Post-secretory synthesis of a natural analog of iron-gall ink in the black nectar of Melianthus spp.
ellagic acid
gallic acid
iron
iron-gall ink
nectar
nectaries
nectary
pollinator
Journal
The New phytologist
ISSN: 1469-8137
Titre abrégé: New Phytol
Pays: England
ID NLM: 9882884
Informations de publication
Date de publication:
09 2023
09 2023
Historique:
received:
16
12
2022
accepted:
20
02
2023
medline:
3
8
2023
pubmed:
8
3
2023
entrez:
7
3
2023
Statut:
ppublish
Résumé
The black nectar produced by Melianthus flowers is thought to serve as a visual attractant to bird pollinators, but the chemical identity and synthesis of the black pigment are unknown. A combination of analytical biochemistry, transcriptomics, proteomics, and enzyme assays was used to identify the pigment that gives Melianthus nectar its black color and how it is synthesized. Visual modeling of pollinators was also used to infer a potential function of the black coloration. High concentrations of ellagic acid and iron give the nectar its dark black color, which can be recapitulated through synthetic solutions containing only ellagic acid and iron(iii). The nectar also contains a peroxidase that oxidizes gallic acid to form ellagic acid. In vitro reactions containing the nectar peroxidase, gallic acid, hydrogen peroxide, and iron(iii) fully recreate the black color of the nectar. Visual modeling indicates that the black color is highly conspicuous to avian pollinators within the context of the flower. Melianthus nectar contains a natural analog of iron-gall ink, which humans have used since at least medieval times. This pigment is derived from an ellagic acid-Fe complex synthesized in the nectar and is likely involved in the attraction of passerine pollinators endemic to southern Africa.
Substances chimiques
Plant Nectar
0
Ellagic Acid
19YRN3ZS9P
Ferric Compounds
0
Peroxidases
EC 1.11.1.-
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
2026-2040Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2023 The Authors. New Phytologist © 2023 New Phytologist Foundation.
Références
Baum SF, Eshed Y, Bowman JL. 2001. The Arabidopsis nectary is an ABC-independent floral structure. Development 128: 4657-4667.
Bender R, Klinkenberg P, Jiang Z, Bauer B, Karypis G, Nguyen N, Perera MADN, Nikolau BJ, Carter CJ. 2012. Functional genomics of nectar production in the Brassicaceae. Flora 207: 491-496.
Bender RL, Fekete ML, Klinkenberg PM, Hampton M, Bauer B, Malecha M, Lindgren K, AM J, Perera MA, Nikolau BJ et al. 2013. PIN6 is required for nectary auxin response and short stamen development. The Plant Journal 74: 893-904.
Bolten AB, Feinsinger P, Baker HG, Baker I. 1979. On the calculation of sugar concentration in flower nectar. Oecologia 41: 301-304.
Bouwmeester H, Schuurink RC, Bleeker PM, Schiestl F. 2019. The role of volatiles in plant communication. The Plant Journal 100: 892-907.
Bowman JL, Smyth DR. 1999. CRABS CLAW, a gene that regulates carpel and nectary development in Arabidopsis, encodes a novel protein with zinc finger and helix-loop-helix domains. Development 126: 2387-2396.
Bray NL, Pimentel H, Melsted P, Pachter L. 2016. Near-optimal probabilistic RNA-seq quantification. Nature Biotechnology 34: 525-527.
Carter C, Shafir S, Yehonatan L, Palmer RG, Thornburg R. 2006. A novel role for proline in plant floral nectars. Naturwissenschaften 93: 72-79.
Carter C, Thornburg RW. 2000. Tobacco nectarin I. Purification and characterization as a germin-like, manganese superoxide dismutase implicated in the defense of floral reproductive tissues. Journal of Biological Chemistry 275: 36726-36733.
Carter C, Thornburg RW. 2004. Is the nectar redox cycle a floral defense against microbial attack? Trends in Plant Science 9: 320-324.
Carter CJ, Thornburg RW. 2004. Tobacco nectarin V is a flavin-containing berberine bridge enzyme-like protein with glucose oxidase activity. Plant Physiology 134: 460-469.
Celedon JM, Bohlmann J. 2019. Oleoresin defenses in conifers: chemical diversity, terpene synthases and limitations of oleoresin defense under climate change. New Phytologist 224: 1444-1463.
Davies KM, Landi M, van Klink JW, Schwinn KE, Brummell DA, Albert NW, Chagne D, Jibran R, Kulshrestha S, Zhou Y et al. 2022. Evolution and function of red pigmentation in land plants. Annals of Botany 130: 613-636.
Decraene LPR, Linder HP, Dlamini T, Smets EF. 2001. Evolution and development of floral diversity of Melianthaceae, an enigmatic southern African family. International Journal of Plant Sciences 162: 59-82.
Defossez E, Pitteloud C, Descombes P, Glauser G, Allard PM, Walker TWN, Fernandez-Conradi P, Wolfender JL, Pellissier L, Rasmann S. 2021. Spatial and evolutionary predictability of phytochemical diversity. Proceedings of the National Academy of Sciences, USA 118: e2013344118.
Eloff JN, Angeh IE, McGaw LJ. 2017. Solvent-solvent fractionation can increase the antifungal activity of a Melianthus comosus (Melianthaceae) acetone leaf extract to yield a potentially useful commercial antifungal product. Industrial Crops and Products 110: 103-112.
Fairnie ALM, Yeo MTS, Gatti S, Chan E, Travaglia V, Walker JF, Moyroud E. 2022. Eco-evo-devo of petal pigmentation patterning. Essays in Biochemistry 66: 753-768.
Gonzalez-Teuber M, Eilmus S, Muck A, Svatos A, Heil M. 2009. Pathogenesis-related proteins protect extrafloral nectar from microbial infestation. The Plant Journal 58: 464-473.
Gonzalez-Teuber M, Pozo MJ, Muck A, Svatos A, Adame-Alvarez RM, Heil M. 2010. Glucanases and chitinases as causal agents in the protection of acacia extrafloral nectar from infestation by phytopathogens. Plant Physiology 152: 1705-1715.
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q et al. 2011. Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nature Biotechnology 29: 644-652.
Grundhofer P, Niemetz R, Schilling G, Gross GG. 2001. Biosynthesis and subcellular distribution of hydrolyzable tannins. Phytochemistry 57: 915-927.
Hansen DM, Olesen JM, Mione T, Johnson SD, Muller CB. 2007. Coloured nectar: distribution, ecology, and evolution of an enigmatic floral trait. Biological Reviews of the Cambridge Philosophical Society 82: 83-111.
Heinrich B, Raven PH. 1972. Energetics and pollination ecology. Science 176: 597-602.
Henning J. 2003. Further studies with Melianthus L.: a molecular phylogeny, evolutionary patterns of diversification in the genus and pollinator syndromes. Cape Town, South Africa: University of Cape Town.
Johnson SD, Hargreaves AL, Brown M. 2006. Dark, bitter-tasting nectar functions as a filter of flower visitors in a bird-pollinated plant. Ecology 87: 2709-2716.
Kamel MY, Saleh NA, Ghazy AM. 1977. Gallic acid oxidation by turnip peroxidase. Phytochemistry 16: 521-524.
Knudsen C, Gallage NJ, Hansen CC, Moller BL, Laursen T. 2018. Dynamic metabolic solutions to the sessile life style of plants. Natural Products Reports 35: 1140-1155.
Kobayashi T, Nozoye T, Nishizawa NK. 2019. Iron transport and its regulation in plants. Free Radical Biology and Medicine 133: 11-20.
Kram BW, Carter CJ. 2009. Arabidopsis thaliana as a model for functional nectary analysis. Sexual Plant Reproduction 22: 235-246.
Kurilla A, Toth T, Dorgai L, Darula Z, Lakatos T, Silhavy D, Kerenyi Z, Dallmann G. 2019. Nectar- and stigma exudate-specific expression of an acidic chitinase could partially protect certain apple cultivars against fire blight disease. Planta 251: 20.
Lautie E, Russo O, Ducrot P, Boutin JA. 2020. Unraveling plant natural chemical diversity for drug discovery purposes. Frontiers in Pharmacology 11: 397.
Lee H, Kim WI, Youn W, Park T, Lee S, Kim TS, Mano JF, Choi IS. 2018. Iron gall ink revisited: in situ oxidation of Fe(II)-tannin complex for fluidic-interface engineering. Advanced Materials 30: e1805091.
Lee JY, Baum SF, Alvarez J, Patel A, Chitwood DH, Bowman JL. 2005a. Activation of CRABS CLAW in the nectaries and carpels of Arabidopsis. Plant Cell 17: 25-36.
Lee JY, Baum SF, Oh SH, Jiang CZ, Chen JC, Bowman JL. 2005b. Recruitment of CRABS CLAW to promote nectary development within the eudicot clade. Development 132: 5021-5032.
Lin IW, Sosso D, Chen LQ, Gase K, Kim SG, Kessler D, Klinkenberg PM, Gorder MK, Hou BH, Qu XQ et al. 2014. Nectar secretion requires sucrose phosphate synthases and the sugar transporter SWEET9. Nature 508: 546-549.
Linder HP, Dlamini T, Henning J, Verboom GA. 2006. The evolutionary history of Melianthus (Melianthaceae). American Journal of Botany 93: 1052-1064.
Love MI, Huber W, Anders S. 2014. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biology 15: 550.
Luo SH, Liu Y, Hua J, Niu XM, Jing SX, Zhao X, Schneider B, Gershenzon J, Li SH. 2012. Unique proline-benzoquinone pigment from the colored nectar of “Bird's Coca Cola Tree” functions in bird attractions. Organic Letters 14: 4146-4149.
Melo MJ, Otero V, Nabais P, Teixeira N, Pina F, Casanova C, Fragoso S, Sequeira SO. 2022. Iron-gall inks: a review of their degradation mechanisms and conservation treatments. Heritage Science 10: 145.
Minami A, Kang X, Carter CJ. 2021. A cell wall invertase controls nectar volume and sugar composition. The Plant Journal 107: 1016-1028.
Nicolson SW. 2007. Amino acid concentrations in the nectars of Southern African bird-pollinated flowers, especially Aloe and Erythrina. Journal of Chemical Ecology 33: 1707-1720.
Pauw A, Stanway R. 2015. Unrivalled specialization in a pollination network from South Africa reveals that specialization increases with latitude only in the Southern Hemisphere. Journal of Biogeography 42: 652-661.
Perez-Riverol Y, Bai JW, Bandla C, Garcia-Seisdedos D, Hewapathirana S, Kamatchinathan S, Kundu DJ, Prakash A, Frericks-Zipper A, Eisenacher M et al. 2022. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Research 50: D543-D552.
Riemer J, Hoepken HH, Czerwinska H, Robinson SR, Dringen R. 2004. Colorimetric ferrozine-based assay for the quantitation of iron in cultured cells. Analytical Biochemistry 331: 370-375.
Rodriguez-Concepcion M, Daros JA. 2022. Transient expression systems to rewire plant carotenoid metabolism. Current Opinion in Plant Biology 66: 102190.
Roy R, Moreno N, Brockman SA, Kostanecki A, Zambre A, Holl C, Solhaug EM, Minami A, Snell-Rood EC, Hampton M et al. 2022. Convergent evolution of a blood-red nectar pigment in vertebrate-pollinated flowers. Proceedings of the National Academy of Sciences, USA 119: e2114420119.
Roy R, Schmitt AJ, Thomas JB, Carter CJ. 2017. Review: nectar biology: from molecules to ecosystems. Plant Science 262: 148-164.
Schmitt AJ, Sathoff AE, Holl C, Bauer B, Samac DA, Carter CJ. 2018. The major nectar protein of Brassica rapa is a non-specific lipid transfer protein, BrLTP2.1, with strong antifungal activity. Journal of Experimental Botany 69: 5587-5597.
Scott-Elliot GF, Cantab MA. 1890. Ornithophilous fowers in South Africa. Annals of Botany 4: 265-280.
Shigeto J, Tsutsumi Y. 2016. Diverse functions and reactions of class III peroxidases. New Phytologist 209: 1395-1402.
Solhaug EM, Johnson E, Carter CJ. 2019a. Carbohydrate metabolism and signaling in squash nectaries and nectar throughout floral maturation. Plant Physiology 180: 1930-1946.
Solhaug EM, Roy R, Chatt EC, Klinkenberg PM, Mohd-Fadzil NA, Hampton M, Nikolau BJ, Carter CJ. 2019b. An integrated transcriptomics and metabolomics analysis of the Cucurbita pepo nectary implicates key modules of primary metabolism involved in nectar synthesis and secretion. Plant Direct 3: e00120.
Teufel F, Almagro Armenteros JJ, Johansen AR, Gislason MH, Pihl SI, Tsirigos KD, Winther O, Brunak S, von Heijne G, Nielsen H. 2022. SignalP 6.0 predicts all five types of signal peptides using protein language models. Nature Biotechnology 40: 1023-1025.
Teulier L, Weber JM, Crevier J, Darveau CA. 2016. Proline as a fuel for insect flight: enhancing carbohydrate oxidation in hymenopterans. Proceedings of the Royal Society B: Biological Sciences 283: 20160333.
Verdcourt B. 1956. Notes on the genus Bersama in Africa. Kew Bulletin 1950: 233-244.
Wagh SA. 2010. Bioconversion of tannic acid to gallic acid by using fungal tannase. Pune, India: University of Pune.
Wagner WL, Weller SG, Sakai AK. 2005. Monograph of Schiedea (Caryophyllaceae - Alsinoideae). Systematic Botany Monographs 72: 1-169.
Wailes RB. 1935. Things to make in your home laboratory. Popular Science Monthly 126: 54-55.
Wiesen LB, Bender RL, Paradis T, Larson A, Perera MADN, Nikolau BJ, Olszewski NE, Carter CJ. 2016. A role for GIBBERELLIN 2-OXIDASE6 and gibberellins in regulating nectar production. Molecular Plant 9: 753-756.
Wilkesman J, Castro D, Contreras LM, Kurz L. 2014. Guaiacol peroxidase zymography for the undergraduate laboratory. Biochemistry and Molecular Biology Education 42: 420-426.
Ye S, Yin D, Sun X, Chen Q, Min T, Wang H, Wang L. 2022. Molecular cloning, expression, and functional analysis of glycosyltransferase (TbUGGT) gene from Trapa bispinosa Roxb. Molecules 27: 8374.