|
|
Expression profiles of genes and enzymes related to ascorbic acid metabolism in fruits of Ziziphus jujuba Mill. ‘Jinsixiaozao’ |
Yingying CHEN1,Zhihui ZHAO1,Jin ZHAO2,*(),Mengjun LIU1,*() |
1. Research Center of Chinese Jujube, Agricultural University of Hebei, Baoding 071001, China 2. College of Life Science, Agricultural University of Hebei, Baoding 071000, China |
|
|
Abstract The fruit of Chinese jujube (Ziziphus jujuba) possesses extremely high concentrations of ascorbic acid (AsA). The accumulation of AsA, the expression patterns of the nine genes related to AsA metabolism as well as the activities of five enzymes involved in AsA synthesis, oxidation and recycling were investigated during fruit development in Z. jujuba Mill. ‘Jinsixiaozao’. The results showed that the high level of AsA accumulation in jujube fruit is due to a contribution from both AsA biosynthesis and AsA recycling. It is suggested that L-galactono-1,4-lactone dehydrogenase, ascorbate peroxidase and monodehydro-ascorbate reductase are the crucial genes/enzymes of jujube AsA synthesis, oxidization and recycling, respectively. These results provide useful new insights into the regulatory mechanisms of AsA accumulation in Chinese jujube.
|
Keywords
Chinese jujube
ascorbic acid
metabolism
gene
enzyme
|
Corresponding Author(s):
Jin ZHAO,Mengjun LIU
|
Just Accepted Date: 25 April 2016
Online First Date: 10 May 2016
Issue Date: 05 July 2016
|
|
1 |
Veljovic-Jovanovic S D, Pignocchi C, Noctor G, Foyer C H. Low ascorbic acid in the vtc1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiology, 2001, 127(2): 426–435
https://doi.org/10.1104/pp.010141
|
2 |
Smirnoff N, Conklin P L, Loewus F A. Biosynthesis of ascorbic acid in plants: a renaissance. Annual Review of Plant Biology, 2001, 52(1): 437–467
https://doi.org/10.1146/annurev.arplant.52.1.437
|
3 |
Zhang C, Liu J, Zhang Y, Cai X, Gong P, Zhang J, Wang T, Ye Z. Over expression of SlGMEs leads to ascorbate accumulation with enhanced oxidative stress, cold, and salt tolerance in tomato. Plant Cell Reports, 2011, 30(3): 389–398
https://doi.org/10.1007/s00299-010-0939-0
|
4 |
Barth C, De T M, Conklin P. The role of ascorbic acid in the control of flowering time and the onset of senescence. Journal of Experimental Botany, 2006, 57(8): 1657–1665
https://doi.org/10.1093/jxb/erj198
|
5 |
De Tullio M C, Liso R, Arrigoni O. Ascorbic acid oxidase: an enzyme in search of a role. Biologia Plantarum, 2004, 48(2): 161–166
https://doi.org/10.1023/B:BIOP.0000033439.34635.a6
|
6 |
Davey M W, Montagu M V, Inzé D, Sanmartin M, Kanellis A, Smirnoff N,Benzie I J J, Strain J J, Favell D, Fletcher J. Plant L-ascorbic acid: chemistry, function, metabolism, bioavailability and effects of processing. Journal of the Science of Food and Agriculture, 2000, 80(7): 825–860
https://doi.org/10.1002/(SICI)1097-0010(20000515)80:7<825::AID-JSFA598>3.0.CO;2-6
|
7 |
Gao Y R. Analysis of vitamins in Chinese jujube and wild jujube with high-performance liquid chromatography. Hebei: Agricultural University of Hebei, 2011 (in Chinese)
|
8 |
Wheeler G L, Jones M A, Smirnoff N. The biosynthetic pathway of vitamin C in higher plants. Nature, 1998, 393(6683): 365–369
https://doi.org/10.1038/30728
|
9 |
Wolucka B A, Van Montagu M. GDP-mannose-3′, 5′-epimerase forms GDP-L-gulose, a putative intermediate for the de novo biosynthesis of vitamin C in plants. Journal of Biological Chemistry, 2003, 278(48): 47483–47490
https://doi.org/10.1074/jbc.M309135200
|
10 |
Agius F, González-Lamothe R, Caballero J L, Muñoz-Blanco J, Botella M A, Valpuesta V. Engineering increased vitamin C levels in plants by overexpression of a D-galacturonic acid reductase. Nature Biotechnology, 2003, 21(2): 177–181
https://doi.org/10.1038/nbt777
|
11 |
Lorence A, Chevone B I, Mendes P, Nessler C L. Myo-inositol oxygenase offers a possible entry point into plant ascorbate biosynthesis. Plant Physiology, 2004, 134(3): 1200–1205
https://doi.org/10.1104/pp.103.033936
|
12 |
Dowdle J, Ishikawa T, Gatzek S, Rolinski S, Smirnoff N. Two genes in Arabidopsis thaliana encoding GDP-L-galactose phosphorylase are required for ascorbate biosynthesis and seedling viability. Plant Journal, 2007, 52(4): 673–689
https://doi.org/10.1111/j.1365-313X.2007.03266.x
|
13 |
Imai T, Ban Y, Terakami S, Yamamoto T, Moriguchi T. L-ascorbate biosynthesis in peach: Cloning of six L-galactose pathway related genes and their expression during peach fruit development. Physiologia Plantarum, 2009, 136(2): 139–149
https://doi.org/10.1111/j.1399-3054.2009.01213.x
|
14 |
Li M, Ma F, Guo C, Liu J. Ascorbic acid formation and profiling of genes expressed in its synthesis and recycling in apple leaves of different ages. Plant Physiology and Biochemistry, 2010, 48(4): 216–224
https://doi.org/10.1016/j.plaphy.2010.01.015
|
15 |
Bulley S, Wright M, Rommens C, Yan H, Rassam M, Lin-Wang K, Andre C, Brewster D, Karunairetnam S, Allan A C, Laing W A. Enhancing ascorbate in fruits and tubers through over-expression of the L-galactose pathway gene GDP-L-galactose phosphorylase. Plant Biotechnology Journal, 2012, 10(4): 390–397
https://doi.org/10.1111/j.1467-7652.2011.00668.x
|
16 |
Bulley S M, Rassam M, Hoser D, Otto W, Schünemann N, Wright M, MacRae E, Gleave A, Laing W. Gene expression studies in kiwifruit and gene over-expression in Arabidopsis indicates that GDP-L-galactose guanyltransferase is a major control point of vitamin C biosynthesis. Journal of Experimental Botany, 2009, 60(3): 765–778
https://doi.org/10.1093/jxb/ern327
|
17 |
Li M J, Ma F W, Zhang M, Pu F. Distribution and metabolism of ascorbic acid in apple fruits (Malus domestica Borkh cv Gala). Plant Science, 2008, 174(6): 606–612
https://doi.org/10.1016/j.plantsci.2008.03.008
|
18 |
Cruz-Rus E, Amaya I, Sánchez-Sevilla J F, Botella M A, Valpuesta V. Regulation of L-ascorbic acid content in strawberry fruits. Journal of Experimental Botany, 2011, 62(12): 4191–4201
https://doi.org/10.1093/jxb/err122
|
19 |
Liu M J, Zhao J, Cai Q L, Liu G C, Wang J R, Zhao Z H, Liu P, Dai L, Yan G J, Wang W J, Li X S, Chen Y, Sun Y D, Liu Z G, Lin M J, Xiao J, Chen Y Y, Li X F, Wu B, Ma Y, Jian J B, Yang W, Yuan Z, Sun X C, Wei Y L, Yu L L, Zhang C, Liao S G, He R J, Guang X M, Wang Z, Zhang Y Y, Luo L H. The complex jujube genome provides insights into fruit tree biology. Nature Communications, 2014, 5: 5315
https://doi.org/10.1038/ncomms6315
|
20 |
Xu Q, Chen L, Ruan X, Chen D, Zhu A, Chen C, Bertrand D, Jiao W, Hao B, Lyon M P, Chen J, Gao S, Xing F, Lan H, Chang J, Ge X, Lei Y, Hu Q, Miao Y, Wang L, Xiao S, Biswas M K, Zeng W, Guo F, Cao H, Yang X, Xu X, Cheng Y, Xu J, Liu J, Luo O, Tang Z, Guo W, Kuang H, Zhang H, Roose M, Nagarajan N, Deng X X, Ruan Y. The draft genome of sweet orange (Citrus sinensis). Nature Genetics, 2013, 45(1): 59–66
https://doi.org/10.1038/ng.2472
|
21 |
Huang S, Ding J, Deng D, Tang W, Sun H, Liu D, Zhang L, Niu X, Zhang X, Meng M, Yu J, Liu J, Han Y, Shi W, Zhang D, Cao S, Wei Z, Cui Y, Xia Y, Zeng H, Bao K, Lin L, Min Y, Zhang H, Miao M, Tang X, Zhu Y, Sui Y, Li G, Sun H, Yue J, Sun J, Liu F, Zhou L, Lei L, Zheng X, Liu M, Huang L, Song J, Xu C, Li J, Ye K, Zhong S, Lu B, He G, Xiao F, Wang H, Zheng H, Fei Z, Liu Y. Draft genome of the kiwifruit Actinidia chinensis. Nature Communications, 2013, 4: 2640
https://doi.org/10.1038/ncomms3640
|
22 |
Zhao J, Liu Z C, Dai L, Liu M J. Isolation of total RNA for different organs and tissues of Ziziphus jujuba Mill. Journal of Plant Genetic Resources, 2009, 10: 111–117 (in Chinese)
|
23 |
Sun H F, Meng Y P, Cui G M, Cao Q F, Li J, Liang A H. Selection of housekeeping genes for gene expression studies on the development of fruit bearing shoots in Chinese jujube (Ziziphus jujuba Mill). Molecular Biology Reports, 2009, 36(8): 2183– 2190
https://doi.org/10.1007/s11033-008-9433-y
|
24 |
Livak K J, Schmittgen T D. Analysis of relative gene expression data using Real-Time Quantitative PCR and the 2-DDCT method.Met<?Pub Caret?>hods, 2001, 25(4): 402–408
https://doi.org/10.1006/meth.2001.1262
|
25 |
An H M. Physiological mechanism of accumulating high level ascorbic acid and molecular cloning and expression of its key biosynthetic enyzme in Rosa roxburghii Tratt. Zhejiang: Zhejiang University, 2004 (in Chinese)
|
26 |
Esaka M, Hattori T, Fujisawa K, Sakajo S, Asahi T. Molecular cloning and nucleotide sequence of full-length cDNA for ascorbate oxidase from cultured pumpkin cells. European Journal of Biochemistry, 1990, 191(3): 537–541
https://doi.org/10.1111/j.1432-1033.1990.tb19154.x
|
27 |
De Pinto M C, Francis D, De Gara L. The redox state of the ascorbate-dehydroascorbate pair as a specific sensor of cell division in tobacco BY-2 cells. Protoplasma, 1999, 209(1–2): 90–97
https://doi.org/10.1007/BF01415704
|
28 |
Imai T, Ban Y, Terakami S, Yamamoto T, Moriguchi T. L-Ascorbate biosynthesis in peach: cloning of six L-galactose pathway-related genes and their expression during peach fruit development. Physiologia Plantarum, 2009, 136(2): 139–149
https://doi.org/10.1111/j.1399-3054.2009.01213.x
|
29 |
Gournas C, Papageorgiou I, Diallinas G. The nucleobase-ascorbate transporter (NAT) family: genomics, evolution, structure-function relationships and physiological role. Molecular BioSystems, 2008, 4(5): 404–416
https://doi.org/10.1039/b719777b
|
30 |
Bulley S M, Rassam M, Hoser D, Otto W, Schünemann N, Wright M, MacRae E, Gleave A, Laing W. Gene expression studies in kiwifruit and gene over-expression in Arabidopsis indicates that GDP-L-galactose guanyltransferase is a major control point of vitamin C biosynthesis. Journal of Experimental Botany, 2009, 60(3): 765–778
https://doi.org/10.1093/jxb/ern327
|
31 |
Cruz-Rus E, Botella M A, Valpuesta V, Gomez-Jimenez M C. Analysis of genes involved in L-ascorbic acid biosynthesis during growth and ripening of grape berries. Journal of Plant Physiology, 2010, 167(9): 739–748
https://doi.org/10.1016/j.jplph.2009.12.017
|
32 |
Ioannidi E, Kalamaki M S, Engineer C, Pateraki I, Alexandrou D, Mellidou I, Giovannonni J, Kanellis A K. Expression profiling of ascorbic acid-related genes during tomato fruit development and ripening and in response to stress conditions. Journal of Experimental Botany, 2009, 60(2): 663–678
https://doi.org/10.1093/jxb/ern322
|
33 |
Cruz-Rus E, Amaya I, Sánchez-Sevilla J F, Botella M A, Valpuesta V. Regulation of L-ascorbic acid content in strawberry fruits. Journal of Experimental Botany, 2011, 62(12): 4191–4201
https://doi.org/10.1093/jxb/err122
|
34 |
Lunde C, Baumann U, Shirley N J, Drew D P, Fincher G B. Gene structure and expression pattern analysis of three monodehydroascorbate reductase (MDHAR) genes in Physcomitrella patens: implications for the evolution of the MDHAR family in plants. Plant Molecular Biology, 2006, 60(2): 259–275
https://doi.org/10.1007/s11103-005-3881-8
|
35 |
Alhagdow M, Mounet F, Gilbert L, Nunes-Nesi A, Garcia V, Just D, Petit J, Beauvoit B, Fernie A R, Rothan C, Baldet P. Silencing of the mitochondrial ascorbate synthesizing enzyme L-galactono-1,4-lactone dehydrogenase affects plant and fruit development in tomato. Plant Physiology, 2007, 145(4): 1408–1422
https://doi.org/10.1104/pp.107.106500
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|