Identification and expression profiling of low oxygen regulated genes from Citrus flavedo tissues using RT-PCR differential display

Journal of Experimental Botany

Volumn 58, Issue 8, 2007, Pages 2203-2216

  Pasentsis, Konstantinos ^a,b   Falara, Vasiliki ^a   Pateraki, Irene ^a   Gerasopoulos, Dimitrios ^a   Kanellis, Angelos K ^a  

^a ARISTOTLE UNIVERSITY OF THESSALONIKI   (Greece)

^b INFORMATION TECHNOLOGIES INSTITUTE   (Greece)

Author keywords

Anoxia; Citrus; Citrus sinensis L.; Flavedo; Gene expression; Hypoxia; mRNA differential display; Orange fruit; Stress

Indexed keywords

BIOSYNTHESIS; FRUITS; RNA; TISSUE;

ANOXIA; BIOINFORMATIC ANALYSIS; CITRUS SINENSIS L.; DIFFERENTIAL DISPLAY (DD); HYPOXIA;

GENE EXPRESSION;

ETHYLENE; ETHYLENE DERIVATIVE; MESSENGER RNA; OXYGEN;

ADAPTATION; ARTICLE; BIOLOGY; CITRUS FRUIT; DNA SEQUENCE; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; MOLECULAR CLONING; PROMOTER REGION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION;

ADAPTATION, PHYSIOLOGICAL; CITRUS; CLONING, MOLECULAR; COMPUTATIONAL BIOLOGY; ETHYLENES; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; OXYGEN; PROMOTER REGIONS (GENETICS); REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SEQUENCE ANALYSIS, DNA;

CITRUS; CITRUS SINENSIS;

EID: 34547659280     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erm078     Document Type: Article

References (74)

1. Adams-Phillips L, Barry C, Giovannoni J. 2004. Signal transduction systems regulating fruit ripening. Trends in Plant Science 9, 331-338.
2. 2 stress-associated cDNA clones from the flooding-stress- tolerant FR13A rice genotype. Annals of Botany 96, 831-844.
3. Alexander L, Grierson D. 2002. Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. Journal of Experimental Botany 53, 2039-2055.
4. Bailey-Serres J, Chang R. 2005. Sensing and signaling in response to oxygen deprivation in plants and other organisms. Annals of Botany 96, 507-518.
5. Basse CW. 2005. Dissecting defense-related and developmental transcriptional responses of maize during Ustilago maydis infection and subsequent tumor formation. Plant Physiology 138, 1774-1784.
6. Battini JL, Rasko JE, Miller AD. 1999. A human cell-surface receptor for xenotropic and polytropic murine leukemia viruses: possible role in G protein-coupled signal transduction. Proceedings of the National Academy of Sciences, USA 96, 1385-1390.
7. Baxter-Burrell A, Yang Z, Springer PS, Bailey-Serres J. 2002. RopGAP4-dependent Rop GTPase rheostat control of Arabidopsis oxygen deprivation tolerance. Science 296, 2026-2028.
8. Bouche N, Fromm H. 2004. GABA in plants: just a metabolite? Trends in Plant Science 9, 110-115.
9. Bown AW, Shelp BJ. 1997. The metabolism and functions of γ-aminobutyric acid. Plant Physiology 115, 1-5.
10. Branco-Price C, Kawaguchi R, Ferreira RB, Bailey-Serres J. 2005. Genome-wide analysis of transcript abundance and translation in Arabidopsis seedlings subjected to oxygen deprivation. Annals of Botany 96, 647-660.
11. Carginale V, Maria G, Capasso C, Ionata E, La Cara F, Pastore M, Bertaccini A, Capasso A. 2004. Identification of genes expressed phytoplasma infection in leaves of Prunus armeniaca RNA differential display. Gene 332, 29-34.
12. Chang WWP, Huang L, Shen M, Webster C, Burlingame AL, Roberts JKM. 2000. Patterns of protein synthesis and tolerance of anoxia in root tips of maize seedlings acclimated to a low-oxygen environment, and identification of proteins by mass spectrometry. Plant Physiology 122, 295-318.
13. Chevalier C, Gourgeois E, Pradet A, Raymond P. 1995. Molecular cloning and characterization of six cDNAs expressed during glucose starvation in excised maize root tips. Plant Molecular Biology 28, 473-485.
14. Church GM, Gilbert W. 1984. Genomic sequencing. Proceedings of the National Academy of Sciences, USA 81, 1991-1995.
15. Davies C Robinson S. 2000. Differential screening indicates a dramatic change in mRNA profiles during grape berry ripening. Cloning and characterization of cDNAs encoding putative cell wall and stress responsive proteins. Plant Physiology 122, 803-812.
16. de Vetten NC, Ferl RJ. 1995. Characterization of a maize G-box binding factor that is induced by hypoxia. The Plant Journal 7, 589-601.
17. Dolferus R, Jacobs M, Peacock WJ, Dennis ES. 1994. Differential interactions of promoter elements in stress responses of the Arabidopsis Adh gene. Plant Physiology 105, 1075-1087.
18. Dordas C, Hasinoff BB, Igamberdiev AU, Manac'h N, Rivoal J, Hill RD. 2003. Expression of a stress-induced hemoglobin affects NO levels produced by alfalfa root cultures under hypoxic stress. The Plant Journal 35, 763-770.
19. Dordas C, Hasinoff BB, Rivoal J, Hill RD. 2004. Class-1 hemoglobins, nitrate and NO levels in anoxic maize cell-suspension cultures. Planta 219, 66-72.
20. Drew MC. 1997. Oxygen deficiency and root metabolism: injury and acclimation under hypoxia and anoxia. Annual Review of Plant Physiology and Plant Molecular Biology 48, 223-250.
21. Ellis MH, Dennis ES, Peacock WJ. 1999. Arabidopsis roots and shoots have different mechanisms for hypoxic stress tolerance. Plant Physiology 119, 57-64.
22. Fenglong L, VanToai T, Moy LP, Bock G, Linford LD, Quackenbush J. 2005. Global transcription profiling reveals comprehensive insights into hypoxic response in arabidopsis. Plant Physiology 137, 1115-1129.
23. Fukao T, Bailey-Serres J. 2004. Plant responses to hypoxia: is survival a balancing act? Trends in Plant Science 9, 449-456.
24. Geigenberger P. 2003. Response of plant metabolism to too little oxygen. Current Opinion in Plant Biology 6, 247-256.
25. Giovannoni J. 2001. Molecular biology of fruit maturation and ripening. Annual Review of Plant Physiology and Plant Molecular Biology 52, 725-749.
26. Giovannoni J. 2004. Genetic regulation of fruit development and ripening. The Plant Cell 16, S170-S180.
27. Gracey AY, Troll JV, Somero GN. 2001. Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proceedings of the National Academy of Sciences, USA 98, 1993-1998.
28. Griffiths A, Barry C, Alpuche-Solis AG, Grierson D. 1999. Ethylene and developmental signals regulate expression of lipoxygenase genes during tomato fruit ripening. Journal of Experimental Botany 50, 793-798.
29. He CJ, Morgan PW, Drew MC. 1996. Transduction of an ethylene signal is required for programmed cell death and lysis in the root cortex of maize during aerenchyma formation induced by hypoxia. Plant Physiology 112, 463-472.
30. Hoeren F, Dolferus R, Wu Y, Peacock WJ, Dennis ES. 1998. Evidence for a role for AtMYB2 in the induction of the Arabidopsis alcohol dehydrogenase (ADH1) gene by low oxygen. Genetics 149, 479-490.
31. Kader AA. 1986. Biochemical and physiological basis for effects of controlled and modified atmospheres on fruits and vegetables. Food Technology 40, 99-104.
32. Kanellis AK. 1994. Oxygen regulation of protein synthesis and gene expression in ripening fruits: future outlook. In: Woltering E, ed. Proceedings of the International Symposium on Postharvest Treatment of Fruits and Vegetables. The Netherlands: Oosterbeek, 19-22 October 1994.
33. 2 with and without ethylene. Plant Physiology 40, 251-258.
34. Kanellis AK, Solomos T, Mattoo AK. 1989b. Hydrolytic enzyme activities and protein pattern of avocado fruit ripened in air and in low oxygen with and without ethylene. Plant Physiology 90, 259-266.
35. 2 correlates with lower cellulase protein and gene transcript levels. Plant Cell Physiology 30, 829-834.
36. Kanellis AK, Solomos T, Roubelakis-Angelakis KA. 1991. Suppression of cellulase and polygalacturonase and induction of alcohol dehydrogenase isoenzymes in avocado fruit mesocarp subjected to low oxygen stress. Plant Physiology 96, 269-274.
37. Kanellis AK, Loulakakis KA, Hassan M, Roubelakis-Angelakis KA. 1993. Biochemical and molecular aspects of the low oxygen action on fruit ripening. In: Pech CJ, Latche A, Balague C, eds. Cellular and molecular aspects of biosynthesis and action of the plant hormone ethylene. Dordrecht: Kluwer Academic Publishers, 117-122.
38. Kinnersley AM, Turano FJ. 2000. Gamma aminobutyric acid (GABA) and plant responses to stress. Critical Review in Plant Science 19, 479-509.
39. Kita M, Hirata Y, Moriguchi T, Endo-Inagaki T, Matsumoto R, Hasegawa S, Suhayda CG, Omura M. 2000. Molecular cloning and characterization of a novel gene encoding limonoid UDP-glucosyltransferase in Citrus. FEBS Letters 469, 173-178.
40. Klok EJ, Wilson IW, Wilson D, Chapman SC, Ewing RM, Somerville SC, Peacock WJ, Dolferus R, Dennis ES. 2002. Expression profile analysis of the low-oxygen response in Arabidopsis root cultures. The Plant Cell 14, 2481-2494.
41. Koag MC, Fenton RD, Wilkens S, Close TJ. 2003. The binding of maize DHN1 to lipid vesicles. Gain of structure and lipid specificity. Plant Physiology 131, 309-316.
42. Kristo P, Saarelainen R, Fagerstrom R, Aho S, Korhola M. 1996. Protein purification, and cloning and characterization of the cDNA and gene for xylose isomerase of barley. European Journal of Biochemistry 237, 240-246.
43. Kuno N, Muramatsu T, Hamazato F, Furuya M. 2000. Identification by large-scale screening of phytochrome-regulated genes in etiolated seedlings of Arabidopsis using a fluorescent differential display technique. Plant Physiology 122, 15-24.
44. Lang PC, Zhang K, Ebel RC, Dane F, Dozier WA. 2005. Identification of cold acclimated genes in leaves of Citrus unshiu mRNA differential display. Gene 10, 111-118.
45. Lenburg ME, O'Shea EK. 1996. Signaling phosphate starvation. Trends in Biochemical Sciences 10, 383-387.
46. Li J, Nagpal P, Vitart V, McMorris TC, Chory J. 1996. A role for brassinosteroids in light-dependent development of Arabidopsis. Science 272, 398-401.
47. Liang P, Pardee AB. 1992. Differential display of eukaryotic messenger RNA by means of the polymerase chain reaction. Science 257, 967-971.
48. Liang P, Pardee AB. 1998. Differential display. A general protocol. Molecular Biotechnology 3, 261-267.
49. Liu F, Vantoai T, Moy L, Bock G, Linford LD, Quackenbush J. 2005. Global transcription profiling reveals novel insights into hypoxic response in Arabidopsis. Plant Physiology 137, 1115-1129.
50. Loreti E, Poggi A, Novi G, Alpi A, Perata P. 2005. A genomewide analysis of the effects of sucrose on gene expression in Arabidopsis seedlings under anoxia. Plant Physiology 137, 1130-1138.
51. Loulakakis K, Hassan M, Gerasopoulos G, Kanellis AK. 2006. Effects of low oxygen on in vitro translation products of poly(A)+ RNA, cellulase and alcohol dehydrogenase expression in preclimacteric and ripening-initiated avocado fruit. Postharvest Biology and Technology 39, 29-37.
52. Mattana M, Coraggio I, Bertani A, Reggiani R. 1994. Expression of the enzymes of nitrate reduction during the anaerobic germination of rice. Plant Physiology 106, 1605-1608.
53. Mohanty BS, Krishnan PT, Swarup S, Bajic VB. 2005. Detection and preliminary analysis of motifs in promoters of anaerobically induced genes of different plant species. Annals of Botany 96, 669-681.
54. Olive MR, Peacock WJ, Dennis ES. 1991. The anaerobic responsive element contains two GC-rich sequences essential for binding a nuclear protein and hypoxic activation of the maize Adh1 promoter. Nucleic Acids Research 19, 7053-7060.
55. Olson DC, Oetiker JH, Yang SF. 1995. Analysis of LE-ACS3, a 1-aminocyclopropane-1-carboxylic acid synthase gene expressed during flooding in the roots of tomato plants. Journal of Biological Chemistry 270, 14056-14061.
56. Paul AL, Schuerger AC, Popp MP, Richards JT, ManakMS Ferl RJ. 2004. Hypobaric biology: Arabidopsis gene expression at low atmospheric pressure. Plant Physiology 134, 215-223.
57. Porat R, Pasentsis K, Rozenzvieg D, Gerasopoulos D, Falara V, Samach A, Lurie S, Kanellis AK. 2004. Isolation of a dehydrin cDNA from orange and grapefruit citrus fruit that is specifically induced by the combination of heat followed by chilling temperatures. Physiologia Plantarum 120, 256-264.
58. Ramonell KM, Kuang A, Porterfield DM, Crispi ML, Xiao Y, McClure G, Musgrave ME. 2001. influence of atmospheric oxygen on leaf structure and starch deposition in Arabidopsis thaliana. Plant, Cell and Environment 24, 419-428.
59. Roussis A, Flemetakis E, Dimou M, Kavroulakis N, Venieraki A, Aivalakis G, Katinakis P. 2003. Nodulin PvNOD33, a putative phosphatase whose expression is induced during Phaseolus vulgaris nodule development. Plant Physiology and Biochemistry 41, 719-725.
60. Saab IN, Sachs MM. 1996. A flooding-induced xyloglucan endotransglycosylase homolog in maize is responsive to ethylene and associated with aerenchyma. Plant Physiology 112, 385-391.
61. Seymour GB, Taylor JE, Tucker GA (eds). 1993. Biochemistry of fruit ripening. London: Chapman and Hall.
62. Shellie KC. 2002. Ultra-low oxygen refrigerated storage of 'Rio Red' grapefruit: fungistatic activity and fruit quality. Postharvest Biology and Technology 25, 73-85.
63. Shellie KC, Mangan RL, Ingle SJ. 1997. Tolerance of grapefruit to Mexican fruit fly larvae to heated controlled atmospheres. Postharvest Biology and Technology 10, 179-186.
64. Shi JX, Porat R, Goren R, Goldschmidt EE. 2005. Physiological responses of 'Murcott' mandarins and 'Star Ruby' grapefruit to anaerobic stress conditions and their relation to fruit taste, quality and emission of off-flavor volatiles. Postharvest Biology and Technology 38, 99-105.
65. Sokolov BP, Prockop DJ. 1994. A rapid and simple PCR-based method for isolation of cDNAs from differentially expressed genes. Nucleic Acids Research 22, 4009-4015.
66. 2 concentration on fruit respiration: nature of respiratory diminution. In: Richardson DG, Meheriuk M, eds. Controlled atmospheres for storage and transport of perishable agricultural commodities. Beaverton: Timber Press, 171-178.
67. Solomos T, Kanellis AK. 1997. Hypoxia and fruit ripening. In: Kanellis AK, Chang C, Kende H, Grierson D, eds. Biology and biotechnology of the plant hormone ethylene. Dordrecht: Kluwer Academic Publishers, 239-252.
68. Spain BH, Koo D, Ramakrishnan M, Dzudzor B, Colicelli J. 1995. Truncated forms of a novel yeast protein suppress the lethality of a G protein alpha subunit deficiency by interacting with the beta subunit. Journal of Biological Chemistry 270, 25435-25444.
69. Subbaiah CC, Sachs MM. 2003. Molecular and cellular adaptations of maize to flooding stress. Annals of Botany 91, 119-127.
70. Szekeres M, Nemeth K, Koncz-Kalman Z, Mathur J, Kauschmann A, Altman T, Redei GP, Nagy F, Schell J, Koncz C. 1996. Brassinosteroids rescue the deficiency of CYP90, a cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85, 171-182.
71. Tailor CS, Nouri A, Lee CG, Kozak C, Kabat D. 1999. Cloning and characterization of a cell surface receptor for xenotropic and polytropic murine leukemia viruses. Proceedings of the National Academy of Sciences, USA 96, 927-932.
72. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J. 2002. A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296, 343-346.
73. Vriezen WH, Hulzink R, Mariani C, Voesenek LACJ. 1999. 1-Aminocyclopropane-1-carboxylate oxidase activity limits ethylene biosynthesis in Rumex palustris during submergence. Plant Physiology 121, 189-195.
74. Zegzouti H, Marty C, Jones B, Bouquin T, Latche A, Pech JC, Bouzayen M. 1997. Improved screening of cDNAs generated by mRNA differential display enables the selection of true positives and the isolation of weakly expressed messages. Plant Molecular Biology Reporter 15, 236-245.