دورية أكاديمية
Dynamics of annatto pigment synthesis and accumulation in seeds of Bixa orellana L. revealed by integrated chemical, anatomical, and RNA-Seq analyses.
| العنوان: | Dynamics of annatto pigment synthesis and accumulation in seeds of Bixa orellana L. revealed by integrated chemical, anatomical, and RNA-Seq analyses. |
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| المؤلفون: | Moreira VS; Instituto Federal de Educação Ciência E Tecnologia da Bahia, Euclides da Cunha, Bahia, 48500-000, Brazil., de Souza VC; Departamento de Ciências da Computação, Universidade Federal de Juiz de Fora, Juiz de Fora, Minas Gerais, 36036-900, Brazil., Soares VLF; Centro de Biotecnologia E Genética, Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilheus, Bahia, 45662-900, Brazil., Sousa AO; Centro Multidisciplinar Do Campus Luís Eduardo Magalhães, Universidade Federal Do Oeste da Bahia, Luis Eduardo Magalhães, Bahia, 47850‑000, Brazil., de Nascimento KTS; Centro de Biotecnologia E Genética, Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilheus, Bahia, 45662-900, Brazil., de Santana MR; Centro de Biotecnologia E Genética, Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilheus, Bahia, 45662-900, Brazil., Rebouças TNH; Departamento de Fitotecnia E Zootecnia, Universidade Estadual Do Sudoeste da Bahia, Vitoria da Conquista, Bahia, 45083-900, Brazil., Leitão CAE; Departamento de Ciências Naturais, Universidade Estadual Do Sudoeste da Bahia, Vitoria da Conquista, Bahia, 45083-900, Brazil., Goliatt PVZC; Departamento de Ciências da Computação, Universidade Federal de Juiz de Fora, Juiz de Fora, Minas Gerais, 36036-900, Brazil., Faria DV; Departamento de Biologia Vegetal/BIOAGRO, Universidade Federal de Viçosa, Vicosa, Minas Gerais, 36570-900, Brazil., Otoni WC; Departamento de Biologia Vegetal/BIOAGRO, Universidade Federal de Viçosa, Vicosa, Minas Gerais, 36570-900, Brazil., Costa MGC; Centro de Biotecnologia E Genética, Departamento de Ciências Biológicas, Universidade Estadual de Santa Cruz, Ilheus, Bahia, 45662-900, Brazil. marciogc.costa@gmail.com. |
| المصدر: | Protoplasma [Protoplasma] 2023 Jul; Vol. 260 (4), pp. 1207-1219. Date of Electronic Publication: 2023 Feb 14. |
| نوع المنشور: | Journal Article |
| اللغة: | English |
| بيانات الدورية: | Publisher: Springer Country of Publication: Austria NLM ID: 9806853 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1615-6102 (Electronic) Linking ISSN: 0033183X NLM ISO Abbreviation: Protoplasma Subsets: MEDLINE |
| أسماء مطبوعة: | Publication: <1998->: Wien ; New York : Springer Original Publication: Leipzig : Verlag von Gebrüder Borntraeger, 1927- |
| مواضيع طبية MeSH: | Bixaceae*/genetics , Bixaceae*/metabolism , Carotenoids*/metabolism, RNA-Seq ; Seeds |
| مستخلص: | Bixin is a commercially valuable apocarotenoid pigment found in the seed aril of Bixa orellana. The dynamics and regulation of its biosynthesis and accumulation during seed development remain largely unknown. Here, we combined chemical, anatomical, and transcriptomic data to provide stage-specific resolution of the cellular and molecular events occurring during B. orellana seed development. Seeds at five developmental stages (S1-S5) were used for analysis of bixin content and seed anatomy, and three of them (S1, S3, and S4) were selected for Illumina HiSeq sequencing. Bixin accumulated in large quantities in seeds compared with other tissues analyzed, particularly during the S2 stage, peaking at the S4 stage, and then decreasing slightly in the S5 stage. Anatomical analysis revealed that bixin accumulated in the large central vacuole of specialized cells, which were scattered throughout the developing mesotesta at the S2 stage, but enlarged progressively at later stages, until they occupied most of the parenchyma in the aril. A total of 13 million reads were generated and assembled into 73,381 protein-encoding contigs, from which 312 were identified as containing 1-deoxy-D-xylulose-5-phosphate/2-C-methyl-D-erythritol-4-phosphate (DOXP/MEP), carotenoid, and bixin pathways genes. Differential transcriptome expression analysis of these genes revealed that 50 of them were sequentially and differentially expressed through the seed developmental stages analyzed, including seven carotenoid cleavage dioxygenases, eight aldehyde dehydrogenases, and 22 methyltransferases. Taken together, these results show that bixin synthesis and accumulation in seeds of B. orellana are a developmentally regulated process involving the coordinated expression of DOXP/MEP, carotenoid, and bixin biosynthesis genes. (© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Austria, part of Springer Nature.) |
| References: | Andrews S (2010) FastQC: a quality control tool for high throughput sequence data. Babraham Inst. Available online at: http://www.bioinformatics.babraham.ac.uk/projects/fastqc . Accessed 10 June 2021. Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina Sequence Data. Bioinforma 30:2114–2120. (PMID: 10.1093/bioinformatics/btu170) Bouvier F, Dogbo O, Camara B (2003) Biosynthesis of the food and cosmetic plant pigment bixin (annatto). Sci 300:2089–2091. (PMID: 10.1126/science.1085162) Bouvier F, Suire C, Mutterer J, Camara B (2003) Oxidative remodeling of chromoplast carotenoids identification of the carotenoid dioxygenase CsCCD and CsZCD genes involved in Crocus secondary metabolite biogenesis. Plant Cell 15:47–62. (PMID: 10.1105/tpc.00653612509521143450) Carballo-Uicab VM, Cárdenas-Conejo Y, Vallejo-Cardona AA, Aguilar-Espinosa M, Rodríguez-Campos J, Serrano-Posada H, Narváez-Zapata JA, Vázquez-Flota F, Rivera-Madrid R (2019) Isolation and functional characterization of two dioxygenases putatively involved in bixin biosynthesis in annatto (Bixa orellana L.). PeerJ 7:e7064. (PMID: 10.7717/peerj.7064312757446592262) Cárdenas-Conejo Y, Carballo-Uicab V, Lieberman M, Aguilar-Espinosa M, Comai L, Rivera-Madrid R (2015) De novo transcriptome sequencing in Bixa orellana to identify genes involved in methylerythritol phosphate, carotenoid and bixin biosynthesis. BMC Genomics 16:877. (PMID: 10.1186/s12864-015-2065-4265110104625570) Carvalho PRN, Silva MG, Fabri EG, Tavares PER, Martins ALM, Spatti LR (2010) Concentração de bixina e lipídios em sementes de urucum da coleção do Instituto Agronômico (IAC). Bragantia 69:519–524. (PMID: 10.1590/S0006-87052010000300002) D’Auria JC, Chen F, Pichersky E (2003) The SABATH family of methyltransferases in Arabidopsis thaliana and other plant species. Recent Adv Phytochem 37:9–125. Faria DV, Correia LNFC, Souza MVC, Ríos-Ríos AM, Vital CE, Batista DS, Costa MGC, Otoni WC (2019) Irradiance and light quality affect two annatto (Bixa orellana L.) cultivars with contrasting bixin production. J Photochem Photobiol B 197:111549. (PMID: 10.1016/j.jphotobiol.2019.11154931302348) Faria DV, Correia LNF, Batista DS, Vital CE, Heringer AS, De-la-Peña C, Costa MGC, Guerra MP, Otoni WC (2020) 5-Azacytidine downregulates the SABATH methyltransferase genes and augments bixin content in Bixa orellana L. leaves. Plant Cell Tissue Organ Cult 142:425–434. (PMID: 10.1007/s11240-020-01857-8) Fester T, Hause B, Schmidt D, Halfmann K, Schmidt J, Wray V, Hause G, Strack D (2002) Occurrence and localization of apocarotenoids in arbuscular mycorrhizal roots. Plant Cell Physiol 43:256–265. (PMID: 10.1093/pcp/pcf02911917079) Galpaz N, Ronen G, Khalfa Z, Zamir D, Hirschberg J (2006) A chromoplast-specific carotenoid biosynthesis pathway is revealed by cloning of the tomato white-flower locus. Plant Cell 18:1947–1960. (PMID: 10.1105/tpc.105.039966168161371533990) Giuliano G, Rosati C, Bramley PM (2003) To dye or not to dye: biochemistry of annatto unveiled. Trends Biotechnol 21:513–516. (PMID: 10.1016/j.tibtech.2003.10.00114624856) Gómez-Gómez L, Parra-Veja V, Rivas-Sendra A, Seguí-Simarro JM, Molina RV, Pallotti C, Rubio-Moraga A, Diretto G, Prieto A, Ahrazem O (2017) Unraveling massive crocins transport and accumulation through proteome and microscopy tools during the development of saffron stigma. Int J Mol Sci 18:76. (PMID: 10.3390/ijms18010076280454315297711) Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-seq data without a reference genome. Nat Biotechnol 29:644–652. (PMID: 10.1038/nbt.1883215724403571712) Han Y, Gasic K, Korban SS (2007) Multiple-copy cluster-type organization and evolution of genes encoding o-methyltransferases in apple. Genet 176:2625–2635. (PMID: 10.1534/genetics.107.073650) Hou X, Rivers J, León P, McQuinn RP, Pogson BJ (2016) Synthesis and function of apocarotenoid signals in plants. Trends Plant Sci 21:792–803. (PMID: 10.1016/j.tplants.2016.06.00127344539) Jako C, Coutu C, Roewer I, Reed DW, Pelcher LE, Covello PS (2002) Probing carotenoid biosynthesis in developing seed coats of Bixa orellana (Bixaceae) through expressed sequence tag analysis. Plant Sci 163:141–145. (PMID: 10.1016/S0168-9452(02)00083-3) Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. J Cell Biol 27:137–138. Lichtenthaler HK (1999) The 1-deoxy-D-xylulose-5-phosphate pathway of isoprenoid biosynthesis in plants. Annu Rev Plant Physiol Plant Mol Biol 50:47–65. (PMID: 10.1146/annurev.arplant.50.1.4715012203) Louro RP, Santiago LJ (2016) Development of carotenoid storage cells in Bixa orellana L. seed arils. Protoplasma 253:77–86. (PMID: 10.1007/s00709-015-0789-225786349) Machado KLG (2022) The module mir156/spl affects bixin biosynthesis pathway in annatto (Bixa orellana L.). PhD thesis, Universidade Federal de Viçosa, Viçosa, Brazil. https://doi.org/10.47328/ufvbbt.2022.323. Mercadante AZ, Pfander H (1998) Carotenoids from annatto: a review. Recent Res Devel Agric Food Chem 2:79–91. Mercadante AZ, Steck A, Pfander H (1997) Isolation and identification of new apocarotenoids from annatto (Bixa orellana) seeds. J Agric Food Chem 45:1050–1054. (PMID: 10.1021/jf960412k) Moreira VS, Soares VLF, Silva RJS, Sousa AO, Otoni WC, Costa MGC (2018) Selection and validation of reference genes for quantitative gene expression analyses in various tissues and seeds at different developmental stages in Bixa orellana L. Physiol Mol Biol Plants 24:369–378. (PMID: 10.1007/s12298-018-0528-1296925455911269) Nair RB, Bastress KL, Ruegger MO, Denault JW, Chapple C (2004) The Arabidopsis thaliana REDUCED EPIDERMAL FLUORESCENCE1 gene encodes an aldehyde dehydrogenase involved in ferulic acid and sinapic acid biosynthesis. Plant Cell 16:544–554. (PMID: 10.1105/tpc.01750914729911341923) Ohmiya A (2009) Carotenoid cleavage dioxygenases and their apocarotenoid products in plants. Plant Biotechnol 25:351–358. (PMID: 10.5511/plantbiotechnology.26.351) Peng G, Wang C, Song S, Fu X, Azam M, Grierson D, Xu C (2013) The role of 1-deoxy-d-xylulose-5-phosphate synthase and phytoene synthase gene family in citrus carotenoid accumulation. Plant Physiol Biochem 71:67–76. (PMID: 10.1016/j.plaphy.2013.06.03123883976) Rivera-Madrid R, Burnell J, Aguilar-Espinosa ML, Rodríguez-Ávila NL, Lugo-Cervantes E, Saenz-Carbonell LA (2013) Control of carotenoid gene expression in Bixa orellana L. leaves treated with norflurazon. Plant Mol Biol Rep 31:1422–1432. (PMID: 10.1007/s11105-013-0604-1) Rodríguez-Ávila NL, Narváez-Zapata JA, Ramírez-Benítez JE, Aguilar-Espinosa ML, Rivera-Madrid R (2011) Identification and expression pattern of a new carotenoid cleavage dioxygenase gene member from Bixa orellana. J Exp Bot 62:5385–5395. (PMID: 10.1093/jxb/err201218137963223038) Ronen G, Carmel-Goren L, Zamir D, Hirschberg J (2000) An alternative pathway to β-carotene formation in plant chromoplasts discovered by map-based cloning of Beta and old-gold color mutations in tomato. Proc Natl Acad Sci USA 97:11102–11107. (PMID: 10.1073/pnas.1901774971099546427155) Sahu SS, Loaiza CD, Kaundal R (2020) Plant-mSubP: a computational framework for the prediction of single- and multi-target protein subcellular localization using integrated machine-learning approaches. AoB Plants 12:plz068. (PMID: 10.1093/aobpla/plz06832528639) Saladié M, Wright LP, Garcia-Mas J, Rodríguez-Concepción M, Phillips MA (2014) The 2-C-methylerythritol 4-phosphate pathway in melon is regulated by specialized isoforms for the first and last steps. J Exp Bot 65:5077–5092. (PMID: 10.1093/jxb/eru275250131194144782) Sankari M, Hridya H, Sneha P, Doss CGP, Christopher JG, Mathew J, Zayed H, Ramamoorthy S (2019) Implication of salt stress induces changes in pigment production, antioxidant enzyme activity, and qRT-PCR expression of genes involved in the biosynthetic pathway of Bixa orellana L. Funct Integr Genomics 19:565–574. (PMID: 10.1007/s10142-019-00654-730694406) Soares VLF, Rodrigues SM, de Oliveira TM, de Queiroz TO, Lima LS, Hora-Júnior BT, Gramacho KP, Micheli F, Cascardo JCM, Otoni WC, Gesteira AS, Costa MGC (2011) Unraveling new genes associated with seed development and metabolism in Bixa orellana L. by expressed sequence tag (EST) analysis. Mol Biol Rep 38:1329–1340. (PMID: 10.1007/s11033-010-0234-820563648) Sun T, Yuan H, Cao H, Yazdani M, Tadmor Y, Li L (2018) Carotenoid metabolism in plants: the role of plastids. Mol Plant 11:58–74. (PMID: 10.1016/j.molp.2017.09.01028958604) Tirimanna ASL (1981) Study of the carotenoid pigments of Bixa orellana L. seeds by thin layer chromatography. Microchim Acta 2:11–16. (PMID: 10.1007/BF01197299) Tola AJ, Jaballi A, Germain H, Missihoun TD (2021) Recent development on plant aldehyde dehydrogenase enzymes and their functions in plant development and stress signaling. Genes 12:51. (PMID: 10.3390/genes12010051) Us-Camas R, Aguilar-Espinosa M, Rodríguez-Campos J, Vallejo-Cardona AA, Carballo-Uicab VM, Serrano-Posada H, Rivera-Madrid R (2022) Identifying Bixa orellana L. new carotenoid cleavage dioxygenases 1 and 4 potentially involved in bixin biosynthesis. Front Plant Sci 13:829089. (PMID: 10.3389/fpls.2022.829089352224868874276) Vishnevetsky M, Ovadis M, Vainstein A (1999) Carotenoid sequestration in plants: the role of carotenoid-associated proteins. Trends Plant Sci 4:232–235. (PMID: 10.1016/S1360-1385(99)01414-410366880) Wu S, Watanabe N, Mita S, Ueda Y, Shibuya M, Ebizuka Y (2003) Two o-methyltransferases isolated from flower petals of Rosa chinensis var. spontanea involved in scent biosynthesis. J Biosci Bioeng 96:119–128. (PMID: 10.1016/S1389-1723(03)90113-716233496) Xie J, Deng L, Zhou Y, Yao S, Zeng K (2018) Analysis of changes in volatile constituents and expression of genes involved in terpenoid metabolism in oleocellosis peel. Food Chem 243:269–276. (PMID: 10.1016/j.foodchem.2017.09.14229146338) Yabiku HY, Takahashi MY (1991) Avaliação dos métodos analíticos para determinação da bixina em grãos de urucum e suas correlações. In: Seminário de Corantes Naturais para Alimentos, 2: Simpósio Internacional de Urucum. ITAL/IAC, Campinas, SP, pp 275–279. |
| معلومات مُعتمدة: | 473619/04-04 Conselho Nacional de Desenvolvimento Científico e Tecnológico; 2757/2010 Coordenação de Aperfeiçoamento de Pessoal de Nível Superior; 2004-1-22 Banco do Nordeste do Brasil; APQ- 02372-17 Fundação de Amparo à Pesquisa do Estado de Minas Gerais; APQ-00772-19 Fundação de Amparo à Pesquisa do Estado de Minas Gerais; 00220.1100.787 Universidade Estadual de Santa Cruz |
| فهرسة مساهمة: | Keywords: Apocarotenoids; Bixa orellana; Bixin; Carotenoid; Transcriptome |
| المشرفين على المادة: | 9L7T4VB66G (bixin) 6PQP1V1B6O (annatto) 36-88-4 (Carotenoids) |
| تواريخ الأحداث: | Date Created: 20230214 Date Completed: 20230608 Latest Revision: 20230608 |
| رمز التحديث: | 20230608 |
| DOI: | 10.1007/s00709-023-01842-w |
| PMID: | 36787048 |
| قاعدة البيانات: | MEDLINE |
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Full Text Finder | تدمد: | 1615-6102 |
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| DOI: | 10.1007/s00709-023-01842-w |