Expression profile of transcripts encoding cell wall remodelling proteins in tomato fruit cv. Micro-Tom subjected to 15°C storage
Gabriela L. Müller A , Claudio O. Budde B , Martin A. Lauxmann A C , Agustina Triassi A , Carlos S. Andreo A , María F. Drincovich A and María V. Lara A D
+ Author Affiliations
- Author Affiliations
A Centro de Estudios Fotosintéticos y Bioquímicos (CEFOBI). Facultad de Ciencias Bioquímicas y Farmacéuticas. Suipacha 531. Rosario (2000), Argentina.
B Estación Experimental San Pedro, Instituto Nacional de Tecnología Agropecuaria (INTA), Ruta Nacional n° 9 Km 170, San Pedro, Argentina.
C Present address: Max Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1 14476, Potsdam, Golm, Germany.
D Corresponding author. Email: lara@cefobi-conicet.gov.ar
Functional Plant Biology 40(5) 449-458 https://doi.org/10.1071/FP12272
Submitted: 14 September 2012 Accepted: 23 December 2012 Published: 11 February 2013
Abstract
To extend fruit market life, tomatoes are harvested before red ripe and kept at temperatures below optimum (20°C). In this work, Micro-Tom tomatoes stored at 20°C (normal ripening) were compared with those stored at 15°C or 4°C (chilling injury inducer) for 7 days. In contrast to 4°C, storage at 15°C delayed ripening with the benefit of not enhancing oxidative metabolism and of enabling ripening upon being transferred to 20°C. The transcriptional expression profile of enzymes related to cell wall metabolism was compared at the three temperatures. Although endo-β-1,4-glucanase (Cel1), which is associated with fruit decay, was largely increased after removal from 4°C storage, its expression was not modified in fruits stored at 15°C. Enhanced transcriptional expression of xyloglucan endotransgylcosylase/hydrolases (XTHs) XTH1, –2, –10 and –11, and of two β-xylosidases (Xyl1–2) was detected in fruits stored at 15°C with respect to those at 20°C. Following 2 days at 20°C, these transcripts remained higher in fruits stored at 15°C and XHT3 and –9 also increased. Ethylene evolution was similar in fruits kept at 15°C and 20°C; thus, the changes in the transcript profile and fruit properties between these treatments may be under the control of factors other than ethylene.
Additional keywords: cell wall metabolism, chilling injury, cold-storage, endotransgylcosylase/hydrolase, ripening, xyloglucan β-xylosidase.
References
Almeida MPF, Huber DJ (2008) In vivo pectin solubility in ripening and chill injured tomato fruit. Plant Science 174, 174–182.| In vivo pectin solubility in ripening and chill injured tomato fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlemsA%3D%3D&md5=d6f73b1ce868ed5373b62c5b74c4189eCAS |
Aoki K, Yano K, Suzuki A, Kawamura S, Sakurai N, Suda K, Kurabayashi A, Suzuki T, Tsugane T, Watanabe M, Egusa M, Kodama M, Ichinose Y, Kikuchi M, Fukushima S, Okabe A, Arie T, Sato Y, Yazawa K, Satoh S, Omura T, Ezura H, Shibata D (2010) Large-scale analysis of full-length cDNAs from the tomato (Solanum lycopersicum) cultivar Micro-Tom, a reference system for the Solanaceae genomics. BMC Genomics 11, 210
| Large-scale analysis of full-length cDNAs from the tomato (Solanum lycopersicum) cultivar Micro-Tom, a reference system for the Solanaceae genomics.Crossref | GoogleScholarGoogle Scholar |
Bewley JD, Banik M, Bourgault R, Feurtado JS, Toorop P, Hilhorst HWM (2000) Endo-β-mannanase activity increases in the skin and outer pericarp of tomato fruits during ripening. Journal of Experimental Botany 51, 529–538.
| Endo-β-mannanase activity increases in the skin and outer pericarp of tomato fruits during ripening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXit1Kmsr8%3D&md5=b142a02de1d15d28925a3892bcf39019CAS |
Bradford MM (1976) Rapid and quantitative method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
| Rapid and quantitative method for quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE28XksVehtrY%3D&md5=bead43c1adb6f57157bea3eab849e63cCAS |
Brummell DA, Harpster MH (2001) Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Molecular Biology 47, 311–339.
| Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXmslGmtrw%3D&md5=4e645cbb330b07236ce627f6a4928244CAS |
Brummell DA, Harpster MH, Dunsmuir P (1999a) Differential expression of expansin gene family members during growth and ripening of tomato fruit. Plant Molecular Biology 39, 161–169.
| Differential expression of expansin gene family members during growth and ripening of tomato fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhvVynu7g%3D&md5=3e7a881f8c9b70c6bd962706559a8d12CAS |
Brummell DA, Harpster MH, Civello PM, Palys JM, Bennett AB, Dunsmuir P (1999b) Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. The Plant Cell 11, 2203–2216.
Budde CO, Polenta G, Lucangeli CD, Murray RE (2006) Air immersion heat treatments affect ethylene production and organoleptic quality of ‘Dixiland’ peaches. Postharvest Biology and Technology 41, 32–37.
| Air immersion heat treatments affect ethylene production and organoleptic quality of ‘Dixiland’ peaches.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XltFOksr8%3D&md5=127b035a4b80238ff34f5a0d375867a2CAS |
Cantu D, Vicente AR, Labavitch JM, Bennett AB, Powell ALT (2008) Strangers in the matrix: plant cell walls and pathogen susceptibility. Trends in Plant Science 13, 610–617.
| Strangers in the matrix: plant cell walls and pathogen susceptibility.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlartL7J&md5=9d2ae90d73f9c537eb334b5abadc8eb6CAS |
Casati P, Lara MV, Andreo CS (2002) Regulation of enzymes involved in C4 photosynthesis and the antioxidant metabolism by UV-B radiation in Egeria densa, a submersed aquatic species. Photosynthesis Research 71, 251–264.
| Regulation of enzymes involved in C4 photosynthesis and the antioxidant metabolism by UV-B radiation in Egeria densa, a submersed aquatic species.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XlslWjtbs%3D&md5=dccc6464c3b0b5806a13d47bddfd8550CAS |
Čikoš S, Bukovská A, Koppel J (2007) Relative quantification of mRNA: comparison of methods currently used for real-time PCR data analysis. BMC Molecular Biology 8, 113
| Relative quantification of mRNA: comparison of methods currently used for real-time PCR data analysis.Crossref | GoogleScholarGoogle Scholar |
Dan Y, Yan H, Munyikwa T, Dong J, Zhang Y, Armstrong CL (2006) MicroTom –a high-throughput model transformation system for functional genomics. Plant Cell Reports 25, 432–441.
| MicroTom –a high-throughput model transformation system for functional genomics.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs1Kksrs%3D&md5=be869e04d57a3aa062156077c7c4ebafCAS |
FAOSTAT (2009) Food and Agriculture Organization of the United Nations Statistical Database. Available at http://faostat.fao.org/ [Accessed 22 April 2009]
Flors V, Leyva MO, Vicedo B, Finiti I, Real MD, García-Agustín P, Bennett AB, González-Bosch C (2007) Absence of the endo-β-1,4-glucanases Cel1 and Cel2 reduces susceptibility to Botrytis cinerea in tomato. The Plant Journal 52, 1027–1040.
| Absence of the endo-β-1,4-glucanases Cel1 and Cel2 reduces susceptibility to Botrytis cinerea in tomato.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXns1WksQ%3D%3D&md5=a09282818d681be3ba624ad0fab89b6eCAS |
Fonseca S, Monteiro L, Barreiro MG, Pais MS (2005) Expression of genes encoding cell wall modifying enzymes is induced by cold storage and reflects changes in pear fruit texture. Journal of Experimental Botany 56, 2029–2036.
| Expression of genes encoding cell wall modifying enzymes is induced by cold storage and reflects changes in pear fruit texture.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXmt1Gmsrk%3D&md5=f0c99e766cab1f26f0db22a38cf0ef23CAS |
Gómez P, Ferrer MA, Fernández-Trujillo JP, Calderón A, Artés F, Egea-Cortines M, Weiss J (2009) Structural changes, chemical composition and antioxidant activity of cherry tomato fruits (cv. Micro-Tom) stored under optimal and chilling conditions. Journal of the Science of Food and Agriculture 89, 1543–1551.
| Structural changes, chemical composition and antioxidant activity of cherry tomato fruits (cv. Micro-Tom) stored under optimal and chilling conditions.Crossref | GoogleScholarGoogle Scholar |
Hobson GE (1981) The short-term storage of tomato fruit. Journal of Horticultural Science 56, 363–368.
Hobson GE (1987) Low temperature injury and the storage of ripening tomatoes. Journal of Horticultural Science 62, 55–62.
Itai A, Ishihara K, Bewley JD (2003) Characterization of expression and cloning, of β-D-xylosidase and α-L-arabinofuranosidase in developing and ripening tomato (Lycopersicon esculentum Mill.) fruit. Journal of Experimental Botany 54, 2615–2622.
| Characterization of expression and cloning, of β-D-xylosidase and α-L-arabinofuranosidase in developing and ripening tomato (Lycopersicon esculentum Mill.) fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXpvVemtb4%3D&md5=4205f63adf08a8885fa098e029ea3dddCAS |
Jackman RL, Yada RY, Marangoni A, Parkinz KL, Stanley DW (1988) Chilling injury. A review of quality aspects. Journal of Food Quality 11, 253–278.
| Chilling injury. A review of quality aspects.Crossref | GoogleScholarGoogle Scholar |
Kramer M, Sanders R, Bolkan H, Waters C, Sheehy RE, Hiatt WR (1992) Postharvest evaluation of transgenic tomatoes with reduced levels of polygalacturonase: processing, firmness and disease resistance. Postharvest Biology and Technology 1, 241–255.
| Postharvest evaluation of transgenic tomatoes with reduced levels of polygalacturonase: processing, firmness and disease resistance.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhsVKmsrs%3D&md5=35c81e90d7307bfcb0ce0fd17b70883fCAS |
Lana MM, Tijskens LMM, van Kooten O (2005) Effects of storage temperature and fruit ripening on firmness of fresh cut tomatoes. Postharvest Biology and Technology 35, 87–95.
| Effects of storage temperature and fruit ripening on firmness of fresh cut tomatoes.Crossref | GoogleScholarGoogle Scholar |
Lim CS, Kang SM, Cho SL, Gross K (2009) Antioxidizing enzyme activities in chilling-sensitive and chilling tolerant pepper fruit as affected by stage of ripeness and storage temperature. Journal of the American Society for Horticultural Science 134, 156–163.
Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔ C T. Methods 25, 402–408.
| Analysis of relative gene expression data using real-time quantitative PCR and the 2ΔΔ C T.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtFelt7s%3D&md5=cda22da73d6034ad2e4c74827f633baaCAS |
López Camelo AF (2004) Storage. In ‘Manual for the preparation and sale of fruits and vegetables from field to market’. pp. 47–74. (FAO: Rome)
Malacrida C, Valle EM, Boggio SB (2006) Postharvest chilling induces oxidative stress response in the dwarf tomato cultivar Micro-Tom. Physiologia Plantarum 127, 10–18.
| Postharvest chilling induces oxidative stress response in the dwarf tomato cultivar Micro-Tom.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xksleqt7o%3D&md5=d84843df5571dd2c7f479d10985f3d69CAS |
Marangoni AG, Jackman RL, Stanley DW (1995) Chilling-associated softening of tomato fruit is related to increased pectinmethylesterase activity. Journal of Food Science 60, 1277–1281.
| Chilling-associated softening of tomato fruit is related to increased pectinmethylesterase activity.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XhsVaitQ%3D%3D&md5=844f2d980370d3c8fbc49a462e6ac4b6CAS |
Martí E, Gisbert C, Bishop GJ, Dixon MS, Garcia-Martinez JL (2006) Genetic and physiological characterization of tomato cv. Micro-Tom. Journal of Experimental Botany 57, 2037–2047.
| Genetic and physiological characterization of tomato cv. Micro-Tom.Crossref | GoogleScholarGoogle Scholar |
Matsukura C, Aoki K, Fukuda N, Mizoguchi T, Asamizu E, Saito T, Shibata D, Ezura H (2008) Comprehensive resources for tomato functional genomics based on the miniature model tomato micro-tom. Current Genomics 9, 436–443.
| Comprehensive resources for tomato functional genomics based on the miniature model tomato micro-tom.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXhtlWiurnK&md5=9574d44c5ff14d98ce6a32cebd025b84CAS |
Miedes E, Lorences EP (2009) Xyloglucanendotransglucosylase/hydrolases (XTHs) during tomato fruit growth and ripening. Journal of Plant Physiology 166, 489–498.
| Xyloglucanendotransglucosylase/hydrolases (XTHs) during tomato fruit growth and ripening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXltVeqt7g%3D&md5=07432b065f045d08f33a1ba504858174CAS |
Miedes E, Herbers K, Sonnewald U, Lorences EP (2010) Overexpression of a cell wall enzyme reduces xyloglucan depolymerization and softening of transgenic tomato fruits. Journal of Agricultural and Food Chemistry 58, 5708–5713.
| Overexpression of a cell wall enzyme reduces xyloglucan depolymerization and softening of transgenic tomato fruits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjvFWmu7o%3D&md5=f9f9c05e0f01aa7bc9c29479f882e67eCAS |
Nagata M, Yamashita I (1992) Simple method for simultaneous determination of chlorophyll and carotenoids in tomato fruit. Journal of the Japanese Society for Food Science and Technology 39, 925–928.
| Simple method for simultaneous determination of chlorophyll and carotenoids in tomato fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXhvFShsrc%3D&md5=b4e6454afd03447497a1ff3cf324943fCAS |
Page D, Gouble B, Valot B, Bouchet JP, Callot C, Kretzschmar A, Causse M, Renard CMCG, Faurobert M (2010) Protective proteins are differentially expressed in tomato genotypes differing for their tolerance to low-temperature storage. Planta 232, 483–500.
| Protective proteins are differentially expressed in tomato genotypes differing for their tolerance to low-temperature storage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXnsFGqsr8%3D&md5=5b7a2ea221a193d4ab50275fe24c3460CAS |
Perotti VE, Del Vecchio HA, Sansevich A, Meier G, Bello F, Cocco M, Garrán SM, Anderson C, Vázquez D, Podestá FE (2011) Proteomic, metabalomic, and biochemical analysis of heat treated Valencia oranges during storage. Postharvest Biology and Technology 62, 97–114.
| Proteomic, metabalomic, and biochemical analysis of heat treated Valencia oranges during storage.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtFait7jI&md5=7d61cc99530c2359a525540608f963e2CAS |
Real MD, Company P, García-Agustín P, Bennett AB, González-Bosch C (2004) Characterization of tomato endo-β-1,4-glucanase Cel1 protein in fruit during ripening and after fungal infection. Planta 220, 80–86.
| Characterization of tomato endo-β-1,4-glucanase Cel1 protein in fruit during ripening and after fungal infection.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXptlSmtbw%3D&md5=9bb6b2aa35c7a32997933b10a3825f6aCAS |
Rugkong A, Rose JKC, Lee SJ, Giovannoni JJ, Neill MA, Watkins CB (2010) Cell wall metabolism in cold-stored tomato fruit. Postharvest Biology and Technology 57, 106–113.
| Cell wall metabolism in cold-stored tomato fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFansLc%3D&md5=46c22ddede0a54b93aaaf9bc7f46122eCAS |
Rugkong A, McQuinn R, Giovannoni JJ, Rose JKC, Watkins CB (2011) Expression of ripening-related genes in cold-stored tomato fruit. Postharvest Biology and Technology 61, 1–14.
| Expression of ripening-related genes in cold-stored tomato fruit.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXlt1Shurs%3D&md5=5b16e2fdce31bc2499039527ba50e595CAS |
Saeed AI, Sharov V, White J, Li J, Liang W, Bhagabati N, Braisted J, Klapa M, Currier T, Thiagarajan M, et al (2003) TM4: a free, open-source system for microarray data management and analysis. BioTechniques 34, 374–378.
Sala JM (1998) Involvement of oxidative stress in chilling injury in cold-stored mandarin fruits. Postharvest Biology and Technology 13, 255–261.
| Involvement of oxidative stress in chilling injury in cold-stored mandarin fruits.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXks1Olu7k%3D&md5=bb230405920c4cf65101e3d24070326bCAS |
Saladié M, Rose JKC, Cosgrove DJ, Catalá C (2006) Characterization of a new xyloglucan endotransglucosylase/ hydrolase (XTH) from ripening tomato fruit and implications for the diverse modes of enzymic action The Plant Journal 47, 282–295.
| Characterization of a new xyloglucan endotransglucosylase/ hydrolase (XTH) from ripening tomato fruit and implications for the diverse modes of enzymic actionCrossref | GoogleScholarGoogle Scholar |
Saltveit ME, Morris LL (1990) Overview of chilling injury of horticultural crops. In ‘Chilling injury of horticultural crops’. (Ed. CY Wang) pp. 3–15. (CRC Press: Boca Raton, FL)
Schuch W, Kanczler J, Robertson D, Hobson G, Tucker G, Grierson D, Bright S, Bird C (1991) Fruit quality characteristics of transgenic tomato fruit with altered polygalacturonase activity. HortScience 26, 1517–1520.
Scott JW, Harbaugh BK (1989) Micro-Tom-a miniature dwarf tomato. Florida Agricultural Experiment Station Circular 370, 1–6.
Smith DL, Gross KC (2000) A family of at least seven β-galactosidase genes is expressed during tomato fruit development. Plant Physiology 123, 1173–1184.
| A family of at least seven β-galactosidase genes is expressed during tomato fruit development.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXlt1SltLw%3D&md5=ea5d2928a917c0f783a3f9aef5ef15f8CAS |
Smith DL, Abbott JA, Gross KC (2002) Down-regulation of tomato β-galactosidase 4 results in decreased fruit softening. Plant Physiology 129, 1755–1762.
| Down-regulation of tomato β-galactosidase 4 results in decreased fruit softening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38Xmtl2gt7g%3D&md5=6be6f384921271ba3379247d139679e5CAS |
Thakur BR, Singh RK, Handa AK (1996) Effect of an antisense pectin methylesterase gene on the chemistry of pectin in tomato (Lycopersicon esculentum) juice. Journal of Agricultural and Food Chemistry 44, 628–630.
| Effect of an antisense pectin methylesterase gene on the chemistry of pectin in tomato (Lycopersicon esculentum) juice.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK28XmslKksg%3D%3D&md5=98e6d562902e568d00eabc06b248e710CAS |
Wang A, Li J, Zhang B, Xu X, Bewley JD (2009) Expression and location of endo-β-mannanase during the ripening of tomato fruit, and the relationship between its activity and softening. Journal of Plant Physiology 166, 1672–1684.
| Expression and location of endo-β-mannanase during the ripening of tomato fruit, and the relationship between its activity and softening.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhtlShtbfK&md5=138420d9af7db233b2e73f38f50d9bb1CAS |
Watkins CB, Picton S, Grierson D (1990) Stimulation and inhibition of expression of ripening-related mRNAs in tomatoes as influenced by chilling temperatures. Journal of Plant Physiology 136, 318–323.
| Stimulation and inhibition of expression of ripening-related mRNAs in tomatoes as influenced by chilling temperatures.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3cXkslGjsrc%3D&md5=66e322b5f9549b3415e60a3250072f3dCAS |
