Transcriptional dynamics of the developing sweet cherry (Prunus avium L.) fruit: Sequencing, annotation and expression profiling of exocarp-Associated genes

Horticulture Research

Volumn 1, Issue , 2014, Pages

  Alkio, Merianne ^a   Jonas, Uwe ^a   Declercq, Myriam ^a   Van Nocker, Steven ^b   Knoche, Moritz ^a  

^a LEIBNIZ UNIVERSITY HANNOVER   (Germany)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84905977116     PISSN: None     EISSN: 20527276     Source Type: Journal    
DOI: 10.1038/hortres.2014.11     Document Type: Article

References (93)

1. Esau K. Anatomy of Seed Plants. 2nd ed. New York: John Wiley & Sons, 1977.
2. Baur P, Stulle K, Schönherr J, Uhlig B. [Absorption of radiation in the UV-B to blue light range by leave cuticles of selected crop plants]. Gartenbauwissenschaft 1998; 63: 145-152. German.
3. Martin JT, Juniper BE. The Cuticles of Plants. Edinburgh: Edward Arnold Ltd, 1970.
4. Kerstiens G. Plant Cuticles-An Integrated Functional Approach. Oxford: BIOS Scientific Publishers, 1996.
5. Lalel HJD, Singh Z, Tan SC. Distribution of aroma volatile compounds in different parts of mango fruit. J Hort Sci Biotechnol 2003; 78: 131-138.
6. Knoche M, Beyer M, Peschel S, Oparlakov B, Bukovac MJ. Changes in strain and deposition of cuticle in developing sweet cherry fruit. Physiol Plant 2004; 120: 667-677.
7. Leide J, Hildebrandt U, Reussing K, RiedererM, Vogg G. The developmental pattern of tomato fruit wax accumulation and its impact on cuticular transpiration barrier properties: effects of a deficiency in a beta-ketoacyl-coenzyme A synthase (LeCER6). Plant Physiol 2007; 144: 1667-1679.
8. Peschel S, Franke R, Schreiber L, Knoche M. Composition of the cuticle of developing sweet cherry fruit. Phytochemistry 2007; 68: 1017-1025.
9. Thompson DS, Davies WJ, Ho LC. Regulation of tomato fruit growth by epidermal cell wall enzymes. Plant Cell Environ 1998; 21: 589-599.
10. Bargel H, Neinhuis C. Tomato (Lycopersicon esculentum Mill.) fruit growth and ripening as related to the biomechanical properties of fruit skin and isolated cuticle. J Exp Bot 2005; 56: 1049-1060.
11. The Tomato Genome Consortium. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 2012; 485: 635-641.
12. Park S, Sugimoto N, Larson MD, Beaudry R, van Nocker S. Identification of genes with potential roles in apple fruit development and biochemistry through large-scale statistical analysis of expressed sequence tags. Plant Physiol 2006; 141: 811-824.
13. Janssen BJ, Thodey K, Schaffer RJ et al. Global gene expression analysis of apple fruit development from the floral bud to ripe fruit. BMC Plant Biol 2008; 8: 16.
14. Costa F, Alba R, Schouten H et al. Use of homologous and heterologous gene expression profiling tools to characterize transcription dynamics during apple fruit maturation and ripening. BMC Plant Biol 2010; 10: 1-17.
15. Da Silva FG, Iandolino A, Al-Kayal F et al. Characterizing the grape transcriptome. Analysis of expressed sequence tags from multiple Vitis species and development of a compendium of gene expression during berry development. Plant Physiol 2005; 139: 574-597.
16. Pilati S, Perazzolli M, Malossini A et al. Genome-wide transcriptional analysis of grapevine berry ripening reveals a set of genes similarly modulated during three seasons and the occurrence of an oxidative burst at vè raison. BMC Genomics 2007; 8: 428.
17. Trainotti L, Bonghi C, Ziliotto F et al. The use ofmicroarray mPEACH1.0 to investigate transcriptome changes during transition from pre-climacteric to climacteric phase in peach fruit. Plant Sci 2006; 170: 606-613.
18. Manganaris GA, Rasori A, Bassi D et al. Comparative transcript profiling of apricot (Prunus armeniaca L.) fruit development and on-Tree ripening. Tree Genet Genomes 2011; 7: 609-616.
19. Yin YX, Zhang XW, Fang YJ et al.High-Throughput sequencing-based gene profiling on multi-staged fruit development of date palm (Phoenix dactylifera, L.). Plant Mol Biol 2012; 78: 617-626.
20. Lemaire-Chamley M, Petit J, Garcia V. Changes in transcriptional profiles are associated with early fruit tissue specialization in tomato. Plant Physiol 2005; 139: 750-769.
21. Mintz-Oron S, Mandel T, Rogachev I et al. Gene expression and metabolism in tomato fruit surface tissues. Plant Physiol 2008; 147: 823-851.
22. Yeats T, Howe K, Matas A. Mining the surface proteome of tomato (Solanum lycopersicum) fruit for proteins associated with cuticle biogenesis. J Exp Bot 2010; 61: 3759-3771.
23. Ali MB, Howard S, Chen SW et al. Berry skin development in Norton grape: distinct patterns of transcriptional regulation and flavonoid biosynthesis. BMC Plant Biol 2011; 11: 1-23.
24. Vecchietti A, Lazzari B, Ortugno C et al. Comparative analysis of expressed sequence tags from tissues in ripening stages of peach (Prunus persica L. Batsch). Tree Genet Genomes 2009; 5: 377-391.
25. Grimplet J, Deluc LG, Tillett RL et al. Tissue-specific mRNA expression profiling in grape berry tissues. BMC Genomics 2007; 8: 184.
26. Matas AJ, Yeats TH, Buda GJ et al. Tissue-And cell-Type specific transcriptome profiling of expanding tomato fruit provides insights into metabolic and regulatory specialization and cuticle formation. Plant Cell 2011; 23: 3893-3910.
27. Matas AJ, Agusti J, Tadeo FR, Talon M, Rose JK. Tissue-specific transcriptome profiling of the citrus fruit epidermis and subepidermis using laser capture microdissection. J Exp Bot 2010; 61: 3321-3330.
28. Ono NN, Britton MT, Fass JN, Nicolet CM, Lin DW, Tian L. Exploring the transcriptome landscape of pomegranate fruit peel for natural product biosynthetic gene and SSR marker discovery. J Integr Plant Biol 2011; 53: 800-813.
29. Alkio M, Jonas U, Sprink T, van Nocker S, Knoche M. Identification of putative candidate genes involved in cuticle formation in Prunus avium (sweet cherry) fruit. Ann Bot 2012; 110: 101-112.
30. Knoche M, Peschel S, Hinz M, Bukovac MJ. Studies on water transport through the sweet cherry fruit surface: II. Conductance of the cuticle in relation to fruit development. Planta 2001; 213: 927-936.
31. Khanal BP, Grimm E, Finger S, Blume A, Knoche M. Intracuticular wax fixes and restricts strain in leaf and fruit cuticles. New Phytol 2013; 200: 1-10.
32. Grimm E, Peschel S, Knoche M. Mottling on sweet cherry fruit is caused by exocarp strain. J Am Soc Hort Sci 2013; 138: 18-23.
33. Grimm E, Peschel S, Becker T, Knoche M. Stress and strain in the sweet cherry skin. J Am Soc Hort Sci 2012; 137: 383-390.
34. Aronesty E. ea-utils: Command-line tools for processing biological sequencing data. 2011. Available at http://code.google.com/p/ea-utils (accessed July 2011)
35. Salmela L, Schroeder J. Correcting errors in short reads by multiple alignments. Bioinformatics 2011; 27: 1455-1461.
36. Edgar RC. Search and clustering orders of magnitude faster than BLAST. Bioinformatics 2010; 26: 2460-2461.
37. Zerbino DR, Birney E. Velvet: Algorithms for de novo short read assembly using de Bruijn graphs. Genome Res 2008; 18: 821-829.
38. Soderlund C, Johnson E, BomhoffM, Descour A. PAVE: program for assembling and viewing ESTs. BMC Genomics 2009; 10: 400.
39. Huang XQ, Madan A. CAP3: A DNA sequence assembly program. Genome Res 1999; 9: 868-877.
40. Langmead B, Trapnell C, Pop M, Salzberg SL. Ultrafast and memory-efficient alignment of short DNA sequences to the human genome. Genome Biol 2009; 10: R25.
41. Altschul SF, Madden TL, Schäffer AA et al. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res 1997; 25: 3389-3402.
42. Verde I, Abbott AG, Scalabrin S et al. The high-quality draft genome of peach (Prunus persica) identifies unique patterns of genetic diversity, domestication and genome evolution. Nat Genet 2013; 45: 487-494.
43. Velasco R, Zharkikh A, Affourtit J et al. The genome of the domesticated apple (Malus 3 domestica Borkh.). Nat Genet 2010; 42: 833-839.
44. JaillonO, Aury JM, Noel B et al. The grapevine genome sequence suggests ancestral hexaploidization in major angiosperm phyla. Nature 2007; 449: 463-467.
45. Swarbreck D, Wilks C, Lamesch P et al. The Arabidopsis Information Resource (TAIR): gene structure and function annotation. Nucleic Acids Res 2008; 36: D1009-D1014.
46. Goodstein DM, Shu S, Howson R et al. Phytozome: A comparative platform for green plant genomics. Nucleic Acids Res 2012; 40: D1178-D1186.
47. Conesa A, Götz S, García-Gómez JM, Terol J, Talón M, Robles M. Blast2GO: A universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 2005; 21: 3674-3676.
48. The Uniprot Consortium. Reorganizing the protein space at the Universal Protein Resource (UniProt). Nucleic Acids Res 2012; 40: D71-D75.
49. Zdobnov E, Apweiler R. InterProScan-An integration platform for the signaturerecognition methods in InterPro. Bioinformatics 2001; 17: 847-848.
50. Du Z, Zhou X, Ling Y, Zhang ZH, Su Z. agriGO: A GO analysis toolkit for the agricultural community. Nucleic Acids Res 2010; 38: W64-W70.
51. Trapnell C, Williams BA, Pertea G et al. Transcript assembly and quantification by RNA-Seq reveals unannotated transcripts and isoform switching during cell differentiation. Nat Biotechnol 2010; 28: 511-5.
52. Battke F, Symons S, Nieselt K. Mayday-integrative analytics for expression data. BMC Bioinformatics 2010; 11: 1-10.
53. Lilleland O, Newsome L. A growth study of the cherry fruit. Proc Am Soc Hortic Sci 1934; 32: 291-299.
54. Schliesky S, Gowik U, Weber APM, Braütigam A. RNA-Seq assembly-Are we there yet? Front Plant Sci 2012; 3: 1-12.
55. The ENCODE Consortium. Standards, Guidelines and Best Practices for RNA-Seq V1.0. 2011. Available at http://encodeproject.org/ENCODE/dataS (accessed July 2011).
56. Wang L, Feng Z, Wang X, Wang X, Zhang X. DEGseq: An R package for identifying differentially expressed genes from RNA-seq data. Bioinformatics 2010; 26: 136-138.
57. St Laurent G, Shtokalo D, Tackett MR et al. Intronic RNAs constitute the major fraction of the non-coding RNA in mammalian cells. BMC Genomics 2012; 13: 504.
58. Zhang H, Jin J, Tang L et al. PlantTFDB 2.0: update and improvement of the comprehensive plant transcription factor database. Nucleic Acids Res 2011; 39: D1114-D1117.
59. Fils-Lycaon B, Wiersma P, Kenneth C, Sautiere P. A cherry protein and its gene, abundantly expressed in ripening fruit, have been identified as thaumatin-like. Plant Physiol 1996; 111: 269-273.
60. Leszczyszyn OI, Imam HT, Blindauer CA. Diversity and distribution of plant metallothioneins: A review of structure, properties and functions. Metallomics 2013; 5: 1146-1169.
61. Kader JC. Lipid-Transfer proteins in plants. Annu Rev Plant Phys 1996; 47: 627-654.
62. Kusano T, Berberich T, Tateda C, Takahashi Y. Polyamines: essential factors for growth and survival. Planta 2008; 228: 367-381.
63. Liu P, Goh CJ, Loh CS, Pua EC. Differential expression and characterization of three metallothionein-like genes in Cavendish banana (Musa acuminata). Physiol Plant 2002; 114: 241-250.
64. Moyle R, Fairbairn DJ, Ripi J, Crowe M, Botella JR. Developing pineapple fruit has a small transcriptome dominated by metallothionein. J Exp Bot 2005; 56: 101-112.
65. Pollard M, Beisson F, Li Y, Ohlrogge JB. Building lipid barriers: biosynthesis of cutin and suberin. Trends Plant Sci 2008; 13: 236-246.
66. Broekaert WF, Cammue BP, DeBolle MF, Thevissen K, DeSamblanx GW, Osborn RW. Antimicrobial peptides from plants. CRC Crit Rev Plant Sci 1997; 16: 297-323.
67. Develey-Riviere MP, Galiana E. Resistance to pathogens and host developmental stage: A multifaceted relationship within the plant kingdom. New Phytol 2007; 175: 405-416.
68. Nahirñak V, Almasia NI, Fernandez PV et al. Potato snakin-1 gene silencing affects cell division, primary metabolism, and cell wall composition. Plant Physiol 2012; 158: 252-263.
69. LüS, Song T, Kosma DK, Parsons EP, Rowland O, Jenks MA. Arabidopsis CER8 encodes LONG-CHAIN ACYL-COA SYNTHETASE 1 (LACS1) that has overlapping functions with LACS2 in plant wax and cutin synthesis. Plant J 2009; 59: 553-564.
70. Baumann K, Perez-Rodriguez M, Bradley D et al. Control of cell and petal morphogenesis by R2R3 MYB transcription factors. Development 2007; 134: 1691-1701.
71. Segura A, Moreno M, Madueno F, Molina A, Garcia-Olmedo F. Snakin-1, a peptide from potato that is active against plant pathogens. Mol PlantMicrobe Interact 1999; 12: 16-23.
72. Goulao LF, Santos J, de Sousa I, Oliveira CM. Patterns of enzymatic activity of cell wall-modifying enzymes during growth and ripening of apples. Postharvest Biol Technol 2007; 43: 307-318.
73. Yoo SD, Gao ZF, Cantini C, Loescher WH, van Nocker S. Fruit ripening in sour cherry: Changes in expression of genes encoding expansins and other cell-wall-modifying enzymes. J Am Soc Hort Sci 2003; 128: 16-22.
74. Kurdyukov S, Faust A, Nawrath C. The epidermis-specific extracellular BODYGUARD controls cuticle development and morphogenesis in Arabidopsis. Plant Cell 2006; 18: 321-339.
75. Marchler-Bauer A, Zheng CJ, Chitsaz F et al. CDD: conserved domains and protein three-dimensional structure. Nucleic Acids Res 2013; 41: D348-D352.
76. Yeats T, Martin L, Viart H. The identification of cutin synthase: formation of the plant polyester cutin. Nat Chem Biol 2012; 8: 8-10.
77. Girard AL, Mounet F, Lemaire-Chamley M et al. Tomato GDSL1 is required for cutin deposition in the fruit cuticle. Plant Cell 2012; 24: 3119-3134.
78. Aharoni A, Dixit S, Jetter R. The SHINE clade of AP2 domain transcription factors activates wax biosynthesis, alters cuticle properties, and confers drought tolerance when overexpressed in Arabidopsis. Plant Cell 2004; 16: 2463-2480.
79. Shi JX, Malitsky S, de Oliveira S et al. SHINE transcription factors act redundantly to pattern the archetypal surface of Arabidopsis flower organs. PLoS Genet 2011; 7: e1001388.
80. Shi JX, Adato A, Alkan N et al. The tomato SlSHINE3 transcription factor regulates fruit cuticle formation and epidermal patterning. New Phytol 2013; 197: 468-480.
81. Ren J, Sun L, Wu J et al. Cloning and expression analysis of cDNAs for ABA 89-hydroxylase during sweet cherry fruit maturation and under stress conditions. J Plant Physiol 2010; 167: 1486-1493.
82. Kondo S, Inoue K. Abscisic acid (ABA) and 1-Aminocyclopropane-1-carboxylic acid (ACC) content during growth of ''Satohnishiki'' cherry fruit, and the effect of ABA and ethephon application on fruit quality. J Hort Sci Biotechnol 1997; 72: 221-228.
83. Gao ZF, Maurousset L, Lemoine R, Yoo SD, van Nocker S, Loescher W. Cloning, expression, and characterization of sorbitol transporters from developing sour cherry fruit and leaf sink tissues. Plant Physiol 2003; 131: 1566-1575.
84. Kondo S, Danjo C. Cell wall polysaccharidemetabolism during fruit development in sweet cherry ''Satohnishiki'' as affected by gibberellic acid. J Jpn Soc Hort Sci 2001; 70: 178-184.
85. Kubo H, Peeters AJ, Aarts MG, Pereira A, Koornneef M. ANTHOCYANINLESS2, a homeobox gene affecting anthocyanin distribution and root development in Arabidopsis. Plant Cell 1999; 11: 1217-1226.
86. Isaacson T, Kosma DK, Matas AJ et al. Cutin deficiency in the tomato fruit cuticle consistently affects resistance to microbial infection and biomechanical properties, but not transpirational water loss. Plant J 2009; 60: 363-377.
87. Nadakuduti SS, Pollard M, Kosma DK, Allen C, Ohlrogge JB, Barry CS. Pleiotropic phenotypes of the sticky peel mutant provide new insight into the role of CUTIN DEFICIENT2 in epidermal cell function in tomato. Plant Physiol 2012; 159: 945-960.
88. Lin-Wang K, Bolitho K, Grafton K et al. An R2R3 MYB transcription factor associated with regulation of the anthocyanin biosynthetic pathway in Rosaceae. BMC Plant Biol 2010; 10: 50.
89. Sooriyapathirana SS, Khan A, Sebolt AM et al. QTL analysis and candidate gene mapping for skin and flesh color in sweet cherry fruit (Prunus avium L.). Tree Genet Genomes 2010; 6: 821-832.
90. Cosgrove DJ. Growth of the plant cell wall. Nat Rev Mol Cell Biol 2005; 6: 850-861.
91. Kent C. Eukaryotic phospholipid biosynthesis. Annu Rev Biochem 1995; 64: 315-343.
92. Chang YF, Carman GM. CTP synthetase and its role in phospholipid synthesis in the yeast Saccharomyces cerevisiae. Prog Lipid Res 2008; 47: 333-339.
93. Li-Beisson Y, Pollard M, Sauveplane V, Pinot F, Ohlrogge J, Beisson F. Nanoridges that characterize the surface morphology of flowers require the synthesis of cutin polyester. Proc Natl Acad Sci USA 2009; 106: 22008-220013.