Elusive partners: a review of the auxiliary proteins guiding metabolic flux in flavonoid biosynthesis.


Journal

The Plant journal : for cell and molecular biology
ISSN: 1365-313X
Titre abrégé: Plant J
Pays: England
ID NLM: 9207397

Informations de publication

Date de publication:
10 2021
Historique:
revised: 20 07 2021
received: 01 04 2021
accepted: 22 07 2021
pubmed: 29 7 2021
medline: 27 1 2022
entrez: 28 7 2021
Statut: ppublish

Résumé

Flavonoids are specialized metabolites widely distributed across the plant kingdom. They are involved in the growth and survival of plants, conferring the ability to filter ultra-violet rays, conduct symbiotic partnerships, and respond to stress. While many branches of flavonoid biosynthesis have been resolved, recent discoveries suggest missing auxiliary components. These overlooked elements can guide metabolic flux, enhance production, mediate stereoselectivity, transport intermediates, and exert regulatory functions. This review describes several families of auxiliary proteins from across the plant kingdom, including examples from specialized metabolism. In flavonoid biosynthesis, we discuss the example of chalcone isomerase-like (CHIL) proteins and their non-catalytic role. CHILs mediate the cyclization of tetraketides, forming the chalcone scaffold by interacting with chalcone synthase (CHS). Loss of CHIL activity leads to derailment of the CHS-catalyzed reaction and a loss of pigmentation in fruits and flowers. Similarly, members of the pathogenesis-related 10 (PR10) protein family have been found to differentially bind flavonoid intermediates, guiding the composition of anthocyanins. This role comes within a larger body of PR10 involvement in specialized metabolism, from outright catalysis (e.g., (S)-norcoclaurine synthesis) to controlling stereochemistry (e.g., enhancing cis-trans cyclization in catnip). Both CHILs and PR10s hail from larger families of ligand-binding proteins with a spectrum of activity, complicating the characterization of their enigmatic roles. Strategies for the discovery of auxiliary proteins are discussed, as well as mechanistic models for their function. Targeting such unanticipated components will be crucial in manipulating plants or engineering microbial systems for natural product synthesis.

Identifiants

pubmed: 34318549
doi: 10.1111/tpj.15446
doi:

Substances chimiques

Cannabinoids 0
Flavonoids 0
Plant Proteins 0
Acyltransferases EC 2.3.-
flavanone synthetase EC 2.3.1.74
Intramolecular Lyases EC 5.5.-
chalcone isomerase EC 5.5.1.6

Types de publication

Journal Article Research Support, Non-U.S. Gov't Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

314-329

Informations de copyright

© 2021 Society for Experimental Biology and John Wiley & Sons Ltd.

Références

Akiyama, T., Shibuya, M., Liu, H.-M. & Ebizuka, Y. (2001) p-Coumaroyltriacetic acid synthase, a new homologue of chalcone synthase, from Hydrangea macrophylla var. thunbergii. European Journal of Biochemistry, 263(3), 834-839. https://doi.org/10.1046/j.1432-1327.1999.00562.x.
Alpy, F. & Tomasetto, C. (2005) Give lipids a START: the StAR-related lipid transfer (START) domain in mammals. Journal of Cell Science, 118, 2791-2801. https://doi.org/10.1242/jcs.02485.
Ames, B.D., Korman, T.P., Zhang, W., Smith, P., Vu, T., Tang, Y. et al. (2008) Crystal structure and functional analysis of tetracenomycin ARO/CYC: implications for cyclization specificity of aromatic polyketides. Proceedings of the National Academy of Sciences, 105(14), 5349-5354. https://doi.org/10.1073/pnas.0709223105.
Archambault, A. & Strömvik, M.V. (2011) PR-10, defensin and cold dehydrin genes are among those over expressed in Oxytropis (Fabaceae) species adapted to the arctic. Functional & Integrative Genomics, 11, 497-505. https://doi.org/10.1007/s10142-011-0223-6.
Bais, H.P., Vepachedu, R., Lawrence, C.B., Stermitz, F.R. & Vivanco, J.M. (2003) Molecular and biochemical characterization of an enzyme responsible for the formation of hypericin in St. John's wort (Hypericum perforatum L.). Journal of Biological Chemistry, 278(34), 32413-32422. https://doi.org/10.1074/jbc.M301681200.
Ban, Z., Qin, H., Mitchell, A.J., Liu, B., Zhang, F., Weng, J.-K. et al. (2018) Noncatalytic chalcone isomerase-fold proteins in Humulus lupulus are auxiliary components in prenylated flavonoid biosynthesis. Proceedings of the National Academy of Sciences, 115(22), E5223-E5232. https://doi.org/10.1073/pnas.1802223115.
Bednar, R.A. & Hadcock, J.R. (1988) Purification and characterization of chalcone isomerase from soybeans. Journal of Biological Chemistry, 263, 9582-9588. https://doi.org/10.1016/S0021-9258(19)81556-9.
Biesiadka, J., Bujacz, G., Sikorski, M.M. & Jaskolski, M. (2002) Crystal structures of two homologous pathogenesis-related proteins from yellow lupine. Journal of Molecular Biology, 319, 1223-1234. https://doi.org/10.1016/S0022-2836(02)00385-6.
Blatt-Janmaat, K. & Qu, Y. (2021) The biochemistry of phytocannabinoids and metabolic engineering of their production in heterologous systems. International Journal of Molecular Sciences, 22(5), 2454. https://doi.org/10.3390/ijms22052454.
Breiteneder, H., Pettenburger, K., Bito, A., Valenta, R., Kraft, D., Rumpold, H. et al. (1989) The gene coding for the major birch pollen allergen Betv1, is highly homologous to a pea disease resistance response gene. The EMBO Journal, 8, 1935-1938. https://doi.org/10.1002/j.1460-2075.1989.tb03597.x.
Burbulis, I.E. & Winkel-Shirley, B. (1999) Interactions among enzymes of the Arabidopsis flavonoid biosynthetic pathway. Proceedings of the National Academy of Sciences of the United States of America, 96(2), 12929-12934. https://doi.org/10.1073/pnas.96.22.12929.
Burke, J.R., La Clair, J.J., Philippe, R.N., Pabis, A., Corbella, M., Jez, J.M. et al. (2019) Bifunctional substrate activation via an arginine residue drives catalysis in chalcone isomerases. ACS Catalysis, 9(9), 8388-8396. https://doi.org/10.1021/acscatal.9b01926.
Calderon, M.A., Demoly, P., Gerth Van Wijk, R., Bousquet, J., Sheikh, A. Frew, A. et al. (2012) EAACI: a European declaration on immunotherapy. Designing the future of allergen specific immunotherapy. Clinical and Translational Allergy, 2(1), 20. https://doi.org/10.1186/2045-7022-2-20.
Casañal, A., Zander, U., Muñoz, C., Dupeux, F., Luque, I., Botella, M.A. et al. (2013) The strawberry pathogenesis-related 10 (PR-10) Fra a proteins control flavonoid biosynthesis by binding to metabolic intermediates. Journal of Biological Chemistry, 288, 35322-35332. https://doi.org/10.1074/jbc.M113.501528. Accessed January 25, 2021.
Chadha, P. & Das, R.H. (2006) A pathogenesis related protein, AhPR10 from peanut: an insight of its mode of antifungal activity. Planta, 225, 213-222. https://doi.org/10.1007/s00425-006-0344-7.
Chen, L., Zhang, S., Illa, E., Song, L., Wu, S., Howad, W. et al. (2008) Genomic characterization of putative allergen genes in peach/almond and their synteny with apple. BMC Genomics, 9(1), 543.
Chen, X., Hagel, J.M., Chang, L., Tucker, J.E., Shiigi, S.A., Yelpaala, Y. et al. (2018) A pathogenesis-related 10 protein catalyzes the final step in thebaine biosynthesis. Nature Chemical Biology, 14, 738-743.
Cheng, A.-X., Zhang, X., Han, X.-J., Zhang, Y.-Y., Gao, S., Liu, C.-J. et al. (2018) Identification of chalcone isomerase in the basal land plants reveals an ancient evolution of enzymatic cyclization activity for synthesis of flavonoids. New Phytologist, 217, 909-924. https://doi.org/10.1111/nph.14852.
Chwastyk, M., Jaskolski, M. & Cieplak, M. (2014) Structure-based analysis of thermodynamic and mechanical properties of cavity-containing proteins-case study of plant pathogenesis-related proteins of class 10. FEBS Journal, 281, 416-429.
Clark, B.J., Wells, J., King, S.R. & Stocco, D.M. (1994) The purification, cloning, and expression of a novel luteinizing hormone- induced mitochondrial protein in MA-10 mouse Leydig tumor cells. Characterization of the Steroidogenic Acute Regulatory protein (StAR). Journal of Biological Chemistry, 269, 28314-28322.
Colgate, E.C., Miranda, C.L., Stevens, J.F., Bray, T.M. & Ho, E. (2007) Xanthohumol, a prenylflavonoid derived from hops induces apoptosis and inhibits NF-kappaB activation in prostate epithelial cells. Cancer Letters, 246, 201-209.
Commichau, F.M., Herzberg, C., Tripal, P., Valerius, O. & Stülke, J. (2007) A regulatory protein-protein interaction governs glutamate biosynthesis in Bacillus subtilis: the glutamate dehydrogenase RocG moonlights in controlling the transcription factor GltC. Molecular Microbiology, 65, 642-654. Available at: https://pubmed.ncbi.nlm.nih.gov/17608797/. Accessed March 28, 2021.
Cornilescu, G., Cornilescu, C.C., Zhao, Q., Frederick, R.O., Peterson, F.C., Thao, S. et al. (2004) Letter to the editor: solution structure of a homodimeric hypothetical protein, At5g22580, a structural genomics target from Arabidopsis thaliana. Journal of Biomolecular NMR, 29, 387-390. Available at: https://link.springer.com/article/ https://doi.org/10.1023/B:JNMR.0000032525.70677.16. Accessed March 10, 2021.
Dastmalchi, M., Bernards, M.A. & Dhaubhadel, S. (2016) Twin anchors of the soybean isoflavonoid metabolon: evidence for tethering of the complex to the endoplasmic reticulum by IFS and C4H. The Plant Journal, 85, 689-706. https://doi.org/10.1111/tpj.13137.
Dastmalchi, M., Chen, X., Hagel, J.M., Chang, L., Chen, R., Ramasamy, S. et al. (2019) Neopinone isomerase is involved in codeine and morphine biosynthesis in opium poppy. Nature Chemical Biology, 15, 384-390. Available at: https://www.nature.com/articles/s41589-019-0247-0. Accessed March 19, 2019.
Davies, K.M., Jibran, R., Zhou, Y., Albert, N.W., Brummell, D.A., Jordan, B.R. et al. (2020) The evolution of flavonoid biosynthesis: a bryophyte perspective. Frontiers in Plant Science, 11, 1.
Debeaujon, I., Peeters, A.J.M., Léon-Kloosterziel, K.M. & Koornneef, M. (2001) The transparent testa12 gene of Arabidopsis encodes a multidrug secondary transporter-like protein required for flavonoid sequestration in vacuoles of the seed coat endothelium. The Plant Cell, 13, 853-871.
Diller, R.A., Riepl, H.M., Rose, O., Frias, C., Henze, G. & Prokop, A. (2005) Synthesis of demethylxanthohumol, a new potent apoptosis-inducing agent from hops. Chemistry & Biodiversity, 2, 1331-1337. Available at: https://pubmed.ncbi.nlm.nih.gov/17191934/. Accessed February 4, 2021.
Feng, J., Zhang, M., Yang, K.N. & Zheng, C.X. (2020) Salicylic acid-primed defence response in octoploid strawberry ‘Benihoppe’ leaves induces resistance against Podosphaera aphanis through enhanced accumulation of proanthocyanidins and upregulation of pathogenesis-related genes. BMC Plant Biology, 20, 149.
Fernandes, H., Bujacz, A., Bujacz, G., Jelen, F., Jasinski, M., Kachlicki, P. et al. (2009) Cytokinin-induced structural adaptability of a Lupinus luteus PR-10 protein. FEBS Journal, 276, 1596-1609.
Fernandes, H., Michalska, K., Sikorski, M. & Jaskolski, M. (2013) Structural and functional aspects of PR-10 proteins. FEBS Journal, 280(5), 1169-1199. https://doi.org/10.1111/febs.12114.
Fujino, N., Tenma, N., Waki, T., Ito, K., Komatsuzaki, Y., Sugiyama, K. et al. (2018) Physical interactions among flavonoid enzymes in snapdragon and torenia reveal the diversity in the flavonoid metabolon organization of different plant species. The Plant Journal, 94, 372-392.
Gagne, S.J., Stout, J.M., Liu, E., Boubakir, Z., Clark, S.M. & Page, J.E. (2012) Identification of olivetolic acid cyclase from Cannabis sativa reveals a unique catalytic route to plant polyketides. Proceedings of the National Academy of Sciences, 109(31), 12811-12816. https://doi.org/10.1073/pnas.1200330109.
Galanie, S., Thodey, K., Trenchard, I.J., Interrante, M.F. & Smolke, C.D. (2015) Complete biosynthesis of opioids in yeast. Science, 349, 1095-1100.
Gao, Z.S., van de Weg, W.E., Schaart, J.G., Schouten, H.J., Tran, D.H., Kodde, L.P. et al. (2005) Genomic cloning and linkage mapping of the Mal d 1 (PR-10) gene family in apple (Malus domestica). Theoretical and Applied Genetics, 111, 171-183.
Gianinazzi, S., Martin, C. & Vallée, J.C. (1970) Hypersensitivity to viruses, temperature and soluble proteins in Nicotiana xanthi n.c. Appearance of new macromolecules at the repression of viral synthesis. Comptes Rendus Hebdomadaires des séances de l'Académie des Sciences. Série D: Sciences Naturelles, 270, 2383-2386.
Goiris, K., Muylaert, K., Voorspoels, S., Noten, B., Paepe, D.D., Baart, E. et al. (2014) Detection of flavonoids in microalgae from different evolutionary lineages. Journal of Phycology, 50, 483-492 Available at: https://pubmed.ncbi.nlm.nih.gov/26988321/. Accessed March 30, 2021.
Gollwitzer, J., Lenz, R., Hampp, N. & Zenk, M.H. (1993) The transformation of neopinone to codeinone in morphine biosynthesis proceeds non-enzymatically. Tetrahedron Letters, 34, 5703-5706.
Gu, R., Fonseca, S., Puskas, L.G., Hackler, L., Zvara, A., Dudits, D. et al. (2004) Transcript identification and profiling during salt stress and recovery of Populus euphratica. Tree Physiology, 24, 265-276. https://doi.org/10.1093/treephys/24.3.265.
Gülck, T., Booth, J.K., Carvalho, A., Khakimov, B., Crocoll, C., Motawia, M.S. et al. (2020) Synthetic Biology of Cannabinoids and Cannabinoid Glucosides in Nicotiana benthamiana and Saccharomyces cerevisiae. Journal of Natural Products, 83, 2877-2893. https://doi.org/10.1021/acs.jnatprod.0c00241.
Gülck, T. & Møller, B.L. (2020) Phytocannabinoids: origins and biosynthesis. Trends in Plant Science, 25(10), 985-1004. https://doi.org/10.1016/j.tplants.2020.05.005.
Hauser, T., Popilka, L., Hartl, F.U. & Hayer-Hartl, M. (2015) Role of auxiliary proteins in Rubisco biogenesis and function. Nature Plants, 1(6), 1-11. Available at: www.nature.com/natureplants. Accessed March 18, 2021.
Hjernø, K., Alm, R., Canbäck, B., Matthiesen, R., Trajkovski, K., Björk, L. et al. (2006) Down-regulation of the strawberry Bet v 1-homologous allergen in concert with the flavonoid biosynthesis pathway in colorless strawberry mutant. Proteomics, 6, 1574-1587. Available at: https://pubmed.ncbi.nlm.nih.gov/16447153/. Accessed December 20, 2018.
Ishibashi, M., Nabe, T., Nitta, Y., Tsuruta, H., Iduhara, M. & Uno, Y. (2018) Analysis of major paralogs encoding the Fra a 1 allergen based on their organ-specificity in Fragaria × ananassa. Plant Cell Reports, 37, 411-424 Available at: http://www.ncbi.nlm.nih.gov/pubmed/29177844. Accessed May 5, 2020.
Jain, D., Khandal, H., Khurana, J.P. & Chattopadhyay, D. (2016) A pathogenesis related-10 protein CaARP functions as aldo/keto reductase to scavenge cytotoxic aldehydes. Plant Molecular Biology, 90, 171-187.
Jang, M., Cai, L., Udeani, G.O., Slowing, K.V., Thomas, C.F., Beecher, C.W. et al. (1997) Cancer chemopreventive activity of resveratrol, a natural product derived from grapes. Science, 275, 218-220.
Jez, J.M., Bowman, M.E., Dixon, R.A. & Noel, J.P. (2000) Structure and mechanism of the evolutionarily unique plant enzyme chalcone isomerase. Natural Structural Biology, 7, 786-791.
Jiang, W., Yin, Q., Wu, R., Zheng, G., Liu, J., Dixon, R.A. et al. (2015) Role of a chalcone isomerase-like protein in flavonoid biosynthesis in Arabidopsis thaliana. Journal of Experimental Botany, 66, 7165-7179. Available at: http://www.affymetrix.com/. Accessed March 26, 2020.
Ka, S., Koirala, M., Mérindol, N. & Desgagné-Penix, I. (2020) Biosynthesis and biological activities of newly discovered amaryllidaceae alkaloids. Molecules, 25, 4901. Available at: https://pubmed.ncbi.nlm.nih.gov/33113950/. Accessed March 23, 2021.
Kaltenbach, M., Burke, J.R., Dindo, M., Pabis, A., Munsberg, F.S., Rabin, A. et al. (2018) Evolution of chalcone isomerase from a noncatalytic ancestor. Nature Chemical Biology, 14, 548-555.
Karlsson, A.L., Aim, R., Ekstrand, B., Fjelkner-Modig, S., Schiött, A., Bengtsson, U. et al. (2004) Bet v 1 homologues in strawberry identified as IgE-binding proteins and presumptive allergens. Allergy, 59(12), 1277-1284. Available at: https://pubmed.ncbi.nlm.nih.gov/15507096/. Accessed January 25, 2021.
Kodan, A., Kuroda, H. & Sakai, F. (2002) A stilbene synthase from Japanese red pine (Pinus densiflora): implications for phytoalexin accumulation and down-regulation of flavonoid biosynthesis. Proceedings of the National Academy of Sciences, 99(5), 3335-3339.
Kofler, S., Asam, C., Eckhard, U., Wallner, M., Ferreira, F. & Brandstetter, H. (2012) Crystallographically mapped ligand binding differs in high and low IgE binding isoforms of birch pollen allergen bet v 1. Journal of Molecular Biology, 422, 109-123.
Kreuzaler, F. & Hahlbrock, K. (1972) Enzymatic synthesis of aromatic compounds in higher plants: Formation of naringenin (5,7,4′-trihydroxyflavanone) from p-coumaroyl coenzyme A and malonyl coenzyme A. FEBS Letters, 28, 69-72. https://doi.org/10.1016/0014-5793%2872%2980679-3.
Kurze, E., Kock, V., Scalzo, R.L., Olbricht, K. & Schwab, W. (2018) Effect of the strawberry genotype, cultivation and processing on the Fra a 1 allergen content. Nutrients, 10, 2072-6643. Available at: https://www.mdpi.com/2072-6643/10/7/857/htm. Accessed July 14, 2021.
Laursen, T., Borch, J., Knudsen, C., Bavishi, K., Torta, F., Martens, H.J. et al. (2016) Characterization of a dynamic metabolon producing the defense compound dhurrin in sorghum. Science, 354, 890-893. https://doi.org/10.1126/science.aag2347.
Lebel, S., Schellenbaum, P., Walter, B. & Maillot, P. (2010) Characterisation of the Vitis vinifera PR10 multigene family. BMC Plant Biology, 10, 184.
Lee, S.C. & Luan, S. (2012) ABA signal transduction at the crossroad of biotic and abiotic stress responses. Plant, Cell and Environment, 35, 53-60. https://doi.org/10.1111/j.1365-3040.2011.02426.x.
Lenz, R. & Zenk, M. (1995) Acetyl coenzyme A:salutaridinol-7-O-acetyltransferase from Papaver somniferum plant cell cultures. The enzyme catalyzing the formation of thebaine in morphine biosynthesis. Journal of Biological Chemistry, 270, 31091-31096. Available at: https://pubmed.ncbi.nlm.nih.gov/8537369/. Accessed July 19, 2021.
Li, Q., Ramasamy, S., Singh, P., Hagel, J.M., Dunemann, S.M., Chen, X. et al. (2020) Gene clustering and copy number variation in alkaloid metabolic pathways of opium poppy. Nature Communications, 11.
Lichman, B.R., Godden, G.T., Hamilton, J.P., Palmer, L., Kamileen, M.O., Zhao, D. et al. (2020) The evolutionary origins of the cat attractant nepetalactone in catnip. Science Advances, 6(20), eaba0721.
Miranda, C.L., Stevens, J.F., Helmrich, A., Henderson, M.C., Rodriguez, R.J., Yang, Y.H. et al. (1999) Antiproliferative and cytotoxic effects of prenylated flavonoids from hops (Humulus lupulus) in human cancer cell lines. Food and Chemical Toxicology, 37, 271-285.
Miyakawa, T., Fujita, Y., Yamaguchi-Shinozaki, K. & Tanokura, M. (2013) Structure and function of abscisic acid receptors. Trends in Plant Science, 18, 259-266.
Møller, B.L. & Laursen, T. (2021) Metabolons and bio-condensates: The essence of plant plasticity and the key elements in development of green production systems. In Advances in Botanical Research. Academic Press Inc, pp. 185-223.
Morita, Y., Takagi, K., Fukuchi-Mizutani, M., Ishiguro, K., Tanaka, Y., Nitasaka, E. et al. (2014) A chalcone isomerase-like protein enhances flavonoid production and flower pigmentation. The Plant Journal, 78, 294-304. https://doi.org/10.1111/tpj.12469.
Morris, J.S., Caldo, K.M., Liang, S. & Facchini, P.J. (2020) PR10/Bet v 1-like proteins as novel contributors to plant biochemical diversity. ChemBioChem, 22. https://doi.org/10.1002/cbic.202000354.
Morris, J.S., Dastmalchi, M., Li, J., Chang, L., Chen, X., Hagel, J.M. et al. (2016) Plug-and-play benzylisoquinoline alkaloid biosynthetic gene discovery in engineered yeast. In Methods in Enzymology. Academic Press, pp. 143-178. Available at: https://linkinghub.elsevier.com/retrieve/pii/S0076687916300039. Accessed November 19, 2018.
Muñoz, C., Hoffmann, T., Escobar, N.M., Ludemann, F., Botella, M.A., Valpuesta, V. et al. (2010) The strawberry fruit Fra a allergen functions in flavonoid biosynthesis. Molecular Plant, 3(1), 113-124. Available at: https://www.sciencedirect.com/science/article/pii/S1674205214604019?via%3Dihub. Accessed December 20, 2018.
Nakayama, T., Takahashi, S. & Waki, T. (2019) Formation of flavonoid metabolons: functional significance of protein-protein interactions and impact on flavonoid chemodiversity. Frontiers in Plant Science, 10, 821.
Nesi, N., Debeaujon, I., Jond, C., Pelletier, G., Caboche, M. & Lepiniec, L. (2000) The TT8 gene encodes a basic helix-loop-helix domain protein required for expression of DFR and BAN genes in Arabidopsis siliques. The Plant Cell, 12, 1863.
Nesi, N., Debeaujon, I., Jond, C., Stewart, A.J., Jenkins, G.I., Caboche, M. et al. (2002) The transparent testa 16 locus encodes the Arabidopsis BSISTER MADS domain protein and is required for proper development and pigmentation of the seed coat. The Plant Cell, 14, 2463-2479.
Nesi, N., Jond, C., Debeaujon, I., Caboche, M. & Lepiniec, L. (2001) The Arabidopsis TT2 gene encodes an R2R3 MYB domain protein that acts as a key determinant for proanthocyanidin accumulation in developing seed. The Plant Cell, 13, 2099-2114.
Nessler, C.L., Allen, R.D. & Galewsky, S. (1985) Identification and characterization of latex-specific proteins in opium poppy. Plant Physiology, 79, 499-504.
Ngaki, M.N., Louie, G.V., Philippe, R.N., Manning, G., Pojer, F., Bowman, M.E. et al. (2012) Evolution of the chalcone-isomerase fold from fatty-acid binding to stereospecific catalysis. Nature, 485, 530-533. Available at: http://www.nature.com/articles/nature11009. Accessed September 9, 2019.
Ni, R., Zhu, T.-T., Zhang, X.-S., Wang, P.-Y., Sun, C.-J., Qiao, Y.-N. et al. (2020) Identification and evolutionary analysis of chalcone isomerase-fold proteins in ferns. Journal of Experimental Botany, 71, 290-304. Available at: http://swissmodel.expasy.org. Accessed March 26, 2020.
Orozco-Navarrete, B., Song, J., Casañal, A., Sozzani, R., Flors, V., Sánchez-Sevilla, J.F. et al. (2021) Down-regulation of Fra a 1.02 in strawberry fruits causes transcriptomic and metabolic changes compatible with an altered defense response. Horticulture Research, 8, 1-13. Available at: https://www.nature.com/articles/s41438-021-00492-4. Accessed July 14, 2021.
Park, C.-J., Kim, K.-J., Shin, R., Park, J.M., Shin, Y.-C. & Paek, K.-H. (2004) Pathogenesis-related protein 10 isolated from hot pepper functions as a ribonuclease in an antiviral pathway. The Plant Journal, 37, 186-198.
Pasternak, O., Biesiadka, J., Dolot, R., Handschuh, L., Bujacz, G., Sikorski, M.M. et al. (2005) Structure of a yellow lupin pathogenesis-related PR-10 protein belonging to a novel subclass. Acta Crystallographica, Section D: Biological Crystallography, 61, 99-107.
Prashek, J., Bouyain, S., Fu, M., Li, Y., Berkes, D. & Yao, X. (2017) Interaction between the PH and START domains of ceramide transfer protein competes with phosphatidylinositol 4-phosphate binding by the PH domain. Journal of Biological Chemistry, 292, 14217-14228. Available at: http://wwpdb.org/. Accessed March 30, 2021.
Radauer, C., Lackner, P. & Breiteneder, H. (2008) The Bet v 1 fold: an ancient, versatile scaffold for binding of large, hydrophobic ligands. BMC Evolutionary Biology, 8, 286.
Ralston, L., Subramanian, S., Matsuno, M. & Yu, O. (2005) Partial reconstruction of flavonoid and isoflavonoid biosynthesis in yeast using soybean type I and type II chalcone isomerases. Plant Physiology, 137, 1375-1388. Available at: http://www.ncbi.nlm.nih.gov/pubmed/15778463.
Rizhsky, L., Liang, H. & Mittler, R. (2002) The combined effect of drought stress and heat shock on gene expression in tobacco. Plant Physiology, 130(3), 1143-1151.
Saito, K., Yonekura-Sakakibara, K., Nakabayashi, R., Higashi, Y., Yamazaki, M., Tohge, T. et al. (2013) The flavonoid biosynthetic pathway in Arabidopsis: structural and genetic diversity. Plant Physiology and Biochemistry, 72, 21-34. Available at: http://www.ncbi.nlm.nih.gov/pubmed/23473981.
Samanani, N. & Facchini, P.J. (2002) Purification and characterization of norcoclaurine synthase. Journal of Biological Chemistry, 277, 33878-33883. Available at: http://www.jbc.org/content/277/37/33878.long. Accessed March 29, 2019.
Schenk, M.F., Gilissen, L.J.W.J., Esselink, G.D. & Smulders, M.J.M. (2006) Seven different genes encode a diverse mixture of isoforms of Bet v I, the major birch pollen allergen. BMC Genomics, 7, 168.
Schmid, L.M., Ohler, L., Möhlmann, T., Brachmann, A., Muiño, J.M., Leister, D. et al. (2019) PUMPKIN, the sole plastid UMP kinase, associates with group II introns and alters their metabolism. Plant Physiology, 179, 248-264. https://doi.org/10.1104/pp.18.00687.
Seppänen, S.K., Syrjälä, L., Weissenberg, K.V., Teeri, T.H., Paajanen, L. & Pappinen, A. (2004) Antifungal activity of stilbenes in in vitro bioassays and in transgenic Populus expressing a gene encoding pinosylvin synthase. Plant Cell Reports, 22, 584-593.
Shirley, B.W., Hanley, S. & Goodman, H.M. (1992) Effects of ionizing radiation on a plant genome: analysis of two Arabidopsis transparent testa mutations. The Plant Cell, 4, 333-347. Available at: https://academic.oup.com/plcell/article/4/3/333-347/5984356. Accessed February 17, 2021.
Singh, A., Massicotte, M.-A., Garand, A., Tousignant, L., Ouellette, V., Bérubé, G. et al. (2018) Cloning and characterization of norbelladine synthase catalyzing the first committed reaction in Amaryllidaceae alkaloid biosynthesis. BMC Plant Biology, 18.
Singh, A., Menéndez-Perdomo, I.M. & Facchini, P.J. (2019) Benzylisoquinoline Alkaloid Biosynthesis in Opium Poppy: An Update. Springer.
Sliwiak, J., Dauter, Z. & Jaskolski, M. (2016) Crystal Structure of Hyp-1, a Hypericum perforatum PR-10 Protein, in Complex with Melatonin. Frontiers in Plant Science, 7, 668.
Sliwiak, J., Sikorski, M. & Jaskolski, M. (2018) PR-10 proteins as potential mediators of melatonin-cytokinin cross-talk in plants: crystallographic studies of LlPR-10.2B isoform from yellow lupine. FEBS Journal, 285, 1907-1922.
Somssich, I.E., Schmelzer, E., Bollmann, J. & Hahlbrock, K. (1986) Rapid activation by fungal elicitor of genes encoding "pathogenesis-related" proteins in cultured parsley cells. Proceedings of the National Academy of Sciences, 83, 2427-2430. Available at: https://www.pnas.org/content/83/8/2427. Accessed March 18, 2021.
Stafford, H.A. (1991) Flavonoid evolution: an enzymic approach. Plant Physiology, 96, 680-685.
Strömvik, M.V., Sundararaman, V.P. & Vodkin, L.O. (1999) A novel promoter from soybean that is active in a complex developmental pattern with and without its proximal 650 base pairs. Plant Molecular Biology, 41, 217-231. Available at: https://pubmed.ncbi.nlm.nih.gov/10579489/. Accessed March 23, 2021.
Su, B., Qian, Z., Li, T., Zhou, Y. & Wong, A. (2019) PlantMP: A database for moonlighting plant proteins. Database, 2019, baz050.
Taura, F., Tanaka, S., Taguchi, C., Fukamizu, T., Tanaka, H., Shoyama, Y. et al. (2009) Characterization of olivetol synthase, a polyketide synthase putatively involved in cannabinoid biosynthetic pathway. FEBS Letters, 583, 2061-2066. Available at: https://pubmed.ncbi.nlm.nih.gov/19454282/. Accessed March 10, 2021.
Thompson, T.B., Katayama, K., Watanabe, K., Hutchinson, C.R. & Rayment, I. (2004) Structural and functional analysis of tetracenomycin F2 cyclase from Streptomyces glaucescens: A type II polyketide cyclase. Journal of Biological Chemistry, 279, 37956-37963. Available at: https://pubmed.ncbi.nlm.nih.gov/15231835/. Accessed March 10, 2021.
Tropf, S., Lanz, T., Rensing, S.A., Schröder, J. & Schröder, G. (1994) Evidence that stilbene synthases have developed from chalcone synthases several times in the course of evolution. Journal of Molecular Evolution, 38, 610-618.
Tsujishita, Y. & Hurley, J.H. (2000) Structure and lipid transport mechanism of a StAr-related domain. Nature Structural Biology, 7, 408-414. Available at: http://structbio.nature.com. Accessed March 16, 2021.
Ukaji, N., Kuwabara, C., Takezawa, D., Arakawa, K. & Fujikawa, S. (2004) Accumulation of pathogenesis-related (PR) 10/Bet v 1 protein homologues in mulberry (Morus bombycis Koidz.) tree during winter. Plant, Cell and Environment, 27, 1112-1121.
Van Loon, L.C. & Van Kammen, A. (1970) Polyacrylamide disc electrophoresis of the soluble leaf proteins from Nicotiana tabacum var. ‘Samsun’ and ‘Samsun NN’: II. Changes in protein constitution after infection with tobacco mosaic virus. Virology, 40, 199-211.
Waki, T., Mameda, R., Nakano, T., Yamada, S., Terashita, M., Ito, K. et al. (2020) A conserved strategy of chalcone isomerase-like protein to rectify promiscuous chalcone synthase specificity. Nature Communications, 11(1), 1-14. https://doi.org/10.1038/s41467-020-14558-9.
Waki, T., Yoo, D., Fujino, N., Mameda, R., Denessiouk, K., Yamashita, S. et al. (2016) Identification of protein-protein interactions of isoflavonoid biosynthetic enzymes with 2-hydroxyisoflavanone synthase in soybean (Glycine max (L.) Merr.). Biochemical and Biophysical Research Communications, 469, 546-551. Available at: https://linkinghub.elsevier.com/retrieve/pii/S0006291X15310433.
Warner, S.A.J., Gill, A. & Draper, J. (1994) The developmental expression of the asparagus intracellular PR protein (AoPR1) gene correlates with sites of phenylpropanoid biosynthesis. The Plant Journal, 6, 31-43. https://doi.org/10.1046/j.1365-313X.1994.6010031.x.
Watkinson, J.I., Bowerman, P.A., Crosby, K.C., Hildreth, S.B., Helm, R.F. & Winkel, B.S.J. (2018) Identification of MOS9 as an interaction partner for chalcone synthase in the nucleus. PeerJ, 6, e5598.
Williams, C.A. & Grayer, R.J. (2004) Anthocyanins and other flavonoids. Natural Product Reports, 21, 539-573. Available at: https://pubs.rsc.org/en/content/articlehtml/2004/np/b311404j. Accessed March 31, 2021.
Xu, W., Bobet, S., Le Gourrierec, J., Grain, D., De Vos, D., Berger, A. et al. (2017) TRANSPARENT TESTA 16 and 15 act through different mechanisms to control proanthocyanidin accumulation in Arabidopsis testa. Journal of Experimental Botany, 68(11), 2859-2870.
Yamaguchi, T., Kurosaki, F., Suh, D.-Y., Sankawa, U., Nishioka, M., Akiyama, T. et al. (1999) Cross-reaction of chalcone synthase and stilbene synthase overexpressed in Escherichia coli. FEBS Letters, 460, 457-461. https://doi.org/10.1016/S0014-5793%2899%2901403-9.
Yang, X., Matsui, T., Kodama, T., Mori, T., Zhou, X., Taura, F. et al. (2016) Structural basis for olivetolic acid formation by a polyketide cyclase from Cannabis sativa. FEBS Journal, 283, 1088-1106. https://doi.org/10.1111/febs.13654.
Yin, R., Messner, B., Faus-Kessler, T., Hoffmann, T., Schwab, W., Hajirezaei, M.-R. et al. (2012) Feedback inhibition of the general phenylpropanoid and flavonol biosynthetic pathways upon a compromised flavonol-3-O-glycosylation. Journal of Experimental Botany, 63, 2465-2478.
Yonekura-Sakakibara, K., Higashi, Y. & Nakabayashi, R. (2019) The origin and evolution of plant flavonoid metabolism. Frontiers in Plant Science, 10, 943. Available at: www.frontiersin.org. Accessed March 11, 2021.
Zhang, H., Matsuda, H., Yamashita, C., Nakamura, S. & Yoshikawa, M. (2009) Hydrangeic acid from the processed leaves of Hydrangea macrophylla var. thunbergii as a new type of anti-diabetic compound. European Journal of Pharmacology, 606, 255-261.
Zhao, J. & Dixon, R.A. (2009) MATE transporters facilitate vacuolar uptake of epicatechin 3′-O-glucoside for proanthocyanidin biosynthesis in Medicago truncatula and Arabidopsis. The Plant Cell, 21, 2323-2340.

Auteurs

Mehran Dastmalchi (M)

Department of Plant Science, McGill University, Sainte-Anne-de-Bellevue, Québec, H9X 3V9, Canada.

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