Evaluation of RNA extraction methods and identification of putative reference genes for real-time quantitative polymerase chain reaction expression studies on olive (olea europaea L.) fruits

Journal of Agricultural and Food Chemistry

Volumn 60, Issue 27, 2012, Pages 6855-6865

  Nonis, Alberto ^a   Vezzaro, Alice ^a   Ruperti, Benedetto ^a  

^a UNIVERSITY OF PADOVA   (Italy)

Author keywords

fruit development; gene expression; normalization; qPCR; reference gene

Indexed keywords

DIFFERENTIALLY EXPRESSED GENE; FRUIT DEVELOPMENT; MARKER GENES; NORMALIZATION; OLEA EUROPAEA; OLEA EUROPAEA L; QPCR; QUANTITATIVE APPROACH; QUANTITATIVE POLYMERASE CHAIN REACTION; RNA EXTRACTION; ROBUST METHODS;

FRUITS; POLYMERASE CHAIN REACTION; RNA;

GENE EXPRESSION;

MESSENGER RNA; PLANT RNA; VEGETABLE PROTEIN;

ARTICLE; CHEMISTRY; EVALUATION STUDY; FRACTIONATION; FRUIT; GENE EXPRESSION REGULATION; GENETICS; ISOLATION AND PURIFICATION; METABOLISM; METHODOLOGY; OLIVE TREE; REAL TIME POLYMERASE CHAIN REACTION; STANDARD;

CHEMICAL FRACTIONATION; FRUIT; GENE EXPRESSION REGULATION, PLANT; OLEA; PLANT PROTEINS; REAL-TIME POLYMERASE CHAIN REACTION; REFERENCE STANDARDS; RNA, MESSENGER; RNA, PLANT;

OLEA EUROPAEA;

EID: 84863921250     PISSN: 00218561     EISSN: 15205118     Source Type: Journal    
DOI: 10.1021/jf300419w     Document Type: Article

References (53)

1. Alagna, F.; D'Agostino, N.; Torchia, L.; Servili, M.; Rao, R.; Pietrella, M.; Giuliano, G.; Chiusano, M. L.; Baldoni, L.; Perrotta, G. Comparative 454 pyrosequencing of transcripts from two olive genotypes during fruit development BMC Genomics 2009, 10, 399
2. Galla, G.; Barcaccia, G.; Ramina, A.; Collani, S.; Alagna, F.; Baldoni, L.; Cultrera, N. G. M.; Martinelli, F.; Sebastiani, L.; Tonutti, P. Computational annotation of genes differentially expressed along olive fruit development BMC Plant Biol. 2009, 9, 128
3. Hernández, L. M.; Padilla, M. N.; Mancha, M.; Martínez- Rivas, J. M. Expression analysis identifies FAD2-2 as the olive oleate desaturase gene mainly responsibile for the linoleic acid content in virgin olive oil J. Agric. Food Chem. 2009, 57, 6199-6206
4. Matteucci, M.; D'Angeli, S.; Errico, S.; Lamanna, R.; Perrotta, G.; Altamura, M. M. Cold affects the transcription of fatty acid desaturases and oil quality in the fruit of Olea europaea L. genotypes with different cold hardiness J. Exp. Bot. 2011, 62, 3403-3420
5. Vezzaro, A.; Krause, S. T.; Nonis, A.; Ramina, A.; Degenhardt, J.; Ruperti, B. Isolation and characterisation of terpene synthases potentially involved in flavour development of ripening olive (Olea europaea L.) fruits J. Plant Physiol. 2012, 169, 908-914
6. Dheda, K.; Huggett, J. F.; Chang, J. S.; Kim, L. U.; Bustin, S. A.; Johnson, M. A.; Rook, G. A. W.; Zumla, A. The implications of using an inappropriate reference gene for real-time reverse transcription PCR data normalization Anal. Biochem. 2005, 344, 141-143
7. Vandesompele, J.; De Preter, K.; Pattyn, F.; Poppe, B.; Van Roy, N.; De Paepe, A.; Speleman, F. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes Genome Biol. 2002, 3 (7) RESEARCH0034
8. Bustin, S. A.; Benes, V.; Garson, J. A.; Hellemans, J.; Huguett, J.; Kubista, M.; Mueller, R.; Nolan, T.; Pfaffl, M. W.; Shipley, G. L.; Vandesompele, J.; Wittwer, C. T. The MIQE Guidelines: minimum information for publication of quantitative real-time PCR experiments Clin. Chem. 2009, 55, 611-622
9. Bustin, S. A.; Beaulieu, J. F.; Huggett, J.; Jaggi, R.; Kibenge, F. S.; Olsvik, P. A.; Penning, L. C.; Toegel, S. MIQE precis: practical implementation of minimum standard guidelines for fluorescence-based quantitative real-time PCR experiments BMC Mol. Biol. 2010, 11, 74
10. Manoli, A.; Sturaro, A.; Trevisan, S.; Quaggiotti, S.; Nonis, A. Evaluation of candidate reference genes for qPCR in maize J. Plant Physiol. 2012, 169, 807-815
11. Reid, K. E.; Olsson, N.; Schlosser, J.; Peng, F.; Lund, S. T. An optimized grapevine RNA isolation procedure and statistical determination of reference genes for real-time RT-PCR during berry development BMC Plant Biol. 2006, 6, 27
12. Nicot, N.; Hausman, J. F.; Hoffmann, L.; Evers, D. Housekeeping gene selection for real-time RT-PCR normalization in potato during biotic and abiotic stress J. Exp. Bot. 2005, 56, 2907-2914
13. Jain, M.; Nijhawan, A.; Tyagi, A. K.; Khurana, J. P. Validation of housekeeping genes as internal control for studying gene expression in rice by quantitative real-time PCR Biochem. Biophys. Res. Commun. 2006, 345, 646-651
14. Chen, L.; Zhong, H. Y.; Kuang, J. F.; Li, J. G.; Lu, W. J.; Chen, J. Y. Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions Planta 2011, 234, 377-390
15. Cruz, F.; Kalaoun, S.; Nobile, P.; Colombo, C.; Almeida, J.; Barros, L.; Romano, E.; Grossi-De-Sá, M. F.; Vaslin, M.; Alves-Ferreira, M. Evaluation of coffee reference genes for relative expression studies by quantitative real-time RT-PCR Mol. Breed. 2009, 23, 607-616
16. Lin, Y. L.; Lai, Z. X. Reference gene selection for qPCR analysis during somatic embryogenesis in longan tree Plant Sci. 2010, 178, 359-365
17. Tong, Z.; Gao, Z.; Wang, F.; Zhou, J.; Zhang, Z. Selection of reliable reference genes for gene expression studies in peach using realtime PCR BMC Mol. Biol. 2009, 10, 71
18. Andersen, C. L.; Jensen, J. L.; ørntoft, T. F. Normalization of real-time quantitative reverse transcription-PCR data: a model-based variance estimation approach to identify genes suited for normalization, applied to bladder and colon cancer data sets Cancer Res. 2004, 64, 5245-5250
19. Hellemans, J.; Mortier, G.; De Paepe, A.; Speleman, F.; Vandesompele, J. qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data Genome Biol. 2007, 8, R19
20. Guénin, S.; Mauriat, M.; Pelloux, J.; Van Wuytswinkel, O.; Bellini, C.; Gutierrez, L. Normalization of qRT-PCR data: the necessity of adopting a systematic, experimental conditions-specific, validation of references J. Exp. Bot. 2009, 60, 487-493
21. Iandolino, A. B.; Goes da Silva, F.; Lim, H.; Choi, H.; Williams, L. E.; Cook, D. R. High-quality RNA, cDNA, and derived EST libraries from grapevine (Vitis vinifera L.) Plant Mol. Biol. Rep. 2004, 22, 269-278
22. Nonis, A.; Ruperti, B.; Pierasco, A.; Canaguier, A.; Adam-Blondon, A. F.; Di Gaspero, G.; Vizzotto, G. Neutral invertases in grapevine and comparative analysis with Arabidopsis, poplar and rice Planta 2008, 229, 129-142
23. Wan, C. Y.; Wilkins, T. A. A modified hot borate method significantly enhances the yield of high-quality RNA from cotton (Gossypium hirsutum L.) Anal. Biochem. 1994, 15, 7-12
24. Conde, C.; Agasse, A.; Silva, P.; Lemoine, R.; Delrot, S.; Tavares, R.; Gerós, H. OeMST2 encodes a monosaccharide transporter expressed throughout olive fruit maturation Plant Cell Physiol. 2007, 48, 1299-1308
25. Falchi, R.; Cipriani, G.; Marrazzo, T.; Nonis, A.; Vizzotto, G.; Ruperti, B. Identification and differential expression dynamics of peach small GTPases encoding genes during fruit development and ripening J. Exp. Bot. 2010, 61, 2829-2842
26. Rozen, S.; Skaletsky, H. J. Primer3 on the WWW for general users and for biologist programmers. In Bioinformatics methods and protocols: methods in molecular biology; Krawetz, S.; Misener, S., Eds.; Humana Press: Totowa, NJ, 2000; pp 365-386.
27. Kibbe, W. A. OligoCalc: an online oligonucleotide properties calculator Nucleic Acids Res. 2007, 35, W43-W46
28. Nonis, A.; Scortegagna, M.; Nonis, A.; Ruperti, B. PRaTo: a web-tool to select optimal primer pairs for qPCR Biochem. Biophys. Res. Commun. 2011, 415, 707-708
29. Muzzalupo, I.; Stefanizzi, F.; Perri, E.; Chiappetta, A. A. Transcript levels of chl p gene, antioxidants and chlorophylls contents in olive (Olea europaea L.) pericarps: a comparative study on eleven olive cultivars harvested in two ripening stages Plant Foods Hum. Nutr. 2011, 66, 1-10
30. Santos Macedo, E.; Cardoso, H. G.; Hernández, A.; Peixe, A. A.; Polidoros, A.; Ferreira, A.; Cordeiro, A.; Arnholdt-Schmitt, B. Physiologic responses and gene diversity indicate olive alternative oxidase as a potential source for markers involved in efficient adventitious root induction Physiol. Plant. 2009, 137, 532-552
31. Schroeder, A.; Mueller, O.; Stocker, S.; Salowsky, R.; Leiber, M.; Gassmann, M.; Lightfoot, S.; Menzel, W.; Granzow, M.; Ragg, T. The RIN: an RNA integrity number for assigning integrity values to RNA measurements BMC Mol. Biol. 2006, 7, 3
32. Barsalobres-Cavallari, C. F.; Severino, F. E.; Maluf, M. P.; Maia, I. G. Identification of suitable internal control genes for expression studies in Coffea arabica under different experimental conditions BMC Mol. Biol. 2009, 10, 1
33. Maroufi, A.; Bockstaele, E. V.; Loose, M. D. Validation of reference genes for gene expression analysis in chicory (Cichorium intybus) using quantitative real-time PCR BMC Mol. Biol. 2010, 11, 15
34. Die, J. V.; Román, B.; Nadal, S.; González-Verdejo, C. I. Evaluation of candidate reference genes for expression studies in Pisum sativum under different experimental conditions Planta 2010, 232, 145-153
35. Qi, J.; Yu, S.; Zhang, F.; Shen, X.; Zhao, X.; Yu, Y.; Zhang, D. Reference gene selection for real-time quantitative polymerase chain reaction of mRNA transcript levels in Chinese cabbage (Brassica rapa L. ssp. pekinensis) Plant Mol. Biol. Rep. 2010, 28, 597-604
36. Gu, C.; Chen, S.; Liu, Z.; Shan, H.; Luo, H.; Guan, Z.; Chen, F. Reference gene selection for quantitative real-time PCR in chrysanthemum subjected to biotic and abiotic stress Mol. Biotechnol. 2011, 49, 192-197
37. Gutierrez, N.; Giménez, M. J.; Palomino, C.; Avila, C. M. Assessment of candidate reference genes for expression studies in Vicia faba L. by real-time quantitative PCR Mol. Breed. 2011, 28, 13-24
38. Huis, R.; Hawkins, S.; Neutelings, G. Selection of reference genes for quantitative gene expression normalization in flax (Linum usitatissimum L.) BMC Plant Biol. 2010, 10, 71
39. Zhong, H. Y.; Chen, J. W.; Li, C. Q.; Chen, L.; Wu, J. Y.; Chen, J. Y.; Lu, W. J.; Li, J. G. Selection of reliable reference genes for expression studies by reverse transcription quantitative real-time PCR in litchi under different experimental conditions Plant Cell. Rep. 2011, 30, 641-653
40. Brunner, A. M.; Yakovlev, I. A.; Strauss, S. H. Validating internal controls for quantitative plant gene expression studies BMC Plant Biol. 2004, 4, 14
41. Schmidt, G. W.; Delaney, S. K. Stable internal reference genes for normalization of real-time RT-PCR in tobacco (Nicotiana tabacum) during development and abiotic stress Mol. Genet. Genomics 2010, 283, 233-241
42. Obrero, A.; Die, J. V.; Román, B.; Gómez, P.; Nadal, S.; González-Verdejo, C. I. Selection of reference genes for gene expression studies in zucchini (Cucurbita pepo) using qPCR J. Agric. Food Chem. 2011, 59, 5402-5411
43. Vashisth, T.; Johnson, L. K.; Malladi, A. An efficient RNA isolation procedure and identification of reference genes for normalization of gene expression in blueberry Plant Cell Rep. 2011, 30, 2167-2176
44. Artico, S.; Nardeli, S. M.; Brilhante, O.; Grossi-de-Sa, M. F.; Alves-Ferreira, M. Identification and evaluation of new reference genes in Gossypium hirsutum for accurate normalization of real-time quantitative RT-PCR data BMC Plant Biol. 2010, 10, 49
45. Czechowski, T.; Stitt, M.; Altman, T.; Udvardi, M. K.; Scheible, W. R. Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis Plant Physiol. 2005, 139, 5-17
46. Nonis, A.; Ruperti, B.; Falchi, R.; Casatta, E.; Thamasebi Enferadi, S.; Vizzotto, G. Differential expression and regulation of a neutral invertase encoding gene from peach (Prunus persica): evidence for a role in fruit development Physiol. Plant. 2007, 129, 436-446
47. Sekhon, R. S.; Lin, H.; Childs, K. L.; Hansey, C. N.; Robin Buell, C.; de Leon, N.; Kaeppler, S. M. Genome-wide atlas of transcription during maize development Plant J. 2011, 66, 553-563
48. Dellapenna, D.; Alexander, D. C.; Bennett, A. B. Molecular cloning of tomato fruit polygalacturonase: Analysis of polygalacturonase mRNA levels during ripening Proc. Natl. Acad. Sci. U.S.A. 1986, 83, 6420-6424
49. Tacken, E.; Ireland, H.; Gunaseelan, K.; Karunairetnam, S.; Wang, D.; Schultz, K.; Bowen, J.; Atkinson, R. G.; Johnston, J. W.; Putterill, J.; Hellens, R. P.; Schaffer, R. J. The role of ethylene and cold temperature in the regulation of the apple POLYGALACTURONASE1 gene and fruit softening Plant Physiol. 2010, 153, 294-305
50. Gaffe, J.; Bru, J. P.; Causse, M.; Vidal, A.; Stamitti-Bert, L.; Carde, J. P.; Gallusci, P. LEFPS1, a tomato farnesyl pyrophosphate gene highly expressed during early fruit development Plant Physiol. 2000, 123, 1351-1362
51. Huggett, J.; Bustin, S. A. Standardisation and reporting for nucleic acid quantification Accredit. Qual. Assur. 2011, 16, 399-405
52. Tricarico, C.; Pinzani, P.; Bianchi, S.; Paglierani, M.; Distante, V.; Pazzagli, M.; Bustin, S. A.; Orlando, C. Quantitative real-time reverse transcription polymerase chain reaction: normalization to rRNA or single housekeeping genes is inappropriate for human tissue biopsies Anal. Biochem. 2002, 309, 293-300
53. Bustin, S. A. Absolute quantification of mRNA using real-time reverse transcription polymerase chain reaction assays J. Mol. Endocrinol. 2000, 25, 169-193