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Supplementary Information an Independent Evolutionary Origin For Supplementary information An independent evolutionary origin for insect deterrent cucurbitacins in Iberis amara Lemeng Dong1,6*, Aldo Almeida1, Jacob Pollier2,3, Bekzod Khakimov4, Jean-Etienne Bassard1, Karel Miettinen2,3, Dan Stærk5, Rahimi, Mehran6, Carl Erik Olsen1, Mohammed Saddik Motawia1, Alain Goossens2,3, and Søren Bak1* 1Department of Plant and Environmental Science, University of Copenhagen, Thorvaldsensvej 40, DK-1871 Frederiksberg C, Denmark. 2Ghent University, Department of Plant Biotechnology and Bioinformatics, Technologiepark 71, 9052 Ghent, Belgium. 3VIB Center for Plant Systems Biology, Technologiepark 71, 9052 Ghent, Belgium. 4Department of Food Science, University of Copenhagen, Rolighedsvej 26, DK-1958 Frederiksberg C, Denmark. 5Department of Drug Design and Pharmacology, Faculty of Health and Medical Sciences, University of Copenhagen, Universitetsparken 2, DK-2100 Copenhagen, Denmark. 6Plant Hormone Biology group, Swammerdam Institute for Life Science, University of Amsterdam, Science Park 904, 1098 XH Amsterdam, the Netherlands *[email protected] [email protected] This PDF file includes: Supplementary Figure 1 to Figure 11, Supplementary Table 1 to Table 6, Supplementary NMR data (general experimental procedures, data interpretation of compound 1-5, supplementary Figure 12 to Figure 19, Supplementary Table 7 to Table 11), and References A Intensity one-week old 1.0 x108 roots 0.5 0.0 1.5 aerial 1.0 0.5 0.0 8.0 standard mix 4.0 D I B E 0.0 1 2 3 4 5 6 7 8 9 Time [min] B Intensity four-week old 1.5 x108 roots 1.0 0.5 0.0 0.8 aerial 0.4 0.0 8.0 standard mix D I B E 4.0 0.0 1 2 3 4 5 6 7 8 9 Time [min] Supplementary Figure 1 Cucurbitacin E, I, and B accumulate in both roots and aerial parts of I. amara. (A) LC-ESI-MS extracted ion chromatograms (EIC) of extracts from roots and aerial parts of one-week-old I. amara plants. (B) LC-ESI-MS extracted ion chromatograms (EIC) of extracts from roots and aerial parts of four-week-old I. amara plants. Extracted ions at m/z 539, 537, 581, and 579 are representative for sodium adducts of cucurbitacin D, I, B, E, respectively. Peaks indicated by blue, gray and black arrows verified by the mass spectrum compare to the cucurbitacin standard I, B E, respectively. Intensity x106 4 E B 3 I D 2 1 0 16 17 18 19 20 21 22 23 Time [min] Stamen Pistil Female petal Male petal Leaf Root Stem Tendril Fruit Cotyledon Stem tip Cucurbitacins standard mix Supplementary Figure 2 Cucurbitacins accumulate mainly in roots and leaves in Citrullus lanatus. LC-QTOF-MS extracted ion chromatograms (EIC) of extracts from C. lanatus stamen, female petals, leaves, stems, fruits, stem tips, pistils, male petals, roots, tendrils, cotyledons. Extracted ions at m/z 539, 537, 581, and 579 are representative for sodium adducts of cucurbitacin D, I, B, E, respectively. Peaks indicated by blue, gray and black arrows were verified by comparing their mass spectrum to the corresponding mass spectrum of standards of cucurbitacin I, B E, respectively. Note, the LC-MS analysis program changed for analyzing C. lanatus extracts (see materials and methods), giving rise to the observed changes in retention times. IaCPQ IaCAS IaOSC3 IaOSC4 IaOSC5 M Root Leaf Root Leaf 3kbp Root Leaf Root Leaf Root Leaf 2kbp Supplementary Figure 3 Agarose gel image of PCR product of 5 full-length OSCs from I. amara. Lane M, 1kb DNA ladder. 134 69 100 394 100 100 393 379 EI-MS cucurbitadienol in yeast EI-MS cycloartenol in yeast 90 EI-MS 31-norcycloartenol A 90 C 90 E 408 80 80 80 69 70 70 70 95 60 60 60 365 109 50 50 50 135 339 40 40 69 40 274 30 133 30 408 30 173 189 93 20 20 20 203 163 231 187 286 281 325 231 483 10 469 10 483 498 10 484 0 0 0 100 150 200 250 300 350 400 450 500 50 100 150 200 250 300 350 400 450 500 100 150 200 250 300 350 400 450 500 100 69 134 EI-MS cucurbitadienol standard (NMR) B 100 D 90 EI-MS cycloartenol standard 90 80 80 70 70 60 408 60 365 50 95 50 40 40 73 135 339 30 30 175 274 20 203 95 408 20 231 286 173 10 483 10 483 498 0 0 100 150 200 250 300 350 400 450 500 50 100 150 200 250 300 350 400 450 500 Supplementary Figure 4 EI-MS fragmentation spectrum of trimethylsilylated cycloartenol, 31-norcycloartenol and cucurbitadienol. (A) EI-MS of the cucurbitadienol peak in extracts of spent medium from yeast expressing IaCPQ. (B) EI-MS of a cucurbitadienol standard confirmed by NMR. (C) EI-MS of the cycloartenol peak in extracts of spent medium from yeast expressing with IaCAS. (D) EI-MS of a cycloartenol standard. (E) EI-MS of the 31-norcycloartenol peak in extracts of spent medium from yeast expressing with IaCAS. A B IaCPQ IaCAS CpCPQ CpCAS CsCPQ CsCAS IaCPQ 100% 86% 68% 70% 68% 72% IaCAS 86% 100% 68% 73% 68% 74% CpCPQ 68% 68% 100% 69% 89% 70% CpCAS 70% 73% 69% 100% 69% 93% CsCPQ 68% 68% 89% 69% 100% 70% CsCAS 72% 74% 70% 93% 70% 100% Supplementary Figure 5 Amino acid sequences % identity matrix (A) and alignment (B) between cucurbitadienol synthases (CPQs) and cycloartenol synthases (CASs) from I. amara, C. pepo and C. sativus. Red boxes indicate the amino acids different between CPQs and CASs. ClCPQ-eGFP CYP-mRFP1 A 700 C 600 500 400 Supplementary Figure 6 Organ-specific expression pattern of C. 300 200 lanatus cucurbitadienol synthase and its subcellular localization 100 ClCPQ-eGFP CYP-mRFP1 0 to the ER. (A) Relative expression of ClCPQ in different C. lanatus organs quantified by qPCR. (B) Representative confocal images of roots fruits pistils stems Relative expression (fold) expression Relative leaves stamen tendrils the epidermal cell space and the nucleus of N. benthamiana leaves Stem tips Stem cotyledons male petals male expressing N-terminally tagged proteins are shown. mRFP1 and femal petals femal B CYP98A1 (P450) are used as controls for cytosolic and ER localization, respectively. Soluble mRFP1 is found in the nucleus and fills in gaps between plant cell compartments. ER-localized proteins (CpCPQ and CYP98A1) are restricted to nuclear membranes and a well-defined ER membrane network. Scale bars = 10 mm. (C) Representative confocal images of the epidermal cell space and the nucleus of N. benthamiana leaves expressing C- terminally tagged proteins are shown. ER-localized CYP98A1 (P450) is used as a control. ClCPQ is restrained to nuclear membranes and the ER membrane network. Scale bars = 10 mm. HsLAS IaCPQ CpCPQ ClCPQ A B HsLAS IaCPQ CpCPQ ClCPQ Supplementary Figure 7 Homology modeling of OSCs and membrane interaction analysis using Positioning of Proteins in Membrane server. (A) The structure of LAS (PDB:1W6J) and homology models of IaCPQ, CpCPQ, and ClCPQ and the interaction with an empirical membrane (blue). Amino acid resides which interact with the membrane are marked in red. (B) The amino acid residues of membrane inserting sites of LAS, IaCPQ, CpCPQ, and ClCPQ are marked in green (hydrophobic) and purple (polar), and interact with fragments of lipids (cyan). OiSMT A B Abundance 134 TMSi TMSiO TMSiO Abundance 134 1000000 1800000 Trimethylsilylated hydroxy-cucurbitadienol Trimethylsilylated cucurbitadienol 73 900000 1600000 M+-2TMSiOH + + 800000 M -2TMSiOH-CH3 M -CH3 1400000 TMSi 347 700000 1200000 571 600000 73 1000000 297 + + 500000 M -TMSiOH M -TMSiOH-CH3 800000 400000 600000 274 187 + 300000 408 M+-CH M 173 3 400000 200000 M+ 481 200000 241 391 205 339 483 406437 527 586 100000 241 307 371 442 498 0 0 50 100 150 200 250 300 350 400 450 500 550 600 650 50 100 150 200 250 300 350 400 450 500 m/z--> m/z--> Supplementary Figure 8 EI-MS fragmentation patterns of trimethylsilylated 16β-hydroxy-cucurbitadienol and cucurbitadienol. (A) 16b- hydroxy-cucurbitadienol peak in N. benthamiana leaves coexpressing IaCPQ and CYP708A16. (B) Cucurbitadienol peak in N. benthamiana leaves expressing IaCPQ. M+, parent ion; TMSi, trimethylsilyl group; TMSiOH, trimethylsilanol. 2TMSiOH, two trimethylsilanol groups. Intens. O O A x106 IaCPQ+CYP708A15v2 2.50 CYP708A15v2 OH 2.00 IaCPQ 1.50 HO HO C H O C30H48O3 1.00 30 48 2 [C30H49O2]+ [C30H49O3]+ 0.50 0.00 20 22 24 26 28 30 32 Time [min] Intens. B x105 441.3724 1.00 IaCPQ+CYP708A15v2 +MS, 28.7min 0.75 118.0860 282.2789 0.50 99.5117 225.1958 297.2574 409.2739 0.25 127.1117156.1010 256.2633 315.2683 0.00 100 150 200 250 300 350 400 450 m/z Intens. C IaCPQ+CYP708A15v2 +MS, 32.5min 439.3566 x105 4.00 457.3671 2.00 421.3461 282.2789 297.2576 315.2682 0.00 280 300 320 340 360 380 400 420 440 460 m/z Supplementary Figure 9 LC-MS chromatograms and spectrums of extracts from N. benthamiana leaves agro-infiltrated with vectors expressing IaCPQ, CYP708A15v2, and IaCPQ+CYP708A15v2. (A) LC-ESI-MS total ion chromatograms (TIC) indicating two new peaks in N. benthamiana leaves coexpressing IaCPQ+CYP708A15v2, and their postulated structures and formulas based on the accurate masses. (B) MS spectrum of the first new peak at the retention time 28.7 min. (C) MS spectrum of the second new peak at the retention time 32.5 min. A B Supplementary Figure 10 Genome localization between cucurbitacin biosynthetic genes in I. amara and cucurbitaceous species. (A) Synteny between cucurbitacin biosynthetic gene clusters in C.
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