Chin Bull Bot ›› 2018, Vol. 53 ›› Issue (6): 856-866.doi: 10.11983/CBB17185

• SPECIAL TOPICS • Previous Articles    

Advances in the Molecular and Physiological Mechanisms of Early Development of Tomato Fruit

Zhang Tianpeng, Yang Xinghong*()   

  1. State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Tai’an 271000, China
  • Received:2017-10-12 Online:2018-12-05 Published:2018-11-01
  • Contact: Yang Xinghong E-mail:xhyang@sdau.edu.cn

Abstract:

Tomato is one of the most widely cultivated and the most popular vegetable crops. It is also an important model plant of Solanaceae. The development of tomato fruit can be divided into early fruit development and fruit ripening, but fruit morphological structure and size are mainly determined by the early stage of fruit development. This review focuses on the early development of tomato fruit, including the molecular mechanism of plant hormones, cell cycle, epigenetics, and source-sink metabolism, to understand the basic biological problems of plant growth and development, as well as promoting the application of basic theoretical research results in production.

Key words: tomato, early development, plant hormones, cell cycle, epigenetic, source-sink metabolism

Figure 1

Fruit development in tomato The development of tomato fruit can be divided into early fruit growth and fruit ripening, but for fruit morphological structure and fruit size, they are mainly determined the early stage of fruit development. In the period of tomato fruit early development, the characteristic is cell division and cell expansion. For the cell division process, the number of cell layers across the pericarp will be increased and fruit will be bigger than before. Fruit growth then proceeds into the cell expansion phase, in this phase, cell layers will not increase but cell enlargement occurred, leading to size increase of tomato fruit rapidly. The main characteristic of fruit ripening is the changes of fruit color and metabolites in tomato."

Figure 2

Related pathways regulate early fruit growth in tomato Arrows represent positive regulation, barred arrows represent negative regulation. CDKA1: Cyclin-dependent protein kinase A1; CDKB: Cyclin-dependent protein kinase B; CWIN: Cell wall invertase; GLK2: Golden 2-like; HMT: Histone methyltransferase; IMA: Inhibitor of meristem activity; SWEET: Sugar transporter"

[1] 许智宏, 李家洋 (2006). 中国植物激素研究: 过去、现在和未来. 植物学通报 23, 433-442.
doi: 10.3969/j.issn.1674-3466.2006.05.001
[2] Adachi S, Nobusawa T, Umeda M (2009). Quantitative and cell type-specific transcriptional regulation of A-type cyclin-dependent kinase in Arabidopsis thaliana. Dev Biol 329, 306-314.
doi: 10.1016/j.ydbio.2009.03.002 pmid: 19285489
[3] Albacete A, Cantero-Navarro E, Balibrea ME, GroBkinsky DK, De La Cruz González M, Martlnez-Andújar C, Smigocki AC, Roitsch T, Pérez-Alfocea F (2014). Hormonal and metabolic regulation of tomato fruit sink activity and yield under salinity.J Exp Bot 65, 6081-6095.
doi: 10.1093/jxb/eru347. pmid: 4203140
[4] Alpert KB, Grandillo S, Tanksley SD (1995). fw2.2: a major QTL controlling fruit weight is common to both red- and green-fruited tomato species. Theor Appl Genet 91, 994-1000.
doi: 10.1007/BF00223911 pmid: 24169988
[5] Alpert KB, Tanksley SD (1996). High-resolution mapping and isolation of a yeast artificial chromosome contig containing fw2.2: a major fruit weight quantitative trait locus in tomato. Proc Natl Acad Sci USA 93, 15503-15507.
doi: 10.1073/pnas.93.26.15503
[6] álvaro F, Royo C, Garcla del Moral LF, Villegas D (2008). Grain filling and dry matter translocation responses to source-sink modifications in a historical series of durum wheat.Crop Sci 48, 1523-1531.
doi: 10.2135/cropsci2007.10.0545
[7] Azzi L, Deluche C, Gévaudant F, Frangne N, Delmas F, Hernould M, Chevalier C (2015). Fruit growth-related genes in tomato.J Exp Bot 66, 1075-1086.
doi: 10.1093/jxb/eru527 pmid: 25573859
[8] Balibrea ME, Parra M, Bolarln MC, Pérez-Alfocea F (1999). Cytoplasmic sucrolytic activity controls tomato fruit growth under salinity.Funct Plant Biol 26, 561-568.
doi: 10.1071/PP99026
[9] Bermúdez L, de Godoy F, Baldet P, Demarco D, Osorio S, Quadrana L, Almeida J, Asis R, Gibon Y, Fernie AR, Rossi M, Carrari F (2014). Silencing of the tomato sugar partitioning affecting protein (SPA) modifies sink strength through a shift in leaf sugar metabolism.Plant J 77, 676-687.
doi: 10.1111/tpj.12418 pmid: 24372694
[10] Bermúdez L, Urias U, Milstein D, Kamenetzky L, Asis R, Fernie AR, Van Sluys MA, Carrari F, Rossi M (2008). A candidate gene survey of quantitative trait loci affecting chemical composition in tomato fruit.J Exp Bot 59, 2875-2890.
doi: 10.1093/jxb/ern146 pmid: 18552354
[11] Carrari F, Fernie AR (2006). Metabolic regulation underlying tomato fruit development. J Exp Bot 57, 1883-1897.
doi: 10.1093/jxb/erj020 pmid: 16449380
[12] Chan SWL, Henderson IR, Jacobsen SE (2005). Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6, 351-360.
[13] Chen LQ, Hou BH, Lalonde S, Takanaga H, Hartung ML, Qu XQ, Guo WJ, Kim JG, Underwood W, Chaudhuri B, Chermak D, Antony G, White FF, Somerville SC, Mudgett MB, Frommer WB (2010). Sugar transporters for intercellular exchange and nutrition of pathogens.Nature 468, 527-532.
doi: 10.1038/nature09606 pmid: 3000469
[14] Chen LQ, Qu XQ, Hou BH, Sosso D, Osorio S, Fernie AR, Frommer WB (2012). Sucrose efflux mediated by SWEET proteins as a key step for phloem transport.Science 335, 207-211.
doi: 10.1126/science.1213351 pmid: 22157085
[15] Cheniclet C, Rong WY, Causse M, Frangne N, Bolling L, Carde JP, Renaudin JP (2005). Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growth.Plant Phy- siol 139, 1984-1994.
doi: 10.1104/pp.105.068767
[16] Chevalier C, Bourdon M, Pirrello J, Cheniclet C, Gévaudant F, Frangne N (2014). Endoreduplication and fruit growth in tomato: evidence in favour of the karyoplasmic ratio theory.J Exp Bot 65, 2731-2746.
doi: 10.1093/jxb/ert366 pmid: 24187421
[17] Chinnusamy V, Zhu JK (2009). Epigenetic regulation of stress responses in plants.Curr Opin Plant Biol 12, 133-139.
doi: 10.1016/j.pbi.2008.12.006 pmid: 19179104
[18] Choudhary SP, Kanwar M, Bhardwaj R, Yu JQ, Tran LSP (2012). Chromium stress mitigation by polyamine-brassi- nosteroid application involves phytohormonal and physio- logical strategies in Raphanus sativus L. PLoS One 7, e33210.
[19] Cigliano RA, Sanseverino W, Cremona G, Ercolano MR, Conicella C, Consiglio FM (2013). Genome-wide analysis of histone modifiers in tomato: gaining an insight into their developmental roles.BMC Genomics 14, 57.
doi: 10.1186/1471-2164-14-57 pmid: 23356725
[20] Cong B, Barrero LS, Tanksley SD (2008). Regulatory change in YABBY-like transcription factor led to evolution of extreme fruit size during tomato domestication.Nat Genet 40, 800-804.
doi: 10.1038/ng.144 pmid: 18469814
[21] Czerednik A, Busscher M, Angenent GC, de Maagd RA (2015). The cell size distribution of tomato fruit can be changed by overexpression of CDKA1. Plant Biotechnol J 13, 259-268.
doi: 10.1111/pbi.12268 pmid: 25283700
[22] Czerednik A, Busscher M, Bielen BAM, Wolters-Arts M, de Maagd RA, Angenent GC (2012). Regulation of tomato fruit pericarp development by an interplay between CDKB and CDKA1 cell cycle genes. J Exp Bot 63, 2605-2617.
doi: 10.1093/jxb/err451 pmid: 3346228
[23] Damon S, Hewitt J, Nieder M, Bennett AB (1988). Sink metabolism in tomato fruit. II. Phloem unloading and sugar uptake.Plant Physiol 87, 731-736.
doi: 10.1104/pp.87.3.731 pmid: 16666216
[24] de Jong M, Wolters-Arts M, Garcla-Martlnez JL, Mariani C, Vriezen WH (2011). The Solanum lycopersicum AUXIN RESPONSE FACTOR 7 (SlARF7) mediates cross-talk between auxin and gibberellin signaling during tomato fruit set and development. J Exp Bot 62, 617-626.
doi: 10.1093/jxb/erq293 pmid: 20937732
[25] de Jong M, Wolters-Arts M, Schimmel BCJ, Stultiens CLM, de Groot PFM, Powers SJ, Tikunov YM, Bovy AG, Mariani C, Vriezen WH, Rieu I (2015). Solanum lycopersicum AUXIN RESPONSE FACTOR 9 regulates cell division activity during early tomato fruit development. J Exp Bot 66, 3405-3416.
doi: 10.1093/jxb/erv152 pmid: 4449553
[26] Feng SH, Cokus SJ, Zhang XY, Chen PY, Bostick M, Goll MG, Hetzel J, Jain J, Strauss SH, Halpern ME, Ukomad UC, Sadler KC, Pradhan S, Pellegrini M, Jacobsen SE (2010). Conservation and divergence of methylation patterning in plants and animals.Proc Natl Acad Sci USA 107, 8689-8694.
doi: 10.1073/pnas.1002720107 pmid: 20395551
[27] Fos M, Nuez F, Garcla-Martlnez JL (2000). The gene pat-2, which induces natural parthenocarpy, alters the gibberellin content in unpollinated tomato ovaries. Plant Physiol 122, 471-480.
doi: 10.1104/pp.122.2.471
[28] Frary A, Nesbitt TC, Frary A, Grandillo S, Van Der Knaap E, Cong B, Liu JP, Meller J, Elber R, Alpert KB, Tanksley SD (2000). fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289, 85-88.
doi: 10.1126/science.289.5476.85 pmid: 10884229
[29] Gao XP, Wang XF, Lu YF, Zhang LY, Shen YY, Liang Z, Zhang DP (2004). Jasmonic acid is involved in the water-stress-induced betaine accumulation in pear leaves.Plant Cell Environ 27, 497-507.
doi: 10.1111/j.1365-3040.2004.01167.x pmid: 15215509
[30] Gillaspy G, Ben-David H, Gruissem W (1993). Fruits: a developmental perspective.Plant Cell 5, 1439-1451.
doi: 10.1105/tpc.5.10.1439
[31] Giovannoni JJ (2004). Genetic regulation of fruit development and ripening.Plant Cell 16, S170-S180.
doi: 10.1105/tpc.019158 pmid: 15010516
[32] Gonzalez N, Gévaudant F, Hernould M, Chevalier C, Mouras A (2007). The cell cycle-associated protein kinase WEE1 regulates cell size in relation to endoreduplication in developing tomato fruit.Plant J 51, 642-655.
doi: 10.1111/j.1365-313X.2007.03167.x pmid: 17587306
[33] Hancock JT, Neill SJ, Wilson ID (2011). Nitric oxide and ABA in the control of plant function.Plant Sci 181, 555-559.
doi: 10.1016/j.plantsci.2011.03.017
[34] He YH (2012). Chromatin regulation of flowering.Trends Plant Sci 17, 556-562.
doi: 10.1016/j.tplants.2012.05.001
[35] Hemerly AS, Ferreira P, de Almeida Engler J, Van Montagu M, Engler G, Inzé D (1993). cdc2a expression in Arabidopsis is linked with competence for cell division. Plant Cell 5, 1711-1723.
doi: 10.2307/3869688 pmid: 8305869
[36] Ho LC (1996). The mechanism of assimilate partitioning and carbohydrate compartmentation in fruit in relation to the quality and yield of tomato.J Exp Bot 47, 1239-1243.
doi: 10.1093/jxb/47.Special_Issue.1239 pmid: 21245255
[37] Huang ZJ, van der Knaap E (2011). Tomato fruit weight 11.3 maps close to fasciated on the bottom of chromosome 11. Theor Appl Genet 123, 465-474.
[38] Iwakawa H, Shinmyo A, Sekine M (2006). Arabidopsis CDKA;1, a cdc2 homologue, controls proliferation of gene- rative cells in male gametogenesis. Plant J 45, 819-831.
[39] Jin Y, Ni DA, Ruan YL (2009). Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level.Plant Cell 21, 2072-2089.
doi: 10.1105/tpc.108.063719 pmid: 19574437
[40] Johannes F, Porcher E, Teixeira FK, Saliba-Colombani V, Simon M, Agier N, Bulski A, Albuisson J, Heredia F, Audigier P, Bouchez D, Dillmann C, Guerche P, Hospital F, Colot V (2009). Assessing the impact of transgenerational epigenetic variation on complex traits.PLoS Genet 5, e1000530.
doi: 10.1371/journal.pgen.1000530 pmid: 2696037
[41] Joubès J, Chevalier C, Dudits D, Heberle-Bors E, Inzé D, Umeda M, Renaudin JP (2000). CDK-related protein kinases in plants. In: Inzé D, ed. The Plant Cell Cycle. Dordrecht: Springer. pp. 607-620.
[42] Joubès J, Phan TH, Just D, Rothan C, Bergounioux C, Raymond P, Chevalier C (1999). Molecular and biochemical characterization of the involvement of cyclin- dependent kinase A during the early development of tomato fruit.Plant Physiol 121, 857-869.
doi: 10.1046/j.1365-2923.2000.00553.x pmid: 10557234
[43] Kit AH, Boureau L, Stammitti-Bert L, Rolin D, Teyssier E, Gallusci P (2010). Functional analysis of SlEZ1 a tomato Enhancer of zeste (E(z)) gene demonstrates a role in flower development. Plant Mol Biol 74, 201-213.
[44] Klee HJ, Giovannoni JJ (2011). Genetics and control of tomato fruit ripening and quality attributes.Annu Rev Genet 45, 41-59.
doi: 10.1146/annurev-genet-110410-132507 pmid: 22060040
[45] Kumar R, Khurana A, Sharma AK (2014). Role of plant hormones and their interplay in development and ripening of fleshy fruits.J Exp Bot 65, 4561-4575.
doi: 10.1093/jxb/eru277 pmid: 25028558
[46] Lauria M, Rossi V (2011). Epigenetic control of gene regulation in plants.Biochim Biophys Acta Gene Regul Mech 1809, 369-378.
doi: 10.1016/j.bbagrm.2011.03.002 pmid: 21414429
[47] Law JA, Jacobsen SE (2010). Establishing, maintaining and modifying DNA methylation patterns in plants and animals.Nat Rev Genet 11, 204-220.
doi: 10.1038/nrg2719
[48] Leiva-Neto JT, Grafi G, Sabelli PA, Dante RA, Woo YM, Maddock S, Gordon-Kamm WJ, Larkins BA (2004). A dominant negative mutant of cyclin-dependent kinase A reduces endoreduplication but not cell size or gene expression in maize endosperm.Plant Cell 16, 1854-1869.
doi: 10.1105/tpc.022178
[49] Li B, Carey M, Workman JL (2007). The role of chromatin during transcription.Cell 128, 707-719.
doi: 10.1016/j.cell.2007.01.015 pmid: 17320508
[50] Li N, Parsons BL, Liu DR, Mattoo AK (1992). Accumulation of wound-inducible ACC synthase transcript in tomato fruit is inhibited by salicylic acid and polyamines.Plant Mol Biol 18, 477-487.
doi: 10.1007/BF00040664 pmid: 1371404
[51] Lin T, Zhu GT, Zhang JH, Xu XY, Yu QH, Zheng Z, Zhang ZH, Lun YY, Li S, Wang XX, Huang ZJ, Li JM, Zhang CZ, Wang TT, Zhang YY, Wang AX, Zhang YC, Lin K, Li CY, Xiong GS, Xue YB, Mazzucato A, Causse M, Fei ZJ, Giovannoni JJ, Chetelat RT, Zamir D, Städler T, Li JF, Ye ZB, Du YC, Huang SW (2014). Genomic analyses provide insights into the history of tomato breeding.Nat Genet 46, 1220-1226.
doi: 10.1038/ng.3117 pmid: 25305757
[52] Lippman ZB, Semel Y, Zamir D (2007). An integrated view of quantitative trait variation using tomato interspecific introgression lines.Curr Opin Genet Dev 17, 545-552.
doi: 10.1016/j.gde.2007.07.007 pmid: 17723293
[53] Liu J, Van Eck J, Cong B, Tanksley SD (2002). A new class of regulatory genes underlying the cause of pear-shaped tomato fruit.Proc Natl Acad Sci USA 99, 13302-13306.
doi: 10.1073/pnas.162485999 pmid: 12242331
[54] Liu YH, Offler CE, Ruan YL (2016). Cell wall invertase promotes fruit set under heat stress by suppressing ROS- independent cell death.Plant Physiol 172, 163-180.
doi: 10.1104/pp.16.00959 pmid: 27462084
[55] Mariotti L, Picciarelli P, Lombardi L, Ceccarelli N (2011). Fruit-set and early fruit growth in tomato are associated with increases in indoleacetic acid, cytokinin, and bioactive gibberellin contents.J Plant Growth Regul 30, 405-415.
doi: 10.1007/s00344-011-9204-1
[56] Masood A, Per TS, Asgher M, Fatma M, Khan MIR, Rasheed F, Hussain SJ, Khan NA (2016). Glycine betaine: role in shifting plants toward adaptation under extreme environments. In: Iqbal N, Nazar R, Khan NA, eds. Osmolytes and Plants Acclimation to Changing Environment: Emerging Omics Technologies. New Delhi: Spring- er.pp. 69-82.
[57] Matsuo S, Kikuchi K, Fukuda M, Honda I, Imanishi S (2012). Roles and regulation of cytokinins in tomato fruit development.J Exp Bot 63, 5569-5579.
doi: 10.1093/jxb/ers207 pmid: 3444270
[58] McAtee P, Karim S, Schaffer R, David K (2013). A dynamic interplay between phytohormones is required for fruit development, maturation, and ripening.Front Plant Sci 4, 79.
doi: 10.3389/fpls.2013.00079 pmid: 3628358
[59] McCurdy DW, Dibley S, Cahyanegara R, Martin A, Patrick JW (2010). Functional characterization and RNAi-medi- ated suppression reveals roles for hexose transporters in sugar accumulation by tomato fruit.Mol Plant 3, 1049-1063.
doi: 10.1093/mp/ssq050 pmid: 20833733
[60] Mehta RA, Cassol T, Li N, Ali N, Handa AK, Mattoo AK (2002). Engineered polyamine accumulation in tomato enhances phytonutrient content, juice quality, and vine life.Nat Biotechnol 20, 613-618.
doi: 10.1038/nbt0602-613 pmid: 12042867
[61] Michaels SD (2009). Flowering time regulation produces much fruit.Curr Opin Plant Biol 12, 75-80.
doi: 10.1016/j.pbi.2008.09.005 pmid: 2644822
[62] Mirouze M, Paszkowski J (2011). Epigenetic contribution to stress adaptation in plants.Curr Opin Plant Biol 14, 267-274.
doi: 10.1016/j.pbi.2011.03.004 pmid: 21450514
[63] Mu Q, Huang ZJ, Chakrabarti M, Illa-Berenguer E, Liu XX, Wang YP, Ramos A, van der Knaap E (2017). Fruit weight is controlled by Cell Size Regulator encoding a novel protein that is expressed in maturing tomato fruits. PLoS Genet 13, e1006930.
doi: 10.1371/journal.pgen.1006930 pmid: 5560543
[64] Munos S, Ranc N, Botton E, Bérard A, Rolland S, Duffé P, Carretero Y, Le Paslier MC, Delalande C, Bouzayen M, Brunel D, Causse M (2011). Increase in tomato locule number is controlled by two single-nucleotide polymorphisms located near WUSCHEL. Plant Physiol 156, 2244-2254.
doi: 10.1104/pp.111.173997 pmid: 21673133
[65] Nguyen CV, Vrebalov JT, Gapper NE, Zheng Y, Zhong SL, Fei ZJ, Giovannoni JJ (2014). Tomato GOLDEN2-LIKE transcription factors reveal molecular gradients that function during fruit development and ripening.Plant Cell 26, 585-601.
doi: 10.1105/tpc.113.118794 pmid: 24510723
[66] Nitsch L, Kohlen W, Oplaat C, Charnikhova T, Cristescu S, Michieli P, Wolters-Arts M, Bouwmeester H, Mariani C, Vriezen WH, Rieu I (2012). ABA-deficiency results in reduced plant and fruit size in tomato.J Plant Physiol 169, 878-883.
doi: 10.1016/j.jplph.2012.02.004 pmid: 22424572
[67] Noreen S, Athar HUR, Ashraf M (2013). Interactive effects of watering regimes and exogenously applied osmoprotectants on earliness indices and leaf area index in cotton (Gossypium hirsutum L.) crop. Pak J Bot 45, 1873-1881.
[68] Ozga JA, Reinecke DM (2003). Hormonal interactions in fruit development.J Plant Growth Regul 22, 73-81.
doi: 10.1007/s00344-003-0024-9
[69] Pan Y, Bradley G, Pyke K, Ball G, Lu CG, Fray R, Marshall A, Jayasuta S, Baxter C, van Wijk R, Boyden L, Cade R, Chapman NH, Fraser PD, Hodgman C, Seymour GB (2013). Network inference analysis identifies an APRR2- Like gene linked to pigment accumulation in tomato and pepper fruits. Plant Physiol 161, 1476-1485.
doi: 10.1104/pp.112.212654 pmid: 23292788
[70] Park EJ, Jeknic Z, Chen THH, Murata N (2007). The codA transgene for glycinebetaine synthesis increases the size of flowers and fruits in tomato. Plant Biotechnol J 5, 422-430.
doi: 10.1111/j.1467-7652.2007.00251.x pmid: 17362485
[71] Powell ALT, Nguyen CV, Hill T, Cheng KL, Figueroa- Balderas R, Aktas H, Ashrafi H, Pons C, Fernández-Munoz R, Vicente A, Lopez-Baltazar J, Barry CS, Liu YS, Chetelat R, Granell A, Van Deynze A, Giovannoni JJ, Bennett AB (2012). Uniform ripening encodes a GOLDEN 2-LIKE transcription factor regulating tomato fruit chloroplast development.Science 336, 1711-1715.
doi: 10.1126/science.1222218 pmid: 22745430
[72] Reyes JC (2006). Chromatin modifiers that control plant development.Curr Opin Plant Biol 9, 21-27.
doi: 10.1016/j.pbi.2005.11.010 pmid: 16337828
[73] Rodrlguez GR, Munos S, Anderson C, Sim SC, Michel A, Causse M, Gardener BBM, Francis D, van der Knaap E (2011). Distribution of SUN, OVATE, LC, and FAS in the tomato germplasm and the relationship to fruit shape diversity. Plant Physiol 156, 275-285.
doi: 10.1104/pp.110.167577 pmid: 21441384
[74] Ruan YL (2014). Sucrose metabolism: gateway to diverse carbon use and sugar signaling.Annu Rev Plant Biol 65, 33-67.
doi: 10.1146/annurev-arplant-050213-040251 pmid: 24579990
[75] Ruan YL, Patrick JW (1995). The cellular pathway of postphloem sugar transport in developing tomato fruit.Planta 196, 434-444.
doi: 10.1007/BF00203641
[76] Ruan YL, Patrick JW, Bouzayen M, Osorio S, Fernie AR (2012). Molecular regulation of seed and fruit set.Trends Plant Sci 17, 656-665.
doi: 10.1016/j.tplants.2012.06.005 pmid: 22776090
[77] Sahu PP, Pandey G, Sharma N, Puranik S, Muthamilarasan M, Prasad M (2013). Epigenetic mechanisms of plant stress responses and adaptation.Plant Cell Rep 32, 1151-1159.
doi: 10.1007/s00299-013-1462-x pmid: 23719757
[78] Schmitz RJ, Schultz MD, Lewsey MG, O’Malley RC, Urich MA, Libiger O, Schork NJ, Ecker JR (2011). Transgene- rational epigenetic instability is a source of novel methylation variants.Science 334, 369-373.
doi: 10.1126/science.1212959 pmid: 21921155
[79] Segers G, Gadisseur I, Bergounioux C, de Almeida Engler J, Jacqmard A, van Montagu M, Inzé D (1996). The Arabidopsis cyclin-dependent kinase gene cdc2bAt is preferentially expressed during S and G2 phases of the cell cycle. Plant J 10, 601-612.
doi: 10.1046/j.1365-313X.1996.10040601.x pmid: 8893539
[80] Serrani JC, Sanjuán R, Ruiz-Rivero O, Fos M, Garcla- Martlnez JL (2007). Gibberellin regulation of fruit set and growth in tomato.Plant Physiol 145, 246-257.
doi: 10.1104/pp.107.098335 pmid: 17660355
[81] Seymour G, Poole M, Manning K, King GJ (2008). Gene- tics and epigenetics of fruit development and ripening.Curr Opin Plant Biol 11, 58-63.
doi: 10.1016/j.pbi.2007.09.003 pmid: 17997126
[82] Seymour GB, Ostergaard L, Chapman NH, Knapp S, Martin C (2013). Fruit development and ripening.Annu Rev Plant Biol 64, 219-241.
doi: 10.1146/annurev-arplant-050312-120057
[83] Shen HS, He H, Li JG, Chen W, Wang XC, Guo L, Peng ZY, He GM, Zhong SW, Qi YJ, Terzaghi W, Deng XW (2012). Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids.Plant Cell 24, 875-892.
doi: 10.1105/tpc.111.094870
[84] Sheng J, Ye J, Shen L, Luo Y (2003). Effect of lipoxygenase and jasmonic acid on ethylene biosynthesis during tomato fruit ripening.Acta Hortic 620, 119-125.
doi: 10.17660/ActaHortic.2003.620.12
[85] Shinozaki Y, Hao SH, Kojima M, Sakakibara H, Ozeki-Iida Y, Zheng Y, Fei ZJ, Zhong SL, Giovannoni JJ, Rose JKC, Okabe Y, Heta Y, Ezura H, Ariizumi T (2015). Ethy- lene suppresses tomato (Solanum lycopersicum) fruit set through modification of gibberellin metabolism. Plant J 83, 237-251.
doi: 10.1111/tpj.12882 pmid: 25996898
[86] Sicard A, Petit J, Mouras A, Chevalier C, Hernould M (2008). Meristem activity during flower and ovule deve- lopment in tomato is controlled by the mini zinc finger gene INHIBITOR OF MERISTEM ACTIVITY. Plant J 55, 415-427.
[87] Srivastava A, Handa AK (2005). Hormonal regulation of tomato fruit development: a molecular perspective.J Plant Growth Regul 24, 67-82.
doi: 10.1007/s00344-005-0015-0
[88] Strahl BD, Allis CD (2000). The language of covalent histone modifications.Nature 403, 41-45.
doi: 10.1038/47412 pmid: 10638745
[89] Sun L, Rodriguez GR, Clevenger JP, Illa-Berenguer E, Lin JS, Blakeslee JJ, Liu WL, Fei ZJ, Wijeratne A, Meulia T, van der Knaap E (2015). Candidate gene selection and detailed morphological evaluations of fs8.1, a quantitative trait locus controlling tomato fruit shape. J Exp Bot 66, 6471-6482.
doi: 10.1093/jxb/erv361 pmid: 4588892
[90] Tanksley SD (2004). The genetic, developmental, and molecular bases of fruit size and shape variation in tomato.Plant Cell 16, S181-S189.
doi: 10.1016/j.laa.2009.09.019 pmid: 15131251
[91] Teyssier E, Bernacchia G, Maury S, Kit AH, Stammitti- Bert L, Rolin D, Gallusci P (2008). Tissue dependent variations of DNA methylation and endoreduplication le- vels during tomato fruit development and ripening.Planta 228, 391-399.
doi: 10.1007/s00425-008-0743-z
[92] Teyssier E, Boureau L, Chen WW, Liu RE, Degraeve- Guibault C, Stammitti L, Hong YG, Gallusci P (2015). Epigenetic regulation during fleshy fruit development and ripening. In: Poltronieri P, Hong YG, eds. Applied Plant Genomics and Biotechnology. Amsterdam: Elsevier. pp. 133-151.
[93] The Tomato Genome Consortium (2012). The tomato genome sequence provides insights into fleshy fruit evolution.Nature 485, 635-641.
doi: 10.1038/nature11119 pmid: 22660326
[94] Tilman D, Balzer C, Hill J, Befort BL (2011). Global food demand and the sustainable intensification of agriculture.Proc Natl Acad Sci USA 108, 20260-20264.
doi: 10.1073/pnas.1116437108
[95] van der Knaap E, Chakrabarti M, Chu YH, Clevenger JP, Illa-Berenguer E, Huang ZJ, Keyhaninejad N, Mu Q, Sun L, Wang YP (2014). What lies beyond the eye: the molecular mechanisms regulating tomato fruit weight and shape.Front Plant Sci 5, 227.
doi: 10.3389/fpls.2014.00227 pmid: 4034497
[96] Vardhini BV, Rao SSR (2002). Acceleration of ripening of tomato pericarp discs by brassinosteroids.Phytochemistry 61, 843-847.
doi: 10.1016/S0031-9422(02)00223-6 pmid: 12453577
[97] Verkest A, Manes CLD, Vercruysse S, Maes S, Van Der Schueren E, Beeckman T, Genschik P, Kuiper M, Inzé D, De Veylder L (2005). The cyclin-dependent kinase inhibitor KRP2 controls the onset of the endoreduplication cycle during Arabidopsis leaf development through inhibition of mitotic CDKA;1 kinase complexes.Plant Cell 17, 1723-1736.
doi: 10.1105/tpc.105.032383
[98] Vermaak D, Ahmad K, Henikoff S (2003). Maintenance of chromatin states: an open-and-shut case.Curr Opin Cell Biol 15, 266-274.
doi: 10.1016/S0955-0674(03)00043-7 pmid: 12787767
[99] Wollmann H, Berger F (2012). Epigenetic reprogramming during plant reproduction and seed development.Curr Opin Plant Biol 15, 63-69.
doi: 10.1016/j.pbi.2011.10.001 pmid: 22035873
[100] Wu S, Xiao H, Cabrera A, Meulia T, van der Knaap E (2011). SUN regulates vegetative and reproductive organ shape by changing cell division patterns. Plant Physiol 157, 1175-1186.
[101] Xiao H, Jiang N, Schaffner E, Stockinger EJ, van der Knaap E (2008). A retrotransposon-mediated gene duplication underlies morphological variation of tomato fruit.Science 319, 1527-1530.
doi: 10.1126/science.1153040 pmid: 18339939
[102] Yang JC, Zhang JH (2010). Crop management techniques to enhance harvest index in rice.J Exp Bot 61, 3177-3189.
doi: 10.1364/AO.36.000144 pmid: 20421195
[103] Yu SM, Lo SF, Ho THD (2015). Source-sink communication: regulated by hormone, nutrient, and stress cross-signaling.Trends Plant Sci 20, 844-857.
doi: 10.1016/j.tplants.2015.10.009 pmid: 26603980
[104] Zanor MI, Osorio S, Nunes-Nesi A, Carrari F, Lohse M, Usadel B, Kühn C, Bleiss W, Giavalisco P, Willmitzer L, Sulpice R, Zhou YH, Fernie AR (2009). RNA interference of LIN5 in tomato confirms its role in controlling Brix content, uncovers the influence of sugars on the levels of fruit hormones, and demonstrates the importance of sucrose cleavage for normal fruit development and fertility. Plant Physiol 150, 1204-1218.
doi: 10.1104/pp.109.136598 pmid: 19439574
[105] Zhang JH, Jia WS, Yang JC, Ismail AM (2006). Role of ABA in integrating plant responses to drought and salt stresses.Field Crops Res 97, 111-119.
doi: 10.1016/j.fcr.2005.08.018
[106] Zhang X, Shiu S, Cal A, Borevitz JO (2008). Global analysis of genetic, epigenetic and transcriptional polymorphisms in Arabidopsis thaliana using whole genome tiling arrays. PLoS Genet 4, e1000032.
doi: 10.1371/journal.pgen.1000032 pmid: 18369451
[107] Zhao XA, Harashima H, Dissmeyer N, Pusch S, Weimer AK, Bramsiepe J, Bouyer D, Rademacher S, Nowack MK, Novak B, Sprunck S, Schnittger A (2012). A general G1/S-phase cell-cycle control module in the flowering plant Arabidopsis thaliana. PLoS Genet 8, e1002847.
[108] Zhong SL, Fei ZJ, Chen YR, Zheng Y, Huang MY, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J, Shao Y, Giovannoni JJ (2013). Single-base resolution methylomes of tomato fruit development reveal epigenome modifica- tions associated with ripening.Nat Biotechnol 31, 154-159.
doi: 10.1038/nbt.2462 pmid: 23354102
[1] Chen Wei,Yang Yingzeng,Chen Feng,Zhou Wenguan,Shu Kai. Stress Memory Mediated by Epigenetic Modification in Plants [J]. Chin Bull Bot, 2019, 54(6): 779-785.
[2] Ma Aimin, Qi Xiaoquan. The Mechanism of Metabolite Changes in Tomato Breeding by a Multi-Omics Approach [J]. Chin Bull Bot, 2018, 53(5): 578-580.
[3] Du Kangxi, Shen Wenhui, Dong Aiwu. Advances in Epigenetic Regulation of Abiotic Stress Response in Plants [J]. Chin Bull Bot, 2018, 53(5): 581-593.
[4] Hongliang Wang, Siyi Guo, Pengtao Wang, Chunpeng Song. Research Progress in Stomatal Development Mechanism [J]. Chin Bull Bot, 2018, 53(2): 164-174.
[5] Shujuan Xu, Kang Chong. Mechanism of The “Pioneer” Transcription Factor LEC1 in Resetting Vernalized State in Early Embryos [J]. Chin Bull Bot, 2018, 53(1): 1-4.
[6] Linfeng Li, Bao Liu. The roles of epigenetic variation in plant hybridization and polyploidization [J]. Biodiv Sci, 2017, 25(6): 600-607.
[7] De-Xing Zhang. Unorthodox reflections on molecular ecology research in China [J]. Biodiv Sci, 2015, 23(5): 559-569.
[8] De-Xing Zhang. Unorthodox reflections on molecular ecology research in China [J]. Biodiv Sci, 2015, 23(5): 559-569.
[9] Tao Wang, Menglong Chen, Ling Liu, Chuanli Ning, Binhua Cai, Zhen Zhang, Yushan Qiao. Changes in Genome and Gene Expression During Plant Polyploidization [J]. Chin Bull Bot, 2015, 50(4): 504-515.
[10] Lei Deng, Minmin Du, Chuanyou Li. Chinese Scientists Made Breakthrough Progresses in Studies on Domestication and Fruit Quality in Tomato and Cucumber [J]. Chin Bull Bot, 2015, 50(3): 275-278.
[11] Qi Fang, Jiahong Dong, Kuanyu Zheng, Zhongkai Zhang. Cytopathological Characterization of Tobacco on Co-infection with Tomato zonate spot virus and Potato virus Y [J]. Chin Bull Bot, 2014, 49(6): 704-709.
[12] Tongwen Yang, Chengwei Li. Epigenetic Regulation of Leaf Senescence in Plants [J]. Chin Bull Bot, 2014, 49(6): 729-737.
[13] Xiaoqiang Han, Yumei Xiao, Huizhe Lu, Zhaohai Qin. Research Advances in Antimetabolic and Photostable Analogues of Abscisic Acid [J]. Chin Bull Bot, 2013, 48(3): 329-343.
[14] Meishan Zhang, Bao Liu. Epigenetic Regulation in Plant Endosperm Development [J]. Chin Bull Bot, 2012, 47(2): 101-110.
[15] Aiqing Sun, Shujuan Ge, Jiedao Zhang. Use of Matrix Attachment Region in Regulating Transgene Expression of Tomato [J]. Chin Bull Bot, 2011, 46(6): 688-693.
Viewed
Full text


Abstract

Cited

  Shared   
  Discussed   
[1] Lu Zhong-shu. Plant Growth Regutators in Relation to Plant Water Status[J]. Chin Bull Bot, 1985, 3(04): 1 -6 .
[2] Li Da Jue;Han Yun-zhou and Wan Li-ping. Studies on Germplasm Collections of Carthamus tinctorius IV Screening of the characterization of Seed Domancy[J]. Chin Bull Bot, 1990, 7(02): 50 -52 .
[3] . [J]. Chin Bull Bot, 1999, 16(增刊): 45 -46 .
[4] Yang Hong-yuan. Basic Principle and Method of Fluorescence Microscopy[J]. Chin Bull Bot, 1984, 2(06): 45 -48 .
[5] LU Jin-Yao;LUO Ai-Ling and LIANG Zheng. Some Improvement of TD-PAGE Technology[J]. Chin Bull Bot, 1998, 15(03): 69 -72 .
[6] LI Ling-Hao and CHEN Zuo-Zhong. The Global Carbon Cycle in Grassland Ecosystems and Its Responses to Global Change I . Carbon Flow Compartment Model, Inputs and Storage[J]. Chin Bull Bot, 1998, 15(02): 14 -22 .
[7] Huanhuan Xu, Jian Kang, Mingxiang Liang. Research Advances in the Metabolism of Fructan in Plant Stress Resistance[J]. Chin Bull Bot, 2014, 49(2): 209 -220 .
[8] . [J]. Chin Bull Bot, 2013, 48(1): 4 -5 .
[9] . [J]. Chin Bull Bot, 1996, 13(专辑): 45 .
[10] SHU Qun-Fang;ZHOU Lu;LI Wen-Bin;ZHANG LI-Ming and SUN Yong-Ru. Study on Gel Electrophoresis of Protein from Plant and Our Improved Methods[J]. Chin Bull Bot, 1998, 15(06): 73 -78 .