Research Progress of Betalain in Response to Adverse Stresses and Evolutionary Relationship Compared with Anthocyanin
Abstract
:1. Introduction
1.1. Basic Information Discerning Betalains and Anthocyanins
1.2. Identification and Detection of Betalains
1.3. The Roles of Betalains in Humans and Plants
1.4. The Significance of Betalains and Anthocyanins in Plants
2. Comprehensive Effects of Plants in Response to Various Stresses
3. Functions of Anthocyanins and Betalains in Plant Responses to Adverse Environmental Conditions
3.1. Flavonoids and Anthocyanins in Plant Responses to Adverse Environmental Conditions
3.2. Betalains in Plant Response to Adverse Environmental Conditions
4. Comparison of the Biosynthesis Pathways of Betalains and Anthocyanins
5. Evolutionary Relationship between Betalains and Anthocyanins
6. Conclusions and Outlook
Funding
Conflicts of Interest
References
- Brockington, S.F.; Walker, R.H.; Glover, B.J.; Soltis, P.S.; Soltis, D.E. Complex pigment evolution in the Caryophyllales. New Phytol. 2011, 190, 854–864. [Google Scholar] [CrossRef] [PubMed]
- Lloyd, A.; Brockman, A.; Aguirre, L.; Campbell, A.; Bean, A.; Cantero, A.; Gonzalez, A. Advances in the MYB-bHLH-WD repeat (MBW) pigment regulatory model: Addition of a WRKY factor and co-option of an anthocyanin MYB for betalain regulation. Plant Cell Physiol. 2017, 58, 1431–1441. [Google Scholar] [CrossRef] [PubMed]
- Gandía-Herrero, F.; García-Carmona, F. Biosynthesis of betalains: Yellow and violet plant pigments. Trends Plant Sci. 2013, 18, 334–343. [Google Scholar] [CrossRef] [PubMed]
- Polturak, G.; Aharoni, A. “La Vie en Rose”: Biosynthesis, sources, and applications of betalain pigments. Mol. Plant 2018, 11, 7–22. [Google Scholar] [CrossRef] [PubMed]
- Clifford, T.; Howatson, G.; West, D.J.; Stevenson, E.J. The potential benefits of red beetroot supplementation in health and disease. Nutrients 2015, 7, 2801–2822. [Google Scholar] [CrossRef] [PubMed]
- Jain, G.; Gould, K.S. Are betalain pigments the functional homologues of anthocyanins in plants? Environ. Exp. Bot. 2015, 119, 48–53. [Google Scholar] [CrossRef]
- Strack, D.; Vogt, T.; Schliemann, W. Recent advances in betalain research. Phytochemistry 2003, 62, 247–269. [Google Scholar] [CrossRef]
- Contreras-Llano, L.E.; Guerrero-Rubio, M.A.; Lozada-Ramírez, J.D.; García-Carmona, F.; Gandía-Herrero, F. First betalain-producing bacteria break the exclusive presence of the pigments in the plant kingdom. mBio 2019, 10, e00345-19. [Google Scholar] [CrossRef]
- Cai, Y.-Z.; Sun, M.; Corke, H. Characterization and application of betalain pigments from plants of the Amaranthaceae. Trends Food Sci. Technol. 2005, 16, 370–376. [Google Scholar] [CrossRef]
- Stintzing, F.C.; Schieber, A.; Carle, R. Evaluation of colour properties and chemical quality parameters of cactus juices. Eur. Food Res. Technol. 2003, 216, 303–311. [Google Scholar] [CrossRef]
- Wyler, H.; Meuer, U. Zur biogenese der betacyane: Versuche mit [2-14C]-dopaxanthin. Helv. Chim. Acta 1979, 62, 1330–1339. [Google Scholar] [CrossRef]
- Trezzini, G.F.; Zrÿd, J.P. Two betalains from Portulaca grandiflora. Phytochemistry 1991, 30, 1897–1899. [Google Scholar] [CrossRef]
- Kugler, F.; Stintzing, F.C.; Carle, R. Identification of betalains from petioles of differently colored swiss chard (Beta vulgaris L. ssp. cicla [L.] Alef. Cv. bright lights) by high-performance liquid chromatography-electrospray ionization mass spectrometry. J. Agric. Food Chem. 2004, 52, 2975–2981. [Google Scholar] [CrossRef]
- Slatnar, A.; Stampar, F.; Veberic, R.; Jakopic, J. HPLC-MSn identification of betalain profile of different beetroot (Beta vulgaris L. ssp. vulgaris) parts and cultivars. J. Food Sci. 2015, 80, C1952–C1958. [Google Scholar] [CrossRef]
- Henarejos-Escudero, P.; Guadarrama-Flores, B.; Guerrero-Rubio, M.A.; Gómez-Pando, L.R.; García-Carmona, F.; Gandía-Herrero, F. Development of betalain producing callus lines from colored quinoa varieties (Chenopodium quinoa Willd). J. Agric. Food Chem. 2018, 66, 467–474. [Google Scholar] [CrossRef]
- Kujala, T.S.; Vienola, M.S.; Klika, K.D.; Loponen, J.M.; Pihlaja, K. Betalain and phenolic compositions of four beetroot (Beta vulgaris) cultivars. Eur. Food Res. Technol. 2002, 214, 505–510. [Google Scholar] [CrossRef]
- Gandía-Herrero, F.; García-Carmona, F.; Escribano, J. Fluorescent pigments: New perspectives in betalain research and applications. Food Res. Int. 2005, 38, 879–884. [Google Scholar] [CrossRef]
- Stintzing, F.C.; Carle, R. Functional properties of anthocyanins and betalains in plants, food, and in human nutrition. Trends Food Sci. Technol. 2004, 15, 19–38. [Google Scholar] [CrossRef]
- Kapadia, G.J.; Tokuda, H.; Konoshima, T.; Nishino, H. Chemoprevention of lung and skin cancer by Beta vulgaris (beet) root extract. Cancer Lett. 1996, 100, 211–214. [Google Scholar] [CrossRef]
- Li, H.-D.; Meng, X.-M.; Huang, C.; Zhang, L.; Lv, X.-W.; Li, J. Application of herbal traditional chinese medicine in the treatment of acute kidney injury. Front. Pharmacol. 2019, 10, 376. [Google Scholar] [CrossRef]
- Sepúlveda-Jiménez, G.; Rueda-Benítez, P.; Porta, H.; Rocha-Sosa, M. Betacyanin synthesis in red beet (Beta vulgaris) leaves induced by wounding and bacterial infiltration is preceded by an oxidative burst. Physiol. Mol. Plant Pathol. 2004, 64, 125–133. [Google Scholar] [CrossRef]
- Choudhury, F.K.; Rivero, R.M.; Blumwald, E.; Mittler, R. Reactive oxygen species, abiotic stress and stress combination. Plant J. 2017, 90, 856–867. [Google Scholar] [CrossRef]
- Kumar, S.; Brooks, M.S.-L. Use of red beet (Beta vulgaris L.) for antimicrobial applications—A critical review. Food Bioprocess Technol. 2018, 11, 17–42. [Google Scholar] [CrossRef]
- Kanner, J.; Harel, S.; Granit, R. Betalains a new class of dietary cationized antioxidants. J. Agric. Food Chem. 2001, 49, 5178–5185. [Google Scholar] [CrossRef]
- Gliszczyńska-Świgło, A.; Szymusiak, H.; Malinowska, P. Betanin, the main pigment of red beet: Molecular origin of its exceptionally high free radical-scavenging activity. Food Addit. Contam. 2006, 23, 1079–1087. [Google Scholar] [CrossRef] [Green Version]
- Jain, G.; Gould, K.S. Functional significance of betalain biosynthesis in leaves of Disphyma australe under salinity stress. Environ. Exp. Bot. 2015, 109, 131–140. [Google Scholar] [CrossRef]
- Hatlestad, G.J.; Akhavan, N.A.; Sunnadeniya, R.M.; Elam, L.; Cargile, S.; Hembd, A.; Gonzalez, A.; McGrath, J.M.; Lloyd, A.M. The beet Y locus encodes an anthocyanin MYB-like protein that activates the betalain red pigment pathway. Nat. Genet. 2015, 47, 92–96. [Google Scholar] [CrossRef]
- Liu, S.; Zheng, X.; Pan, J.; Peng, L.; Cheng, C.; Wang, X.; Zhao, C.; Zhang, Z.; Lin, Y.; XuHan, X.; et al. RNA-sequencing analysis reveals betalains metabolism in the leaf of Amaranthus tricolor L. PLoS ONE 2019, 14, e0216001. [Google Scholar] [CrossRef]
- Mittler, R.; Vanderauwera, S.; Suzuki, N.; Miller, G.; Tognetti, V.B.; Vandepoele, K.; Gollery, M.; Shulaev, V.; Van Breusegem, F. ROS signaling: The new wave? Trends Plant Sci. 2011, 16, 300–309. [Google Scholar] [CrossRef]
- Hossain, M.A.; Bhattacharjee, S.; Armin, S.-M.; Qian, P.; Xin, W.; Li, H.-Y.; Burritt, D.J.; Fujita, M.; Tran, L.-S.P. Hydrogen peroxide priming modulates abiotic oxidative stress tolerance: Insights from ROS detoxification and scavenging. Front. Plant Sci. 2015, 6, 420. [Google Scholar] [CrossRef]
- Hatier, J.-H.B.; Gould, K.S. Foliar anthocyanins as modulators of stress signals. J. Theor. Biol. 2008, 253, 625–627. [Google Scholar] [CrossRef]
- Raja, V.; Majeed, U.; Kang, H.; Andrabi, K.I.; John, R. Abiotic stress: Interplay between ROS, hormones and MAPKs. Environ. Exp. Bot. 2017, 137, 142–157. [Google Scholar] [CrossRef]
- Wu, D.; Cai, S.; Chen, M.; Ye, L.; Chen, Z.; Zhang, H.; Dai, F.; Wu, F.; Zhang, G. Tissue metabolic responses to salt stress in wild and cultivated barley. PLoS ONE 2013, 8, e55431. [Google Scholar] [CrossRef]
- Marchesini, V.A.; Yin, C.; Colmer, T.D.; Veneklaas, E.J. Drought tolerances of three stem-succulent halophyte species of an inland semiarid salt lake system. Funct. Plant Biol. 2014, 41, 1230–1238. [Google Scholar] [CrossRef] [Green Version]
- Negrão, S.; Schmöckel, S.M.; Tester, M. Evaluating physiological responses of plants to salinity stress. Ann. Bot. 2017, 119, 1–11. [Google Scholar] [CrossRef]
- Zhao, G.; Han, Y.; Sun, X.; Li, S.; Shi, Q.; Wang, C. Salinity stress increases secondary metabolites and enzyme activity in safflower. Ind. Crop Prod. 2015, 64, 175–181. [Google Scholar]
- Flowers, T.J.; Colmer, T.D. Plant salt tolerance: Adaptations in halophytes. Ann. Bot. 2015, 115, 327–331. [Google Scholar] [CrossRef]
- Li, N.; Du, C.; Ma, B.; Gao, Z.; Wu, Z.; Zheng, L.; Niu, Y.; Wang, Y. Functional analysis of ion transport properties and salt tolerance mechanisms of RtHKT1 from the recretohalophyte Reaumuria trigyna. Plant Cell Physiol. 2018, 60, 85–106. [Google Scholar] [CrossRef]
- Parida, A.; Kumari, A.; Panda, A.; Rangani, J.; Agarwal, P. Photosynthetic pigments, betalains, proteins, sugars, and minerals during Salicornia brachiata senescence. Biol. Plant. 2018, 62, 343–352. [Google Scholar] [CrossRef]
- Bernatoniene, J.; Kopustinskiene, D. The role of catechins in cellular responses to oxidative stress. Molecules 2018, 23, 965. [Google Scholar] [CrossRef]
- Hughes, N.M. Winter leaf reddening in ‘evergreen’ species. New Phytol. 2011, 190, 573–581. [Google Scholar] [CrossRef]
- Hughes, N.M.; Carpenter, K.L.; Cannon, J.G. Estimating contribution of anthocyanin pigments to osmotic adjustment during winter leaf reddening. J. Plant Physiol. 2013, 170, 230–233. [Google Scholar] [CrossRef]
- Hamilton, W.D.; Brown, S.P. Autumn tree colours as a handicap signal. Proc. R. Soc. Lond. B Biol. Sci. 2001, 268, 1489–1493. [Google Scholar] [CrossRef]
- Mouradov, A.; Spangenberg, G. Flavonoids: A metabolic network mediating plants adaptation to their real estate. Front. Plant Sci. 2014, 5, 620. [Google Scholar] [CrossRef]
- Li, S.-J.; Bai, Y.-C.; Li, C.-L.; Yao, H.-P.; Chen, H.; Zhao, H.-X.; Wu, Q. Anthocyanins accumulate in tartary buckwheat (Fagopyrum tataricum) sprout in response to cold stress. Acta Physiol. Plant. 2015, 37, 159. [Google Scholar] [CrossRef]
- Sivankalyani, V.; Feygenberg, O.; Diskin, S.; Wright, B.; Alkan, N. Increased anthocyanin and flavonoids in mango fruit peel are associated with cold and pathogen resistance. Postharvest Biol. Technol. 2016, 111, 132–139. [Google Scholar] [CrossRef]
- Zhang, Q.; Liu, M.; Ruan, J. Metabolomics analysis reveals the metabolic and functional roles of flavonoids in light-sensitive tea leaves. BMC Plant Biol. 2017, 17, 64. [Google Scholar] [CrossRef]
- Lotkowska, M.E.; Tohge, T.; Fernie, A.R.; Xue, G.-P.; Balazadeh, S.; Mueller-Roeber, B. The Arabidopsis transcription factor MYB112 promotes anthocyanin formation during salinity and under high light stress. Plant Physiol. 2015, 169, 1862–1880. [Google Scholar] [CrossRef]
- Maier, A.; Hoecker, U. COP1/SPA ubiquitin ligase complexes repress anthocyanin accumulation under low light and high light conditions. Plant Signal. Behav. 2015, 10, e970440. [Google Scholar] [CrossRef]
- Hou, F.Y.; Wang, Q.M.; Dong, S.X.; Li, A.X.; Zhang, H.Y.; Xie, B.T.; Zhang, L.M. Accumulation and gene expression of anthocyanin in storage roots of purple-freshed sweet potato [Ipomoea batatas (L.) Lam] under weak light conditions. Agric. Sci. China 2010, 9, 1588–1593. [Google Scholar] [CrossRef]
- Park, S.-C.; Kim, Y.-H.; Kim, S.H.; Jeong, Y.J.; Kim, C.Y.; Lee, J.S.; Bae, J.-Y.; Ahn, M.-J.; Jeong, J.C.; Lee, H.-S.; et al. Overexpression of the IbMYB1 gene in an orange-fleshed sweet potato cultivar produces a dual-pigmented transgenic sweet potato with improved antioxidant activity. Physiol. Plant. 2015, 153, 525–537. [Google Scholar] [CrossRef]
- Nakabayashi, R.; Yonekura-Sakakibara, K.; Urano, K.; Suzuki, M.; Yamada, Y.; Nishizawa, T.; Matsuda, F.; Kojima, M.; Sakakibara, H.; Shinozaki, K.; et al. Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J. 2014, 77, 367–379. [Google Scholar] [CrossRef]
- Hoffmann, A.M.; Noga, G.; Hunsche, M. High blue light improves acclimation and photosynthetic recovery of pepper plants exposed to UV stress. Environ. Exp. Bot. 2015, 109, 254–263. [Google Scholar] [CrossRef]
- Guidi, L.; Brunetti, C.; Fini, A.; Agati, G.; Ferrini, F.; Gori, A.; Tattini, M. UV radiation promotes flavonoid biosynthesis, while negatively affecting the biosynthesis and the de-epoxidation of xanthophylls: Consequence for photoprotection? Environ. Exp. Bot. 2016, 127, 14–25. [Google Scholar] [CrossRef]
- Nakabayashi, R.; Mori, T.; Saito, K. Alternation of flavonoid accumulation under drought stress in Arabidopsis thaliana. Plant Signal. Behav. 2014, 9, e29518. [Google Scholar] [CrossRef]
- Borgognone, D.; Cardarelli, M.; Rea, E.; Lucini, L.; Colla, G. Salinity source-induced changes in yield, mineral composition, phenolic acids and flavonoids in leaves of artichoke and cardoon grown in floating system. J. Sci. Food Agric. 2014, 94, 1231–1237. [Google Scholar] [CrossRef]
- Shoeva, O.Y.; Khlestkina, E. Differently expressed ‘Early’flavonoid synthesis genes in wheat seedlings become to be co-regulated under salinity stress. Cereal Res. Commun. 2015, 43, 537–543. [Google Scholar] [CrossRef]
- Sarker, U.; Oba, S. Augmentation of leaf color parameters, pigments, vitamins, phenolic acids, flavonoids and antioxidant activity in selected Amaranthus tricolor under salinity stress. Sci. Rep. 2018, 8, 12349. [Google Scholar] [CrossRef]
- Saikachout, S.; Benmansoura, A.; Ennajah, A.; Leclerc, J.; Ouerghi, Z.; Karray Bouraoui, N. Effects of metal toxicity on growth and pigment contents of annual halophyte (A. hortensis and A. rosea). Int. J. Environ. Res. 2015, 9, 613–620. [Google Scholar]
- Rozpądek, P.; Wężowicz, K.; Stojakowska, A.; Malarz, J.; Surówka, E.; Sobczyk, L.; Anielska, T.; Ważny, R.; Miszalski, Z.; Turnau, K. Mycorrhizal fungi modulate phytochemical production and antioxidant activity of Cichorium intybus L. (Asteraceae) under metal toxicity. Chemosphere 2014, 112, 217–224. [Google Scholar] [CrossRef]
- Mathesius, U. Flavonoid functions in plants and their interactions with other organisms. Plants 2018, 7, 30. [Google Scholar] [CrossRef]
- Davies, K.M.; Albert, N.W.; Zhou, Y.; Schwinn, K.E. Functions of flavonoid and betalain pigments in abiotic stress tolerance in plants. In Annual Plant Reviews Online; John Wiley & Sons, Ltd.: New York, NY, USA, 2018. [Google Scholar] [CrossRef]
- Palma-Tenango, M.; Soto-Hernández, M.; Aguirre-Hernández, E. Flavonoids in agriculture. In Flavonoids—From Biosynthesis to Human Health; InTech: London, UK, 2017. [Google Scholar] [CrossRef]
- Zeng, X.-Q.; Chow, W.S.; Su, L.-J.; Peng, X.-X.; Peng, C.-L. Protective effect of supplemental anthocyanins on Arabidopsis leaves under high light. Physiol. Plant. 2010, 138, 215–225. [Google Scholar] [CrossRef]
- Lev-Yadun, S.; Dafni, A.; Flaishman, M.A.; Inbar, M.; Izhaki, I.; Katzir, G.; Ne’eman, G. Plant coloration undermines herbivorous insect camouflage. Bioessays 2004, 26, 1126–1130. [Google Scholar] [CrossRef]
- Lev-Yadun, S.; Gould, K.S. What do red and yellow autumn leaves signal? Bot. Rev. 2007, 73, 279–289. [Google Scholar] [CrossRef]
- Rolshausen, G.; Schaefer, H.M. Do aphids paint the tree red (or yellow)—Can herbivore resistance or photoprotection explain colourful leaves in autumn? Plant Ecol. 2007, 191, 77–84. [Google Scholar] [CrossRef]
- Park, N.I.; Xu, H.; Li, X.; Jang, I.H.; Park, S.; Ahn, G.H.; Lim, Y.P.; Kim, S.J.; Park, S.U. Anthocyanin accumulation and expression of anthocyanin biosynthetic genes in radish (Raphanus sativus). J. Agric. Food Chem. 2011, 59, 6034–6039. [Google Scholar] [CrossRef]
- Duarte, B.; Santos, D.; Marques, J.C.; Caçador, I. Ecophysiological adaptations of two halophytes to salt stress: Photosynthesis, PS II photochemistry and anti-oxidant feedback-implications for resilience in climate change. Plant Physiol. Biochem. 2013, 67, 178–188. [Google Scholar] [CrossRef]
- Sdouga, D.; Amor, F.B.; Ghribi, S.; Kabtni, S.; Tebini, M.; Branca, F.; Trifi-Farah, N.; Marghali, S. An insight from tolerance to salinity stress in halophyte Portulaca oleracea L.: Physio-morphological, biochemical and molecular responses. Ecotoxicol. Environ. Saf. 2019, 172, 45–52. [Google Scholar] [CrossRef]
- Ibdah, M.; Krins, A.; Seidlitz, H.K.; Heller, W.; Strack, D.; Vogt, T. Spectral dependence of flavonol and betacyanin accumulation in Mesembryanthemum crystallinum under enhanced ultraviolet radiation. Plant Cell Environ. 2002, 25, 1145–1154. [Google Scholar] [CrossRef]
- Agarie, S. Physiological roles of betacyanin in a halophyte, Suaeda japonica Makino. Plant Prod. Sci. 2010, 13, 351–359. [Google Scholar]
- Vogt, T.; Ibdah, M.; Schmidt, J.; Wray, V.; Nimtz, M.; Strack, D. Light-induced betacyanin and flavonol accumulation in bladder cells of Mesembryanthemum crystallinum. Phytochemistry 1999, 52, 583–592. [Google Scholar] [CrossRef]
- Polturak, G.; Breitel, D.; Sarrion-Perdigones, A.; Grossman, N.; Weithorn, E.; Pliner, M.; Orzaez, D.; Granell, A.; Rogachev, I.; Aharoni, A. Elucidation of the first step in betalain biosynthesis allows the heterologous production of betalain pigments in plants. Planta Med. 2016, 82, S1–S381. [Google Scholar] [CrossRef]
- Rahimzadeh Karvansara, P.; Razavi, S.M. Physiological and biochemical responses of sugar beet (Beta vulgaris L) to ultraviolet-B radiation. PeerJ 2019, 7, e6790. [Google Scholar] [CrossRef]
- Timoneda, A.; Sheehan, H.; Feng, T.; Lopez-Nieves, S.; Maeda, H.A.; Brockington, S. Redirecting primary metabolism to boost production of tyrosine-derived specialised metabolites in planta. Sci. Rep. 2018, 8, 17256. [Google Scholar] [CrossRef]
- Preczenhak, A.P.; Orsi, B.; Lima, G.P.P.; Tezotto-Uliana, J.V.; Minatel, I.O.; Kluge, R.A. Cysteine enhances the content of betalains and polyphenols in fresh-cut red beet. Food Chem. 2019, 286, 600–607. [Google Scholar] [CrossRef]
- Qingzhu, H.; Chengjie, C.; Zhe, C.; Pengkun, C.; Yuewen, M.; Jingyu, W.; Jian, Z.; Guibing, H.; Jietang, Z.; Yonghua, Q. Transcriptomic analysis reveals key genes related to betalain biosynthesis in pulp coloration of Hylocereus polyrhizus. Front. Plant Sci. 2016, 6, 1179. [Google Scholar] [CrossRef]
- Polturak, G.; Heinig, U.; Grossman, N.; Battat, M.; Leshkowitz, D.; Malitsky, S.; Rogachev, I.; Aharoni, A. Transcriptome and metabolic profiling provides insights into betalain biosynthesis and evolution in Mirabilis jalapa. Mol. Plant 2018, 11, 189–204. [Google Scholar] [CrossRef]
- Polturak, G.; Breitel, D.; Grossman, N.; Sarrion-Perdigones, A.; Weithorn, E.; Pliner, M.; Orzaez, D.; Granell, A.; Rogachev, I.; Aharoni, A. Elucidation of the first committed step in betalain biosynthesis enables the heterologous engineering of betalain pigments in plants. New Phytol. 2016, 210, 269–283. [Google Scholar] [CrossRef]
- Sunnadeniya, R.; Bean, A.; Brown, M.; Akhavan, N.; Hatlestad, G.; Gonzalez, A.; Symonds, V.V.; Lloyd, A. Tyrosine hydroxylation in betalain pigment biosynthesis is performed by cytochrome P450 enzymes in beets (Beta vulgaris). PLoS ONE 2016, 11, e0149417. [Google Scholar] [CrossRef]
- Harris, N.N.; Javellana, J.; Davies, K.M.; Lewis, D.H.; Jameson, P.E.; Deroles, S.C.; Calcott, K.E.; Gould, K.S.; Schwinn, K.E. Betalain production is possible in anthocyanin-producing plant species given the presence of DOPA-dioxygenase and L-DOPA. BMC Plant Biol. 2012, 12, 34. [Google Scholar] [CrossRef]
- Rebello, J.L.; Jensen, R.A. Metabolic interlock. The multi-metabolite control of prephenate dehydratase activity in Bacillus subtilis. J. Biol. Chem. 1970, 245, 3738–3744. [Google Scholar]
- Jensen, R.A. Metabolic interlock. Regulatory interactions exerted between biochemical pathways. J. Biol. Chem. 1969, 244, 2816–2823. [Google Scholar]
- Cui, F.; Jiao, R. Regulation of the biosynthesis of aromatic amino acids in Streptoverticillium caespitosus. Acta Microbiol. Sin. 1996, 36, 445–452. [Google Scholar]
- Liu, J.; Osbourn, A.; Ma, P. MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Mol. Plant 2015, 8, 689–708. [Google Scholar] [CrossRef]
- Xi, X.; Zong, Y.; Li, S.; Cao, D.; Sun, X.; Liu, B. Transcriptome analysis clarified genes involved in betalain biosynthesis in the fruit of red pitayas (Hylocereus costaricensis). Molecules 2019, 24, 445. [Google Scholar] [CrossRef]
- Gandía-Herrero, F.; Escribano, J.; García-Carmona, F. Biological activities of plant pigments betalains. Crit. Rev. Food Sci. Nutr. 2016, 56, 937–945. [Google Scholar] [CrossRef]
- Des Marais, D.L. To betalains and back again: A tale of two pigments. New Phytol. 2015, 207, 939–941. [Google Scholar] [CrossRef]
- Walker, J.F.; Yang, Y.; Feng, T.; Timoneda, A.; Mikenas, J.; Hutchison, V.; Edwards, C.; Wang, N.; Ahluwalia, S.; Olivieri, J.; et al. From cacti to carnivores: Improved phylotranscriptomic sampling and hierarchical homology inference provide further insight into the evolution of Caryophyllales. Am. J. Bot. 2018, 105, 446–462. [Google Scholar] [CrossRef] [Green Version]
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Li, G.; Meng, X.; Zhu, M.; Li, Z. Research Progress of Betalain in Response to Adverse Stresses and Evolutionary Relationship Compared with Anthocyanin. Molecules 2019, 24, 3078. https://doi.org/10.3390/molecules24173078
Li G, Meng X, Zhu M, Li Z. Research Progress of Betalain in Response to Adverse Stresses and Evolutionary Relationship Compared with Anthocyanin. Molecules. 2019; 24(17):3078. https://doi.org/10.3390/molecules24173078
Chicago/Turabian StyleLi, Ge, Xiaoqing Meng, Mingku Zhu, and Zongyun Li. 2019. "Research Progress of Betalain in Response to Adverse Stresses and Evolutionary Relationship Compared with Anthocyanin" Molecules 24, no. 17: 3078. https://doi.org/10.3390/molecules24173078