Transcript Profiles of Auxin Efflux Carrier and IAA-Amido Synthetase Genes Suggest the Role of Auxin on Apple (<i>Malus</i> × <i>domestica</i>) Fruit Maturation Patterns — Oak Academic Publishing
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Transcript Profiles of Auxin Efflux Carrier and IAA-Amido Synthetase Genes Suggest the Role of Auxin on Apple (<i>Malus</i> × <i>domestica</i>) Fruit Maturation Patterns
Tree Fruit Research Laboratory, United States Department of Agriculture, Wenatchee, WA, USA
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Department of Horticulture Science, Kyungpook National University, Daegu, Republic of Korea
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Tree Fruit Research Laboratory, United States Department of Agriculture, Wenatchee, WA, USA
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Tree Fruit Research and Extension Center, Washington State University, Wenatchee, WA, USA
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Tree Fruit Research Laboratory, United States Department of Agriculture, Wenatchee, WA, USA
1 Tree Fruit Research Laboratory, United States Department of Agriculture, Wenatchee, WA, USA
2 Department of Horticulture Science, Kyungpook National University, Daegu, Republic of Korea
3 Tree Fruit Research Laboratory, United States Department of Agriculture, Wenatchee, WA, USA
4 Tree Fruit Research and Extension Center, Washington State University, Wenatchee, WA, USA
5 Tree Fruit Research Laboratory, United States Department of Agriculture, Wenatchee, WA, USA
Auxin has been suggested to play an essential role in regulating apple fruit maturation and ripening, though the molecular function of auxin and its interaction with ethylene during apple fruit development are largely unknown. To understand the function of auxin during apple fruit maturation and ripening, auxin efflux carrier and IAA-amido synthetase encoding genes were identified from the apple genome based on the results of previous microarray analysis. The expression patterns of these genes were analyzed using qRT-PCR during 10 - 12 weeks of fruit maturation for two apple cultivars: “Golden Delicious” (GD) and “Cripps Pink” (CP), which have the distinct patterns of maturation progression. Our results showed that the expressions of auxin efflux carrier and IAA-amido synthetase genes have a correlation with the timing of ethylene biosynthesis pathway activation in both cultivars. The earlier and stronger expression of MdGH3.102 and MdAECFP1 in the fruit of GD, a mid-season cultivar, correlates with the earlier activation of a pre-climacteric ethylene biosynthesis gene of MdACS3, compared with that in CP, a late-ripening apple cultivar. Results of exogenous IAA treatment indicated that the expression patterns of the genes were regulated in a fruit maturity dependent manner. Our results suggested that the dynamics of the auxin level in apple fruit cortex could be one of the key factors influencing the timing of ethylene biosynthesis pathway activation and consequently contributed to the control of the apple maturation progression.
Giovannoni, J.J. (2004) Genetic Regulation of Fruit Development and Ripening. Plant Cell, 16, S170-S180. http://dx.doi.org/10.1105/tpc.019158
McAtee, P., Karim, S., Schaffer, R. and David, K. (2013) A Dynamic Interplay between Phytohormones Is Required for Fruit Development, Maturation, and Ripening. Frontiers in Plant Science, 4, 79. http://dx.doi.org/10.3389/fpls.2013.00079
Osorio, S., Scossa, F. and Fernie, A.R. (2013) Molecular Regulation of Fruit Ripening. Frontiers in Plant Science, 4, 198. http://dx.doi.org/10.3389/fpls.2013.00198
Kazan, K. and Manners, J.M. (2008) Jasmonate Signaling: Toward an Integrated View. Plant Physiology, 146, 1459-1468. http://dx.doi.org/10.1104/pp.107.115717
Kondo, S., Meemak, S., Ban, Y., Moriguchi, T. and Harada, T. (2009) Effects of Auxin and Jasmonates on 1-Amino-cyclopropane-1-carboxylate (ACC) Synthase and ACC Oxidase Gene Expression during Ripening of Apple Fruit. Postharvest Biology and Technology, 51, 281-284. http://dx.doi.org/10.1016/j.postharvbio.2008.07.012
Pauwels, L., Inze, D. and Goossens, A. (2009) Jasmonate-Inducible Gene: What Does It Mean? Trends in Plant Sciences, 14, 87-91. http://dx.doi.org/10.1016/j.tplants.2008.11.005
Shinshi, H. (2008) Ethylene-Regulated Transcription and Crosstalk with Jasmonic Acid. Plant Science, 175, 18-23. http://dx.doi.org/10.1016/j.plantsci.2008.03.017
Lau, O.W., Luk, S.F. and Wong, K.S. (1986) Background Correction Method for the Determination of Ascorbic Acid in Soft Drinks, Fruit Juices and Cordials Using Direct Ultraviolet Spectrophotometry. Analyst, 111, 665-670. http://dx.doi.org/10.1039/an9861100665
Barry, C.S., Llop-Tous, M.I. and Grierson, D. (2000) The Regulation of 1-Aminocyclopropane-1-carboxylic Acid Synthase Gene Expression during the Transition from System-1 to System-2 Ethylene Synthesis in Tomato. Plant Physiology, 123, 979-986. http://dx.doi.org/10.1104/pp.123.3.979
Oraguzie, N.C., Volz, R.K., Whitworth, C.J., Bassett, H.C.M., Hall, A.J. and Gardiner, S.E. (2007) Influence of Md-ACS1 Allelotype and Harvest Season within an Apple Germplasm Collection on Fruit Softening during Cold Air Storage. Postharvest Biology and Technology, 44, 212-219. http://dx.doi.org/10.1016/j.postharvbio.2006.12.013
Rosenfield, C.L., Kiss, E. and Hrazdina, G. (1996) MdACS-2 (Accession No. U73815) and MdACS-3 (Accession No. U73816): Two New 1-Aminocyclopropane-1-carboxylate Synthase Sub Ripening Apple Fruit (PGR96-122). Plant Physiology, 112, 1735.
Varanasi, V., Shin, S., Mattheis, J., Rudell, D. and Zhu, Y. (2011) Expression Profiles of the MdACS3 Gene Suggest a Function as an Accelerator of Apple (Malus × domestica) Fruit Ripening. Postharvest Biology and Technology, 62, 141-148. http://dx.doi.org/10.1016/j.postharvbio.2011.05.005
Devoghalaere, F., Doucen, T., Guitton, B., Keeling, J., Payne, W., Ling, T.J., Ross, J.J., Hallett, I.C., Gunaseelan, K., Dayatilake, G.A., Diak, R., Breen, K.C., Tustin, D.S., Costes, E., Chagne, D., Schaffer, R.J. and David, K.M. (2012) A Genomics Approach to Understanding the Role of Auxin in Apple (Malus × domestica) Fruit Size Control. BMC Plant Biology, 12, 7. http://dx.doi.org/10.1186/1471-2229-12-7
Zhu, Y., Zheng, P., Varanasi, V., Shin, S., Main, D., Curry, E. and Mattheis, J.P. (2012) Multiple Plant Hormones and Cell Wall Metabolism Regulate Apple Fruit Maturation Patterns and Texture Attributes. Tree Genetics & Genomes, 8, 1389-1406. http://dx.doi.org/10.1007/s11295-012-0526-3
Simon, S. and Petrasek, J. (2011) Why Plants Need More than One Type of Auxin. Plant Science, 180, 454-460. http://dx.doi.org/10.1016/j.plantsci.2010.12.007
Zhao, Y. (2010) Auxin Biosynthesis and Its Role in Plant Development. Annual Review of Plant Biology, 61, 49-64. http://dx.doi.org/10.1146/annurev-arplant-042809-112308
Ljung, K. (2013) Auxin Metabolism and Homeostasis during Plant Development. Development, 140, 943-950. http://dx.doi.org/10.1242/dev.086363
Leyser, O. (2010) The Power of Auxin in Plants. Plant Physiology, 154, 501-505. http://dx.doi.org/10.1104/pp.110.161323
Hayashi, K. (2012) The Interaction and Integration of Auxin Signaling Components. Plant and Cell Physiology, 53, 965-975. http://dx.doi.org/10.1093/pcp/pcs035
Vernoux, T., Kronenberger, J., Grandjean, O., Laufs, P. and Traas, J. (2000) PIN-FORMED 1 Regulates Cell Fate at the Periphery of the Shoot Apical Meristem. Development, 127, 5157-5165.
Xu, M., Zhu, L., Shou, H. and Wu, P. (2005) A PIN1 Family Gene, OsPIN1, Involved in Auxin-Dependent Adventitious Root Emergence and Tillering in Rice. Plant and Cell Physiology, 46, 1674-1681. http://dx.doi.org/10.1093/pcp/pci183
Carraro, N., Forestan, C., Canova, S., Traas, J. and Varotto, S. (2006) ZmPIN1a and ZmPIN1b Encode Two Novel Putative Candidates for Polar Auxin Transport and Plant Architecture Determination of Maize. Plant Physiology, 142, 254-264. http://dx.doi.org/10.1104/pp.106.080119
Zazimalova, E., Murphy, A.S., Yang, H., Hoyerova, K. and Hosek, P. (2010) Auxin Transporters—Why So Many? Cold Spring Harbor Perspectives in Biology, 2, a001552. http://dx.doi.org/10.1101/cshperspect.a001552
Swarup, R. and Bennett, M. (2003) Auxin Transport: The Fountain of Life in Plants? Developmental Cell, 5, 824-826. http://dx.doi.org/10.1016/S1534-5807(03)00370-8
Friml, J. (2010) Subcellular Trafficking of PIN Auxin Efflux Carriers in Auxin Transport. European Journal of Cell Biology, 89, 231-235. http://dx.doi.org/10.1016/j.ejcb.2009.11.003
Feraru, E. and Friml, J. (2008) PIN Polar Targeting. Plant Physiology, 147, 1553-1559. http://dx.doi.org/10.1104/pp.108.121756
Vanneste, S. and Friml, J. (2009) Auxin: A Trigger for Change in Plant Development. Cell, 136, 1005-1016. http://dx.doi.org/10.1016/j.cell.2009.03.001
Korasick, D.A., Enders, T.A. and Strader, L.C. (2013) Auxin Biosynthesis and Storage Forms. Journal of Experimental Botany, 64, 2541-2555. http://dx.doi.org/10.1093/jxb/ert080
Ding, X., Cao, Y., Huang, L., Zhao, J., Xu, C., Li, X. and Wang, S. (2008) Activation of the Indole-3-Acetic Acid-Amido Synthetase GH3-8 Suppresses Expansin Expression and Promotes Salicylate- and Jasmonate-Independent Basal Immunity in Rice. Plant Cell, 20, 228-240. http://dx.doi.org/10.1105/tpc.107.055657
Seymour, G.B., Ostergaard, L., Chapman, N.H., Knapp, S. and Martin, C. (2013) Fruit Development and Ripening. Annual Review of Plant Biology, 64, 219-241. http://dx.doi.org/10.1146/annurev-arplant-050312-120057
de Jong, M., Mariani, C. and Vriezen, W.H. (2009) The Role of Auxin and Gibberellin in Tomato Fruit Set. Journal of Experimental Botany, 60, 1523-1532. http://dx.doi.org/10.1093/jxb/erp094
Srivastava, A. and Handa, A.K. (2005) Hormonal Regulation of Tomato Fruit Development: A Molecular Perspective. Journal of Plant Growth Regulation, 24, 67-82. http://dx.doi.org/10.1007/s00344-005-0015-0
Stern, R.A., Flaishman, M., Applebaum, S. and Ben-Arie, R. (2007) Effect of Synthetic Auxins on Fruit Development of “Bing” Cherry (Prunus avium L.). Scientia Horticulturae, 114, 275-280. http://dx.doi.org/10.1016/j.scienta.2007.07.010
Pattison, R.J. and Catala, C. (2012) Evaluating Auxin Distribution in Tomato (Solanum lycopersicum) through an Analysis of the PIN and AUX/LAX Gene Families. Plant Journal, 70, 585-598. http://dx.doi.org/10.1111/j.1365-313X.2011.04895.x
Nishio, S., Moriguchi, R., Ikeda, H., Takahashi, H., Takahashi, H., Fujii, N., Guilfoyle, T.J., Kanahama, K. and Kanayama, Y. (2010) Expression Analysis of the Auxin Efflux Carrier Family in Tomato Fruit Development. Planta, 232, 755-764. http://dx.doi.org/10.1007/s00425-010-1211-0
Mounet, F., Moing, A., Kowalczyk, M., Rohrmann, J., Petit, J., Garcia, V., Maucourt, M., Yano, K., Deborde, C., Aoki, K., Bergès, H., Granell, A., Fernie, A.R., Bellini, C., Rothan, C. and Lemaire-Chamley, M. (2012) Down-Regulation of a Single Auxin Efflux Transport Protein in Tomato Induces Precocious Fruit Development. Journal of Experimental Botany, 63, 4901-4917. http://dx.doi.org/10.1093/jxb/ers167
Dal Cin, V., Velasco, R. and Ramina, A. (2009) Dominance Induction of Fruitlet Shedding in Malus × domestica (L. Borkh): Molecular Changes Associated with Polar Auxin Transport. BMC Plant Biology, 9, 139. http://dx.doi.org/10.1186/1471-2229-9-139
Schaffer, R.J., Ireland, H.S., Ross, J.J., Ling, T.J. and David, K.M. (2013) SEPALLATA1/2-Suppressed Mature Apples Have Low Ethylene, High Auxin and Reduced Transcription of Ripening-Related Genes. AoB Plants, 5, 1-10.
Trainotti, L., Tadiello, A. and Casadoro, G. (2007) The Involvement of Auxin in the Ripening of Climacteric Fruits Comes of Age: The Hormone Plays a Role of Its Own and Has an Intense Interplay with Ethylene in Ripening Peaches. Journal of Experimental Botany, 58, 3299-3308. http://dx.doi.org/10.1093/jxb/erm178
Zaharah, S., Singh, Z., Symons, G. and Reid, J. (2012) Role of Brassinosteroids, Ethylene, Abscisic Acid, and Indole-3-Acetic Acid in Mango Fruit Ripening. Journal of Plant Growth Regulation, 31, 363-372. http://dx.doi.org/10.1007/s00344-011-9245-5
Torrigiani, P., Bressanin, D., Beatriz Ruiz, K., Tadiello, A., Trainotti, L., Bonghi, C., Ziosi, V. and Costa, G. (2012) Spermidine Application to Young Developing Peach Fruits Leads to a Slowing Down of Ripening by Impairing Ripening-Related Ethylene and Auxin Metabolism and Signaling. Physiologia Plantarum, 146, 86-98. http://dx.doi.org/10.1111/j.1399-3054.2012.01612.x
Symons, G.M., Chua, Y.J., Ross, J.J., Quittenden, L.J., Davies, N.W. and Reid, J.B. (2012) Hormonal Changes during Non-Climacteric Ripening in Strawberry. Journal of Experimental Botany, 63, 4741-4750. http://dx.doi.org/10.1093/jxb/ers147
Pitts, R.J., Cernac, A. and Estelle, M. (1998) Auxin and Ethylene Promote Root Hair Elongation in Arabidopsis. Plant Journal, 16, 553-560. http://dx.doi.org/10.1046/j.1365-313x.1998.00321.x
Rahman, A., Hosokawa, S., Oono, Y., Amakawa, T., Goto, N. and Tsurumi, S. (2002) Auxin and Ethylene Response Interactions during Arabidopsis Root Hair Development Dissected by Auxin Influx Modulators. Plant Physiology, 130, 1908-1917. http://dx.doi.org/10.1104/pp.010546
Swarup, R., Parry, G., Graham, N., Allen, T. and Bennett, M. (2002) Auxin Cross-Talk: Integration of Signalling Pathways to Control Plant Development. Plant Molecular Biology, 49, 409-424. http://dx.doi.org/10.1023/A:1015250929138
Ishiki, Y., Oda, A., Yaegashi, Y., Orihara, Y., Arai, T., Hirabayashi, T., Nakagawa, H. and Sato, T. (2000) Cloning of an Auxin-Responsive 1-Aminocyclopropane-1-carboxylate Synthase Gene (CMe-ACS2) from Melon and the Expression of ACS Genes in Etiolated Melon Seedlings and Melon Fruits. Plant Science, 159, 173-181. http://dx.doi.org/10.1016/S0168-9452(00)00298-3
Tatsuki, M., Nakajima, N., Fujii, H., Shimada, T., Nakano, M., Hayashi, K.I., Hayama, H., Yoshioka, H. and Nakamura, Y. (2013) Increased Levels of IAA Are Required for System 2 Ethylene Synthesis Causing Fruit Softening in Peach (Prunus persica L. Batsch). Journal of Experimental Botany, 64, 1049-1059. http://dx.doi.org/10.1093/jxb/ers381
Velasco, R., Zharkikh, A., Affourtit, J., Dhingra, A., Cestaro, A., Kalyanaraman, A., Fontana, P., Bhatnagar, S.K., Troggio, M., Pruss, D., Salvi, S., Pindo, M., Baldi, P., Castelletti, S., Cavaiuolo, M., Coppola, G., Costa, F., Cova, V., Dal Ri, A., Goremykin, V., Komjanc, M., Longhi, S., Magnago, P., Malacarne, G., Malnoy, M., Micheletti, D., Moretto, M., Perazzolli, M., Si-Ammour, A., Vezzulli, S., Zini, E., Eldredge, G., Fitzgerald, L.M., Gutin, N., Lanchbury, J., Macalma, T., Mitchell, J.T., Reid, J., Wardell, B., Kodira, C., Chen, Z., Desany, B., Niazi, F., Palmer, M., Koepke, T., Jiwan, D., Schaeffer, S., Krishnan, V., Wu, C., Chu, V.T., King, S.T., Vick, J., Tao, Q., Mraz, A., Stormo, A., Stormo, K., Bogden, R., Ederle, D., Stella, A., Vecchietti, A., Kater, M.M., Masiero, S., Lasserre, P., Lespinasse, Y., Allan, A.C., Bus, V., Chagne, D., Crowhurst, R.N., Gleave, A.P., Lavezzo, E., Fawcett, J.A., Proost, S., Rouze, P., Sterck, L., Toppo, S., Lazzari, B., Hellens, R.P., Durel, C.E., Gutin, A., Bumgarner, R.E., Gardiner, S.E., Skolnick, M., Egholm, M., Van de Peer, Y., Salamini, F. and Viola, R. (2010) The Genome of the Domesticated Apple (Malus × domestica Borkh.). Nature Genetics, 42, 833-839. http://dx.doi.org/10.1038/ng.654
Brookfield, P., Murphy, P., Harker, R. and MacRae, E. (1997) Starch Degradation and Starch Pattern Indices; Interpretation and Relationship to Maturity. Postharvest Biology and Technology, 11, 23-30. http://dx.doi.org/10.1016/S0925-5214(97)01416-6
Fan, X., Argenta, L. and Mattheis, J.P. (2002) Interactive Effects of 1-MCP and Temperature on “Elberta” Peach Quality. HortScience, 37, 134-138.
Gasic, K., Hernandez, A. and Korban, S. (2004) RNA Extraction from Different Apple Tissues Rich in Polyphenols and Polysaccharides for cDNA Library Construction. Plant Molecular Biology Reporter, 22, 437-438. http://dx.doi.org/10.1007/BF02772687
Zhu, Y., Rudell, D.R. and Mattheis, J.P. (2008) Characterization of Cultivar Differences in Alcohol Acyltransferase and 1-Aminocyclopropane-1-carboxylate Synthase Gene Expression and Volatile Ester Emission during Apple Fruit Maturation and Ripening. Postharvest Biology and Technology, 49, 330-339. http://dx.doi.org/10.1016/j.postharvbio.2008.03.015
Janick, J., Cummins, J.N., Brown, S.K. and Hemmat, M. (1996) Chapter 1: Apples. In: Janick, J. and Moore, J.N., Eds., Fruit Breed, Volume 1: Tree and Tropical Fruits, John Wiley & Sons, Inc., Hoboken, 1-77.
Varanasi, V., Shin, S., Johnson, F., Mattheis, J. and Zhu, Y. (2013) Differential Suppression of Ethylene Biosynthesis and Receptor Genes in “Golden Delicious” Apple by Preharvest and Postharvest 1-MCP Treatments. Journal of Plant Growth Regulation, 32, 585-595. http://dx.doi.org/10.1007/s00344-013-9326-8
Lv, J., Rao, J., Johnson, F., Shin, S. and Zhu, Y. (2014) Genome-Wide Identification of Jasmonate Biosynthetic Genes and Characterization of Their Expression Profiles during Apple (Malus × domestica) Fruit Maturation. Plant Growth Regulation, 75, 355-364.
Shin, S., Lv, J., Fazio, G., Mazzola, M. and Zhu, Y. (2014) Transcriptional Regulation of Ethylene and Jasmonate Mediated Defense Response in Apple (Malus domestica) Root during Pythium ultimum Infection. Horticulture Research, 1, 1-10.
Frenkel, C. and Dyck, R. (1973) Auxin Inhibition of Ripening in Bartlett Pears. Plant Physiology, 51, 6-9. http://dx.doi.org/10.1104/pp.51.1.6
Mousdale, D.M.A. and Knee, M. (1981) Indolyl-3-Acetic Acid and Ethylene Levels in Ripening Apple Fruits. Journal of Experimental Botany, 32, 753-758. http://dx.doi.org/10.1093/jxb/32.4.753
Mravec, J., Skupa, P., Bailly, A., Hoyerova, K., Krecek, P., Bielach, A., Petrasek, J., Zhang, J., Gaykova, V., Stierhof, Y.D., Dobrev, P.I., Schwarzerova, K., Rolcik, J., Seifertova, D., Luschnig, C., Benkova, E., Zazimalova, E., Geisler, M. and Friml, J. (2009) Subcellular Homeostasis of Phytohormone Auxin Is Mediated by the ER-Localized PIN5 Transporter. Nature, 459, 1136-1140. http://dx.doi.org/10.1038/nature08066
Barbez, E., Kubes, M., Rolcik, J., Beziat, C., Pencik, A., Wang, B., Rosquete, M.R., Zhu, J., Dobrev, P.I., Lee, Y., Zazimalova, E., Petrasek, J., Geisler, M., Friml, J. and Kleine-Vehn, J. (2012) A Novel Putative Auxin Carrier Family Regulates Intracellular Auxin Homeostasis in Plants. Nature, 485, 119-122. http://dx.doi.org/10.1038/nature11001