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PLOS ONE  2014 

A Non-Climacteric Fruit Gene CaMADS-RIN Regulates Fruit Ripening and Ethylene Biosynthesis in Climacteric Fruit

DOI: 10.1371/journal.pone.0095559

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Abstract:

MADS-box genes have been reported to play a major role in the molecular circuit of developmental regulation. Especially, SEPALLATA (SEP) group genes play a central role in the developmental regulation of ripening in both climacteric and non-climacteric fruits. However, the mechanisms underlying the regulation of SEP genes to non-climacteric fruits ripening are still unclear. Here a SEP gene of pepper, CaMADS-RIN, has been cloned and exhibited elevated expression at the onset of ripening of pepper. To further explore the function of CaMADS-RIN, an overexpressed construct was created and transformed into ripening inhibitor (rin) mutant tomato plants. Broad ripening phenotypes were observed in CaMADS-RIN overexpressed rin fruits. The accumulation of carotenoid and expression of PDS and ZDS were enhanced in overexpressed fruits compared with rin mutant. The transcripts of cell wall metabolism genes (PG, EXP1 and TBG4) and lipoxygenase genes (TomloxB and TomloxC) accumulated more abundant compared to rin mutant. Besides, both ethylene-dependent genes including ACS2, ACO1, E4 and E8 and ethylene-independent genes such as HDC and Nor were also up-regulated in transgenic fruits at different levels. Moreover, transgenic fruits showed approximately 1–3 times increase in ethylene production compared with rin mutant fruits. Yeast two-hybrid screen results indicated that CaMADS-RIN could interact with TAGL1, FUL1 and itself respectively as SlMADS-RIN did in vitro. These results suggest that CaMADS-RIN affects fruit ripening of tomato both in ethylene-dependent and ethylene-independent aspects, which will provide a set of significant data to explore the role of SEP genes in ripening of non-climacteric fruits.

References

[1]  Ampomah-Dwamena C, Morris BA, Sutherland P, Veit B, Yao J-L (2002) Down-regulation of TM29, a tomato SEPALLATA homolog, causes parthenocarpic fruit development and floral reversion. Plant physiology 130: 605–617. doi: 10.1104/pp.005223
[2]  Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. The Plant Cell 16: S170–S180. doi: 10.1105/tpc.019158
[3]  Goff SA, Klee HJ (2006) Plant volatile compounds: sensory cues for health and nutritional value? Science Signaling 311: 815. doi: 10.1126/science.1112614
[4]  Abeles F, Morgan P, Saltveit M Jr (1992) Jr Ethylene in plant biology. San Diego: Academic.
[5]  Hiwasa K, Kinugasa Y, Amano S, Hashimoto A, Nakano R, et al. (2003) Ethylene is required for both the initiation and progression of softening in pear (Pyrus communis L.) fruit. Journal of experimental botany 54: 771–779. doi: 10.1093/jxb/erg073
[6]  Alexander L, Grierson D (2002) Ethylene biosynthesis and action in tomato: a model for climacteric fruit ripening. Journal of experimental botany 53: 2039–2055. doi: 10.1093/jxb/erf072
[7]  Sandhu JS, Krasnyanski SF, Domier LL, Korban SS, Osadjan MD, et al. (2000) Oral immunization of mice with transgenic tomato fruit expressing respiratory syncytial virus-F protein induces a systemic immune response. Transgenic research 9: 127–135.
[8]  Krasnyanski SF, Sandhu J, Domier LL, Buetow DE, Korban SS (2001) Effect of an enhanced CaMV 35S promoter and a fruit-specific promoter on uida gene expression in transgenic tomato plants. In Vitro Cellular & Developmental Biology-Plant 37: 427–433. doi: 10.1007/s11627-001-0075-1
[9]  Kesanakurti D, Kolattukudy PE, Kirti PB (2012) Fruit-specific overexpression of wound-induced tap1 under E8 promoter in tomato confers resistance to fungal pathogens at ripening stage. Physiologia Plantarum 146: 136–148. doi: 10.1111/j.1399-3054.2012.01626.x
[10]  Giovannoni JJ (2007) Fruit ripening mutants yield insights into ripening control. Current opinion in plant biology 10: 283–289. doi: 10.1016/j.pbi.2007.04.008
[11]  Giovannoni J (2001) Molecular biology of fruit maturation and ripening. Annual review of plant biology 52: 725–749. doi: 10.1146/annurev.arplant.52.1.725
[12]  Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, et al. (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296: 343–346. doi: 10.1126/science.1068181
[13]  Vrebalov J, Pan IL, Arroyo AJM, McQuinn R, Chung MY, et al. (2009) Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. The Plant Cell 21: 3041–3062. doi: 10.1105/tpc.109.066936
[14]  Itkin M, Seybold H, Breitel D, Rogachev I, Meir S, et al. (2009) TOMATO AGAMOUS-LIKE 1 is a component of the fruit ripening regulatory network. The Plant Journal 60: 1081–1095. doi: 10.1111/j.1365-313x.2009.04064.x
[15]  Busi MV, Bustamante C, D’Angelo C, Hidalgo-Cuevas M, Boggio SB, et al. (2003) MADS-box genes expressed during tomato seed and fruit development. Plant molecular biology 52: 801–815. doi: 10.1023/a:1025001402838
[16]  Bemer M, Karlova R, Ballester AR, Tikunov YM, Bovy AG, et al. (2012) The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate ethylene-Independent aspects of fruit ripening. The Plant Cell 24: 4437–4451. doi: 10.1105/tpc.112.103283
[17]  Dong T, Hu Z, Deng L, Wang Y, Zhu M, et al. (2013) A tomato MADS-box transcription factor, SlMADS1, acts as a negative regulator of fruit ripening. Plant physiology 163: 1026–1036. doi: 10.1104/pp.113.224436
[18]  Chervin C, El-Kereamy A, Roustan J-P, Latché A, Lamon J, et al. (2004) Ethylene seems required for the berry development and ripening in grape, a non-climacteric fruit. Plant Science 167: 1301–1305. doi: 10.1016/j.plantsci.2004.06.026
[19]  Cazzonelli CI, Cavallaro AS, Botella JR (1998) Cloning and characterisation of ripening-induced ethylene biosynthetic genes from non-climacteric pineapple (Ananas comosus) fruits. Functional Plant Biology 25: 513–518. doi: 10.1071/pp98013
[20]  Trainotti L, Pavanello A, Casadoro G (2005) Different ethylene receptors show an increased expression during the ripening of strawberries: does such an increment imply a role for ethylene in the ripening of these non-climacteric fruits? Journal of experimental botany 56: 2037–2046. doi: 10.1093/jxb/eri202
[21]  Seymour GB, Ryder CD, Cevik V, Hammond JP, Popovich A, et al. (2011) A SEPALLATA gene is involved in the development and ripening of strawberry (Fragaria×ananassa Duch.) fruit, a non-climacteric tissue*. Journal of experimental botany 62: 1179–1188. doi: 10.1093/jxb/erq360
[22]  Fujisawa M, Nakano T, Ito Y (2011) Identification of potential target genes for the tomato fruit-ripening regulator RIN by chromatin immunoprecipitation. BMC plant biology 11: 26. doi: 10.1186/1471-2229-11-26
[23]  Fujisawa M, Shima Y, Higuchi N, Nakano T, Koyama Y, et al. (2012) Direct targets of the tomato-ripening regulator RIN identified by transcriptome and chromatin immunoprecipitation analyses. Planta 235: 1107–1122. doi: 10.1007/s00425-011-1561-2
[24]  Ito Y, Kitagawa M, Ihashi N, Yabe K, Kimbara J, et al. (2008) DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN. The Plant Journal 55: 212–223. doi: 10.1111/j.1365-313x.2008.03491.x
[25]  Leseberg CH, Eissler CL, Wang X, Johns MA, Duvall MR, et al. (2008) Interaction study of MADS-domain proteins in tomato. Journal of experimental botany 59: 2253–2265. doi: 10.1093/jxb/ern094
[26]  Elitzur T, Vrebalov J, Giovannoni JJ, Goldschmidt EE, Friedman H (2010) The regulation of MADS-box gene expression during ripening of banana and their regulatory interaction with ethylene. Journal of experimental botany 61: 1523–1535. doi: 10.1093/jxb/erq017
[27]  Ireland HS, Yao JL, Tomes S, Sutherland PW, Nieuwenhuizen N, et al. (2013) Apple SEPALLATA1/2-like genes control fruit flesh development and ripening. The Plant Journal 73: 1044–1056. doi: 10.1111/tpj.12094
[28]  Smith CJ, Watson CF, Morris PC, Bird CR, Seymour GB, et al. (1990) Inheritance and effect on ripening of antisense polygalacturonase genes in transgenic tomatoes. Plant molecular biology 14: 369–379. doi: 10.1007/bf00028773
[29]  Smith DL, Abbott JA, Gross KC (2002) Down-regulation of tomato β-galactosidase 4 results in decreased fruit softening. Plant physiology 129: 1755–1762. doi: 10.1104/pp.011025
[30]  Rose JK, Cosgrove DJ, Albersheim P, Darvill AG, Bennett AB (2000) Detection of expansin proteins and activity during tomato fruit ontogeny. Plant physiology 123: 1583–1592. doi: 10.1104/pp.123.4.1583
[31]  Kumar R, Sharma MK, Kapoor S, Tyagi AK, Sharma AK (2012) Transcriptome analysis of rin mutant fruit and in silico analysis of promoters of differentially regulated genes provides insight into LeMADS-RIN-regulated ethylene-dependent as well as ethylene-independent aspects of ripening in tomato. Molecular Genetics and Genomics 287: 189–203. doi: 10.1007/s00438-011-0671-7
[32]  Picton S, Gray JE, Payton S, Barton SL, Lowe A, et al. (1993) A histidine decarboxylase-like mRNA is involved in tomato fruit ripening. Plant molecular biology 23: 627–631. doi: 10.1007/bf00019310
[33]  Tigchelaar E, Tomes M, Kerr E, Barman R (1973) A new fruit ripening mutant, non-ripening (nor). Rep Tomato Genet Coop 23: 33.
[34]  Kobayashi K, Yasuno N, Sato Y, Yoda M, Yamazaki R, et al. (2012) Inflorescence meristem identity in rice is specified by overlapping functions of three AP1/FUL-like MADS box genes and PAP2, a SEPALLATA MADS box gene. The Plant Cell Online 24: 1848–1859. doi: 10.1105/tpc.112.097105
[35]  Lee S, Chung E-J, Joung Y-H, Choi D (2010) Non-climacteric fruit ripening in pepper: increased transcription of EIL-like genes normally regulated by ethylene. Functional & integrative genomics 10: 135–146. doi: 10.1007/s10142-009-0136-9
[36]  Fraser PD, Truesdale MR, Bird CR, Schuch W, Bramley PM (1994) Carotenoid biosynthesis during tomato fruit development (evidence for tissue-specific gene expression). Plant Physiology 105: 405–413.
[37]  Bramley PM (2002) Regulation of carotenoid formation during tomato fruit ripening and development. Journal of experimental botany 53: 2107–2113. doi: 10.1093/jxb/erf059
[38]  Bramley P (1993) Inhibition of carotenoid biosynthesis. Carotenoids in photosynthesis: Springer. 127–159.
[39]  Bird CR, Ray JA, Fletcher JD, Boniwell JM, Bird AS, et al. (1991) Using antisense RNA to study gene function: inhibition of carotenoid biosynthesis in transgenic tomatoes. Nature Biotechnology 9: 635–639. doi: 10.1038/nbt0791-635
[40]  Mellway RD, Lund ST (2013) Interaction analysis of grapevine MIKCc-type MADS transcription factors and heterologous expression of putative véraison regulators in tomato. Journal of Plant Physiology 170: 1424–1433. doi: 10.1016/j.jplph.2013.05.010
[41]  Oeller PW, Lu M, Taylor LP, Pike DA, Theologis A (1991) Reversible inhibition of tomato fruit senescence by antisense RNA. Science (New York, NY) 254: 437. doi: 10.1126/science.1925603
[42]  Blume B, Grierson D (2003) Expression of ACC oxidase promoter–GUS fusions in tomato and Nicotiana plumbaginifolia regulated by developmental and environmental stimuli. The Plant Journal 12: 731–746. doi: 10.1046/j.1365-313x.1997.12040731.x
[43]  Hamilton A, Lycett G, Grierson D (1990) Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants. Nature 346: 284–287. doi: 10.1038/346284a0
[44]  Lincoln JE, Cordes S, Read E, Fischer RL (1987) Regulation of gene expression by ethylene during Lycopersicon esculentum (tomato) fruit development. Proceedings of the National Academy of Sciences 84: 2793–2797. doi: 10.1073/pnas.84.9.2793
[45]  Sung S-K, Moon Y-H, Chung J-E, Lee S-Y, Park HG, et al. (2001) Characterization of MADS box genes from hot pepper. Molecules and cells 11: 352–359.
[46]  Chen G, Hackett R, Walker D, Taylor A, Lin Z, et al. (2004) Identification of a specific isoform of tomato lipoxygenase (TomloxC) involved in the generation of fatty acid-derived flavor compounds. Plant physiology 136: 2641–2651. doi: 10.1104/pp.104.041608
[47]  Penarrubia L, Aguilar M, Margossian L, Fischer RL (1992) An antisense gene stimulates ethylene hormone production during tomato fruit ripening. The Plant Cell 4: 681–687. doi: 10.2307/3869526
[48]  Kneissl ML, Deikman J (1996) The tomato E8 gene influences ethylene biosynthesis in fruit but not in flowers. Plant Physiology 112: 537–547.
[49]  Fray RG, Grierson D (1993) Identification and genetic analysis of normal and mutant phytoene synthase genes of tomato by sequencing, complementation and co-suppression. Plant molecular biology 22: 589–602. doi: 10.1007/bf00047400
[50]  Mann V, Pecker I, Hirschberg J (1994) Cloning and characterization of the gene for phytoene desaturase (Pds) from tomato (Lycopersicon esculentum). Plant molecular biology 24: 429–434. doi: 10.1007/bf00024111
[51]  Pecker I, Chamovitz D, Linden H, Sandmann G, Hirschberg J (1992) A single polypeptide catalyzing the conversion of phytoene to zeta-carotene is transcriptionally regulated during tomato fruit ripening. Proceedings of the National Academy of Sciences 89: 4962–4966. doi: 10.1073/pnas.89.11.4962
[52]  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. doi: 10.1093/jxb/50.335.793
[53]  Ferrie BJ, Beaudoin N, Burkhart W, Bowsher CG, Rothstein SJ (1994) The cloning of two tomato lipoxygenase genes and their differential expression during fruit ripening. Plant Physiology 106: 109–118. doi: 10.1104/pp.106.1.109
[54]  Forth D, Pyke KA (2006) The suffulta mutation in tomato reveals a novel method of plastid replication during fruit ripening. Journal of experimental botany 57: 1971–1979. doi: 10.1093/jxb/erj144

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