Overexpression of a citrus basic helix-loop-helix transcription factor (CubHLH1), which is homologous to Arabidopsis activation-tagged bri1 suppressor 1 interacting factor genes, modulates carotenoid metabolism in transgenic tomato

Plant Science

Volumn 243, Issue , 2016, Pages 35-48

  Endo, Tomoko ^a   Fujii, Hiroshi ^a   Sugiyama, Aiko ^b,c   Nakano, Michiharu ^b,d   Nakajima, Naoko ^a   Ikoma, Yoshinori ^a   Omura, Mitsuo ^b   Shimada, Takehiko ^a  

^a NATIONAL INSTITUTE OF FRUIT TREE SCIENCE   (Japan)

^b SHIZUOKA UNIVERSITY   (Japan)

^c KYOTO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^d HIROSHIMA UNIVERSITY   (Japan)

Author keywords

BHLH; Brassinolide; Carotenoid; Citrus; Light and arabidopsis activation tagged bri1 suppressor 1 interacting factor (AIF); Transcription factor

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CAROTENOID; PLANT PROTEIN;

AMINO ACID SEQUENCE; CITRUS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PHYLOGENY; SEQUENCE ALIGNMENT; TOMATO; TRANSGENIC PLANT;

AMINO ACID SEQUENCE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CAROTENOIDS; CITRUS; GENE EXPRESSION REGULATION, PLANT; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT PROTEINS; PLANTS, GENETICALLY MODIFIED; SEQUENCE ALIGNMENT;

EID: 84949257861     PISSN: 01689452     EISSN: 18732259     Source Type: Journal    
DOI: 10.1016/j.plantsci.2015.11.005     Document Type: Article

References (43)

1. Gross J. Carotenoid Pigment in Fruit 1987, Academic Press, London.
2. Stewart I., Wheaton T.A. Conversion of β-citraurin to reticulataxanthin and β-apo-8'-carotenal to citranaxanthin during the isolation of carotenoids from Citrus. Phytochemistry 1973, 12:2947-2951.
3. Kato M., Ikoma Y., Matsumoto H., Sugiura M., Hyodo H., Yano M. Accumulation of carotenoids and expression of carotenoid biosynthetic genes during maturation in citrus fruit. Plant Physiol. 2004, 134:824-837.
4. Rodrigo M.J., Marcos J.F., Zacarías L. Biochemical and molecular analysis of carotenoid biosynthesis in flavedo of orange (Citrus sinensis L.) during fruit development and maturation. J. Agric. Food Chem. 2004, 52:6724-6731.
5. Goldschmidt E.E., Huberman M., Goren R. Probing the role of endogenous ethylene in the degreening of citrus fruit with ethylene antagonists. Plant Growth Regul. 1993, 12:325-329.
6. Fujii H., Shimada T., Sugiyama A., Nishikawa F., Endo T., Nakano M., Ikoma Y., Shimizu T., Omura M. Profiling ethylene-responsive genes in mature mandarin fruit using c citrus 22K oligoarray. Plant Sci. 2007, 173:340-348.
7. Harpaz-Saad S., Azoulay T., Arazi T., Ben-Yaakov E., Mett A., Shiboleth Y.M., Hö rtensteiner S., Gidoni D., Gal-On A., Goldschmidt E.E., Eyal Y. Chlorophyllase is a rate-limiting enzyme in chlorophyll catabolism and is posttranslationally regulated. Plant Cell 2007, 19:1007-1022.
8. Azoulay-Shemer T., Harpaz-Saad S., Belausov E., Lovat N., Krokhin O., Spicer V., Standing K.G., Goldschmidt E.E., Eyal Y. Citrus chlorophyllase dynamics at ethylene-induced fruit color-break: a study of chlorophyllase expression, posttranslational processing kinetics, and in situ intracellular localization. Plant Physiol. 2008, 148:108-118.
9. Cooper W.C., Henry W.H. Effect of growth regulators on the coloring and abscission in citrus fruit. Isr. J. Agric. Res. 1968, 18:161-174.
10. Fujii H., Shimada T., Sugiyama A., Endo T., Nishikawa F., Nakano M., Ikoma Y., Shimizu T., Omura M. Profiling gibberellin (GA3)-responsive genes in mature mandarin fruit using a citrus 22K oligoarray. Sci. Hortic. 2008, 116:291-298.
11. Harris M.J., Dugger W.M. The occurrence of abscisic acid and abscisyl-β-d-glucopyranoside in developing and mature citrus fruit as determined by enzyme immunoassay. Plant Physiol. 1986, 82:339-345.
12. Rodrigo M.J., Marcos J.F., Alférez F., Mallen M.D., Zacarias L. Characterization of pinalate, a novel citrus sinensis mutant with a fruit-specific alteration that results in yellow pigmentation and decreased ABA content. J. Exp. Bot. 2003, 54:727-738.
13. Zhang L., Ma G., Kato M., Yamawaki K., Takagi T., Kiriiwa Y., Ikoma Y., Matsumoto H., Yoshioka T., Nesumi H. Regulation of carotenoid accumulation and the expression of carotenoid metabolic genes in citrus juice sacs in vitro. J. Exp. Bot. 2012, 63:871-886.
14. Utsunomiya N., Yamada H., Kataoka I., Tomana T. The effect of fruit temperature on the maturation of Satsuma mandarin (Citrus unshiu Marc.) fruits. J. Jpn. Soc. Hortic. Sci. 1982, 51:135-141.
15. Matsumoto H., Ikoma Y., Kato M., Nakajima N., Hasegawa Y. Effect of postharvest temperature and ethylene on carotenoid accumulation in the flavedo and juice sacs of Satsuma mandarin (Citrus unshiu Marc.) fruit. J. Agric. Food Chem. 2009, 57:4724-4732.
16. Ma G., Zhang L., Kato M., Yamawaki K., Kiriiwa Y., Yahata M., Ikoma Y., Matsumoto H. Effect of the combination of ethylene and red LED light irradiation on carotenoid accumulation and carotenogenic gene expressionin the flavedo of citrus fruit. Postharvest Biol. Technol. 2015, 99:99-104.
17. Huff A. Nutritional control of regreening and degreening in citrus peel segments. Plant Physiol. 1983, 73:243-249.
18. Welsch R., Maass D., Voegel T., Dellapenna D., Beyer P. Transcription factor RAP2.2 and its interacting partner SINAT2: stable elements in the carotenogenesis of Arabidopsis leaves. Plant Physiol. 2007, 145:1073-1085.
19. Sugiyama A., Omura M., Shimada T., Fujii H., Endo T., Shimizu T., Nesumi H., Nonaka K., Ikoma Y. Expression quantitative trait loci analysis of carotenoid metabolism-related genes in Citrus. J. Jpn. Soc. Hortic. Sci. 2014, 83:32-43.
20. Wang H., Zhu Y., Fujioka S., Asami T., Li J., Li J. Regulation of Arabidopsis brassinosteroid signaling by atypical basic helix-loop-helix proteins. Plant Cell 2009, 21:3781-3791.
21. Dellaporta S.L., Wood J., Hicks J.B. A plant DNA minipreparation.Version II. Plant Mol. Biol. Rep. 1983, 1:19-21.
22. Ikoma Y., Yano M., Ogawa K., Yoshioka T., Xu Z.C., Hisada S., Omura M., Moriguchi T. Isolation and evaluation of RNA from polysaccharide-rich tissues in fruit for quality by cDNA library construction and RT-PCR. J. Jpn. Soc. Hortic. Sci. 1996, 64:809-814.
23. Fujii H., Kita M., Shimada T., Endo T., Omura M. Expressed sequence tags from citrus albedo at the initiation stage of rind peeling. Bull. Natl. Inst. Fruit Tree Sci. 2003, 2:127-143.
24. Sambrook J., Fritsch E.F., Maniatis T. Molecular Cloning: A Lab Manual 1989, Cold Spring Harbor Laboratory Press, USA.
25. Hisada S., Kita M., Endo-Inagaki T., Omura M., Moriguchi T. Refinement of cDNA clone expression analysis in random sequencing from the rapid cell development phase of citrus fruit. J. Plant Physiol. 1999, 155:699-705.
26. Kobayashi S., Ishimaru M., Hiraoka K., Honda C. Myb-related genes of the Kyoho grape (Vitis labruscana) regulate anthocyanin biosynthesis. Planta 2002, 215:924-933.
27. Sun H.J., Uchii S., Watanabe S., Ezura H. A Highly efficient transformation protocol for micro-tom, a model cultivar for tomato functional genomics. Plant Cell Physiol. 2006, 47:426-431.
28. Shimada S., Shimokawa K. Ethylene-activated chlorophyllase in Satsuma mandarin (Citrus unshiu Mar) fruit. J. Agric. Chem. Soc. Jpn. 1978, 52:489-491. (In Japanese).
29. Kato M., Matsumoto H., Ikoma Y., Okuda H., Yano M. The role of carotenoid cleavage dioxygenases in the regulation of carotenoid profiles during maturation in citrus fruit. J. Exp. Bot. 2006, 57:2153-2164.
30. Huang X.S., Wang W., Zhang Q., Liu J.H. A Basic helix-loop-helix transcription factor, PtrbHLH, of Poncirus trifoliata confers cold tolerance and modulates peroxidase-mediated scavenging of hydrogen peroxide. Plant Physiol. 2013, 162:1178-1194.
31. Nishikawa F., Endo T., Shimada T., Fujii H., Shimizu T., Omura M. Isolation and characterization of a Citrus FT/TFL1 homologue (CuMFT1), which shows quantitatively preferential expression in Citrus seeds. J. Jpn. Soc. Hortic. Sci. 2008, 77:38-46.
32. Mendelova1 A., Fikselová M., Mendel L. Carotenoids and lycopene content in fresh and dried tomato fruits and tomato juice. Acta Univ. Agric. Silvic. Mendelianae Brun. 2013, 61:1329-1337.
33. Isaacson T., Ronen G., Zamir D., Hirschberg J. Cloning of tangerine from tomato reveals a carotenoid isomerase essential for the production of β-carotene and xanthophylls in plants. Plant Cell 2002, 14:333-342.
34. Alquézar B., Rodrigo M.J., Zacarias L. Carotenoid biosynthesis and their regulation in citrus fruit. Tree For. Sci. Biotechnol. 2008, 2:23-35.
35. Toledo-Ortiz G., Huq E., Rodríguez-Concepción M. Direct regulation of phytoene synthase gene expression and carotenoid biosynthesis by phytochrome-interacting factors. Proc. Natl. Acad. Sci. 2010, 107:11626-11631.
36. Ikeda M., Mitsuda N., Ohme-Takagi M. ATBS1 interacting factors negatively regulate Arabidopsis cell elongation in the triantagonistic bHLH system. Plant Signal. Behav. 2013, 8:e23448.
37. Simkin A.J., Schwartz S.H., Auldridge M., Taylor M.G., Klee H.J. The tomato carotenoid cleavage dioxygenase 1 genes contribute to the formation of the flavor volatiles beta-ionone, pseudoionone, and geranylacetone. Plant J. 2004, 40:882-892.
38. Vardhini B.V., Rao S.S. Acceleration of ripening of tomato pericarp discs by brassinosteroids. Phytochemistry 2002, 61:843-847.
39. Liu L., Jia C., Zhang M., Chen D., Chen S., Guo R., Guo D., Wang Q. Ectopic expression of a BZR1-1D transcription factor in brassinosteroid signalling enhances carotenoid accumulation and fruit quality attributes in tomato. Plant Biotechnol. J. 2014, 12:105-115.
40. Castelain M., Le Hir R., Bellini C. The non-DNA-binding bHLH transcription factor PRE3/bHLH135/ATBS1/TMO7 is involved in the regulation of light signaling pathway in Arabidopsis. Physiol. Plant. 2012, 45:450-460.
41. Pizarro L., Stange C. Light-dependent regulation of carotenoid biosynthesis in plants. Cien. Inv. Agr. 2009, 36:143-162.
42. Gao H., Xu J., Liu X., Liu B., Deng X. Light effect on carotenoids production and expression of carotenogenesis genes in citrus callus of four genotypes. Acta Physiol. Plant. 2011, 33:2485-2492.
43. Jeong D.H., Lee S., Kim S.L., Hwang I., An G. Regulation of brassinosteroid responses by Phytochrome B in rice. Plant Cell Environ. 2007, 30:590-599.