Meyve Gelişimi ve Olgunlaşmasında Rol Oynayan Gen Düzenleyici Aktörler

Year 2016, Volume: 26 Issue: 2, 288 - 299, 30.06.2016

Behcet İnal , Koray Özrenk Serdar Altıntaş

Abstract

Meyveler genel olarak Angiospermlerin ayırt edici özelliğidir. Meyveler çok farklı form ve şekillerde meydana gelebilirler. Ayrıca meyveler, insanlar için mineraller, vitaminler, lifler ve antioksidanlar sağlayarak tamamlayıcı diyetin önemli bir kısmını oluştururlar. Meyvelerin olgunlaşması çok karışık bir süreçtir ve gelişimsel süreçle oldukça koordineli bir şekilde meydana gelir. Olgunlaşma işlemi, perikarp katmanlarının kademeli olarak yumuşaması ve/veya odunlaşması, şekerlerin, asitlerin, pigmentlerin biriktirilmesi ve uçucu bileşiklerin açığa çıkması gibi olayları kontrol eden binlerce gen tarafından düzenlenir. Meyve olgunlaşmasının ardındaki genetik ve moleküler mekanizmayı derinlemesine anlamak meyve üretimi ve kalitesinin gelişmesi açısından kilit bir öneme sahiptir. Bu bağlamda son zamanlarda meyve gelişimi ve olgunlaşması üzerinde rol oynayan mikroRNA’lar (miRNA), transkripsiyon faktörleri (TF), uzun kodlanmayan RNA’lar (lnc RNA), gibi genetik aktörler hızla keşfedilmektedir. Ayrıca günümüzde etkili  genom düzenleyici bir teknik olan düzenli aralıklarla bölünmüş palindromik tekrar kümeleri (CRISPR-Cas9) sistemi ve epigenetik yaklaşımlar da meyve gelişiminde rol oynayan moleküler mekanizmaların belirlenmesi için kullanılmaktadır.

Gene Regulatory Actors Involved in Fruit Development and Ripening

Abstract

Fruits are a distinctive features for Angiosperms. They may occur in many different form and shape. Furthermore, fruits are a rich source of supplementary diet, providing various nutrition such as vitamins, minerals, fibers and antioxidants for human. The maturation of fruits is very complex and highly coordinated with developmental process. Maturation process is regulated by thousands of genes controlling events such as gradual softening, or/and lignification  of pericarp layers, accumulation of sugars, acids and pigments, releasing of volatile compounds. Gaining a better and deeper understanding of the mechanism behind fruit maturation plays a key role for fruit production and improvement of quality. In this context, a number of genetic actors regulating fruit development and maturation such as microRNA's, transcription factors and long non-coding RNAs (IncRNAs) have been discovered. Nowadays, Clustered regularly-interspaced short palindromic repeats (CRISPR-Cas9) which is very effective genom regulatory technique and epigenetic approach are used to determine the molecular mechanisms involved in fruit development.

References

• Alba R, et al. (2005). "Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development." The Plant Cell 17(11): 2954-2965.
• Aharonı A, Keızer, LCP, Bouwmeester, HJ, Sun Z, Alvarezhuerta M, Verhoeven HA, Blaas J, Vanhouwelingen AMML, Devos RCH, Vandervoet H, Jansen R., Guis M, Mol J, Davis RW, Schena M, Vantunen AJ, and O’connel AP, 2000. Identification of the SAAT gene involved in strawberry flavor biogenesis by use of DNA microarrays, Plant Cell 12 (2000), pp. 647– 661.
• Aukerman M J, Sakai H (2003). Regulation of flowering time and floral organ identity by a microRNA and its APETALA2-like target genes. The Plant Cell 15, 2730–2741.
• Barry C S and Giovannoni J J (2006). "Ripening in the tomato Green-ripe mutant is inhibited by ectopic expression of a protein that disrupts ethylene signaling." Proceedings of the National Academy of Sciences 103(20): 7923-7928.
• Barry C S, et al. (2008). "Amino acid substitutions in homologs of the STAY-GREEN protein are responsible for the green-flesh and chlorophyll retainer mutations of tomato and pepper." Plant Physiology 147(1): 179-187.
• Bemer M, et al. (2012). "The tomato FRUITFULL homologs TDR4/FUL1 and MBP7/FUL2 regulate etylene-independent aspects of fruit ripening." The Plant Cell 24(11): 4437-4451.
• Bi F, et al (2015). Identification of miRNAs involved in fruit ripening in Cavendish bananas by deep sequencing. BMC genomics. 16;1 : 1.
• Brooks C, et al. (2014). Efficient gene editing in tomato in the first generation using the clustered regularly interspaced short palindromic repeats/CRISPR-associated9 system. Plant Physiology. 166;3 : 1292-1297.
• Carrari F, et al. (2006). "Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior." Plant Physiology 142(4): 1380-1396.
• Cevik V, et al. (2010). "A FRUITFULL-like gene is associated with genetic variation for fruit flesh firmness in apple (Malus domestica Borkh.)." Tree Genetics & Genomes 6(2): 271-279.
• Chai J, et al. (2015). Bioinformatic identification and expression analysis of banana MicroRNAs and their targets. PloS one. 10;4 : e0123083.
• Christian M, et al. (2010). Targeting DNA double-strand breaks with TAL effector nucleases. Genetics. 186;2 : 757-761.
• Cuperus J T, et al.(2011). Evolution and functional diversification of MIRNA genes. The Plant Cell. 23;2 : 431-442.
• Deluc L G, et al. (2007). "Transcriptomic and metabolite analyses of Cabernet Sauvignon grape berry development." BMC genomics 8(1): 1.
• D’Hont A, et al. ( 2012). The banana Musa acuminata genome and the evolution of monocotyledonous plants. Nature. 488;7410 : 213-217.
• Debat H J and D A Ducasse (2014). Plant microRNAs: recent advances and future challenges. Plant Molecular Biology Reporter.32; 6 : 1257-1269.
• Elitzur T, et al. (2010). "The regulation of MADS-box gene expression during ripening of banana and their regulatory interaction with ethylene." Journal of Experimental Botany 61(5): 1523-1535.
• Elkon R, et al. (2013). Alternative cleavage and polyadenylation: extent, regulation and function. Nature Reviews Genetics. 14;7 : 496-506.
• Enfissi E M, et al. (2010). "Integrative transcript and metabolite analysis of nutritionally enhanced DE-ETIOLATED1 downregulated tomato fruit." The Plant Cell 22(4): 1190-1215.
• Eriksson O, Friis E M and Lofgren P. (2000). Seed size, fruit size, and dispersal systems in angiosperms from the early cretaceous to the late tertiary. Am. Nat. 156, 47–58. doi: 10.1086/303367
• Fait A, et al. (2008). "Reconfiguration of the achene and receptacle metabolic networks during strawberry fruit development." Plant Physiology 148(2): 730-750.
• Gagne J M, et al. (2004). Arabidopsis EIN3-binding F-box 1 and 2 form ubiquitin-protein ligases that repress ethylene action and promote growth by directing EIN3 degradation. Proceedings of the National Academy of Sciences of the United States of America. 101,17: 6803-6808.
• Gandikota M, Birkenbihl R P, Hohmann S, Cardon GH, Saedler H, Huijser P (2007).
• The miRNA156/157 recognition element in the 3’ UTR of the Arabidopsis
• SBP box gene SPL3 prevents early flowering by translational inhibition in
• seedlings. Plant J. 49(4):683–93.
• Gao C, et al. (2015). MicroRNA profiling analysis throughout tomato fruit development and ripening reveals potential regulatory role of RIN on microRNAs accumulation. Plant biotechnology journal.13;3: 370-382.
• Giménez E, et al. (2010). "Functional analysis of the Arlequin mutant corroborates the essential role of the Arlequin/TAGL1 gene during reproductive development of tomato." PLoS One 5(12): e14427.
• Giovannoni J J, Noensie E N, Ruezinsky D M, Lu X, Tracy S L, Ganal M W, et al. (1995). Molecular genetic analysis of the ripeninginhibitor and non-ripening loci of tomato: a first step in genetic mapbased cloning of fruit ripening genes. Mol. Gen. Genet. 248, 195–206. doi:10.1007/BF02190801
• Giovannoni J (2001). Molecular biology of fruit maturation and ripening. Annu. Rev. Plant Physiol. Plant Mol. Biol. 52, 725–749. doi: 10.1146/ annurev.arplant.52.1.725
• Giovannoni J J (2007). Fruit ripening mutants yield insights into ripening control. Current opinion in plant biology. 10;3: 283-289.
• Grimplet J, et al. (2007). "Tissue-specific mRNA expression profiling in grape berry tissues." BMC genomics 8(1): 1.
• Guo H and J R Ecker (2003). Plant responses to ethylene gas are mediated by SCF EBF1/EBF2-dependent proteolysis of EIN3 transcription factor. Cell. 115;6 : 667-677.
• Guo H S, et al. (2005). MicroRNA directs mRNA cleavage of the transcription factor NAC1 to downregulate auxin signals for Arabidopsis lateral root development. The Plant Cell.17;5 : 1376-1386.
• Gutierrez L, et al. (2009). Phenotypic plasticity of adventitious rooting in Arabidopsis is controlled by complex regulation of AUXIN RESPONSE FACTOR transcripts and microRNA abundance. The Plant Cell.21;10:3119-3132.
• Gündoğdu R ÇV (2009). RNA İnterferans (RNAi). Erciyes Üniversitesi Fen Bilimleri Enstitüsü Dergisi. 25(1-2):34-47.
• Hamilton, A, et al. (1990). Antisense gene that inhibits synthesis of the hormone ethylene in transgenic plants.
• Hileman L C, et al. (2006). Molecular and phylogenetic analyses of the MADS-box gene family in tomato. Molecular Biology and Evolution 23(11): 2245-2258.
• Hyun T K, et al. (2014). De-novo RNA sequencing and metabolite profiling to identify genes involved in anthocyanin biosynthesis in Korean black raspberry (Rubus coreanus Miquel). PloS one. 9;2: e88292.
• Itkin M, et al. (2009). TOMATO AGAMOUS‐LIKE 1 is a component of the fruit ripening regulatory network. The Plant Journal. 60;6 : 1081-1095.
• Jaakola L, et al. (2010). A SQUAMOSA MADS box gene involved in the regulation of anthocyanin accumulation in bilberry fruits. Plant Physiology 153(4): 1619-1629.
• Ito J Y, M Kitagawa, N Ihashi, K Yabe, J Kimbara, J Yasuda, H Ito, T Inakuma,
• S Hiroi, T Kasumi (2008). DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN, Plant J. 55, 212e223.
• Jinek M, et al. (2012). A programmable dual-RNA–guided DNA endonuclease in adaptive bacterial immunity. Science. 337;6096 : 816-821.
• Karlova R, et al. (2013). Identification of microRNA targets in tomato fruit development using high-throughput sequencing and degradome analysis. Journal of experimental botany. 64;7: 1863-1878.
• Karoğlu Z (2012). Karpuzda (citrullus lanatus l.) izole edilmiş erf transkripsiyon faktör genlerinin karakterizasyonu: SDÜ Fen Bilimleri Enstitüsü.
• Kim Y G, et al. (1996). Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. Proceedings of the National Academy of Sciences. 93;3 : 1156-1160.
• Kumar R, et al. (2014). Role of plant hormones and their interplay in development and ripening of fleshy fruits. Journal of experimental botany. 65;16: 4561-4575.
• Lanahan M B, et al. (1994). "The never ripe mutation blocks ethylene perception in tomato." The Plant Cell 6(4): 521-530.
• Latchman DS. Transcription factors: an overview. The international journal of biochemistry & cell biology.;29(12):1305-12.
• Lea U S, et al. (2007). Nitrogen deficiency enhances expression of specific MYB and bHLH transcription factors and accumulation of end products in the flavonoid pathway. Planta. 225;5 : 1245-1253.
• Lee J M, et al. (2012). "Combined transcriptome, genetic diversity and metabolite profiling in tomato fruit reveals that the ethylene response factor SlERF6 plays an important role in ripening and carotenoid accumulation." The Plant Journal 70(2): 191-204.
• Lee S J, et al. (2004). "Digging deeper into the plant cell wall proteome." Plant physiology and Biochemistry 42(12): 979-988.
• Li J F, et al. (2013). Multiplex and homologous recombination-mediated genome editing in Arabidopsis and Nicotiana benthamiana using guide RNA and Cas9. Nature biotechnology. 31;8 : 688-691.
• Lin Z, et al. (2008). SlTPR1, a tomato tetratricopeptide repeat protein, interacts with the ethylene receptors NR and LeETR1, modulating ethylene and auxin responses and development. Journal of experimental botany. 59;15 : 4271-4287.
• Liu G, et al. (2012). Transcriptomic analysis of ‘Suli’pear Pyrus pyrifolia white pear group buds during the dormancy by RNA-Seq. BMC genomics. 13;1: 1.
• Liu Y, et al. (2004). Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proceedings of the National Academy of Sciences of the United States of America 101(26): 9897-9902.
• Lombardo V A, et al. (2011). Metabolic profiling during peach fruit development and ripening reveals the metabolic networks that underpin each developmental stage. Plant Physiology 157(4): 1696-1710.
• Manning K, et al. (2006). A naturally occurring epigenetic mutation in a gene encoding an SBP-box transcription factor inhibits tomato fruit ripening. Nature genetics. 38;8 : 948-952.
• Martel C, et al. (2011). The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiology. 157;3:1568-1579.
• Matas A J, et al. (2011). Tissue-and cell-type specific transcriptome profiling of expanding tomato fruit provides insights into metabolic and regulatory specialization and cuticle formation. The Plant Cell 23(11): 3893-3910.
• McMurchie E, et al. (1972). Treatment of fruit with propylene gives information about the biogenesis of ethylene.
• Meng Y, Shao C, Wang H, Jin Y (2012). Targetmimics: an embeddedlayer of microRNA-involved gene regulatory networks in plants, BMC Genomics, 13:197. doi:10.1186/1471-2164-13-197.
• Moxon S, et al. (2008). Deep sequencing of tomato short RNAs identifies microRNAs targeting genes involved in fruit ripening. Genome research. 18;10:1602-1609.
• Mustilli A C, et al. (1999). Phenotype of the tomato high pigment-2 mutant is caused by a mutation in the tomato homolog of DEETIOLATED1. The Plant Cell 11(2): 145-157.
• Osorio S, et al. (2011). Systems biology of tomato fruit development: combined transcript, protein, and metabolite analysis of tomato transcription factor (nor, rin) and ethylene receptor (Nr) mutants reveals novel regulatory interactions. Plant Physiology 157(1): 405-425.
• Osorio S, et al. (2012). Integrative comparative analyses of transcript and metabolite profiles from pepper and tomato ripening and development stages uncovers species-specific patterns of network regulatory behavior. Plant Physiology 159(4): 1713-1729.
• Pan I L, et al. (2010). Functional diversification of AGAMOUS lineage genes in regulating tomato flower and fruit development. Journal of experimental botany: erq046.
• Picton S, et al. (1993). Altered fruit ripening and leaf senescence in tomatoes expressing an antisense ethylene‐forming enzyme transgene. The Plant Journal. 3;3 : 469-481.
• Pnueli L, et al. (1994). Isolation of the tomato AGAMOUS gene TAG1 and analysis of its homeotic role in transgenic plants. The Plant Cell 6(2): 163-173.
• Potuschak T, et al. (2003). EIN3-dependent regulation of plant ethylene hormone signaling by two Arabidopsis F box proteins: EBF1 and EBF2. Cell. 115;6 : 679-689.
• Rohrmann J, et al. (2011). Combined transcription factor profiling, microarray analysis and metabolite profiling reveals the transcriptional control of metabolic shifts occurring during tomato fruit development. The Plant Journal 68(6): 999-1013.
• Rose J K. et al. (2004). Tackling the plant proteome: practical approaches, hurdles and experimental tools. The plant journal 39(5): 715-733.
• Saravanan R S. and J K Rose (2004). A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues." Proteomics 4(9): 2522-2532.
• Seymour G B, 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(3): 1179-1188.
• Seymour G B, et al. (2013). Fruit development and ripening. Annual review of plant biology. 64: 219-241.
• Silva E M, et al. (2014) . microRNA156‐targeted SPL/SBP box transcription factors regulate tomato ovary and fruit development. The Plant Journal. 78;4:604-618.
• Smaczniak C, et al. (2012). Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies. Development 139(17): 3081-3098.
• Sorin C, Declerck M, Christ A, Blein T, Ma L, Lelandais-Briere C, et al. (2014). A miR169 isoform regulates specific NF-YA targets and root architecture in Arabidopsis. New Phytol. 202(4):1197–211.
• Tang Q, et al. (2011). An efficient approach to finding Siraitia grosvenorii triterpene biosynthetic genes by RNA-seq and digital gene expression analysis. BMC genomics. 12;1 : 343.
• Tieman D M, et al. (2001). Members of the tomato LeEIL EIN3‐like gene family are functionally redundant and regulate ethylene responses throughout plant development. The Plant Journal. 26;1 : 47-58.
• Thompson AJ, Tor M, Barry CS, Vrebalov J, Orfila C, et al. (1999). Molecular and genetic characterization of a novel pleiotropic tomato-ripening mutant. Plant Physiol. 120:383–89
• Topisirovic I, et al. (2011). Cap and cap‐binding proteins in the control of gene expression. Wiley Interdisciplinary Reviews: RNA. 2;2 : 277-298.
• Tsuji H, Aya K, Ueguchi-Tanaka M, et al. 2006. GAMYB controls different sets of genes and is differentially regulated by microRNA in aleurone cells and anthers. The Plant Journal 47, 427–444.
• Vrebalov J, et al. (2002). A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296(5566): 343-346.
• Vrebalov J, et al. (2009). Fleshy fruit expansion and ripening are regulated by the tomato SHATTERPROOF gene TAGL1. The Plant Cell. 21;10 : 3041-3062.
• Vriezen W H, et al. (2008). Changes in tomato ovary transcriptome demonstrate complex hormonal regulation of fruit set. New Phytologist 177(1): 60-76.
• Wang L, et al. (2015). Evolutionary and expression analysis of a MADS-box gene superfamily involved in ovule development of seeded and seedless grapevines. Molecular Genetics and Genomics. 290;3: 825-846.
• Wang J W, Czech B, Weigel D (2009). miR156-regulated SPL transcription factors
• define an endogenous flowering pathway in Arabidopsis thaliana. Cell.
• (4):738–49
• Wen J Z, et al. (2014). A contig-based strategy for the genome-wide discovery of microRNAs without complete genome resources. PloS one. 9;2:e88179.
• Wu H J, Wang Z M, Wang M, Wang X J (2013). Wide spread long non coding RNAs as endogenous target mimics for micro RNAs in plant. PlantPhysiol, 161, (4):1875-1884.
• Wu H X, et al. (2014). Transcriptome and proteomic analysis of mango Mangifera indica Linn fruits. Journal of proteomics. 105: 19-30.
• Yang X, et al. (2008). Expression profile analysis of genes involved in cell wall regeneration during protoplast culture in cotton by suppression subtractive hybridization and macroarray. Journal of experimental botany. 59; 13: 3661-3674.
• Yang Y, et al. (2010). Silencing Sl-EBF1 and Sl-EBF2 expression causes constitutive ethylene response phenotype, accelerated plant senescence, and fruit ripening in tomato. Journal of experimental botany. 61;3 : 697-708.
• Ye C Y, Xu H, Shen E, Liu Y, Wang Y, Shen Y, Qiu J, Zhu Q H, Fan L (2014). Genome-wide identification of non-codingRNAs interacted with microRNAs in soybean. Front PlantSci5:743. doi:10.3389/fpls.2014.00743.
• Yu K, et al. (2012). Transcriptome changes during fruit development and ripening of sweet orange Citrus sinensis . BMC genomics. 13;1: 1.
• Zamboni A, et al. (2010). Identification of putative stage-specific grapevine berry biomarkers and omics data integration into networks. Plant Physiology 154(3): 1439-1459.
• Zhang X, et al. (2006). Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126(6): 1189-1201.
• Zeng S, et al. (2014). Comparative analysis of anthocyanin biosynthesis during fruit development in two Lycium species. Physiologia plantarum. 150;4: 505-516.
• Zeng S, et al. (2015). Identification and characterization of miRAsin ripening fruit of Lycium barbarum L. using high-throughput sequenching. Plant Metabolism and chemodiversity. 778; 6.
• Zenoni S, et al. (2010). Characterization of transcriptional complexity during berry development in Vitis vinifera using RNA-Seq. Plant Physiology. 152;4: 1787-1795.