Effect of Betanin Synthesis on Photosynthesis and Tyrosine Metabolism in Transgenic Carrot

Overview

Journal BMC Plant Biol

Publisher Biomed Central

Specialty Biology

Date 2023 Aug 24

PMID 37620775

Authors

Bo Wang

Ya-Hui Wang

Yuan-Jie Deng

Quan-Hong Yao

Ai-Sheng Xiong

Affiliations

Soon will be listed here.

Abstract

Background: Betalain is a natural pigment with important nutritional value and broad application prospects. Previously, we produced betanin biosynthesis transgenic carrots via expressing optimized genes CYP76AD1S, cDOPA5GTS and DODA1S. Betanin can accumulate throughout the whole transgenic carrots. But the effects of betanin accumulation on the metabolism of transgenic plants and whether it produces unexpected effects are still unclear.

Results: The accumulation of betanin in leaves can significantly improve its antioxidant capacity and induce a decrease of chlorophyll content. Transcriptome and metabolomics analysis showed that 14.0% of genes and 33.1% of metabolites were significantly different, and metabolic pathways related to photosynthesis and tyrosine metabolism were markedly altered. Combined analysis showed that phenylpropane biosynthesis pathway significantly enriched the differentially expressed genes and significantly altered metabolites.

Conclusions: Results showed that the metabolic status was significantly altered between transgenic and non-transgenic carrots, especially the photosynthesis and tyrosine metabolism. The extra consumption of tyrosine and accumulation of betanin might be the leading causes.

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References

Ling L, Jiang Y, Meng J, Cai L, Cao G . Phloem transport capacity of transgenic rice T1c-19 (Cry1C*) under several potassium fertilizer levels. PLoS One. 2018; 13(3):e0195058. PMC: 5875849. DOI: 10.1371/journal.pone.0195058. View

Ogata T, Toyoshima M, Yamamizo-Oda C, Kobayashi Y, Fujii K, Tanaka K . Virus-Mediated Transient Expression Techniques Enable Functional Genomics Studies and Modulations of Betalain Biosynthesis and Plant Height in Quinoa. Front Plant Sci. 2021; 12:643499. PMC: 8014037. DOI: 10.3389/fpls.2021.643499. View

Kanehisa M, Furumichi M, Sato Y, Kawashima M, Ishiguro-Watanabe M . KEGG for taxonomy-based analysis of pathways and genomes. Nucleic Acids Res. 2022; 51(D1):D587-D592. PMC: 9825424. DOI: 10.1093/nar/gkac963. View

Chung H, Schwinn K, Ngo H, Lewis D, Massey B, Calcott K . Characterisation of betalain biosynthesis in Parakeelya flowers identifies the key biosynthetic gene DOD as belonging to an expanded LigB gene family that is conserved in betalain-producing species. Front Plant Sci. 2015; 6:499. PMC: 4493658. DOI: 10.3389/fpls.2015.00499. View

Li T, Liu J, Deng Y, Duan A, Liu H, Zhuang F . Differential hydroxylation efficiency of the two non-heme carotene hydroxylases: DcBCH1, rather than DcBCH2, plays a major role in carrot taproot. Hortic Res. 2022; 9:uhac193. PMC: 9630967. DOI: 10.1093/hr/uhac193. View

Fujita Y, Uraga Y, Ichisima E . Molecular cloning and nucleotide sequence of the protyrosinase gene, melO, from Aspergillus oryzae and expression of the gene in yeast cells. Biochim Biophys Acta. 1995; 1261(1):151-4. DOI: 10.1016/0167-4781(95)00011-5. View

Esteves L, Pinheiro A, Pioli R, Penna T, Baader W, Correra T . Revisiting the Mechanism of Hydrolysis of Betanin. Photochem Photobiol. 2018; 94(5):853-864. DOI: 10.1111/php.12897. View

Xie F, Hua Q, Chen C, Zhang L, Zhang Z, Chen J . Transcriptomics-based identification and characterization of glucosyltransferases involved in betalain biosynthesis in Hylocereus megalanthus. Plant Physiol Biochem. 2020; 152:112-124. DOI: 10.1016/j.plaphy.2020.04.023. View

Dong N, Lin H . Contribution of phenylpropanoid metabolism to plant development and plant-environment interactions. J Integr Plant Biol. 2020; 63(1):180-209. DOI: 10.1111/jipb.13054. View

10.

Nakatsuka T, Yamada E, Takahashi H, Imamura T, Suzuki M, Ozeki Y . Genetic engineering of yellow betalain pigments beyond the species barrier. Sci Rep. 2013; 3:1970. PMC: 3679504. DOI: 10.1038/srep01970. View

11.

Gandia-Herrero F, Garcia-Carmona F . Characterization of recombinant Beta vulgaris 4,5-DOPA-extradiol-dioxygenase active in the biosynthesis of betalains. Planta. 2012; 236(1):91-100. DOI: 10.1007/s00425-012-1593-2. View

12.

DeLoache W, Russ Z, Narcross L, Gonzales A, Martin V, Dueber J . An enzyme-coupled biosensor enables (S)-reticuline production in yeast from glucose. Nat Chem Biol. 2015; 11(7):465-71. DOI: 10.1038/nchembio.1816. View

13.

Christinet L, Burdet F, Zaiko M, Hinz U, Zryd J . Characterization and functional identification of a novel plant 4,5-extradiol dioxygenase involved in betalain pigment biosynthesis in Portulaca grandiflora. Plant Physiol. 2004; 134(1):265-74. PMC: 316306. DOI: 10.1104/pp.103.031914. View

14.

Xu Z, Feng K, Xiong A . CRISPR/Cas9-Mediated Multiply Targeted Mutagenesis in Orange and Purple Carrot Plants. Mol Biotechnol. 2019; 61(3):191-199. DOI: 10.1007/s12033-018-00150-6. View

15.

Sharma M, Bhat R . Extraction of Carotenoids from Pumpkin Peel and Pulp: Comparison between Innovative Green Extraction Technologies (Ultrasonic and Microwave-Assisted Extractions Using Corn Oil). Foods. 2021; 10(4). PMC: 8067522. DOI: 10.3390/foods10040787. View

16.

Vogt T, Grimm R, Strack D . Cloning and expression of a cDNA encoding betanidin 5-O-glucosyltransferase, a betanidin- and flavonoid-specific enzyme with high homology to inducible glucosyltransferases from the Solanaceae. Plant J. 1999; 19(5):509-19. DOI: 10.1046/j.1365-313x.1999.00540.x. View

17.

Harris N, Javellana J, Davies K, Lewis D, Jameson P, Deroles S . Betalain production is possible in anthocyanin-producing plant species given the presence of DOPA-dioxygenase and L-DOPA. BMC Plant Biol. 2012; 12:34. PMC: 3317834. DOI: 10.1186/1471-2229-12-34. View

18.

Polturak G, Breitel D, Grossman N, Sarrion-Perdigones A, Weithorn E, Pliner M . Elucidation of the first committed step in betalain biosynthesis enables the heterologous engineering of betalain pigments in plants. New Phytol. 2015; 210(1):269-83. DOI: 10.1111/nph.13796. View

19.

Chang Y, Chiu Y, Tsao N, Chou Y, Tan C, Chiang Y . Elucidation of the core betalain biosynthesis pathway in Amaranthus tricolor. Sci Rep. 2021; 11(1):6086. PMC: 7969944. DOI: 10.1038/s41598-021-85486-x. View

20.

Wang L, Wang X, Jin X, Jia R, Huang Q, Tan Y . Comparative proteomics of Bt-transgenic and non-transgenic cotton leaves. Proteome Sci. 2015; 13:15. PMC: 4422549. DOI: 10.1186/s12953-015-0071-8. View