Transcriptome analysis of a spontaneous mutant in sweet orange [Citrus sinensis (L.) Osbeck] during fruit development

Journal of Experimental Botany

Volumn 60, Issue 3, 2009, Pages 801-813

  Liu, Qing ^a   Zhu, Andan ^a   Chai, Lijun ^a   Zhou, Wenjing ^a   Yu, Keqin ^a   Ding, Jian ^a   Xu, Juan ^a   Deng, Xiuxin ^a  

^a HUAZHONG AGRICULTURAL UNIVERSITY   (China)

Author keywords

Bud mutation; Candidate genes; cDNA microarray; Citrus; Real time RT PCR; Suppression subtractive hybridization (SSH)

Indexed keywords

PYRUVIC ACID DERIVATIVE; VEGETABLE PROTEIN;

ARTICLE; CLUSTER ANALYSIS; DNA MICROARRAY; EXPRESSED SEQUENCE TAG; FLOWER; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENE LIBRARY; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MUTATION; NUCLEIC ACID HYBRIDIZATION; PHENOTYPE; PLANT GENE; REGULATOR GENE; REPRODUCIBILITY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SWEET ORANGE;

CITRUS SINENSIS; CLUSTER ANALYSIS; EXPRESSED SEQUENCE TAGS; FLOWERS; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENE LIBRARY; GENES, PLANT; GENES, REGULATOR; METABOLIC NETWORKS AND PATHWAYS; MUTATION; NUCLEIC ACID HYBRIDIZATION; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; PHENOTYPE; PLANT PROTEINS; PYRUVATES; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

CITRUS; CITRUS SINENSIS;

EID: 62349142267     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/ern329     Document Type: Article

References (72)

1. Alba R, Payton P, Fei ZJ, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni JJ. 2005. Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. The Plant Cell 17, 2954-2965.
2. Alos E, Roca M, Iglesias DJ, Minguez-Mosquera MI, Damasceno CMB, Thannhauser TW, Rose JKC, Talon M, Cercos M. 2008. An evaluation of the basis and consequences of a stay-green mutation in the navel negra citrus mutant using transcriptomic and proteomic profiling and metabolite analysis. Plant Physiology 147, 1300-1315.
3. Amitai-Zeigerson H, Scolnik PA, Bar-Zvi D. 1994. Genomic nucleotide sequence of tomato Asr2, a second member of the stress/ripening- induced Asr1 gene family. Plant Physiology 106, 1699-1700.
4. Aradhya MK, Dangl GS, Prins BH, Boursiquot JM, Walker MA, Meredith CP, Simon CJ. 2003. Genetic structure and differentiation in cultivated grape, Vitis vinifera L. Genetical Research 81, 179-192.
5. Asins MJ, Monforte AJ, Mestre PF, Carbonell EA. 1999. Citrus and Prunus copia-like retrotransposons. Theoretical and Applied Genetics 99, 503-510.
6. Bandsma RHJ, Wiegman CH, Herling AW, Burger H-J, ter Harmsel A, Meijer AJ, Romijn JA, Reijngoud D-J, Kuipers F. 2001. Acute inhibition of glucose-6-phosphate translocator activity leads to increased de novo lipogenesis and development of hepatic steatosis without affecting VLDL production in rats. Diabetes 50, 2591-2597.
7. Bell E, Creelman RA, Mullet JE. 1995. A chloroplast lipoxygenase is required for wound-induced jasmonic acid accumulation in Arabidopsis. Proceedings of the National Academy of Sciences, USA 92, 8675-8679.
8. Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate - a practical and powerful approach to multiple testing. Journal of the Royal Statistical Society Series B-Methodological 57, 289-300.
9. Bernet GP, Asins MJ. 2003. Identification and genomic distribution of gypsy like retrotransposons in Citrus and Poncirus. Theoretical and Applied Genetics 108, 121-130.
10. Breto MP, Ruiz C, Pina JA, Asins MJ. 2001. The diversification of Citrus clementina Hort. ex Tan., a vegetatively propagated crop species. Molecular Phylogenetics and Evolution 21, 285-293.
11. Cakir B, Agasse A, Gaillard C, Saumonneau A, Delrot S, Atanassova R. 2003. A grape ASR protein involved in sugar and abscisic acid signaling. The Plant Cell 15, 2165-2180.
12. Cameron JW, Frost HB. 1968. Genetics, breeding and nucellar embryony. Berkeley, CA: University of California Berkeley.
13. Canel C, Bailey-Serres JN, Roose ML. 1995. Pummelo fruit transcript homologous to ripening-induced genes. Plant Physiology 108, 1323-1324.
14. Chatelet P, Laucou V, Fernandez L, Sreekantan L, Lacombe T, Martinez-Zapater JM, Thomas MR, Torregrosa L. 2007. Characterization of Vitis vinifera L. somatic variants exhibiting abnormal flower development patterns. Journal of Experimental Botany 58, 4107-4118.
15. Chen ZH, Walker RP, Tecsi LI, Lea PJ, Leegood RC. 2004. Phosphoenolpyruvate carboxykinase in cucumber plants is increased both by ammonium and by acidification, and is present in the phloem. Planta 219, 48-58.
16. Chiou TJ, Bush DR. 1996. Molecular cloning, immunochemical localization to the vacuole, and expression in transgenic yeast and tobacco of a putative sugar transporter from sugar beet. Plant Physiology 110, 511-520.
17. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. 2005. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674-3676.
18. Deng ZN, Gentile A, Nicolosi E, Domina F, Vardi A, Tribulato E. 1995. Identification of in-vivo and in-vitro lemon mutants by RAPD markers. Journal of Horticultural Science 70, 117-125.
19. Derory J, Leger P, Garcia V, Schaeffer J, Hauser MT, Salin F, Luschnig C, Plomion C, Glossl J, Kremer A. 2006. Transcriptome analysis of bud burst in sessile oak (Quercus petraea). New Phytologist 170, 723-738.
20. Diatchenko L, Lau YFC, Campbell AP, et al. 1996. Suppression subtractive hybridization: a method for generating differentially regulated or tissue-specific cDNA probes and libraries. Proceedings of the National Academy of Sciences, USA 93, 6025-6030.
21. Eriksson EM, Bovy A, Manning K, Harrison L, Andrews J, De Silva J, Tucker GA, Seymour GB. 2004. Effect of the Colorless nonripening mutation on cell wall biochemistry and gene expression during tomato fruit development and ripening. Plant Physiology 136, 4184-4197.
22. Fan J, Gao X, Yang YW, Deng W, Li ZG. 2007. Molecular cloning and characterization of a NAC-like gene in 'navel' orange fruit response to postharvest stresses. Plant Molecular Biology Reporter 25, 145-153.
23. Fang DQ, Roose ML. 1997. Identification of closely related citrus cultivars with inter-simple sequence repeat markers. Theoretical and Applied Genetics 95, 408-417.
24. Fanizza G, Chaabane R, Ricciardi L, Resta P. 2003. Analysis of a spontaneous mutant and selected clones of cv. Italia. (Vitis vinifera) by AFLP markers. Vitis 42, 27-30.
25. Feussner I, Wasternack C. 2002. The lipoxygenase pathway. Annual Review of Plant Biology 53, 275-297.
26. Guex N, Henry H, Flach J, Richter H, Widmer F. 1995. Glyoxysomal malate-dehydrogenase and malate synthase from soybean cotyledons (Glycine max L.) - enzyme association, antibodyproduction and cDNA cloning. Planta 197, 369-375.
27. Guo Y, Guo HY, Zhang L, et al. 2005. Genomic analysis of anti-Hepatitis B virus (HBV) activity by small interfering RNA and lamivudine in stable HBV-producing cells. Journal of Virology 79, 14392-14403.
28. Hegedus D, Yu M, Baldwin D, Gruber M, Sharpe A, Parkin I, Whitwill S, Lydiate D. 2003. Molecular characterization of Brassica napus NAC domain transcriptional activators induced in response to biotic and abiotic stress. Plant Molecular Biology 53, 383-397.
29. Herrero J, Valencia A, Dopazo J. 2001. A hierarchical unsupervised growing neural network for clustering gene expression patterns. Bioinformatics 17, 126-136.
30. Huang XQ, Madan A. 1999. CAP3: a DNA sequence assembly program. Genome Research 9, 868-877.
31. Iusem ND, Bartholomew DM, Hitz WD, Scolnik PA. 1993. Tomato (Lycopersicon esculentum) transcript induced by water deficit and ripening. Plant Physiology 102, 1353-1354.
32. Kato M, Ikoma Y, Matsumoto H, Sugiura M, Hyodo H, Yano M. 2004. Accumulation of carotenoids and expression of carotenoid biosynthetic genes during maturation in citrus fruit. Plant Physiology 134, 824-837.
33. Ke J, Behal RH, Back SL, Nikolau BJ, Wurtele ES, Oliver DJ. 2000. The role of pyruvate dehydrogenase and acetyl-coenzyme A synthetase in fatty acid synthesis in developing Arabidopsis seeds. Plant Physiology 123, 497-508.
34. Kenis K, Keulemans J. 2005. Genetic linkage maps of two apple cultivars (Malus3domestica Borkh.) based on AFLP and microsatellite markers. Molecular Breeding 15, 205-219.
35. Kobayashi S, Goto-Yamamoto N, Hirochika H. 2004. Retrotransposon-induced mutations in grape skin color. Science 304, 982-982.
36. Koornneef M, Alonso-Blanco C, Vreugdenhil D. 2004. Naturally occurring genetic variation in Arabidopsis thaliana. Annual Review of Plant Biology 55, 141-172.
37. Licciardello C, Russo MP, Vale G, Recupero RG. 2008. Identification of differentially expressed genes in the flesh of blood and common oranges. Tree Genetics & Genomes 4, 315-331.
38. Lichtenthaler HK, Schwender J, Disch A, Rohmer M. 1997. Biosynthesis of isoprenoids in higher plant chloroplasts proceeds via a mevalonate-independent pathway. FEBS Letters 400, 271-274.
39. Liu Q, Xu J, Liu YZ, Zhao XL, Deng XX, Guo LL, Gu JQ. 2007. A novel bud mutation that confers abnormal patterns of lycopene accumulation in sweet orange fruit (Citrus sinensis L. Osbeck). Journal of Experimental Botany 58, 4161-4171.
40. Liu YZ, Liu Q, Tao NG, Deng XX. 2006. Efficient isolation of RNA from fruit peel and pulp of ripening navel orange (Citrus sinensis Osbeck). Journal of Huazhong Agricultural University 25, 300-304.
41. Manning K, Tor M, Poole M, Hong Y, Thompson AJ, King GJ, Giovannoni JJ, Seymour GB. 2006. A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nature Genetics 38, 948-952.
42. Mao CZ, Ding WN, Wu YR, Yu J, He XW, Shou HX, Wu P. 2007. Overexpression of a NAC-domain protein promotes shoot branching in rice. New Phytologist 176, 288-298.
43. Marcotrigiano M. 1997. Chimeras and variegation: patterns of deceit. Hortscience 32, 773-784.
44. Mase N, Iketani H, Sato Y. 2007. Analysis of bud sport cultivars of peach (Prunus persica (L.) Batsch) by simple sequence repeats (SSR) and restriction landmark genomic scanning (RLGS). Journal of the Japanese Society for Horticultural Science 76, 20-27.
45. McClintock B. 1951. Chromosome organization and genic expression. Cold Spring Harbor Symposia on Quantitative Biology 16, 13-47.
46. Milisavljevic MD, Timotijevic GS, Radovic SR, Konstantinovic MM, Maksimovic VR. 2007. Two types of aspartic proteinases from buckwheat seed - gene structure and expression analysis. Journal of Plant Physiology doi:10.1016/j.jplph.2007.03.016.
47. Moore GA. 2001. Oranges and lemons: clues to the taxonomy of Citrus from molecular markers. Trends in Genetics 17, 536-540.
48. Olsen AN, Ernst HA, Lo Leggio L, Skriver K. 2005. NAC transcription factors: structurally distinct, functionally diverse. Trends in Plant Science 10, 79-87.
49. Ouyang B, Yang T, Li HX, Zhang L, Zhang YY, Zhang JH, Fei ZJ, Ye ZB. 2007. Identification of early salt stress response genes in tomato root by suppression subtractive hybridization and microarray analysis. Journal of Experimental Botany 58, 507-520.
50. Raghuvanshi SS. 1962. Cytogenetical studies in genus Citrus. 4. Evolution in genus Citrus. Cytologia 27, 172-188.
51. Rico-Cabanas L, Martinez-Izquierdo JA. 2007. CIRE1, a novel transcriptionally active Ty1-copia retrotransposon from Citrus sinensis. Molecular Genetics and Genomics 277, 365-377.
52. Ross CA, Liu Y, Shen QXJ. 2007. The WRKY gene family in rice (Oryza sativa). Journal of Integrative Plant Biology 49, 827-842.
53. Schaller F, Biesgen C, Mussig C, Altmann T, Weiler EW. 2000. 12-Oxophytodienoate reductase 3 (OPR3) is the isoenzyme involved in jasmonate biosynthesis. Planta 210, 979-984.
54. Serpen A, Gokmen V. 2006. A proposed mechanism for the inhibition of soybean lipoxygenase by beta-carotene. Journal of the Science of Food and Agriculture 86, 401-406.
55. Shelp BJ, Bown AW, McLean MD. 1999. Metabolism and functions of gamma-aminobutyric acid. Trends in Plant Science 4, 446-452.
56. Smit A. 2007. Repeat Masker. http://www.repeatmasker.org.
57. Snedden WA, Arazi T, Fromm H, Shelp BJ. 1995. Calcium-calmodulin activation of soybean glutamate-decarboxylase. Plant Physiology 108, 543-549.
58. Snedden WA, Koutsia N, Baum G, Fromm H. 1996. Activation of a recombinant Petunia glutamate decarboxylase by calcium/calmodulin or by a monoclonal antibody which recognizes the calmodulin binding domain. Journal of Biological Chemistry 271, 4148-4153.
59. Spiegel-Roy P, Goldschmidt EE. 1996. Biology of citrus. Cambridge: Cambridge University Press.
60. Sun ZR, Gantt E, Cunningham FX. 1996. Cloning and functional analysis of the beta-carotene hydroxylase of Arabidopsis thaliana. Journal of Biological Chemistry 271, 24349-24352.
61. Takatsuji H. 1998. Zinc-finger transcription factors in plants. Cellular and Molecular Life Sciences 54, 582-596.
62. Tao NG, Wei J, Liu YZ, Cheng YJ, Deng XX. 2006. Copia-like retrotransposons in a precocious mutant of trifoliate orange [Poncirus trifoliata (L.) Raf]. Journal of Horticultural Science & Biotechnology 81, 1038-1042.
63. Terol J, Conesa A, Colmenero JM, et al. 2007. Analysis of 13000 unique Citrus clusters associated with fruit quality, production and salinity tolerance. BMC Genomics 8.
64. Tsuchida K, Arai M, Tanaka Y, Ishihara R, Ryan RO, Maekawa H. 1998. Lipid transfer particle catalyzes transfer of carotenoids between lipophorins of Bombyx mori. Insect Biochemistry and Molecular Biology 28, 927-934.
65. Walker AR, Lee E, Robinson SP. 2006. Two new grape cultivars, bud sports of Cabernet Sauvignon bearing pale-coloured berries, are the result of deletion of two regulatory genes of the berry colour locus. Plant Molecular Biology 62, 623-635.
66. Xie Z, Zhang ZL, Zou XL, Huang J, Ruas P, Thompson D, Shen QJ. 2005. Annotations and functional analyses of the rice WRKY gene superfamily reveal positive and negative regulators of abscisic acid signaling in aleurone cells. Plant Physiology 137, 176-189.
67. Xu BY, Su W, Liu JH, Wang JB, Jin ZQ. 2007. Differentially expressed cDNAs at the early stage of banana ripening identified by suppression subtractive hybridization and cDNA microarray. Planta 226, 529-539.
68. Yang GP, Ross DT, Kuang WW, Brown PO, Weigel RJ. 1999. Combining SSH and cDNA microarrays for rapid identification of differentially expressed genes. Nucleic Acids Research 27, 1517-1523.
69. Yang YH, Dudoit S, Luu P, Lin DM, Peng V, Ngai J, Speed TP. 2002. Normalization for cDNA microarray data: a robust composite method addressing single and multiple slide systematic variation. Nucleic Acids Research 30.
70. Yao JL, Dong YH, Morris BAM. 2001. Parthenocarpic apple fruit production conferred by transposon insertion mutations in a MADSbox transcription factor. Proceedings of the National Academy of Sciences, USA 98, 1306-1311.
71. Yoshida KT, Fujiwara T, Naito S. 2002. The synergistic effects of sugar and abscisic acid on myo-inositol-1-phosphate synthase expression. Physiologia Plantarum 114, 581-587.
72. Zhang M, Deng XX. 2006. Advances in research of citrus cultivars selected by bud mutation and the mechanism of formation of mutated characteristics. Journal of Fruit Science 23, 871-876.