acid synthesis.

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Section: Discussionmentioning

confidence: 86%

WRINKLED1 Rescues Feedback Inhibition of Fatty Acid Synthesis in Hydroxylase-Expressing Seeds

2016

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“…<1.6‐fold), including the phospholipid acyl hydrolase genes PLA1 and PLA2 (Figure a,b), the non‐specific phospholipase C genes (Figure c) and summed expression for several phospholipase D, PLD , isoforms (Figure e). A castor bean PLA2 homologous to AT2G06925 in Arabidopsis was recently shown to reduce HFA accumulation in PC and TAG when expressed in Arabidopsis lines accumulating HFA (Bayon et al ., ). The Physaria homolog was only slightly more highly expressed (maximum 1.4‐fold) in Physaria than in Camelina, and the sequences were 91% identical compared to the mean identity of 89% across the eight Brassicaceae species (Figure i).…”

Section: Resultsmentioning

confidence: 97%

Identification of multiple lipid genes with modifications in expression and sequence associated with the evolution of hydroxy fatty acid accumulation in Physaria fendleri

et al. 2016

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Two Brassicaceae species, Physaria fendleri and Camelina sativa, are genetically very closely related to each other and to Arabidopsis thaliana. Physaria fendleri seeds contain over 50% hydroxy fatty acids (HFAs), while Camelina sativa and Arabidopsis do not accumulate HFAs. To better understand how plants evolved new biochemical pathways with the capacity to accumulate high levels of unusual fatty acids, transcript expression and protein sequences of developing seeds of Physaria fendleri, wild-type Camelina sativa, and Camelina sativa expressing a castor bean (Ricinus communis) hydroxylase were analyzed. A number of potential evolutionary adaptations within lipid metabolism that probably enhance HFA production and accumulation in Physaria fendleri, and, in their absence, limit accumulation in transgenic tissues were revealed. These adaptations occurred in at least 20 genes within several lipid pathways from the onset of fatty acid synthesis and its regulation to the assembly of triacylglycerols. Lipid genes of Physaria fendleri appear to have co-evolved through modulation of transcriptional abundances and alterations within protein sequences. Only a handful of genes showed evidence for sequence adaptation through gene duplication. Collectively, these evolutionary changes probably occurred to minimize deleterious effects of high HFA amounts and/or to enhance accumulation for physiological advantage. These results shed light on the evolution of pathways for novel fatty acid production in seeds, help explain some of the current limitations to accumulation of HFAs in transgenic plants, and may provide improved strategies for future engineering of their production.

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“…For example, variations in HFA content and oil quantity in the same genetic lines have been reported between different sets of experiments performed over a 10-year span (Adhikari et al, 2016;Bates et al, 2014;Bayon, Chen, Weselake, & Browse, 2015;Burgal et al, 2008;Lu et al, 2006;Lunn et al, 2018;van Erp et al, 2011van Erp et al, , 2015.…”

Section: Rcpdat1mentioning

confidence: 99%

The effect of light conditions on interpreting oil composition engineering in Arabidopsis seeds

Karki

Bates

2018

Plant Direct

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Arabidopsis thaliana is the most developed and utilized model plant. In particular, it is an excellent model for proof-of-concept seed oil engineering studies because it accumulates approximately 37% seed oil by weight, and it is closely related to important Brassicaceae oilseed crops. Arabidopsis can be grown under a wide variety of conditions including continuous light; however, the amount of light is strongly correlated with total seed oil accumulation. In addition, many attempts to engineer novel seed oil fatty acid compositions in Arabidopsis have reported significant reductions in oil accumulation; however, the relative reduction from the nontrans- between transgenic lines and nontransgenic controls is dependent on both the light conditions and the type of oil content measurement utilized. In addition, the light conditions effect the relative accumulation of the novel fatty acids between various transgenic lines. Therefore, the success of novel fatty acid proof-of-concept engineering strategies on both oil accumulation and fatty acid composition in Arabidopsis seeds should be considered in light of the select growth and measurement conditions prior to moving engineering strategies into crop plants. K E Y W O R D Shydroxylated fatty acids, light, ricinoleate, triacylglycerol | INTRODUCTIONThe fatty acids within triacylglycerols (TAGs, oils) are the most energy dense form of biological carbon storage. TAGs which accumulate in the seeds of oilseed crops are an important nutritional source for both calories and essential fatty acids required in human diets. In addition, seed oils also represent a renewable resource for industrial chemicals and biofuels (Carlsson, Yilmaz, Green, Stymne, & Hofvander, 2011;Durrett, Benning, & Ohlrogge, 2008;Dyer, Stymne, Green, & Carlsson, 2008). However, many of the most nutritionally valuable or industrially useful fatty acids do not accumulate in major oilseed crops, but accumulate in microalgae or in terrestrial plants with poor agronomic features (Badami & Patil, 1980;Gunstone, Harwood, & Dijkstra, 2007). Therefore, the bioengineering wileyonlinelibrary.com/journal/pld3 | 1 of oilseed crops to accumulate TAG with novel fatty acid compositions for use in food or industrial feedstocks has been a goal of the plant lipid community for over 20 years. Most engineering of plants to produce novel TAG fatty acid compositions has been first demonstrated in Arabidopsis thaliana seeds, and the wide range of unique fatty acid compositions produced has been reviewed extensively (Aznar-Moreno & Durrett, 2017;Bates, 2016;Cahoon et al., 2007;Carlsson et al., 2011;Dyer et al., 2008;Haslam et al., 2013;Lee, Chen, & Kim, 2015;Lu, Napier, Clemente, & Cahoon, 2011;Napier, 2007;Napier, Haslam, Beaudoin, & Cahoon, 2014;Ruiz-Lopez, Usher, Sayanova, Napier, & Haslam, 2015;Singh, Zhou, Liu, Stymne, & Green, 2005;Vanhercke, Wood, Stymne, Singh, & Green, 2013).Despite the over two decades of plant lipid engineering, we still cannot predict the effect of most engineering approaches on the final f...

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A Small Phospholipase A2-α from Castor Catalyzes the Removal of Hydroxy Fatty Acids from Phosphatidylcholine in Transgenic Arabidopsis Seeds

Cited by 50 publications

References 58 publications

WRINKLED1 Rescues Feedback Inhibition of Fatty Acid Synthesis in Hydroxylase-Expressing Seeds

WRINKLED1 Rescues Feedback Inhibition of Fatty Acid Synthesis in Hydroxylase-Expressing Seeds

Identification of multiple lipid genes with modifications in expression and sequence associated with the evolution of hydroxy fatty acid accumulation in Physaria fendleri

The effect of light conditions on interpreting oil composition engineering in Arabidopsis seeds

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