MADS Box Transcript Amount is Affected by Ethylene during Abscission

DOI: 10.4236/ajps.2011.23035   PDF   HTML     5,231 Downloads   10,055 Views   Citations


Thinning of young fruit is an important agronomical practice to ensure the maximum economic production. This practice is based on the control of the natural self thinning process occurring during fruit development. At the early stages of fruit development (fruitlet), the vegetative part of the tree is competing with the reproductive part of the tree and within the fruit clusters the different fruitlets are competing with each other. As a result the least fit organ abscises, Ethylene and auxin play a central role in this event but the role of ethylene is not thoroughly understood because in other systems abscission occurs partly with ethylene independent processes. We have followed the early development of fruitlets and studied the transcription patterns of MADS-box and ethylene related transcripts. Furthermore, we verified that ethylene has an effect on the expression of some ethylene related and MADS BOX genes. We propose that the ethylene burst during abscission induction is similar to a stage 2 ethylene system and it is related to fruitlet growth by affecting transcript amount of MADS-BOXes which modulate seed development and cortex growth.

Share and Cite:

Cin, V. and Ramina, A. (2011) MADS Box Transcript Amount is Affected by Ethylene during Abscission. American Journal of Plant Sciences, 2, 308-317. doi: 10.4236/ajps.2011.23035.

Conflicts of Interest

The authors declare no conflicts of interest.


[1] L. Calvin and P. Martin, “The U.S. Produce Industry and Labor: Facingthe Future in a Global Economy,” Economic Research Report No. (ERR-106), November 2010, p. 106.
[2] H. Link, “Significance of Flower and Fruit Thinning on Fruit Quality,” Plant Growth Regulation, Vol. 31, No. 1-2, 2000, pp. 17-26. doi:10.1023/A:1006334110068
[3] V. Dal Cin, M. Danesin, A. Botton, A. Boschetti, A. Dorigoni and A. Ramina, “Fruit Load and Elevation Affect Ethylene Biosynthesis and Action in Apple Fruit (Malus domestica L. Borkh) during Development, Maturation and Ripening,” Plant Cell and Environment, Vol. 30, No. 11, 2007, pp. 1480-1485. doi:10.1111/j.1365-3040.2007.01723.x
[4] K. M. Jones, S. A. Bound, M. J. Oakford and P. Gillard, “Modelling Thinning of Pome Fruits,” Plant Growth Regulation, Vol. 31, No. 1-2, 2000, pp. 75-84. doi:10.1023/A:1006315000499
[5] S. J. Wertheim, “Developments in the Chemical Thinning of Apple and Pear,” Plant Growth Regulation, Vol. 31, No. 1-2, 2000, pp. 85-100. doi:10.1023/A:1006383504133
[6] L. Sun, M. John Bukovac, P. Forsline and S. van Nocker, “Natural Variation in Fruit Abscission-Related Traits in Apple (Malus domestica),” Euphytica, Vol. 165, No. 1, 2009, pp. 55-67. doi:10.1007/s10681-008-9754-x
[7] F. Bangerth, “Abscission and Thinning of Young Fruit and Their Regulation by Plant Hormones and Bioregulators,” Plant Growth Regulation, Vol. 31, No. 1, 2000, pp. 43-59.
[8] V. Dal Cin, A. Boschetti, A. Dorigoni and A. Ramina, “Benzylaminopurine Application on Two Different Apple Cultivars (Malus domestica L. Borkh) Displays New and Unexpected Fruitlet Abscission Features,” Annals of Botany, Vol. 99, No. 6, 2007, 1195-1202. doi:10.1093/aob/mcm062
[9] J. Taylor and C. Whitelaw, “Signals in Abscission,” New Phytologist, Vol. 151, No. 2, 2001, pp. 323-339. doi:10.1046/j.0028-646x.2001.00194.x
[10] V. Dal Cin, E. Barbaro, M. Danesin, H. Murayama, R Velasco and A. Ramina, “Fruitlet Abscission: A cDNA AFLP Approach to Study Genes Differentially Expressed during Shedding of Immature Fruits Reveals the Involvement of a Putative Auxin Hydrogen Symporter in Apple (Malus domestica L. Borkh),” Gene, Vol. 442, No. 1-2, 2009, pp. 26-36.
[11] C. Zhou, A. Lakso, T. Robinson and S.Gan, “Isolation and Characterization of Genes Associated with Shade- Induced Apple Abscission,” Molecular Genetics and Genomics, Vol. 280, No. 1, 2008, pp. 83-92. doi:10.1007/s00438-008-0348-z
[12] V. Dal Cin, M. Danesin, A. Boschetti, A. Dorigoni and A. Ramina, “Ethylene Biosynthesis and Perception in Apple Fruitlet Abscission (Malus domestica L. Borkh),” Journal of Experimental Botany, Vol. 56, 2005, No. 421, pp. 2995-3005.
[13] V. Dal Cin, R. Velasco and A. Ramina, “Dominance Induction of Fruitlet Shedding in Malus × domestica (L. Borkh): Molecular Changes Associated with Polar Auxin Transport,” BMC Plant Biology, Vol. 9, 2009, p. 139. doi:10.1186/1471-2229-9-139
[14] C. Chang, “Ethylene Biosynthesis, Perception, and Response,” Journal of Plant Growth Regulation, Vol. 26, No. 2, 2007, pp. 89-91. doi:10.1007/s00344-007-9003-x
[15] P. A. Wiersma, H. Zhang, C. Lu, A. Quail and P. M. A. Toivonen, “Survey of the Expression of Genes for Ethylene Synthesis and Perception during Maturation and Ripening of ‘Sunrise’ and ‘Golden Delicious’ Apple Fruit,” Postharvest Biology and Technology, Vol. 44, No. 3, 2007, pp. 204-211. doi:10.1016/j.postharvbio.2006.12.016
[16] F. B. Abeles, P. W. Morgan and M. E. Saltveit Jr., “Ethylene in Plant Biology,” Academic Press, Inc., Cambridge, 1992.
[17] Y. H. Dong, B. J. Janssen, L. B. J. Bieleski, R. G. Atkinson, B. A. M. Morris and R. C. Gardner, “Isolating and Characterizing Genes Differentially Expressed Early in Apple Fruit Development,” Journal of the American Society for Horticultural Sciences, Vol. 122, No. 6, 1997, pp. 752-756.
[18] C. Pratt, “Apple Flower and Fruit: Morphology and Anatomy,” Horticultural Reviews, Vol. 10, 1988, pp. 273-280. doi:10.1002/9781118060834.ch8
[19] P. Boonkorkaew, S. Hikosaka and N. Sugiyama, “Effect of Pollination on Cell Division, Cell Enlargement, and Endogenous Hormones in Fruit Development in a Gynoecious Cucumber,” Scientia Horticulturae, Vol. 116, No. 1, 2008, pp. 1-7. doi:10.1016/j.scienta.2007.10.027
[20] Y. H. Dong, A. Kvarnheden, J.-L. Yao, P. W. Sutherland, R. G. Atkinson, B. A. Morris and R. C. Gardner, “Identification of Pollination-Induced Genes from the Ovary of Apple (Malus domestica),” Sexual Plant Reproduction, Vol. 11, No. 5, 1998, pp. 277-283. doi:10.1007/s004970050154
[21] J. J. Giovannoni, “Molecular Biology of Fruit Maturation And Ripening,” Annual Review of Plant Physiology & Plant Molecular Biology, Vol. 52, 2001, p. 725-749. doi:10.1146/annurev.arplant.52.1.725
[22] J. J. Giovannoni, “Genetic Regulation of Fruit Development and Ripening,” The Plant Cell, Vol. 16, 2004, pp. S170-S180. doi:10.1105/tpc.019158
[23] J. J. Giovannoni, “Fruit Ripening Mutants Yield Insights into Ripening Control,” Current Opinion in Plant Biology, Vol. 10, No. 3, 2007, pp. 283-289. doi:10.1016/j.pbi.2007.04.008
[24] H. Sommer, J. Beltran, P. Huijser, H. Pape, W. Lonnig, H. Saedler and Z. Schwarz-Sommer, “Deficiens, A Homeotic Gene Involved in the Control of Flower Morphogenesis in Antirrhinum majus: The Protein Shows Homology to Transcription Factors,” The EMBO Journal, Vol. 9, No. 3, 1990, pp. 605-613.
[25] E. Coen and E. Meyerowitz, “The War of the Whorls: Genetic Interactions Controlling Flower Development,” Nature, Vol. 353, 1991, pp. 31-37.
[26] T. Elitzur, J. Vrebalov, J. J. Giovannoni, E. E. Goldschmidt, and H. Friedman, “The Regulation of MADS- Box Gene Expression during Ripening of Banana and Their Regulatory Interaction with Ethylene,” Journal of Experimental Botany, Vol. 61, No. 5, 2010, pp. 1523- 1535. doi:10.1093/jxb/erq017
[27] L. Fernandez, L. Torregrosa, N. Terrier L. Sreekantan, J. Grimplet, D. Davies, M. R. Thomas, C. Romieu and A. Ageorges, “Identification of Genes Associated with Flesh Morphogenesis during Grapevine Fruit Development,” Plant Molecular Biology, Vol. 63, No. 3, 2007, pp. 307-323. doi:10.1007/s11103-006-9090-2
[28] J. Diaz-Riquelme, D. Lijavetzky, J. M. Martinez-Zapater and M. J. Carmona, “Genome-Wide Analysis of MIKCC-Type MADS Box Genes in Grapevine,” Plant Physiology, Vol. 149, No. 1, 2009, pp. 354-369. doi:10.1104/pp.108.131052
[29] M. J. Poupin, F. Federici, C. Medina, J. T. Matus, T. Timmermann and P. Arce-Johnson, “Isolation of the Three Grape Sub-Lineages of B-Class MADS-box TM6, PISTILLATA and APETALA3 Genes Which Are Differentially Expressed during Flower and Fruit Development,” Gene, Vol. 404, No. 1-2, 2007, pp. 10-24.
[30] Y. Xu, L. Zhang, H. Xie, Y.-Q. Zhang, M. Oliveira and R.-C. Ma, “Expression Analysis and Genetic Mapping of Three SEPALLATA-Like Genes from Peach (Prunus persica (L.) Batsch),” Tree Genetics & Genomes, Vol. 4, No. 4, 2008, pp. 693-703. doi:10.1007/s11295-008-0143-3
[31] M. K. Filipecki, H. Sommer and S. Malepszy, “The MADS-Box Gene CUS1 Is Expressed during Cucumber Somatic Embryogenesis,” Plant Science, Vol. 125, No. 1, 1997, pp. 63-74. doi:10.1016/S0168-9452(97)00056-3
[32] S.-K. Sung, G.-H. Yu, J. Nam, D.-H. Jeong and G. An, “Developmentally Regulated Expression of Two MADS- Box Genes, MdMADS3 and MdMADS4, in the Morphogenesis of Flower Buds and Fruits in Apple,” Planta, Vol. 210, No. 4, 2000, pp. 519-528.
[33] S.-K. Sung, G.-H. Yu and G. An, “Characterization of MdMADS2, a Member of the SQUAMOSA Subfamily of genes, in Apple,” Plant Physiology, Vol. 120, No. 4, 1999, pp. 969-978. doi:10.1104/pp.120.4.969
[34] T. Foster, R. Johnston and A. Seleznyova, “A Morphological and Quantitative Characterization of Early Floral Development in Apple (Malus × domestica Borkh.),” Annals of Botany, Vol. 92, No. 2, 2003, pp. 199-206.
[35] S.-K. Sung and G. An, “Molecular Cloning and Characterization of a MADS-Box cDNA Clone of the Fuji Apple,” Plant Cell Physiology, Vol. 38, No. 4, 1997, pp. 484-489.
[36] F. García-Maroto, M. J. Carmona, J. A. Garrido, M. Vilches-Ferrón, J. Rodríguez-Ruiz and D. López Alonso, “New Roles for MADS-box Genes in Higher Plants,” Biologia Plantarum, Vol. 46, No. 3, 2003, pp. 321-330.
[37] C. G. van der Linden, B. Vosman and M. J. M. Smulders, “Cell and Molecular Biology, Biochemistry and Molecular Physiology. Cloning and Characterization of Four Apple MADS Box Genes Isolated from Vegetative Tissue,” Journal of Experimental Botany, Vol. 53, No. 371, 2002, pp. 1025-1036.
[38] T. Jack, “Plant Development Going MADS,” Plant Molecular Biology, Vol. 46, No. 5, 2001, pp. 515-520. doi:10.1023/A:1010689126632
[39] S. Rounsley, G. Ditta and M. Yanofsky, “Diverse Roles for MADS Box Genes in Arabidopsis Development,” The Plant Cell, Vol. 7, No. 8, 1995, pp. 1259-1269.
[40] H. Flachowsky, A. Peil, T. Sopanen, A. Elo and V. Hanke, “Overexpression of BpMADS4 from Silver Birch (Betula pendula Roth.) Induces Early-Flowering in Apple (Malus × domestica Borkh.),” Plant Breeding, Vol. 126, No. 2, 2007, pp. 137-145. doi:10.1111/j.1439-0523.2007.01344.x
[41] N. Kotoda and M.Wada, “MdTFL1, a TFL1-LIke Gene of Apple, Retards the Transition from the Vegetative to Reproductive Phase in Transgenic Arabidopsis,” Plant Science, Vol. 168, No. 1, 2005, pp. 95-104. doi:10.1016/j.plantsci.2004.07.024
[42] V. Dal Cin, F. Rizzini, A. Botton and P. Tonutti, “The Ethylene Biosynthetic and Signal Transduction Pathways Are Differently Affected by 1-MCP in Apple and Peach Fruit,” Postharvest Biology and Technology, Vol. 42, No. 2, 2006, pp. 125-133.
[43] H. Link, “Significance of Flower and Fruit Thinning on Fruit Quality,” Plant Growth Regulation, Vol. 31, No. 1-2, 2000, pp. 17-26. doi:10.1023/A:1006334110068
[44] V. Dal Cin, G. Galla, A. Boschetti, A. Dorigoni, R. Velasco and A. Ramina, “Ethylene Involvement in Auxin Transport during Apple Fruitlet Abscission. (Malus × domestica L. Borkh.),” Advances in Plant Ethylene Research, Vol. 2, 2007, pp. 89-93.
[45] V. Dal Cin, G. Galla and A. Ramina, “MdACO Expression during Abscission. The Use of 33P Labeled Primers in Transcript Quantitation,” Molecular Biotechnology, Vol. 36, No. 1, 2007, pp. 9-13. doi:10.1007/s12033-007-0004-6
[46] V. Dal Cin, M. Danesin, F. Rizzini and A. Ramina, “RNA Extraction from Plant Tissues: The Use of Calcium to Precipitate Contaminating Pectic Sugars,” Molecular Biotechnology, Vol. 31, No. 2, 2005 pp. 113-120. doi:10.1385/MB:31:2:113
[47] P. Nguyen and V. Dal Cin, “The Role of Light on Foliage Colour Development in Coleus (Solenostemon scutellariodes (L.) Codd),” Plant Physiology and Biochemistry, Vol. 47, No. 10, 2009, pp. 934-945.
[48] C. Schleiermacher, “GeneFisher—Software Support for the Detection of Postulated Genes,” International Conference on Intelligent Systems for Molecular Biology, Vol. 4, 1996, pp. 68-77.
[49] S. Altschul, T. Madden, A. Schaffer, J. Zhang, Z. Zhang, W. Miller and D. Lipman, “Gapped BLAST and PSI- BLAST: A New Generation of Protein Database Search Programs,” Nucleic Acids Research, Vol. 25, No. 17, 1997, pp. 3389-3402. doi:10.1093/nar/25.17.3389
[50] K. Tamura, J. Dudley, M. Nei and S. Kumar, (2007). “MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) Software Version 4.0,” Molecular Biology and Evolution, Vol. 24, No. 8, 2007, pp. 1596-1599. doi:10.1093/molbev/msm092
[51] L. Parenicova, S. de Folter, M. Kieffer, D. S. Horner, C. Favalli, J. Busscher, H. E. Cook, R. M. Ingram, M. M. Kater, B. Davies, G. C. Angenent and L. Colombo, “Molecular and Phylogenetic Analyses of the Complete MA- DS-Box Transcription Factor Family in Arabidopsis: New Openings to the MADS World,” The Plant Cell, Vol. 15, No. 7, 2003, pp. 1538-1551. doi:10.1105/tpc.011544
[52] L. C. Hileman, J. F. Sundstrom, A. Litt, M. Chen, T. Shumba and V. F. Irish, “Molecular and Phylogenetic Analyses of the MADS-Box Gene Family in Tomato,” Molecular Biology and Evolution, Vol. 23, No. 11, 2006, pp. 2245-2258. doi:10.1093/molbev/msl095
[53] J. Vrebalov, D. Ruezinsky, V. Padmanabhan, R. White, D. Medrano, R. Drake, W. Schuch and J. Giovannoni, “A MADS-Box Gene Necessary for Fruit Ripening at the Tomato Ripening-Inhibitor (Rin) Locus,” Science, Vol. 296, No. 5566, 2002, pp. 343-346.
[54] E. Tani, A. N. Polidoros, E. Flemetakis, C. Stedel, C. Kalloniati, K. Demetriou, P. Katinakis and A. S. Tsaftaris, “Characterization and Expression Analysis of AGAMOUS-Like, SEEDSTICK-Like, and SEPALLATA-Like MADS-Box Genes in Peach (Prunus persica) Fruit,” Plant Physiology and Biochemistry, Vol. 47, No. 8, 2009, pp. 690-700. doi:10.1016/j.plaphy.2009.03.013
[55] V. Cevik, C. Ryder, A. Popovich, K. Manning, G. King and G. Seymour, “A FRUITFULL-like Gene Is Associated with Genetic Variation for Fruit Flesh Firmness in Apple (Malus domestica Borkh.),” Tree Genetics & Genomes, Vol. 6, No. 2, 2010, pp. 271-279. doi:10.1007/s11295-009-0247-4
[56] J. Vrebalov, I. L. Pan, A. Javier, M. Arroyo, R. McQuinn, M. Y. Chung, M. Poole, J. Rose, G. Seymour, S. Grandillo, J. Giovannoni and V. F. Irish, “Fleshy Fruit Expansion and Ripening Are Regulated by the Tomato SHATTERPROOF Gene TAGL1,” The Plant Cell, Vol. 21, No. 10, 2009, pp. 3041-3062. doi:10.1105/tpc.109.066936
[57] J.-L. Yao, Y.-H Dong and B. A. M. Morris, “Parthenocarpic Apple Fruit Production Conferred by Transposon Insertion Mutations in a MADS-Box Transcription Factor,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 98, No. 3, 2001, pp. 1306-1311. doi:10.1073/pnas.031502498
[58] L. Mao, D. Begum, H.-W. Chuang, M. A. Budiman, E. J. Szymkowiak, E. E. Irish and R. A. Wing, “JOINTLESS Is a MADS-Box Gene Controlling Tomato Flower Abscission Zone Development,” Nature, Vol. 406, 2000, pp. 910-913.
[59] Y. Huang, H. Li, C. E. Hutchison, J. Laskey and J. J. Kieber, “Biochemical and Functional Analysis of CTR1, a Protein Kinase That Negatively Regulates Ethylene Signaling in Arabidopsis,” The Plant Journal, Vol. 33, No. 2, 2003, pp. 221-233. doi:10.1046/j.1365-313X.2003.01620.x
[60] L. Adams-Phillips, C. Barry, P. Kannan, J. Leclercq, M Bouzayen and J. Giovannoni, “Evidence that CTR1-Mediated Ethylene Signal Transduction in Tomato is Encoded by a Multigene Family Whose Members Display Distinct Regulatory Features,” Plant Molecular Biology, Vol. 54, No. 3, 2004, pp. 387-404. doi:10.1023/B:PLAN.0000036371.30528.26
[61] C. A. Frye, D. Z. Tang and R. W. Innes, “Negative Regulation of Defense Responses in Plants by a C. A. Conserved MAPKK Kinase,” Proceedings of the National Academy of Sciences of the United States of America, Vol. 98, No. 1, 2001, pp. 373-378. doi:10.1073/pnas.011405198
[62] Z. Lin, L. Alexander, R. Hackett and D. Grierson, “Le- CTR2, a CTR1-Like Protein Kinase from Tomato, Plays a Role in Ethylene Signalling, Development and Defence,” The Plant Journal, Vol. 54, No. 6, 2008, pp. 1083-1093. doi:10.1111/j.1365-313X.2008.03481.x
[63] H.-L. Zhu, B.-Z. Zhu, Y. Shao, X.-G. Wang, X.-J. Lin, Y.-H. Xie, Y.-C. Li, H.-Y. Gao and Y. B. Luo, “Tomato Fruit Development and Ripening Are Altered by the Silencing of LeEIN2 Gene,” Journal of Integrative Plant Biology, Vol. 48, No. 12, 2006, pp. 1478-1485. doi:10.1111/j.1744-7909.2006.00366.x
[64] D. Gallie and T. Young, “The Ethylene Biosynthetic and Perception Machinery Is Differentially Expressed during Endosperm and Embryo Development in Maize,” Molecular Genetics and Genomics, Vol. 271, No. 3, 2004, pp. 267-281.
[65] V. Dal Cin, M. Danesin, A. Botton, A. Boschetti, A. Dorigoni and A. Ramina, “Ethylene and Preharvest Drop: The Effect of AVG and NAA on Fruit Abscission in Apple (Malus domestica L. Borkh),” Plant Growth Regulation, Vol. 56, No. 3, 2008 pp. 317-325. doi:10.1007/s10725-008-9312-5
[66] A. Botton, G. Eccher, C. Forcato, A. Ferrarini, M. Begheldo, M. Zermiani, S. Moscatello, A. Battistelli, R. Velasco, B. Ruperti and A. Ramina, “Signalling Pathways Mediating the Induction of Apple Fruitlet Abscission,” Plant Physiology, Vol. 155, No. 1, pp. 185-208.
[67] E. Katz, P. Lagunes, J. Riov, D. Weiss and E. Goldschmidt, “Molecular and Physiological Evidence Suggests the Existence of a System II-Like Pathway of Ethylene Production in Non-Climacteric Citrus Fruit,” Planta, Vol. 219, No. 2, 2004, pp. 243-252.
[68] S. T. Malcomber and E. A. Kellogg, “SEPALLATA Gene Diversification: Brave New Whorls,” Trends in Plant Science, Vol. 10, No. 9, 2005, pp. 427-435. doi:10.1016/j.tplants.2005.07.008
[69] A. Mazzucato, I. Olimpieri, F. Siligato, M. E. Picarella and G. P. Soressi, “Characterization of Genes Controlling Stamen Identity and Development in a Parthenocarpic Tomato Mutant Indicates a Role for the DEFICIENS Ortholog in the Control of Fruit Set,” Physiologia Plantarum, Vol. 132, No. 4, 2008, pp. 526-537. doi:10.1111/j.1399-3054.2007.01035.x
[70] C. Ampomah-Dwamena, B. A. Morris, P. Sutherland, B. Veit and J.-L. Yao, “Down-Regulation of TM29, a Tomato SEPALLATA Homolog, Causes Parthenocarpic Fruit Development and Floral Reversion,” Plant Physiology, Vol. 130, No. 2, 2002, pp. 605-617.

comments powered by Disqus

Copyright © 2020 by authors and Scientific Research Publishing Inc.

Creative Commons License

This work and the related PDF file are licensed under a Creative Commons Attribution 4.0 International License.