DOCSLIB.ORG

Chlorophyll Breakdown – How Chemistry Has Helped to Decipher a Striking Biological Enigma

Total Page：16

File Type：pdf, Size：1020Kb

Download full-text PDF Read full-text
Chlorophyll Breakdown – How Chemistry Has Helped to Decipher a Striking Biological Enigma SYNLETT0936-52141437-2096 Georg Thieme Verlag Stuttgart · New York 2019, 30, 263–274 account 263 en Syn lett B. Kräutler Account Chlorophyll Breakdown – How Chemistry Has Helped to Decipher a Striking Biological Enigma Bernhard Kräutler* Institute of Organic Chemistry and Centre of Molecular Biosciences, University of Innsbruck, Innrain 80/82, 6020 Innsbruck, Austria [email protected] Dedicated to Professor Franz-Peter Monforts on the occasion of his 70th birthday. Received: 07.08.2018 etation in spring are probably the most visual signs of life, Accepted after revision: 20.09.2018 observable on Earth from outer space.1 Indeed, the annual Published online: 31.10.2018 DOI: 10.1055/s-0037-1611063; Art ID: st-2018-a0501-a apparent ‘recycling’ of the green pigment Chl is a massive License terms: biological process involving about 1000 million tons, world- wide, and occurring by seasonally alternating de novo Chl 2 Abstract How the fall colors arise and how chlorophyll (Chl) break- biosynthesis and Chl degradation. Strikingly, until about down occurs in higher plants has remained enigmatic until three de- 30 years ago Chl seemed to disappear without leaving a cades ago. Fundamental insights into this fascinating puzzle have been trace, as non-green products of Chl breakdown remained gained, meanwhile, by basic contributions from plant biology and elusive.2,3 In fact, all searches for genuine Chl catabolites chemistry. This short review is a personal account of key advances from synthetic, mechanistic, and structural chemistry that led to the discov- were futile, since they concentrated on the detection of col- ery of the bilin-type Chl catabolites and helped elucidate the metabolic ored remains of the Chls. However, as is now well known, processes that generated them from Chl. Chl breakdown products in higher plants accumulate as col- 1 Introduction orless linear tetrapyrroles, primarily.1,4–7 All the same, the 2 Discovery and Structure Elucidation of a First Non-Green Chl bilin-type Chl catabolites, named phyllobilins (PBs),8 turn Catabolite 9 3 Structure Elucidation of Fleetingly Existent Blue-Fluorescent Chl out to be remarkably related, structurally, to bilins, the col- Catabolites ored products from heme breakdown.10 4 The Red Chl Catabolite – Key Ring-Opened Tetrapyrrole Accessed by Partial Synthesis 5 Synthesis of ‘Primary’ Fluorescent Chl Catabolites by Reduction 2 Discovery and Structure Elucidation of a of Red Chl Catabolite 6 Nonfluorescent Chl Catabolites from Isomerization of Fluores- First Non-Green Chl Catabolite cent Chl Catabolites 7 Persistent Fluorescent Chl Catabolites and Blue-Luminescent Chl breakdown has for a long time been considered to Bananas play a particular role in the recuperation of nitrogen.3 First 8 Discovery, Structure Elucidation, and Biological Formation of Dioxobilin-Type Chl Catabolites traces of non-green Chl breakdown products were traced by 9 Occurrence, Partial Synthesis, and Structure of Phyllochromobi- Matile, Thomas and coworkers by comparing the pigment lins, the Colored Bilin-Type Chl Catabolites pattern of senescent leaves of wild type Festuca pratensis 10 Conclusion and Outlook with those in ‘stay green’ mutants of this grass.11 Remark- ably, colorless compounds could be spotted in the wild type Keywords antioxidants, bilin, catabolite, chlorophyll, fluorescence, glycoside, heterocycles, pigments, porphyrinoids, phyllobilin, senes- that were absent in the green mutant, and which were pre- cence, tetrapyrroles sumed to represent Chl catabolites. These polar compounds were called ‘rusty pigments’, as they rapidly converted into rust-colored products.12 We learned to isolate one such 1 Introduction ‘rusty pigment’ without degradation and color formation, and elucidated its chemical constitution in 1991 with the The appearance of the fall colors is an enchanting and help of heteronuclear NMR spectroscopy and soft ionization puzzling phenomenon. The widespread disappearance of mass spectrometry.4,13 It turned out to be fruitful, to solve chlorophyll (Chl) in autumn and the re-greening of the veg- Georg Thieme Verlag Stuttgart · New York — Synlett 2019, 30, 263–274 264 Syn lett B. Kräutler Account the desired structure directly by purely spectroscopic O H O 5 H means,4 rather than submitting this polar Chl catabolite to 4 O O 19 1 1 NH N 19 H NH HN NH HN R chemical modifications, e.g., in order to decrease its polarity. 20 10 n H n 15 5 15 5 N HN N HN NH HN HO H R OH 5 4 H O H A B 18 O O O 1 3 O N N 19 A CO2Me CO2Me D HO C HO C CO2H HN OH 2 2 HO2C Mg H n NH N N 5 D C NH HN Pheo a (6) pFCC (5) Bn-NCCs 2,3,4 C B E CH3 E Scheme 2 Structural formulae of Pheo a (6), pFCC (5), and of NCCs 2 O H C (R = malonate), 3 (R = 1’--D-glucopyranose), and 4 (R = OH) from se- C CO2Me 3 O CO2Me O O CH3 CH3 HO2C nescent leaves of oil seed rape (Brassica napus) CH3 chlorophyll a (Chl a, R = CH3) Hv-NCC-1(1) 3 Structure Elucidation of Fleetingly Exis- chlorophyll b (Chl b, R = HC=O) tent Blue-Fluorescent Chl Catabolites Scheme 1 Structural formulae of chlorophylls a and b and of Hv-NCC-1 (1) The repeated observation of fleetingly existent blue-flu- The colorless ‘rusty pigment’ from de-greened leaves of orescent compounds alongside of the NCCs in extracts of barley (Hordeum vulgare) was unambiguously revealed to senescent leaves suggested their relevance in Chl break- be a bilane-type linear tetrapyrrole that carried structural down.17 In vitro experiments by Hörtensteiner and Matile hallmarks of the Chls, such as their characteristic ring C/E- showed the requirement for molecular oxygen and identi- portion.4 It was classified as a nonfluorescent Chl catabolite fied the Mg-free and dephytylated Chl derivative pheophor- (NCC) and given the phenomenological name Hv-NCC-1 bide a (Pheo a, 6) as a precursor for the presumed Chl (1).14 More recently, it was classified semisystematically as catabolites.18 From a preparation with Pheo a as the sub- a 1-formyl-19-oxo-16,19-dihydrophyllobilane,5,8 see strate by using an enzyme active extract of senescent leaves Scheme 1. The structure of 1 indicated oxidative ring open- of oil seed rape (Brassica napus), a rather instable blue-fluo- ing of the Chl macrocycle at the ‘northern’ meso position, rescent compound became available in small quantities, be- between C4 and C5, thus, representing a 4,5-secophytopor- lieved to be a Chl catabolite. By spectroscopic means its phyrinoid.4,13 This cleavage site contrasted with all expecta- structure was, again, revealed as a linear tetrapyrrole, 19 tions from Chl chemistry,15 but turned out to be strikingly closely related to 1, and to three polar Brassica napus NCCs reminiscent of the site of ring opening in heme break- that had meanwhile been found in senescent cotyledons of down.16 However, in contrast to the typical colored bilins oil seed rape20 (typical UV/Vis absorption spectra are col- from heme breakdown,9,16 the meso-carbon C5 of Chl a was lected in the reviews5,8). The fluorescent compound was, retained in the formyl group of the NCC 1, and its three re- therefore, phenomenologically named Bn-FCC-2 (5) and maining meso positions were saturated. Additional periph- classified as a fluorescent Chl catabolite (FCC) (see Scheme eral polar functionality of 1 pointed to puzzling catabolic 2).19 The chemical constitution of 5 supported its hypothet- reactions in its formation, raising further questions to its ical role as a biological precursor of the Bn-NCCs 2–4. The biochemical formation and to the general relevance of its molecular formula of the FCC 5 also indicated a close rela- structure for the general problem of Chl breakdown in tionship to 6, involving the mere formal incorporation of higher plants. two oxygen atoms and four hydrogen atoms in the course of the presumed formation of 5 from 6. Hence, the moderately polar FCC 5 was deduced to represent a straight forward Biographical Sketch Bernhard Kräutler studied lumbia University, New York University of Innsbruck, where chemistry at the ETH in Zürich, City) he returned to the ETH to he has been Professor Emeritus where he received his PhD start his own research group. In since October 2015. His current working with Prof. Albert the fall of 1985 he was a visiting research interests include the Eschenmoser. After postdoctor- Professor at the Roger Adams chemistry and chemical biology al studies with Prof. Allen J. Bard Labs of the University of Illinois. of chlorophyll and vitamin B12. (University of Texas, Austin) and In 1991 he became Full Profes- with Prof. Nicholas J. Turro (Co- sor of Organic Chemistry at the Georg Thieme Verlag Stuttgart · New York — Synlett 2019, 30, 263–274 265 Syn lett B. Kräutler Account (‘primary’) product of the breakdown of 6, and was as- 4 The Red Chl Catabolite – Key Ring-Opened signed the specific role as ‘primary’ FCC (pFCC).19 As the rel- Tetrapyrrole Accessed by Partial Synthesis ative configuration of the three stereocenters of pFCC (5) at C82, C12, and C13 was the same as that in Pheo a (6), their Since a red Chl catabolite was unknown in higher plants, absolute configuration was also inferred to be retained. we set out to prepare the likely candidate by partial synthe- Hence, pFCC (5) is a 82R,12S,13S,10Z,16n-1-formyl-19-oxo- sis from the methyl ester of Pheo a (6), in order to help test 19,12,13,16-tetrahydrophyllobilene-b.5,8 the suggested intermediacy of such a red bilin-type Chl However, in extracts of senescent leaves of sweet pep- catabolite in higher plants.
Load more

Recommended publications
  • Urobiliverdin, a New Bile Pigment Deriving from Uroporphyrin Eva Benedikt and Hans-Peter Köst Botanisches Institut, Universität München, Menzingerstr
    Urobiliverdin, a New Bile Pigment Deriving from Uroporphyrin Eva Benedikt and Hans-Peter Köst Botanisches Institut, Universität München, Menzingerstr. 67, D-8000 München 19, Bundesrepublik Deutschland Z. Naturforsch. 38 c, 753-757 (1983); received May 4, 1983 Semisynthetic Bile Pigments, Urobiliverdin III, Coprobiliverdin III, Biliverdin IX, Uroporphyrin III 5-Aminolevulinic acid is incubated with a crude enzyme extract from Rhodopseudomonas spheroides, mutant R 26. The formed porphyrins (main product: uroporphyrin III) are isolated. Incorporation of iron, ring-splitting by coupled oxydation and subsequent iron removal leads to a mixture of pigments, from which urobiliverdin, a new bile pigment with eight carboxylic acid side chains, is isolated. It is characterized by its chromatographic behaviour, chromic acid degra­ dation and UV-vis spectroscopy. Introduction the photosynthetic bacteria, Rhodopseudomonas spheroides, mutant R26 was a gift from Prof. Naturally occurring open chained tetrapyrrolic H. Scheer, Munich. Marker porphyrins were pur­ systems (bile pigments) usually bear two carboxylic chased from Porphyrin products (Logan, USA). acid side chains, namely propionic acid side chains. Chromic acid degradation was performed accord­ Examples are phycocyanobilin [1-5], phycoerythro- ing to the procedure developed by Rüdiger [21]; the bilin [5, 6], phytochromobilin [7, 8], the biliar pig­ degradation products were separated on silicagel 60 ment bilirubin ([9], here older literature) and sterco- coated HPTLC plates (E. Merck, Darmstadt, FRG) bilin [9] which is encountered in the faeces. using the solvent system chloroform-ethyl acetate- All of these pigments probably derive from proto­ cyclohexane = 6:3:1. The imides formed were heme as has been shown experimentally in a identified by comparison with authentic standards.
    [Show full text]
  • PDF File Includes: Main Text Figures 1 to 4 Supplemental Text Supplemental Figures S1 to S8 Supplemental Tables
    bioRxiv preprint doi: https://doi.org/10.1101/2020.12.08.414581; this version posted December 9, 2020. The copyright holder for this preprint (which was not certified by peer review) is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under aCC-BY-NC-ND 4.0 International license. Structural basis of the protochromic green/red photocycle of the chromatic acclimation sensor RcaE Takayuki Nagaea, Masashi Unnob, Taiki Koizumic, Yohei Miyanoirid, Tomotsumi Fujisawab, Kento Masuif, Takanari Kamof, Kei Wadae, Toshihiko Ekif, Yutaka ItoC, Yuu Hirosef and Masaki Mishimac aSynchrotron Radiation Research Center, Nagoya University, Chikusa, Nagoya 464-8603, Japan; bDepartment of Chemistry and Applied Chemistry, Faculty of Science and Engineering, Saga University, Saga 840-8502, Japan; cDepartment of Chemistry, Graduate School of Science, Tokyo Metropolitan University, 1-1 Minamiosawa, Hachioji 192-0397, Japan; dInstitute for Protein Research , Osaka University , 3-2 Yamadaoka , Suita , Osaka 565-0871 , Japan; eDepartment of Medical Sciences, University of Miyazaki, Miyazaki 889-1692, Japan; fDepartment of Environmental and Life Sciences, Toyohashi University of Technology, Toyohashi, Aichi 441-8580, Japan 1To whom correspondence should be addressed 1Masaki Mishima Email: [email protected] 1Yuu Hirose Email: [email protected] 1 Masashi Unno Email: [email protected] Takayuki Nagae: 0000-0001-7016-5183 Tomotsumi Fujisawa: 0000-0002-3282-6814 Masashi Unno: 0000-0002-5016-6274 Yohei Miyanoiri: 0000-0001-6889-5160 Yuu Hirose: 0000-0003-1116-8979 Kei Wada: 0000-0001-7631-4151 Yutaka Ito: 0000-0002-1030-4660 Masaki Mishima: 0000-0001-7626-7287 Classification Biological Sciences Keywords cyanobacteriochrome, phytochrome, bilin, NMR, crystallography Author Contributions MM, YH, and MU designed the research and wrote the manuscript.
    [Show full text]
  • Enzymatic Encoding Methods for Efficient Synthesis Of
    (19) TZZ__T (11) EP 1 957 644 B1 (12) EUROPEAN PATENT SPECIFICATION (45) Date of publication and mention (51) Int Cl.: of the grant of the patent: C12N 15/10 (2006.01) C12Q 1/68 (2006.01) 01.12.2010 Bulletin 2010/48 C40B 40/06 (2006.01) C40B 50/06 (2006.01) (21) Application number: 06818144.5 (86) International application number: PCT/DK2006/000685 (22) Date of filing: 01.12.2006 (87) International publication number: WO 2007/062664 (07.06.2007 Gazette 2007/23) (54) ENZYMATIC ENCODING METHODS FOR EFFICIENT SYNTHESIS OF LARGE LIBRARIES ENZYMVERMITTELNDE KODIERUNGSMETHODEN FÜR EINE EFFIZIENTE SYNTHESE VON GROSSEN BIBLIOTHEKEN PROCEDES DE CODAGE ENZYMATIQUE DESTINES A LA SYNTHESE EFFICACE DE BIBLIOTHEQUES IMPORTANTES (84) Designated Contracting States: • GOLDBECH, Anne AT BE BG CH CY CZ DE DK EE ES FI FR GB GR DK-2200 Copenhagen N (DK) HU IE IS IT LI LT LU LV MC NL PL PT RO SE SI • DE LEON, Daen SK TR DK-2300 Copenhagen S (DK) Designated Extension States: • KALDOR, Ditte Kievsmose AL BA HR MK RS DK-2880 Bagsvaerd (DK) • SLØK, Frank Abilgaard (30) Priority: 01.12.2005 DK 200501704 DK-3450 Allerød (DK) 02.12.2005 US 741490 P • HUSEMOEN, Birgitte Nystrup DK-2500 Valby (DK) (43) Date of publication of application: • DOLBERG, Johannes 20.08.2008 Bulletin 2008/34 DK-1674 Copenhagen V (DK) • JENSEN, Kim Birkebæk (73) Proprietor: Nuevolution A/S DK-2610 Rødovre (DK) 2100 Copenhagen 0 (DK) • PETERSEN, Lene DK-2100 Copenhagen Ø (DK) (72) Inventors: • NØRREGAARD-MADSEN, Mads • FRANCH, Thomas DK-3460 Birkerød (DK) DK-3070 Snekkersten (DK) • GODSKESEN,
    [Show full text]
  • An Efficient Synthesis of Porphyrins with Different Meso Substituents That Avoids Scrambling in Aqueous Media
    An Efficient Synthesis of Porphyrins with Different meso Substituents that Avoids Scrambling in Aqueous Media Agnieszka Nowak-Krol, Rémi Plamont, Gabriel Canard, J.A. Edzang, Daniel T. Gryko, Teodor Silviu Balaban To cite this version: Agnieszka Nowak-Krol, Rémi Plamont, Gabriel Canard, J.A. Edzang, Daniel T. Gryko, et al.. An Efficient Synthesis of Porphyrins with Different meso Substituents that Avoids Scrambling inAque- ous Media. Chemistry - A European Journal, Wiley-VCH Verlag, 2015, 21 (4), pp.1488-1498. 10.1002/chem.201403677. hal-01130057 HAL Id: hal-01130057 https://hal.archives-ouvertes.fr/hal-01130057 Submitted on 7 Feb 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. An Efficient Synthesis of Porphyrins with Different Meso Substituents that Avoids Scrambling in Aqueous Media Agnieszka Nowak-Król,a,† Rémi Plamont,b,† Gabriel Canard,b,c Judicaelle Andeme Edzang,b,c Daniel T. Grykoa,* and Teodor Silviu Balabanb,* To the memory of Alan Roy Katritzky, magister of heterocyclic chemistry [a] Institute of Organic Chemistry of the Polish Academy of Sciences, Kasprzaka 44/52, 01-224 Warsaw, Poland E-mail: [email protected] [b] Aix Marseille Université, Centrale Marseille, CNRS, Institut des Sciences Moléculaires de Marseille (iSm2), UMR 7313, Chirosciences, Avenue Escadrille Normandie Niemen, St.
    [Show full text]
  • Retrograde Bilin Signaling Enables Chlamydomonas Greening and Phototrophic Survival
    Retrograde bilin signaling enables Chlamydomonas greening and phototrophic survival Deqiang Duanmua, David Caserob,c, Rachel M. Dentd, Sean Gallahere, Wenqiang Yangf, Nathan C. Rockwella, Shelley S. Martina, Matteo Pellegrinib,c, Krishna K. Niyogid,g,h, Sabeeha S. Merchantb,e, Arthur R. Grossmanf, and J. Clark Lagariasa,1 aDepartment of Molecular and Cellular Biology, University of California, Davis, CA 95616; bInstitute for Genomics and Proteomics, cDepartment of Molecular, Cell and Developmental Biology, and eDepartment of Chemistry and Biochemistry, University of California, Los Angeles, CA 90095; dDepartment of Plant and Microbial Biology, gHoward Hughes Medical Institute, and hPhysical Biosciences Division, Lawrence Berkeley National Laboratory, University of California, Berkeley, CA 94720; and fDepartment of Plant Biology, Carnegie Institution for Science, Stanford, CA 94305 Contributed by J. Clark Lagarias, December 20, 2012 (sent for review October 30, 2012) The maintenance of functional chloroplasts in photosynthetic share similar mechanisms for light sensing and retrograde sig- eukaryotes requires real-time coordination of the nuclear and naling. However, many chlorophyte genomes lack phytochromes plastid genomes. Tetrapyrroles play a significant role in plastid-to- (21–24), a deficiency offset by a larger complement of flavin- and nucleus retrograde signaling in plants to ensure that nuclear gene retinal-based sensors (25–30). expression is attuned to the needs of the chloroplast. Well-known Despite the absence of phytochromes, all known chlorophyte sites of synthesis of chlorophyll for photosynthesis, plant chlor- genomes retain cyanobacterial-derived genes for the two key oplasts also export heme and heme-derived linear tetrapyrroles enzymes required for bilin biosynthesis (Fig. 1A): a heme oxygen- (bilins), two critical metabolites respectively required for essential ase (HMOX1) and a ferredoxin-dependent bilin reductase (PCYA).
    [Show full text]
  • I Topic - Algal Pigments and Algal Classification(ALGAE) Prepared by –Prof.(Dr.)Jainendra Kumar Coordinated By: Prof.(Dr) Shyam Nandan Prasad
    Course- M.Sc. Botany Part -I Paper -I Topic - Algal Pigments and algal Classification(ALGAE) Prepared by –Prof.(Dr.)Jainendra Kumar Coordinated by: Prof.(Dr) Shyam Nandan Prasad The algae were broadly divided by F.F.Fritsch (1935) into eleven classes according to their colour - 1. Chlorophyceae or green algae 2. Xanthophyceae or yellow-green algae 3. Chrysophyceae 4. Bacillariophyceae or golden-brown algae 5. Cryptophyceae 6. Dinophyceae 7. Chloromonadineae 8. Eugleninae 9. Phaeophyceae or brown algae 10. Rhodophyceae or red algae, and 11. Myxophyceae or blue-green algae Normally, classification of algae is based on - 1. Nuclear Organization 2. Nature of Cell Wall Components 3. Pigmentation and Photosynthetic Apparatus The pigment is one of the most important criteria used in differentiation of classes in algae. The pigments in algae can be chlorophylls, carotenoids and biloproteins. These pigments are present in sac like structures called thylakoids. The thylakoids are arranged in stacks in the granum of the chloroplasts. Different groups of algae have different types of pigments and organization of thylakoids in chloroplast. The chlorophylls in algae are chlorophyll a, b, c, d and e types. Chlorophyll a is present in all classes of algae. Chlorophyll b is primary pigment of Chlorophyceae and Euglenineae. Chlorophyll c is found in Phaeophyceae and Cryptophyceae. Chlorophyll d is found in Rhodophyceae. Chlorophyll e is confined to Tribonema of Xanthophyceae. Pigments are chemical compounds which reflect only certain wavelengths of visible light. This makes them appear colourful. More important than their reflection of light is the ability of pigments to absorb certain wavelengths. Since each pigment reacts with only a narrow range of the spectrum, it is important for algae to produce pigments of different colours to capture more of the sun's energy.
    [Show full text]
  • Quantify Chlorophyll a and Chlorophyll B with a Custom Method
    APPLICATION NOTE NanoDrop One/OneC No. T141 Quantify chlorophyll a and chlorophyll b with a custom method Using the NanoDrop One Spectrophotometer Abstract Scientists can accurately quantify chlorophyll a and chlorophyll b on the Thermo Scientific™ NanoDrop™ One/OneC Microvolume UV-Vis Spectrophotometer using a user-defined custom method. Introduction Chlorophyll a is the principal pigment that converts light energy to chemical energy, and chlorophyll b is the accessory photosynthetic pigment that transfers light it absorbs to chlorophyll a. Chlorophyll a is found in all plants, green algae, and cyanobacteria, and chlorophyll b is found in plants and green algae. Chlorophyll quantitation is valuable in a vast array of disciplines including but not limited to plant biology, environmental science, ecotoxicology, disease prevention, and medical drug discovery. Spectrophotometry is a common method used to measure the absorbance of light by the chlorophyll molecules. The NanoDrop One/OneC UV-Vis Spectrophotometer can be used to measure the absorbance of chlorophyll. Chlorophyll a and chlorophyll b absorb light at slightly different wavelengths. peaks (Figure 1). With this information, a user-defined Chlorophyll a absorbs light at 433 nm and 666 nm custom method including user-defined formulas can be and chlorophyll b absorbs light at 462 nm and 650 created to measure the absorbance and determine the nm. The NanoDrop One/OneC UV-Vis application can concentration of chlorophyll. be used to observe the spectrum of each chlorophyll a and chlorophyll b and identify major absorbance chlorophyll a Figure 2. Chlorophyll Content custom method created to quantify chlorophyll a and chlorophyll b samples suspended in 100% DMSO.
    [Show full text]
  • Expanding the Eggshell Colour Gamut: Uroerythrin and Bilirubin from Tinamou (Tinamidae) Eggshells Randy Hamchand1, Daniel Hanley2, Richard O
    www.nature.com/scientificreports OPEN Expanding the eggshell colour gamut: uroerythrin and bilirubin from tinamou (Tinamidae) eggshells Randy Hamchand1, Daniel Hanley2, Richard O. Prum3 & Christian Brückner1* To date, only two pigments have been identifed in avian eggshells: rusty-brown protoporphyrin IX and blue-green biliverdin IXα. Most avian eggshell colours can be produced by a mixture of these two tetrapyrrolic pigments. However, tinamou (Tinamidae) eggshells display colours not easily rationalised by combination of these two pigments alone, suggesting the presence of other pigments. Here, through extraction, derivatization, spectroscopy, chromatography, and mass spectrometry, we identify two novel eggshell pigments: yellow–brown tetrapyrrolic bilirubin from the guacamole- green eggshells of Eudromia elegans, and red–orange tripyrrolic uroerythrin from the purplish-brown eggshells of Nothura maculosa. Both pigments are known porphyrin catabolites and are found in the eggshells in conjunction with biliverdin IXα. A colour mixing model using the new pigments and biliverdin reproduces the respective eggshell colours. These discoveries expand our understanding of how eggshell colour diversity is achieved. We suggest that the ability of these pigments to photo- degrade may have an adaptive value for the tinamous. Birds’ eggs are found in an expansive variety of shapes, sizes, and colourings 1. Te diverse array of appearances found across Aves is achieved—in large part—through a combination of structural features, solid or patterned colorations, the use of two diferent dyes, and diferential pigment deposition. Eggshell pigments are embedded within the white calcium carbonate matrix of the egg and within a thin outer proteinaceous layer called the cuticle2–4. Tese pigments are believed to play a key role in crypsis5,6, although other, possibly dynamic 7,8, roles in inter- and intra-species signalling5,9–12 are also possible.
    [Show full text]
  • Phyllobilins – the Abundant Bilin-Type Tetrapyrrolic Catabolites Of
    Chemical Society Reviews Phyllobilins – the Abundant Bilin -Type Tetrapyrrolic Catabolites of the Green Plant Pigment Chlorophyll Journal: Chemical Society Reviews Manuscript ID: CS-TRV-02-2014-000079.R1 Article Type: Tutorial Review Date Submitted by the Author: 02-May-2014 Complete List of Authors: Krautler, Bernhard; University of Innsbruck, Institute of Organic Chemistry Page 1 of 30 Chemical Society Reviews Phyllobilins-TutRev-BKräutler 2-May-14 1 Phyllobilins – the Abundant Bilin-type Tetrapyrrolic Catabolites of the Green Plant Pigment Chlorophyll Bernhard Kräutler Institute of Organic Chemistry and Centre of Molecular Biosciences, University of Innsbruck, Innrain 80/82, A-6020 Innsbruck, Austria E-mail: [email protected] Abstract . The seasonal disappearance of the green plant pigment chlorophyll in the leaves of deciduous trees has long been a fascinating biological puzzle. In the course of the last two and a half decades, important aspects of the previously enigmatic breakdown of chlorophyll in higher plants were elucidated. Crucial advances in this field were achieved by the discovery and structure elucidation of tetrapyrrolic chlorophyll catabolites, as well as by complementary biochemical and plant biological studies. Phyllobilins, tetrapyrrolic, bilin-type chlorophyll degradation products, are abundant chlorophyll catabolites, which occur in fall leaves and in ripe fruit. This tutorial review outlines ‘how’ chlorophyll is degraded in higher plants, and gives suggestions as to ‘why’ the plants dispose of their valuable green pigments during senescence and ripening. Insights into chlorophyll breakdown help satisfy basic human curiosity and enlighten school teaching. They contribute to fundamental questions in plant biology and may have practical consequences in agriculture and horticulture.
    [Show full text]
  • Characterisation, Classification and Conformational Variability Of
    Characterisation, Classification and Conformational Variability of Organic Enzyme Cofactors Julia D. Fischer European Bioinformatics Institute Clare Hall College University of Cambridge A thesis submitted for the degree of Doctor of Philosophy 11 April 2011 This dissertation is the result of my own work and includes nothing which is the outcome of work done in collaboration except where specifically indicated in the text. This dissertation does not exceed the word limit of 60,000 words. Acknowledgements I would like to thank all the members of the Thornton research group for their constant interest in my work, their continuous willingness to answer my academic questions, and for their company during my time at the EBI. This includes Saumya Kumar, Sergio Martinez Cuesta, Matthias Ziehm, Dr. Daniela Wieser, Dr. Xun Li, Dr. Irene Pa- patheodorou, Dr. Pedro Ballester, Dr. Abdullah Kahraman, Dr. Rafael Najmanovich, Dr. Tjaart de Beer, Dr. Syed Asad Rahman, Dr. Nicholas Furnham, Dr. Roman Laskowski and Dr. Gemma Holli- day. Special thanks to Asad for allowing me to use early development versions of his SMSD software and for help and advice with the KEGG API installation, to Roman for knowing where to find all kinds of data, to Dani for help with R scripts, to Nick for letting me use his E.C. tree program, to Tjaart for python advice and especially to Gemma for her constant advice and feedback on my work in all aspects, in particular the chemistry side. Most importantly, I would like to thank Prof. Janet Thornton for giving me the chance to work on this project, for all the time she spent in meetings with me and reading my work, for sharing her seemingly limitless knowledge and enthusiasm about the fascinating world of enzymes, and for being such an experienced and motivational advisor.
    [Show full text]
  • ABSTRACT ZHANG, SHAOFEI. Synthesis Of
    ABSTRACT ZHANG, SHAOFEI. Synthesis of Bacteriochlorins and the Full Skeleton of Bacteriochlorophylls. (Under the direction of Professor Jonathan S. Lindsey.) Bacteriochlorins, the core macrocycle ring of natural bacteriochlorophylls, are characterized by their ability to absorb near infrared light (700 – 900 nm), which makes them attractive candidates in variety of photophysical studies and applications. The previously established de novo synthesis, which relies on the acid-catalyzed self-condensation of dihydrodipyrrin–acetal, provides access towards diverse bacteriochlorins, but has its limitations. This dissertation describes the development of new strategies for bacteriochlorin synthesis. Firstly, a route towards previously unknown tetra-alkyl bacteriochlorins (e.g., alkyl = Me, or –CH2CO2Me) is established (Ch. 2). Secondly, explorations of synthetic approaches to unsymmetrically substituted bacteriochlorins through electrocyclic reactions of linear tetrapyrrole intermediates are described. Four new unsymmetrically substituted bacteriochlorins and one new tetradehydrocorrin were produced, albeit in low yields (Ch. 3). Thirdly, a new method to construct bacteriochlorin macrocycle with concomitant Nazarov cyclization to form the annulated isocyclic ring, is established. Five new bacteriochlorins, which are closely anlogues of bacteriochlorophyll a, bearing various substituents (alkyl/alkyl, aryl, and alkyl/ester) at positions 2 and 3 and 132 carboalkoxy groups (R = Me or Et) were constructed in 37−61% yield from the bilin analogues
    [Show full text]
  • Phycoerythrin-Specific Bilin Lyase–Isomerase Controls Blue-Green
    Phycoerythrin-specific bilin lyase–isomerase controls blue-green chromatic acclimation in marine Synechococcus Animesh Shuklaa, Avijit Biswasb, Nicolas Blotc,d,e, Frédéric Partenskyc,d, Jonathan A. Kartyf, Loubna A. Hammadf, Laurence Garczarekc,d, Andrian Gutua,g, Wendy M. Schluchterb, and David M. Kehoea,h,1 aDepartment of Biology, Indiana University, Bloomington, IN 47405; bDepartment of Biological Sciences, University of New Orleans, New Orleans, LA 70148; cUPMC-Université Paris 06, Station Biologique, 29680 Roscoff, France; dCentre National de la Recherche Scientifique, Unité Mixte de Recherche 7144 Adaptation et Diversité en Milieu Marin, Groupe Plancton Océanique, 29680 Roscoff, France; eClermont Université, Université Blaise Pascal, Unité Mixte de Recherche Centre National de la Recherche Scientifique 6023, Laboratoire Microorganismes: Génome et Environnement, 63000 Clermont-Ferrand, France; fMETACyt Biochemical Analysis Center, Department of Chemistry, Indiana University, Bloomington, IN 47405; gDepartment of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02138; and hIndiana Molecular Biology Institute, Indiana University, Bloomington, IN 47405 Edited by Alexander Namiot Glazer, University of California, Berkeley, CA, and approved October 4, 2012 (received for review July 10, 2012) The marine cyanobacterium Synechococcus is the second most Marine Synechococcus are divided into three major pigment abundant phytoplanktonic organism in the world’s oceans. The types, with type 1 PBS rods containing only PC, type 2 containing ubiquity of this genus is in large part due to its use of a diverse PC and PEI, and type 3 containing PC, PEI, and PEII (4). Type 3 set of photosynthetic light-harvesting pigments called phycobilipro- can be further split into four subtypes (3 A–D)onthebasisofthe teins, which allow it to efficiently exploit a wide range of light ratio of the PUB and PEB chromophores bound to PEs.
    [Show full text]