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Overexpression of the olive acyl carrier protein gene (OeACP1) produces alterations in fatty acid composition of tobacco leaves

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Abstract

Taking into account that fatty acid (FA) biosynthesis plays a crucial role in lipid accumulation in olive (Olea europaea L.) mesocarp, we investigated the effect of olive acyl carrier protein (ACP) on FA composition by overexpressing an olive ACP cDNA in tobacco plants. The OeACP1.1A cDNA was inserted in the nucleus or in the chloroplast DNA of different tobacco plants, resulting in extensive transcription of the transgenes. The transplastomic plants accumulated lower olive ACP levels in comparison to nuclear-transformed plants. Moreover, the phenotype of the former plants was characterized by pale green/white cotyledons with abnormal chloroplasts, delayed germination and reduced growth. We suggest that the transplastomic phenotype was likely caused by inefficient olive ACP mRNA translation in chloroplast stroma. Conversely, total lipids from leaves of nuclear transformants expressing high olive ACP levels showed a significant increase in oleic acid (18:1) and linolenic acid (18:3), and a concomitant significant reduction of hexadecadienoic acid (16:2) and hexadecatrienoic acid (16:3). This implies that in leaves of tobacco transformants, as likely in the mesocarp of olive fruit, olive ACP not only plays a general role in FA synthesis, but seems to be specifically involved in chain length regulation forwarding the elongation to C18 FAs and the subsequent desaturation to 18:1 and 18:3.

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Acknowledgments

The work has been partially supported by the Project OLEA—Genomics and Breeding of Olive, funded by MIPAAF, Italy, and by a CNR Short-Term Mobility grant to MB. We thank Dr. Ralph Bock for providing us with the pLW38 transformation vector and with tobacco seeds of plants transformed with the same vector.

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Correspondence to Michele Bellucci.

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Supplemental Figure 1.

Physical maps (not drawn to scale) of the targeting region in tobacco plastome (ptDNA), the plastid transformation vectors pLW38.ACP(Flag) and pLW38.ΔACP(Flag), and the nuclear transformation vector pGREEN.ACP. Filled black boxes represent the transgenes (ACP for OeACP1.1A, aadA and neomycin phosphotransferase, nptII) and grey boxes represent their expression elements, white boxes represent tobacco plastid genes, and boxes filled with black and white lines are the T-DNA borders, left (LB) and right (RB) border. The pLW38.ACP(Flag) plasmid is the same as pLW38.ΔACP(Flag), except for the presence of the ACP 135-bp transit peptide sequence. Genes below the lines are transcribed from right to left, conversely those above the lines are transcribed in the opposite direction. The probe used for Southern blot analysis is shown as black bar corresponding to a PCR fragment covering part of the trnfM/trnG region. The predicted hybridizing fragments are indicated in kb when total DNA digested with NdeI (N) is probed with this probe. The annealing positions of primers P3′RB70, P5′RB70, P10, P11, ACP3 and ACP5 are shown. Pnos and Tnos, nopaline synthase promoter and terminator, respectively (PDF 55 kb)

Supplemental Figure 2.

Accumulation of olive ACP in different tobacco tissues and evaluation of ACP stability by pulse-chase. a Proteins (50 µg) were extracted from tobacco leaves (Le), seed (Se) and flowers (Fl), separated by SDS-PAGE and subjected to immunoblot analysis using anti-ACP antibody. Under the figure the type of tobacco line analysed is indicated. The filter was exposed for a longer time to show the signal of ΔACP(Flag) in leaves of Cl-ACP line 2. b–c Immunoblot of total soluble proteins (50 µg) extracted from a developmental series of eight leaves from the top to the bottom of the Nu-ACP line D (b) and the Cl-ACP line 2 (c). Proteins extracted from a wild-type plant were also loaded (wt). The anti-ACP antibody was used for detection. d Young leaf protoplast isolated from the same plants of the previous figures were pulse-labelled for 1 h and chased for the indicated periods of time. Cells were immunoprecipitated with anti-ACP antibody, and then analyzed by SDS-PAGE and fluorography. The same experiment was repeated with protoplasts pulse-labelled for 15 min but the results did not change (PPTX 1668 kb)

Supplemental Figure 3.

Olive ACP localized in the chloroplasts of tobacco transformed plants. Thin sections prepared from young leaves of wild-type (a, d, g), Cl-ACP plants (b, e, h), and Nu-ACP plants (c, f, i), were incubated with anti-ACP antibody, followed by secondary goat anti-rabbit 10 nm gold complex. Panels g-i are enlargements of panels d-f (boxed area). Except for weak cross contamination (g), gold particles were mainly localized in the stroma or in the stromal side of the thylakoids (white or black arrows). V, vacuole. Cy, cytoplasm. St, stroma. Bars, 5000 nm (a-c), 1000 nm (d-f), or 500 nm (g-i) (PPTX 725 kb)

Supplemental Figure 4.

Phenotypes of seedlings of tobacco wild-type and transformed plants. a The seeds were sowed on Murashige and Skoog medium with or without sucrose and kept in the growth chamber (25 °C and 16 h light/8 h dark photoperiod). The transformed plants showed here are T2 progenies derived from Cl-ACP-2 and Nu-ACP-D lines. Seeds of plant 10 B, transformed with the pLW38 vector, were obtained from Ralph Bock’s lab. b Phenotypes of soil-grown seedlings of tobacco wild-type and transformed plants (PPTX 772 kb)

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De Marchis, F., Valeri, M.C., Pompa, A. et al. Overexpression of the olive acyl carrier protein gene (OeACP1) produces alterations in fatty acid composition of tobacco leaves. Transgenic Res 25, 45–61 (2016). https://doi.org/10.1007/s11248-015-9919-z

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