Comparative analysis of carotenoid accumulation in two goji (Lycium barbarum L. and L. ruthenicumMurr.) fruits

Cazzonelli CI: Goldacre review: carotenoids in nature: insights from plants and beyond. Funct Plant Biol. 2011, 38: 833-847. 10.1071/FP11192.

Frank HA, Cogdell RJ: Carotenoids in photosynthesis. Photochem Photobiol. 2008, 63: 257-264. 10.1111/j.1751-1097.1996.tb03022.x.

Tanaka Y, Sasaki N, Ohmiya A: Biosynthesis of plant pigments: anthocyanins, betalains and carotenoids. Plant J. 2008, 54: 733-749. 10.1111/j.1365-313X.2008.03447.x.

Grotewold E: The genetics and biochemistry of floral pigments. Annu Rev Plant Biol. 2006, 57: 761-780. 10.1146/annurev.arplant.57.032905.105248.

Xie X, Yoneyama K: The strigolactone story. Annu Rev Phytopathol. 2010, 48: 93-117. 10.1146/annurev-phyto-073009-114453.

Walter MH, Floss DS, Strack D: Apocarotenoids: hormones, mycorrhizal metabolites and aroma volatiles. Planta. 2010, 232: 1-17. 10.1007/s00425-010-1156-3.

Parry AD, Horgan R: Carotenoids and abscisic acid (ABA) biosynthesis in higher plants. Physiol Plant. 2006, 82: 320-326. 10.1111/j.1399-3054.1991.tb00100.x.

Havaux M: Carotenoid oxidation products as stress signals in plants. Plant J. 2014, 79 (4): 597-606. 10.1111/tpj.12386.

Rao A, Rao L: Carotenoids and human health. Pharmacol Res. 2007, 55: 207-216. 10.1016/j.phrs.2007.01.012.

Fraser PD, Bramley PM: The biosynthesis and nutritional uses of carotenoids. Prog Lipid Res. 2004, 43: 228-265. 10.1016/j.plipres.2003.10.002.

Weber D, Grune T: The contribution of β-carotene to vitamin A supply of humans. Mol Nutr Food Res. 2012, 56: 251-258. 10.1002/mnfr.201100230.

Sabour-Pickett S, Nolan JM, Loughman J, Beatty S: A review of the evidence germane to the putative protective role of the macular carotenoids for age-related macular degeneration. Mol Nutr Food Res. 2012, 56: 270-286. 10.1002/mnfr.201100219.

Ruiz-Sola M, Rodrguez-Concepcin M: Carotenoid biosynthesis in Arabidopsis: A colorful pathway. The Arabidopsis Book. Edited by: Torii K. The American Society of Plant Biologists, Rockville. 2012, e0158-

R Mer S, Fraser PD: Recent advances in carotenoid biosynthesis, regulation and manipulation. Planta. 2005, 221: 305-308. 10.1007/s00425-005-1533-5.

Hirschberg J: Carotenoid biosynthesis in flowering plants. Curr Opin Plant Biol. 2001, 4: 210-218. 10.1016/S1369-5266(00)00163-1.

Ohmiya A: Qualitative and quantitative control of carotenoid accumulation in flower petals. Sci Hortic. 2013, 163: 10-19. 10.1016/j.scienta.2013.06.018.

Hannoufa A, Hossain Z: Regulation of carotenoid accumulation in plants. Biocatal Agric Biotechnol. 2012, 1: 198-202.

Galpaz N, Ronen G, Khalfa Z, Zamir D, Hirschberg J: A chromoplast-specific carotenoid biosynthesis pathway is revealed by cloning of the tomato white-flower locus. Plant Cell. 2006, 18: 1947-1960. 10.1105/tpc.105.039966.

Ronen G, Carmel-Goren L, Zamir D, Hirschberg J: 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 U S A. 2000, 97: 11102-11107. 10.1073/pnas.190177497.

Ronen G, Cohen M, Zamir D, Hirschberg J: Regulation of carotenoid biosynthesis during tomato fruit development: expression of the gene for lycopene epsilon-cyclase is down-regulated during ripening and is elevated in the mutant Delta . Plant J. 1999, 17: 341-351. 10.1046/j.1365-313X.1999.00381.x.

Giuliano G, Bartley GE, Scolnik PA: Regulation of carotenoid biosynthesis during tomato development. Plant Cell. 1993, 5: 379-387. 10.1105/tpc.5.4.379.

Ohmiya A: Carotenoid cleavage dioxygenases and their apocarotenoid products in plants. Plant Biotechnol. 2009, 26: 351-358. 10.5511/plantbiotechnology.26.351.

Ohmiya A, Kishimoto S, Aida R, Yoshioka S, Sumitomo K: Carotenoid cleavage dioxygenase (CmCCD4a) contributes to white color formation in chrysanthemum petals. Plant Physiol. 2006, 142: 1193-1201. 10.1104/pp.106.087130.

Adami M, De Franceschi P, Brandi F, Liverani A, Giovannini D, Rosati C, Dondini L, Tartarini S: Identifying a carotenoid cleavage dioxygenase (ccd4) gene controlling Yellow/White fruit flesh color of peach. Plant Mol Biol Rep. 2013, 31: 1166-1175. 10.1007/s11105-013-0628-6.

Brandi F, Bar E, Mourgues F, Horvth G, Turcsi E, Giuliano G, Liverani A, Tartarini S, Lewinsohn E, Rosati C: Study of Redhaven peach and its white-fleshed mutant suggests a key role of CCD4 carotenoid dioxygenase in carotenoid and norisoprenoid volatile metabolism. BMC Plant Biol. 2011, 11: 24-10.1186/1471-2229-11-24.

Campbell R, Ducreux LJ, Morris WL, Morris JA, Suttle JC, Ramsay G, Bryan GJ, Hedley PE, Taylor MA: The metabolic and developmental roles of carotenoid cleavage dioxygenase4 from potato. Plant Physiol. 2010, 154: 656-664. 10.1104/pp.110.158733.

Lu S, Van Eck J, Zhou X, Lopez AB, O halloran DM, Cosman KM, Conlin BJ, Paolillo DJ, Garvin DF, Vrebalov J: The cauliflower Or gene encodes a DnaJ cysteine-rich domain-containing protein that mediates high levels of β-carotene accumulation. Plant Cell. 2006, 18: 3594-3605. 10.1105/tpc.106.046417.

Wang Y, Yang Y, Fei Z, Yuan H, Fish T, Thannhauser TW, Mazourek M, Kochian LV, Wang X, Li L: Proteomic analysis of chromoplasts from six crop species reveals insights into chromoplast function and development. J Exp Bot. 2013, 64 (4): 949-961. 10.1093/jxb/ers375.

Cookson P, Kiano J, Shipton C, Fraser P, Romer S, Schuch W, Bramley P, Pyke K: Increases in cell elongation, plastid compartment size and phytoene synthase activity underlie the phenotype of the high pigment-1 mutant of tomato. Planta. 2003, 217: 896-903. 10.1007/s00425-003-1065-9.

Davuluri GR, Van Tuinen A, Fraser PD, Manfredonia A, Newman R, Burgess D, Brummell DA, King SR, Palys J, Uhlig J: Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nat Biotechnol. 2005, 23: 890-895. 10.1038/nbt1108.

Mustilli AC, Fenzi F, Ciliento R, Alfano F, Bowler C: Phenotype of the tomato high pigment-2 mutant is caused by a mutation in the tomato homolog of DEETIOLATED1 . Plant Cell. 1999, 11: 145-157. 10.1105/tpc.11.2.145.

Wang S, Liu J, Feng Y, Niu X, Giovannoni J, Liu Y: Altered plastid levels and potential for improved fruit nutrient content by downregulation of the tomato DDB1-interacting protein CUL4. Plant J. 2008, 55: 89-103. 10.1111/j.1365-313X.2008.03489.x.

Liu Y, Roof S, Ye Z, Barry C, Van Tuinen A, Vrebalov J, Bowler C, Giovannoni J: Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci U S A. 2004, 101: 9897-9902. 10.1073/pnas.0400935101.

Giliberto L, Perrotta G, Pallara P, Weller JL, Fraser PD, Bramley PM, Fiore A, Tavazza M, Giuliano G: Manipulation of the blue light photoreceptor cryptochrome 2 in tomato affects vegetative development, flowering time, and fruit antioxidant content. Plant Physiol. 2005, 137: 199-208. 10.1104/pp.104.051987.

Powell AL, Nguyen CV, Hill T, Cheng KL, Figueroa-Balderas R, Aktas H, Ashrafi H, Pons C, Fernndez-Muoz R, Vicente A: Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science. 2012, 336: 1711-1715. 10.1126/science.1222218.

Pan Y, Bradley G, Pyke K, Ball G, Lu C, Fray R, Marshall A, Jayasuta S, Baxter C, Van Wijk R: Network inference analysis identifies an APRR2-like gene linked to pigment accumulation in tomato and pepper fruits. Plant Physiol. 2013, 161: 1476-1485. 10.1104/pp.112.212654.

Azari R, Tadmor Y, Meir A, Reuveni M, Evenor D, Nahon S, Shlomo H, Chen L, Levin I: Light signaling genes and their manipulation towards modulation of phytonutrient content in tomato fruits. Biotechnol Adv. 2010, 28: 108-118. 10.1016/j.biotechadv.2009.10.003.

Potterat O: Goji (Lycium barbarum and L. chinense): phytochemistry, pharmacology and safety in the perspective of traditional uses and recent popularity. Planta Med. 2010, 76: 7-19. 10.1055/s-0029-1186218.

Chang RC-C, So K-F: Use of anti-aging herbal medicine, Lycium barbarum, against aging-associated diseases. What do we know so far?. Cell Mol Neurobiol. 2008, 28: 643-652. 10.1007/s10571-007-9181-x.

Yao X, Peng Y, Xu LJ, Li L, Wu QL, Xiao PG: Phytochemical and biological studies of Lycium medicinal plants. Chem Biodivers. 2011, 8: 976-1010. 10.1002/cbdv.201000018.

Wang C, Chang S, Inbaraj BS, Chen B: Isolation of carotenoids, flavonoids and polysaccharides from Lycium barbarum L. and evaluation of antioxidant activity. Food Chem. 2010, 120: 184-192. 10.1016/j.foodchem.2009.10.005.

Zheng J, Ding C, Wang L, Li G, Shi J, Li H, Wang H, Suo Y: Anthocyanins composition and antioxidant activity of wild Lycium ruthenicum Murr. from Qinghai-Tibet Plateau. Food Chem. 2011, 126: 859-865. 10.1016/j.foodchem.2010.11.052.

Peng Q, Song J, Lv X, Wang Z, Huang L, Du Y: Structural Characterization of an Arabinogalactan-Protein from the Fruits of Lycium ruthenicum . J Agric Food Chem. 2012, 60: 9424-9429. 10.1021/jf302619c.

Altintas A, Kosar M, Kirimer N, Baser K, Demirci B: Composition of the essential oils of Lycium barbarum and L. ruthenicum fruits. Chem Nat Compd. 2006, 42: 24-25. 10.1007/s10600-006-0028-3.

Zeng S, Wu M, Zou C, Liu X, Shen X, Hayward A, Liu C, Wang Y: Comparative analysis of anthocyanin biosynthesis during fruit development in two Lycium species. Physiol Plant. 2014, 150 (4): 505-516. 10.1111/ppl.12131.

Inbaraj BS, Lu H, Hung CF, Wu WB, Lin CL, Chen BH: Determination of carotenoids and their esters in fruits of Lycium barbarum Linnaeus by HPLC-DAD-APCI-MS. J Pharm Biomed Anal. 2008, 47: 812-818. 10.1016/j.jpba.2008.04.001.

Lois LM, Rodrguez-Concepcin M, Gallego F, Campos N, Boronat A: Carotenoid biosynthesis during tomato fruit development: regulatory role of 1-deoxy-d-xylulose 5-phosphate synthase. Plant J. 2000, 22: 503-513. 10.1046/j.1365-313x.2000.00764.x.

Ikoma Y, Matsumoto H, Kato M: The characteristics of carotenoid biosynthesis in Citrus fruit. Jpn Agric Res Q. 2014, 48: 9-16. 10.6090/jarq.48.9.

Li Q, Farre G, Naqvi S, Breitenbach J, Sanahuja G, Bai C, Sandmann G, Capell T, Christou P, Zhu C: Cloning and functional characterization of the maize carotenoid isomerase and β-carotene hydroxylase genes and their regulation during endosperm maturation. Transgenic Res. 2010, 19: 1053-1068. 10.1007/s11248-010-9381-x.

Li L, Yuan H: Chromoplast biogenesis and carotenoid accumulation. Arch Biochem Biophys. 2013, 539: 102-109. 10.1016/j.abb.2013.07.002.

Bai C, Rivera SM, Medina V, Alves R, Vilaprinyo E, Sorribas A, Canela R, Capell T, Sandmann G, Christou P: An in vitro system for the rapid functional characterization of genes involved in carotenoid biosynthesis and accumulation. Plant J. 2014, 77: 464-475. 10.1111/tpj.12384.

Kilambi HV, Kumar R, Sharma R, Sreelakshmi Y: Chromoplast specific carotenoid associated protein appears to be important for enhanced accumulation of carotenoids in hp1 tomato fruits. Plant Physiol. 2013, 161: 2085-2101. 10.1104/pp.112.212191.

Neta-Sharir I, Isaacson T, Lurie S, Weiss D: Dual role for tomato heat shock protein 21: protecting photosystem II from oxidative stress and promoting color changes during fruit maturation. Plant Cell. 2005, 17: 1829-1838. 10.1105/tpc.105.031914.

Derure J, Romer S, D harlingue A, Backhaus RA, Kuntz M, Camara B: Fibril assembly and carotenoid overaccumulation in chromoplasts: a model for supramolecular lipoprotein structures. Plant Cell. 1994, 6: 119-133. 10.1105/tpc.6.1.119.

Vishnevetsky M, Ovadis M, Vainstein A: Carotenoid sequestration in plants: the role of carotenoid-associated proteins. Trends Plant Sci. 1999, 4: 232-235. 10.1016/S1360-1385(99)01414-4.

Fernndez-Orozco R, Gallardo-Guerrero L, Hornero-Mndez D: Carotenoid profiling in tubers of different potato (Solanum sp) cultivars: Accumulation of carotenoids mediated by xanthophyll esterification. Food Chem. 2013, 141: 2864-2872. 10.1016/j.foodchem.2013.05.016.

Delgado-Pelayo R, Gallardo-Guerrero L, Hornero-Mndez D: Chlorophyll and carotenoid pigments in the peel and flesh of commercial apple fruits varieties. Food Res Int 2014. doi:10.1016/j.foodres.2014.03.025.,

Bramley PM: Regulation of carotenoid formation during tomato fruit ripening and development. J Exp Bot. 2002, 53: 2107-2113. 10.1093/jxb/erf059.

Paetzold H, Garms S, Bartram S, Wieczorek J, Urs-Gracia E-M, Rodrguez-Concepcin M, Boland W, Strack D, Hause B, Walter MH: The isogene 1-deoxy-D-xylulose 5-phosphate synthase 2 controls isoprenoid profiles, precursor pathway allocation, and density of tomato trichomes. Mol Plant. 2010, 3: 904-916. 10.1093/mp/ssq032.

Walter MH, Hans J, Strack D: Two distantly related genes encoding 1-deoxy-d-xylulose 5-phosphate synthases: differential regulation in shoots and apocarotenoid-accumulating mycorrhizal roots. Plant J. 2002, 31: 243-254. 10.1046/j.1365-313X.2002.01352.x.

Stigliani AL, Giorio G, DAmbrosio C: Characterization of P450 carotenoid β-and ε-hydroxylases of tomato and transcriptional regulation of xanthophyll biosynthesis in root, leaf, petal and fruit. Plant Cell Physiol. 2011, 52: 851-865. 10.1093/pcp/pcr037.

Auldridge ME, McCarty DR, Klee HJ: Plant carotenoid cleavage oxygenases and their apocarotenoid products. Curr Opin Plant Biol. 2006, 9: 315-321. 10.1016/j.pbi.2006.03.005.

Tan BC, Joseph LM, Deng WT, Liu L, Li QB, Cline K, McCarty DR: Molecular characterization of the Arabidopsis 9-cis epoxycarotenoid dioxygenase gene family. Plant J. 2003, 35: 44-56. 10.1046/j.1365-313X.2003.01786.x.

Huang F-C, Molnr P, Schwab W: Cloning and functional characterization of carotenoid cleavage dioxygenase 4 genes. J Exp Bot. 2009, 60: 3011-3022. 10.1093/jxb/erp137.

Rozen S, Skaletsky H: Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol. 2000, 132: 365-386.

Lyi SM, Zhou X, Kochian LV, Li L: Biochemical and molecular characterization of the homocysteine S-methyltransferase from broccoli (Brassica oleracea var. italica). Phytochemistry. 2007, 68: 1112-1119. 10.1016/j.phytochem.2007.02.007.

Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol. 2011, 28: 2731-2739. 10.1093/molbev/msr121.

Saitou N, Nei M: The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987, 4: 406-425.