A single amino acid substitution in an ORANGE protein promotes carotenoid overaccumulation in arabidopsis

Plant Physiology

Volumn 169, Issue 1, 2015, Pages 421-431

  Yuan, Hui ^a   Owsiany, Katherine ^a   Sheeja, T E ^a   Zhou, Xiangjun ^a   Rodriguez, Caroline ^a   Li, Yongxi ^c   Welsch, Ralf ^d   Chayut, Noam ^e   Yang, Yong ^a   Thannhauser, Theodore W ^a   Parthasarathy, Mandayam V ^a   Xu, Qiang ^c   Deng, Xiuxin ^c   Fei, Zhangjun ^b   Schaffer, Ari ^e   Katzir, Nurit ^e   Burger, Joseph ^e   Tadmor, Yaakov ^e   Li, Li ^a  

^a Department of Obstetrics Gynecology   (United States)

^b United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^c HUAZHONG AGRICULTURAL UNIVERSITY   (China)

^d UNIVERSITY OF FREIBURG   (Germany)

^e VOLCANI CENTER   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; CAROTENOID;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARABIDOPSIS; BIOSYNTHESIS; CHEMISTRY; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR GENETICS; PLASTID; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT; TRANSGENIC PLANT; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOSYNTHETIC PATHWAYS; CAROTENOIDS; GENE EXPRESSION REGULATION, PLANT; MOLECULAR SEQUENCE DATA; PLANTS, GENETICALLY MODIFIED; PLASTIDS; PROTEIN TRANSPORT; SEQUENCE ALIGNMENT;

EID: 84940913786     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.15.00971     Document Type: Article

References (54)

1. Auldridge ME, McCarty DR, Klee HJ (2006) Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol 9: 315-321
2. Bai C, Rivera SM, Medina V, Alves R, Vilaprinyo E, Sorribas A, Canela R, Capell T, Sandmann G, Christou P, et al. (2014) An in vitro system for the rapid functional characterization of genes involved in carotenoid biosynthesis and accumulation. Plant J 77: 464-475
3. Betts MJ, Russell RB (2003) Amino acid properties and consequences of substitutions. In MR Barnes, IC Gray, eds, Bioinformatics for Geneticists. John Wiley & Sons, Ltd., Chichester, UK, pp 289-316
4. Cao H, Zhang J, Xu J, Ye J, Yun Z, Xu Q, Xu J, Deng X (2012) Comprehending crystalline b-carotene accumulation by comparing engineered cell models and the natural carotenoid-rich system of citrus. J Exp Bot 63: 4403-4417
5. Cazzonelli CI (2011) Carotenoids in nature : insights from plants and beyond. Funct Plant Biol 38: 833-847
6. Cazzonelli CI, Pogson BJ (2010) Source to sink: regulation of carotenoid biosynthesis in plants. Trends Plant Sci 15: 266-274
7. Diretto G, Welsch R, Tavazza R, Mourgues F, Pizzichini D, Beyer P, Giuliano G (2007) Silencing of beta-carotene hydroxylase increases total carotenoid and beta-carotene levels in potato tubers. BMC Plant Biol 7: 11
8. Domonkos I, Kis M, Gombos Z, Ughy B (2013) Carotenoids, versatile components of oxygenic photosynthesis. Prog Lipid Res 52: 539-561
9. Ducreux LJM, Morris WL, Hedley PE, Shepherd T, Davies HV, Millam S, Taylor MA (2005) Metabolic engineering of high carotenoid potato tubers containing enhanced levels of beta-carotene and lutein. J Exp Bot 56: 81-89
10. Egea I, Barsan C, Bian W, Purgatto E, Latché A, Chervin C, Bouzayen M, Pech JC (2010) Chromoplast differentiation: current status and perspectives. Plant Cell Physiol 51: 1601-1611
11. Farré G, Bai C, Twyman RM, Capell T, Christou P, Zhu C (2011) Nutritious crops producing multiple carotenoids-a metabolic balancing act. Trends Plant Sci 16: 532-540
12. Fraser PD, Bramley PM (2004) The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res 43: 228-265
13. Fraser PD, Romer S, Shipton CA, Mills PB, Kiano JW, Misawa N, Drake RG, Schuch W, Bramley PM (2002) Evaluation of transgenic tomato plants expressing an additional phytoene synthase in a fruit-specific manner. Proc Natl Acad Sci USA 99: 1092-1097
14. Galpaz N, Wang Q, Menda N, Zamir D, Hirschberg J (2008) Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J 53: 717-730
15. Giuliano G, Tavazza R, Diretto G, Beyer P, Taylor MA (2008) Metabolic engineering of carotenoid biosynthesis in plants. Trends Biotechnol 26: 139-145
16. Harjes CE, Rocheford TR, Bai L, Brutnell TP, Kandianis CB, Sowinski SG, Stapleton AE, Vallabhaneni R, Williams M, Wurtzel ET, et al. (2008) Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319: 330-333
17. Hirschberg J (2001) Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol 4: 210-218
18. Hugueney P, Bouvier F, Badillo A, d’Harlingue A, Kuntz M, Camara B (1995) Identification of a plastid protein involved in vesicle fusion and/or membrane protein translocation. Proc Natl Acad Sci USA 92: 5630-5634
19. Kilambi HV, Kumar R, Sharma R, Sreelakshmi Y (2013) Chromoplast-specific carotenoid-associated protein appears to be important for enhanced accumulation of carotenoids in hp1 tomato fruits. Plant Physiol 161: 2085-2101
20. Kim SH, Ahn YO, Ahn MJ, Jeong JC, Lee HS, Kwak SS (2013) Cloning and characterization of an Orange gene that increases carotenoid accumulation and salt stress tolerance in transgenic sweetpotato cultures. Plant Physiol Biochem 70: 445-454
21. Kolotilin I, Koltai H, Tadmor Y, Bar-Or C, Reuveni M, Meir A, Nahon S, Shlomo H, Chen L, Levin I (2007) Transcriptional profiling of high pigment-2dg tomato mutant links early fruit plastid biogenesis with its overproduction of phytonutrients. Plant Physiol 145: 389-401
22. Li L, Lu S, Cosman KM, Earle ED, Garvin DF, O’Neill J (2006) b-Carotene accumulation induced by the cauliflower Or gene is not due to an increased capacity of biosynthesis. Phytochemistry 67: 1177-1184
23. Li L, Paolillo DJ, Parthasarathy MV, Dimuzio EM, Garvin DF (2001) A novel gene mutation that confers abnormal patterns of b-carotene accumulation in cauliflower (Brassica oleracea var. botrytis). Plant J 26: 59-67
24. Li L, Van Eck J (2007) Metabolic engineering of carotenoid accumulation by creating a metabolic sink. Transgenic Res 16: 581-585
25. Li L, Yang Y, Xu Q, Owsiany K, Welsch R, Chitchumroonchokchai C, Lu S, Van Eck J, Deng XX, Failla M, et al. (2012) The Or gene enhances carotenoid accumulation and stability during post-harvest storage of potato tubers. Mol Plant 5: 339-352
26. Li L, Yuan H (2013) Chromoplast biogenesis and carotenoid accumulation. Arch Biochem Biophys 539: 102-109
27. Liu Y, Roof S, Ye Z, Barry C, van Tuinen A, Vrebalov J, Bowler C, Giovannoni J (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101: 9897-9902
28. Lopez AB, Van Eck J, Conlin BJ, Paolillo DJ, O’Neill J, Li L (2008) Effect of the cauliflower Or transgene on carotenoid accumulation and chromoplast formation in transgenic potato tubers. J Exp Bot 59: 213-223
29. Lu S, Li L (2008) Carotenoid metabolism: biosynthesis, regulation, and beyond. J Integr Plant Biol 50: 778-785
30. Lu S, Van Eck J, Zhou X, Lopez AB, O’Halloran DM, Cosman KM, Conlin BJ, Paolillo DJ, Garvin DF, Vrebalov J, et al (2006) The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of b-carotene accumulation. Plant Cell 18: 3594-3605
31. Lyi SM, Zhou X, Kochian LV, Li L (2007) Biochemical and molecular characterization of the homocysteine S-methyltransferase from broccoli (Brassica oleracea var. italica). Phytochemistry 68: 1112-1119
32. Maass D, Arango J, Wüst F, Beyer P, Welsch R (2009) Carotenoid crystal formation in Arabidopsis and carrot roots caused by increased phytoene synthase protein levels. PLoS One 4: e6373
33. Moise AR, Al-Babili S, Wurtzel ET (2014) Mechanistic aspects of carotenoid biosynthesis. Chem Rev 114: 164-193
34. Naqvi S, Zhu C, Farre G, Ramessar K, Bassie L, Breitenbach J, Perez Conesa D, Ros G, Sandmann G, Capell T, et al. (2009) Transgenic multivitamin corn through biofortification of endosperm with three vitamins representing three distinct metabolic pathways. Proc Natl Acad Sci USA 106: 7762-7767
35. Nisar N, Li L, Lu S, Khin NC, Pogson BJ (2015) Carotenoid metabolism in plants. Mol Plant 8: 68-82
36. Niyogi KK (1999) Photoprotection revisited: Genetic and molecular approaches. Annu Rev Plant Physiol Plant Mol Biol 50: 333-359
37. Paine JA, Shipton CA, Chaggar S, Howells RM, Kennedy MJ, Vernon G, Wright SY, Hinchliffe E, Adams JL, Silverstone AL, et al. (2005) Improving the nutritional value of Golden Rice through increased provitamin A content. Nat Biotechnol 23: 482-487
38. Paolillo DJ Jr, Garvin DF, Parthasarathy MV (2004) The chromoplasts of Or mutants of cauliflower (Brassica oleracea L. var. botrytis). Protoplasma 224: 245-253
39. Park SC, Kim SH, Park S, Lee HU, Lee JS, Park WS, Ahn MJ, Kim YH, Jeong JC, Lee HS, et al. (2015) Enhanced accumulation of carotenoids in sweetpotato plants overexpressing IbOr-Ins gene in purple-fleshed sweetpotato cultivar. Plant Physiol Biochem 86: 82-90
40. Pogliani L (1994) Structure property relationships of amino acids and some dipeptides. Amino Acids 6: 141-153
41. Rabbani S, Beyer P, Lintig J, Hugueney P, Kleinig H (1998) Induced b-carotene synthesis driven by triacylglycerol deposition in the unicellular alga Dunaliella bardawil. Plant Physiol 116: 1239-1248
42. Rao AV, Rao LG (2007) Carotenoids and human health. Pharmacol Res 55: 207-216
43. Ruiz-Sola MÁ, Rodríguez-Concepción M (2012) Carotenoid biosynthesis in Arabidopsis: a colorful pathway. Arabidopsis Book 10: e0158
44. Sander JD, Joung JK (2014) CRISPR-Cas systems for editing, regulating and targeting genomes. Nat Biotechnol 32: 347-355
45. Shumskaya M, Bradbury LMT, Monaco RR, Wurtzel ET (2012) Plastid localization of the key carotenoid enzyme phytoene synthase is altered by isozyme, allelic variation, and activity. Plant Cell 24: 3725-3741
46. Tzuri G, Zhou X, Chayut N, Yuan H, Portnoy V, Meir A, Sa’ar U, Baumkoler F, Mazourek M, Lewinsohn E, et al (2015) A ‘golden’ SNP in CmOr governs the fruit flesh color of melon (Cucumis melo). Plant J 82: 267-279
47. Walter MH, Strack D (2011) Carotenoids and their cleavage products: biosynthesis and functions. Nat Prod Rep 28: 663-692
48. Welsch R, Arango J, Bär C, Salazar B, Al-Babili S, Beltrán J, Chavarriaga P, Ceballos H, Tohme J, Beyer P (2010) Provitamin A accumulation in cassava (Manihot esculenta) roots driven by a single nucleotide polymorphism in a phytoene synthase gene. Plant Cell 22: 3348-3356
49. Yan J, Kandianis CB, Harjes CE, Bai L, Kim EH, Yang X, Skinner DJ, Fu Z, Mitchell S, Li Q, et al (2010) Rare genetic variation at Zea mays crtRB1 increases beta-carotene in maize grain. Nat Genet 42: 322-327
50. Yang Y, Thannhauser TW, Li L, Zhang S (2007) Development of an integrated approach for evaluation of 2-D gel image analysis: impact of multiple proteins in single spots on comparative proteomics in conventional 2-D gel/MALDI workflow. Electrophoresis 28: 2080-2094
51. Yuan H, Zhang J, Nageswaran D, Li L (2015) Carotenoid metabolism and regulation in horticultural crops. Hortic Res (in press)
52. Zhou X, McQuinn R, Fei Z, Wolters AM, Van Eck J, Brown C, Giovannoni JJ, Li L (2011) Regulatory control of high levels of carotenoid accumulation in potato tubers. Plant Cell Environ 34: 1020-1030
53. Zhou X, Welsch R, Yang Y, Álvarez D, Riediger M, Yuan H, Fish T, Liu J, Thannhauser TW, Li L (2015) Arabidopsis OR proteins are the major posttranscriptional regulators of phytoene synthase in controlling carotenoid biosynthesis. Proc Natl Acad Sci USA 112: 3558-3563
54. Zhu C, Bai C, Sanahuja G, Yuan D, Farré G, Naqvi S, Shi L, Capell T, Christou P (2010) The regulation of carotenoid pigmentation in flowers. Arch Biochem Biophys 504: 132-141