Acetyl-CoA synthetase is activated as part of the PDH-bypass in the oleaginous green alga<i>Chlorella desiccata</i>

Avidan, Omri; Pick, Uri

doi:10.1093/jxb/erv424

Cited by 34 publications

(29 citation statements)

References 65 publications

(90 reference statements)

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“…Such metabolic features are reminiscent of the ‘PDH bypass’ model, a metabolic pathway also reported as ‘aerobic fermentation’, where acetaldehyde produced by the decarboxylation of pyruvate, is converted to acetyl-CoA, thus furnishing the biosynthesis of fatty acids [24]. The PDH bypass has been experimentally documented in aerobic plant tissues [25, 26], and has been proposed to play a role in the rapid development of actively respiring sporophytic tissues during pollen germination [27]. In the context of clubroot infection, this mechanism would fit with above-described unexpected data: 1/ the fermentation response is triggered at a time point where respiration is apparently unaffected in infected roots 2/ clubroot symptoms are similar in the adh1-4 mutant and in the wild type.…”

Section: Discussionmentioning

confidence: 99%

Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot

et al. 2016

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BackgroundThe induction of alcohol fermentation in roots is a plant adaptive response to flooding stress and oxygen deprivation. Available transcriptomic data suggest that fermentation-related genes are also frequently induced in roots infected with gall forming pathogens, but the biological significance of this induction is unclear. In this study, we addressed the role of hypoxia responses in Arabidopsis roots during infection by the clubroot agent Plasmodiophora brassicae.ResultsThe hypoxia-related gene markers PYRUVATE DECARBOXYLASE 1 (PDC1), PYRUVATE DECARBOXYLASE 2 (PDC2) and ALCOHOL DEHYDROGENASE 1 (ADH1) were induced during secondary infection by two isolates of P. brassicae, eH and e2. PDC2 was highly induced as soon as 7 days post inoculation (dpi), i.e., before the development of gall symptoms, and GUS staining revealed that ADH1 induction was localised in infected cortical cells of root galls at 21 dpi. Clubroot symptoms were significantly milder in the pdc1 and pdc2 mutants compared with Col-0, but a null T-DNA insertional mutation of ADH1 did not affect clubroot susceptibility. The Arg/N-end rule pathway of ubiquitin-mediated proteolysis controls oxygen sensing in plants. Mutants of components of this pathway, ate1 ate2 and prt6, that both exhibit constitutive hypoxia responses, showed enhanced clubroot symptoms. In contrast, gall development was reduced in quintuple and sextuple mutants where the activity of all oxygen-sensing Group VII Ethylene Response Factor transcription factors (ERFVIIs) is absent (erfVII and prt6 erfVII).ConclusionsOur data demonstrate that the induction of PDC1 and PDC2 during the secondary infection of roots by P. brassicae contributes positively to clubroot development, and that this is controlled by oxygen-sensing through ERFVIIs. The absence of any major role of ADH1 in symptom development may also suggest that PDC activity could contribute to the formation of galls through the activation of a PDH bypass.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-016-0941-y) contains supplementary material, which is available to authorized users.

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Section: Discussionmentioning

confidence: 99%

Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot

et al. 2016

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“…For instance, acetate can be directly converted into acetyl-CoA from acetyl-CoA synthetase (ACS), and incorporate immediately into the TCA cycle or used in FA synthesis by C. reinhardtii 34. Likewise, Chlorella grown in acetate medium use ACS to directly incorporate acetate into acetyl-CoA, by-passing the PDC route for acetyl-CoA production and enabling a high rate of lipid synthesis under N-depletion63. Furthermore, glucose-fed Chlorella cultures generate more reducing power in the dark than photoautotrophically cultured Chlorella in the light, thus the former accumulates more lipids and less starch64.…”

Section: Discussionmentioning

confidence: 99%

Nitrogen-induced metabolic changes and molecular determinants of carbon allocation in Dunaliella tertiolecta

Tan

Lin

Shen

et al. 2016

Sci Rep

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Certain species of microalgae are natural accumulators of lipids, while others are more inclined to store starch. However, what governs the preference to store lipids or starch is not well understood. In this study, the microalga Dunaliella tertiolecta was used as a model to study the global gene expression profile regulating starch accumulation in microalgae. D. tertiolecta, when depleted of nitrogen, produced only 1% of dry cell weight (DCW) in neutral lipids, while starch was rapidly accumulated up to 46% DCW. The increased in starch content was accompanied by a coordinated overexpression of genes shunting carbon towards starch synthesis, a response not seen in the oleaginous microalgae Nannochloropsis oceanica, Chlamydomonas reinhardtii or Chlorella vulgaris. Genes in the central carbon metabolism pathways, particularly those of the tricarboxylic acid cycle, were also simultaneously upregulated, indicating a robust interchange of carbon skeletons for anabolic and catabolic processes. In contrast, fatty acid and triacylglycerol synthesis genes were downregulated or unchanged, suggesting that lipids are not a preferred form of storage in these cells. This study reveals the transcriptomic influence behind storage reserve allocation in D. tertiolecta and provides valuable insights into the possible manipulation of genes for engineering microorganisms to synthesize products of interest.

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“…Nevertheless, ACS has been identified in the proteomes of lipid droplets in C. reinhardtii [80, 81] and Dunaliella bardawil [82], suggesting a possible role of ACS in providing acetyl-CoA at the early stages of FA synthesis. Indeed, upregulation of ACS has been demonstrated recently to provide an alternative route for acetyl-CoA production in oleaginous C. desiccata , bypassing the traditional pathway catalyzed by plastidial pyruvate dehydrogenase (PDH), resulting in a coordinated large increase in acetyl-CoA levels that precedes TAG accumulation [83]. …”

Section: Introductionmentioning

confidence: 99%

“…, were found to exhibit ACL activity comparable to those in oleaginous heterotrophs [89], indicating that microalgae possess ACL required to utilize citrate as a carbon source for generating acetyl-CoA. Gene expression of cytoplasmic ACL was also upregulated prior to TAG accumulation in C. desiccata , but not in low TAG accumulators such as D. tertiolecta and C. reinhardtii [83]. However, ACL activity would require an efflux of citrate from the mitochondria to the cytoplasm, effectively draining the TCA cycle of its intermediates.…”

Section: Introductionmentioning

confidence: 99%

“…However, ACL activity would require an efflux of citrate from the mitochondria to the cytoplasm, effectively draining the TCA cycle of its intermediates. The contribution of cytoplasmic acetyl-CoA to FA synthesis in oleaginous microalgae also requires further validation [83]. As mitochondria functions in the light to export citrate via the citrate-oxaloacetate shuttle [90], the exported citrate could thus be exploited to produce acetyl-CoA.…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

The dilemma for lipid productivity in green microalgae: importance of substrate provision in improving oil yield without sacrificing growth

Tan

Lee

2016

Biotechnol Biofuels

131

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Rising oil prices and concerns over climate change have resulted in more emphasis on research into renewable biofuels from microalgae. Unlike plants, green microalgae have higher biomass productivity, will not compete with food and agriculture, and do not require fertile land for cultivation. However, microalgae biofuels currently suffer from high capital and operating costs due to low yields and costly extraction methods. Microalgae grown under optimal conditions produce large amounts of biomass but with low neutral lipid content, while microalgae grown in nutrient starvation accumulate high levels of neutral lipids but are slow growing. Producing lipids while maintaining high growth rates is vital for biofuel production because high biomass productivity increases yield per harvest volume while high lipid content decreases the cost of extraction per unit product. Therefore, there is a need for metabolic engineering of microalgae to constitutively produce high amounts of lipids without sacrificing growth. Substrate availability is a rate-limiting step in balancing growth and fatty acid (FA) production because both biomass and FA synthesis pathways compete for the same substrates, namely acetyl-CoA and NADPH. In this review, we discuss the efforts made for improving biofuel production in plants and microorganisms, the challenges faced in achieving lipid productivity, and the important role of precursor supply for FA synthesis. The main focus is placed on the enzymes which catalyzed the reactions supplying acetyl-CoA and NADPH.

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Acetyl-CoA synthetase is activated as part of the PDH-bypass in the oleaginous green algaChlorella desiccata

Abstract: HighlightPlastidic acetyl-CoA synthase (ptACS-2) and ATP citrate lyase are upregulated in the oleaginous alga Chlorella desiccata during nitrogen deprivation. ptACS-2 is part of the pyruvate dehydrogenase bypass which supports triacylglycerol accumulation.

Cited by 34 publications

References 65 publications

Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot

Hypoxia response in Arabidopsis roots infected by Plasmodiophora brassicae supports the development of clubroot

Nitrogen-induced metabolic changes and molecular determinants of carbon allocation in Dunaliella tertiolecta

The dilemma for lipid productivity in green microalgae: importance of substrate provision in improving oil yield without sacrificing growth

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