Comparative transcriptome analysis of cultivated and wild watermelon during fruit development

PLoS ONE

Volumn 10, Issue 6, 2015, Pages

  Guo, Shaogui ^a,b   Sun, Honghe ^b,c   Zhang, Haiying ^b   Liu, Jingan ^b   Ren, Yi ^b   Gong, Guoyi ^b   Jiao, Chen ^c   Zheng, Yi ^c   Yang, Wencai ^a   Fei, Zhangjun ^c,d   Xu, Yong ^b  

^a CHINA AGRICULTURAL UNIVERSITY   (China)

^b BEIJING VEGETABLE RESEARCH CENTER   (China)

^c Boyce Thompson Institute for Plant Research   (United States)

^d ROBERT W HOLLEY CENTER FOR AGRICULTURE AND HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA GALACTOSIDASE; BETA FRUCTOFURANOSIDASE; LONG CHAIN FATTY ACID COENZYME A LIGASE; PHYTOENE SYNTHASE; URIDINE TRIPHOSPHATE GLUCOSE 1 PHOSPHATE URIDYLYLTRANSFERASE; CAROTENOID; ETHYLENE; ETHYLENE DERIVATIVE;

4 COUMARATE COENZYME A LIGASE GENE; ABIOTIC STRESS; ACC OXIDASE GENE; ALPHA GALACTOSIDASE GENE; ALPHA MANNOSIDASE GENE; ARTICLE; BETA CAROTENE HYDROXYLASE GENE; BIOSYNTHESIS; CAROTENOID CLEAVAGE DIOXYGENASE GENE; CELLULOSE SYNTHASE GENE; COMPARATIVE STUDY; CONTROLLED STUDY; CULTIVATED SPECIES; ENERGY METABOLISM; EPOXYCAROTENOID DIOXYGENASE GENE; ETHYLENE RECEPTOR GENE; ETHYLENE RESPONSIVE FACTOR GENE; FLAVOR; FOOD QUALITY; FRUIT DEVELOPMENT; FRUIT RIPENING; FRUIT SUGAR CONTENT; GENE EXPRESSION; GENE IDENTIFICATION; GENOME ANALYSIS; GLUCOSE PYROPHOSPHORYLASE GENE; INTRACELLULAR SIGNALING; INVERTASE GENE; NONHUMAN; PECTINESTERASE GENE; PECTINESTERASE INHIBITOR GENE; PHYTOENE SYNTHASE GENE; PLANT GENE; PLANT GENOME; PLANT PARAMETERS; PLANT RESPONSE; PLANT TISSUE; POLYGALACTURONASE INHIBITOR GENE; SUGAR TRANSPORTER GENE; SWEETNESS; TRANSCRIPTOMICS; UDP GALACTOSE GENE; VITAMIN METABOLISM; WATERMELON; WILD SPECIES; CARBOHYDRATE METABOLISM; CITRULLUS; CYTOLOGY; ENZYMOLOGY; FRUIT; GENE EXPRESSION PROFILING; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; SIGNAL TRANSDUCTION;

CITRULLUS LANATUS; CITRULLUS LANATUS VAR. LANATUS;

CARBOHYDRATE METABOLISM; CAROTENOIDS; CITRULLUS; ETHYLENES; FRUIT; GENE EXPRESSION PROFILING; SIGNAL TRANSDUCTION;

EID: 84937884284     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0130267     Document Type: Article

References (63)

1. Liu J, Guo S, He H, Zhang H, Gong G, Ren Y, et al. Dynamic characteristics of sugar accumulation and related enzyme activities in sweet and non-sweet watermelon fruits. Acta Physiol Plant. 2013; 35: 3213-3222. doi: 10.1007/s11738-013-1356-0
2. FAO Statistics. Available: http://faostat.fao.org.
3. Wechter WP, Levi A, Harris KR, Davis AR, Fei Z, Katzir N, et al. Gene expression in developing watermelon fruit. BMC Genomics. 2008; 9: 275. doi: 10.1186/1471-2164-9-275 PMID: 18534026
4. Guo S, Liu J, Zheng Y, Huang M, Zhang H, Gong G, et al. Characterization of transcriptome dynamics during watermelon fruit development: sequencing, assembly, annotation and gene expression profiles. BMC Genomics. 2011; 12: 454. doi: 10.1186/1471-2164-12-454 PMID: 21936920
5. Yativ M, Harary I, Wolf S. Sucrose accumulation in watermelon fruits: genetic variation and biochemical analysis. J Plant Physiol. 2010; 167: 589-596. doi: 10.1016/j.jplph.2009.11.009 PMID: 20036442
6. Guo S, Zhang J, Sun H, Salse J, Lucas WJ, Zhang H, et al. The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nat Genet. 2013; 45: 51-58. doi: 10.1038/ng. 2470 PMID: 23179023
7. Zhong S, Joung JG, Zheng Y, Chen YR, Liu B, Shao Y, et al. High-throughput illumina strand-specific RNA sequencing library preparation. Cold Spring Harb Protoc. 2011; 2011: 940-949. doi: 10.1101/pdb. prot5652 PMID: 21807852
8. Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014; 30: 2114-2120. doi: 10.1093/bioinformatics/btu170 PMID: 24695404
9. Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, et al. The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Res. 2013; 41: D590-D596. doi: 10.1093/nar/gks1219 PMID: 23193283
10. Langmead B, Trapnell C, Pop M, Salzberg S. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol. 2009; 10: R25. doi: 10.1186/gb-2009-10-3-r25 PMID: 19261174
11. Trapnell C, Pachter L, Salzberg SL. TopHat: discovering splice junctions with RNA-Seq. Bioinformatics. 2009; 25: 1105-1111. doi: 10.1093/bioinformatics/btp120 PMID: 19289445
12. Anders S, Huber W. Differential expression analysis for sequence count data. Genome Biol. 2010; 11: R106. doi: 10.1186/gb-2010-11-10-r106 PMID: 20979621
13. Smyth GK. Linear models and empirical bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol. 2004; 3: Article3. doi: 10.2202/1544-6115.1027
14. Y. B, Y. H. Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. J R Stat Soc Series B Stat Methodol. 1995; 57: 289-300. doi: 10.2307/2346101
15. Boyle EI, Weng S, Gollub J, Jin H, Botstein D, Cherry JM, et al. GO::TermFinder-open source software for accessing Gene Ontology information and finding significantly enriched Gene Ontology terms associated with a list of genes. Bioinformatics. 2004; 20: 3710-3715. doi: 10.1093/bioinformatics/bth456 PMID: 15297299
16. Joung J-G, Corbett AM, Fellman SM, Tieman DM, Klee HJ, Giovannoni JJ, et al. Plant MetGenMAP: An Integrative Analysis System for Plant Systems Biology. Plant Physiol. 2009; 151: 1758-1768. doi: 10.1104/pp.109.145169 PMID: 19819981
17. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative CT method. Nat Protoc. 2008; 3: 1101-1108. doi: 10.1038/nprot.2008.73 PMID: 18546601
18. Fraser PD, Truesdale MR, Bird CR, Schuch W, Bramley PM. Carotenoid Biosynthesis during Tomato Fruit Development (Evidence for Tissue-Specific Gene Expression). Plant Physiol. 1994; 105: 405-413. doi: 10.1104/pp.105.1.405 PMID: 12232210
19. Grassi S, Piro G, Lee JM, Zheng Y, Fei Z, Dalessandro G, et al. Comparative genomics reveals candidate carotenoid pathway regulators of ripening watermelon fruit. BMC Genomics. 2013; 14: 781. doi: 10.1186/1471-2164-14-781 PMID: 24219562
20. Wang Z, Gerstein M, Snyder M. RNA-Seq: a revolutionary tool for transcriptomics. Nat Rev Genet. 2009; 10: 57-63. doi: 10.1038/nrg2484 PMID: 19015660
21. Koenig D, Jimenez-Gomez JM, Kimura S, Fulop D, Chitwood DH, Headland LR, et al. Comparative transcriptomics reveals patterns of selection in domesticated and wild tomato. Proc Natl Acad Sci U S A. 2013; 110: E2655-2662. doi: 10.1073/pnas.1309606110 PMID: 23803858
22. Lee JM, Joung JG, McQuinn R, Chung MY, Fei Z, Tieman D, et al. 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. Plant J. 2012; 70: 191-204. doi: 10.1111/j. 1365-313X.2011.04863.x PMID: 22111515
23. Castro-Rodriguez V, Garcia-Gutierrez A, Canales J, Avila C, Kirby E, Canovas F. The glutamine synthetase gene family in Populus. BMC Plant Biol. 2011; 11: 119. doi: 10.1186/1471-2229-11-119 PMID: 21867507
24. Avila C, Suárez MF, Gómez-Maldonado J, Cánovas FM. Spatial and temporal expression of two cytosolic glutamine synthetase genes in Scots pine: functional implications on nitrogen metabolism during early stages of conifer development. Plant J. 2001; 25: 93-102. doi: 10.1111/j.1365-313X.2001.00938. x PMID: 11169185
25. Mitchell DE, Gadus MV, Madore MA. Patterns of Assimilate Production and Translocation in Muskmelon (Cucumis melo L.): I. Diurnal Patterns. Plant Physiol. 1992; 99: 959-965. doi: 10.1104/pp.99.3.959 PMID: 16669025
26. Schaffer AA, Pharr DM, Madore MA. Cucurbits. In: Zamski E, Schaffer AA, editors. Photoassimilate Distribution in Plants and Crops: Source-Sink Relationships. New York. Marcel Dekker; 1996. pp. 729-757.
27. Hubbard NL, Huber SC, Pharr DM. Sucrose Phosphate Synthase and Acid Invertase as Determinants of Sucrose Concentration in Developing Muskmelon (Cucumis melo L.) Fruits. Plant Physiol. 1989; 91: 1527-1534. doi: 10.1104/pp.91.4.1527 PMID: 16667212
28. Gao Z, Schaffer AA. A novel alkaline alpha-galactosidase from melon fruit with a substrate preference for raffinose. Plant Physiol. 1999; 119: 979-988. doi: 10.1104/pp.119.3.979 PMID: 10069835
29. Carmi N, Zhang G, Petreikov M, Gao Z, Eyal Y, Granot D, et al. Cloning and functional expression of alkaline alpha-galactosidase from melon fruit: similarity to plant SIP proteins uncovers a novel family of plant glycosyl hydrolases. Plant J. 2003; 33: 97-106. doi: 10.1046/j.1365-313X.2003.01609.x PMID: 12943544
30. Godt DE, Roitsch T. Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism. Plant Physiol. 1997; 115: 273-282. doi: 10.1104/pp.115.1.273 PMID: 9306701
31. Tang GQ, Lüscher M, Sturm A. Antisense Repression of Vacuolar and Cell Wall Invertase in Transgenic Carrot Alters Early Plant Development and Sucrose Partitioning. Plant Cell. 1999; 11: 177-189. doi: 10.1105/tpc.11.2.177 PMID: 9927637
32. Dai N, Petreikov M, Portnoy V, Katzir N, Pharr DM, Schaffer AA. Cloning and expression analysis of a UDP-galactose/glucose pyrophosphorylase from melon fruit provides evidence for the major metabolic pathway of galactose metabolism in raffinose oligosaccharide metabolizing plants. Plant Physiol. 2006; 142: 294-304. doi: 10.1104/pp.106.083634 PMID: 16829585
33. Ren Y, McGregor C, Zhang Y, Gong G, Zhang H, Guo S, et al. An integrated genetic map based on four mapping populations and quantitative trait loci associated with economically important traits in watermelon (Citrullus lanatus). BMC Plant Biol. 2014; 14: 33. doi: 10.1186/1471-2229-14-33 PMID: 24443961
34. Rao AV, Rao LG. Carotenoids and human health. Pharmacol Res. 2007; 55: 207-216. doi: 10.1016/j. phrs.2007.01.012 PMID: 17349800
35. Holden JM, Eldridge AL, Beecher GR, Marilyn Buzzard I, Bhagwat S, Davis CS, et al. Carotenoid Content of U.S. Foods: An Update of the Database. J Food Compost Anal. 1999; 12: 169-196. doi: 10. 1006/jfca.1999.0827
36. Schwartz SH, Tan BC, Gage DA, Zeevaart JAD, McCarty DR. Specific Oxidative Cleavage of Carotenoids by VP14 of Maize. Science. 1997; 276: 1872-1874. doi: 10.1126/science.276.5320.1872 PMID: 9188535
37. Schwartz SH, Qin X, Zeevaart JA. Elucidation of the indirect pathway of abscisic acid biosynthesis by mutants, genes, and enzymes. Plant Physiol. 2003; 131: 1591-1601. doi: 10.1104/pp.102.017921 PMID: 12692318
38. Li Q, Li P, Sun L, Wang Y, Ji K, Sun Y, et al. Expression analysis of beta-glucosidase genes that regulate abscisic acid homeostasis during watermelon (Citrullus lanatus) development and under stress conditions. J Plant Physiol. 2012; 169: 78-85. doi: 10.1016/j.jplph.2011.08.005 PMID: 21940067
39. Winterhalter P, Rouseff R. Carotenoid-derived aroma compounds: an introduction. In: Winterhalter P, Rouseff, editors. Carotenoid-derived aroma compounds. Washington, DC, American Chemical Society; 2002. pp. 1-19.
40. Brownleader MD, Jackson P, Mobasheri A, Pantelides AT, Sumar S, Trevan M, et al. Molecular Aspects of Cell Wall Modifications during Fruit Ripening. Crit Rev Food Sci Nutr. 1999; 39: 149-164. doi: 10.1080/10408399908500494 PMID: 10198752
41. Bartley IM, Knee M. The chemistry of textural changes in fruit during storage. Food Chem. 1982; 9: 47-58 doi: 10.1016/0308-8146(82)90068-1
42. Brummell DA, Dal Cin V, Crisosto CH, Labavitch JM. Cell wall metabolism during maturation, ripening and senescence of peach fruit. J Exp Bot. 2004; 55: 2029-2039. doi: 10.1093/jxb/erh227 PMID: 15286150
43. Brummell DA. Cell wall disassembly in ripening fruit. Funct Plant Biol. 2006; 33: 103-119. doi: 10.1071/FP05234
44. Brummell DA, Harpster MH. Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Mol Biol. 2001; 47: 311-340. doi: 10.1023/A:1010656104304 PMID: 11554479
45. Liu J, He H, Guo S, Zhang H, Ren Y, Gong G, et al. Physiological and biochemical mechanism for watermelon fruit ripening and softening. Journal of Fruit Science. 2013; 30: 813-818. doi: 10.13925/j.cnki. gsxb.2013.05.015 PMID: 23695311
46. Soltani B, Ehlting J, Hamberger B, Douglas C. Multiple cis-regulatory elements regulate distinct and complex patterns of developmental and wound-induced expression of Arabidopsis thaliana 4CL gene family members. Planta. 2006; 224: 1226-1238. doi: 10.1007/s00425-006-0296-y PMID: 16738863
47. Saxena IM, Brown RM. Cellulose Biosynthesis: Current Views and Evolving Concepts. Ann Bot. 2005; 96: 9-21. doi: 10.1093/aob/mci155 PMID: 15894551
48. Vicente AR, Ortugno C, Powell ALT, Greve LC, Labavitch JM. Temporal Sequence of Cell Wall Disassembly Events in Developing Fruits. 1. Analysis of Raspberry (Rubus idaeus). J Agric Food Chem. 2007; 55: 4119-4124. doi: 10.1021/jf063547r PMID: 17428067
49. Vicente AR, Powell A, Greve LC, Labavitch JM. Cell wall disassembly events in boysenberry (Rubus idaeus L. × Rubus ursinus Cham. & Schldl.) fruit development. Funct Plant Biol. 2007; 34: 614-623. doi: 10.1071/FP07002
50. Jolie RP, Duvetter T, Van Loey AM, Hendrickx ME. Pectin methylesterase and its proteinaceous inhibitor: a review. Carbohydr Res. 2010; 345: 2583-2595. doi: 10.1016/j.carres.2010.10.002 PMID: 21047623
51. Pinzon-Latorre D, Deyholos M. Characterization and transcript profiling of the pectin methylesterase (PME) and pectin methylesterase inhibitor (PMEI) gene families in flax (Linum usitatissimum). BMC Genomics. 2013; 14: 742. doi: 10.1186/1471-2164-14-742 PMID: 24168262
52. Di Matteo A, Giovane A, Raiola A, Camardella L, Bonivento D, De Lorenzo G, et al. Structural Basis for the Interaction between Pectin Methylesterase and a Specific Inhibitor Protein. Plant Cell. 2005; 17: 849-858. doi: 10.1105/tpc.104.028886 PMID: 15722470
53. Yashoda HM, Prabha TN, Tharanathan RN. Mango ripening-Role of carbohydrases in tissue softening. Food Chem. 2007; 102: 691-698. doi: 10.1016/j.foodchem.2006.06.001
54. Meli VS, Ghosh S, Prabha TN, Chakraborty N, Chakraborty S, Datta A. Enhancement of fruit shelf life by suppressing N-glycan processing enzymes. Proc Natl Acad Sci U S A. 2010; 107: 2413-2418. doi: 10.1073/pnas.0909329107 PMID: 20133661
55. Leliévre J-M, Latché A, Jones B, Bouzayen M, Pech J-C. Ethylene and fruit ripening. Physiol Plant. 1997; 101: 727-739. doi: 10.1111/j.1399-3054.1997.tb01057.x
56. Iannetta PPM, Laarhoven L-J, Medina-Escobar N, James EK, McManus MT, Davies HV, et al. Ethylene and carbon dioxide production by developing strawberries show a correlative pattern that is indicative of ripening climacteric fruit. Physiol Plant. 2006; 127: 247-259. doi: 10.1111/j.1399-3054.2006.00656.x
57. Trainotti L, Pavanello A, Casadoro G. 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 J Exp Bot. 2005; 56: 2037-2046. doi: 10.1093/jxb/eri202 PMID: 15955790
58. Katz E, Lagunes P, Riov J, Weiss D, Goldschmidt E. Molecular and physiological evidence suggests the existence of a system II-like pathway of ethylene production in non-climacteric Citrus fruit. Planta. 2004; 219: 243-252. doi: 10.1007/s00425-004-1228-3 PMID: 15014996
59. Elkashif ME, Huber DJ. Enzymic hydrolysis of placental cell wall pectins and cell separation in watermelon (Citrullus lanatus) fruits exposed to ethylene. Physiol Plant. 1988; 73: 432-439. doi: 10.1111/j. 1399-3054.1988.tb00622.x
60. Yasar K, J HD. Cell wall-degrading enzymes and pectin solubility and depolymerization in immature and ripe watermelon (Citrullus lanatus) fruit in response to exogenous ethylene. Physiol Plant. 2002; 116: 398-405. doi: 10.1034/j.1399-3054.2002.1160316.x
61. Chung MY, Vrebalov J, Alba R, Lee J, McQuinn R, Chung JD, et al. A tomato (Solanum lycopersicum) APETALA2/ERF gene, SlAP2a, is a negative regulator of fruit ripening. Plant J. 2010; 64: 936-947. doi: 10.1111/j.1365-313X.2010.04384.x PMID: 21143675
62. Cara B, Giovannoni JJ. Molecular biology of ethylene during tomato fruit development and maturation. Plant Sci. 2008; 175: 106-113. doi: 10.1016/j.plantsci.2008.03.021
63. Xiao YY, Chen JY, Kuang JF, Shan W, Xie H, Jiang YM, et al. Banana ethylene response factors are involved in fruit ripening through their interactions with ethylene biosynthesis genes. J Exp Bot. 2013; 64: 2499-2510. doi: 10.1093/jxb/ert108 PMID: 23599278