Normalizing gene expression by quantitative PCR during somatic embryogenesis in two representative conifer species: Pinus pinaster and Picea abies

Plant Cell Reports

Volumn 32, Issue 5, 2013, Pages 715-729

  de Vega Bartol, José J ^a,b   Santos, Raquen Raissa ^a,b   Simões, Marta ^a,b   Miguel, Célia M ^a,b  

^a INSTITUTO DE BIOLOGIA EXPERIMENTAL E TECNOLÓGICA   (Portugal)

^b INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

Development; Embryo; Picea abies; Pinus pinaster; qPCR; Reference gene

Indexed keywords

ABIES; CONIFEROPHYTA; PICEA ABIES; PINUS PINASTER;

EID: 84876079521     PISSN: 07217714     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00299-013-1407-4     Document Type: Article

References (72)

1. Alonso P, Cortizo M, Cantón FR, Fernández B, Rodríguez A, Centeno ML, Cánovas FM, Ordás RJ (2007) Identification of genes differentially expressed during adventitious shoot induction in Pinus pinea cotyledons by subtractive hybridization and quantitative PCR. Tree Physiol 27: 1721-1730.
2. Andersen CL, Jensen JL, Orntoft TF (2004) 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 64: 5245-5250.
3. Aquea F, Arce-Johnson P (2008) Identification of genes expressed during early somatic embryogenesis in Pinus radiata. Plant Physiol Biochem 46: 559-568.
4. Artico S, Nardeli SM, Brilhante O, Grossi-de-Sa M, Alves-Ferreira M (2010) Identification and evaluation of new reference genes in Gossypium hirsutum for accurate normalization of real-time quantitative RT-PCR data. BMC Plant Biol 10: 49.
5. Bishop-Hurley SL, Gardner RC, Walter C (2003) Isolation and molecular characterization of genes expressed during somatic embryo development in Pinus radiata. Plant Cell Tiss Organ Cult 74: 267-281.
6. Bomal C, Bedon F, Caron S, Mansfield SD, Levasseur C, Cooke JEK, Blais S, Tremblay L, Morency M-J, Pavy N et al (2008) Involvement of Pinus taeda MYB1 and MYB8 in phenylpropanoid metabolism and secondary cell wall biogenesis: a comparative in planta analysis. J Exp Bot 59: 3925-3939.
7. Bonga JM, Klimaszewska KK, Aderkas P (2009) Recalcitrance in clonal propagation, in particular of conifers. Plant Cell Tiss Organ Cult 100: 241-254.
8. Bustin SA (2002) Quantification of mRNA using real-time reverse transcription PCR (RT-PCR): trends and problems. J Mol Endocrinol 29: 23-39.
9. Che P, Love TM, Frame BR, Wang K, Carriquiry AL, Howell SH (2006) Gene expression patterns during somatic embryo development and germination in maize Hi II callus cultures. Plant Mol Biol 62: 1-14.
10. Chen L, Zhong H-Y, Kuang J-F, Li J-G, Lu W-J, Chen J-Y (2011) Validation of reference genes for RT-qPCR studies of gene expression in banana fruit under different experimental conditions. Planta 234: 377-390.
11. Clapham D, Newton R, Sen S, Von Arnold S (2000) Transformation of Picea species. In: Jain M, Minocha SC (eds) Molecular biology of woody plants, vol 2. Springer, Heidelberg, pp 105-110.
12. Cruz F, Kalaoun S, Nobile P, Colombo C, Almeida J, Barros LMG, Romano E, Grossi-de-Sá MF, Vaslin M, Alves-Ferreira M (2009) Evaluation of coffee reference genes for relative expression studies by quantitative real-time RT-PCR. Mol Breeding 23: 607-616.
13. Czechowski T, Stitt M, Altmann T, Udvardi M, Scheible W (2005) Genome-wide identification and testing of superior reference genes for transcript normalization in Arabidopsis. Plant Physiol 139: 5-17.
14. de Almeida MR, Ruedell CM, Ricachenevsky FK, Sperotto RA, Pasquali G, Fett-Neto AG (2010) Reference gene selection for quantitative reverse transcription-polymerase chain reaction normalization during in vitro adventitious rooting in Eucalyptus globulus Labill. BMC Mol Biol 11: 73.
15. Dheda K, Huggett J, Bustin S, Johnson MA, Rook G, Zumla A (2004) Validation of housekeeping genes for normalizing RNA expression in real-time PCR. Biotechniques 37: 112-119.
16. Die J, Román B, Nadal S, González-Verdejo C (2010) Evaluation of candidate reference genes for expression studies in Pisum sativum under different experimental conditions. Planta 232: 145-153.
17. Edgar R, Domrachev M, Lash AE (2002) Gene expression omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res 30: 207-210.
18. Expósito-Rodríguez M, Borges A, Borges-Pérez A, Pérez J (2008) Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol 8: 131.
19. Giménez MJ, Pistón F, Atienza SG (2011) Identification of suitable reference genes for normalization of qPCR data in comparative transcriptomics analyses in the Triticeae. Planta 233: 163-173.
20. Goldberg RB, de Paiva G, Yadegari R (1994) Plant embryogenesis: zygote to seed. Science 266: 605-614.
21. Gonçalves S, Cairney J, Maroco J, Oliveira M, Miguel C (2005) Evaluation of control transcripts in real-time RT-PCR expression analysis during maritime pine embryogenesis. Planta 222: 556-563.
22. Gonçalves S, Cairney J, Rodríguez MP, Cánovas F, Oliveira M, Miguel C (2007) PpRab1, a Rab GTPase from maritime pine is differentially expressed during embryogenesis. Mol Genet Genomics 278: 273-282.
23. Harvengt L (2005) Somatic embryogenesis in maritime pine (Pinus pinaster Ait.). In: Jain SM, Gupta PK (eds) Protocol of somatic embryogenesis in woody plants, vol. 77. Springer Verlag, Berlin, pp 107-120.
24. Hellemans J, Mortier G, de Paepe A, Speleman F, Vandesompele J (2007) qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol 8: R19.
25. Huggett J, Dheda K, Bustin S, Zumla A (2005) Real-time RT-PCR normalisation; strategies and considerations. Genes Immun 6: 279-284.
26. Huis R, Hawkins S, Neutelings G (2010) Selection of reference genes for quantitative gene expression normalization in flax (Linum usitatissimum L.). BMC Plant Biol 10: 71.
27. Humánez A, Blasco M, Brisa C, Segura J, Arrillaga I (2012) Somatic embryogenesis from different tissues of Spanish populations of maritime pine. Plant Cell Tiss Organ Cult 111: 373-383.
28. Jain M, Khurana JP (2009) Transcript profiling reveals diverse roles of auxin-responsive genes during reproductive development and abiotic stress in rice. FEBS J 276: 3148-3162.
29. Klimaszewska K, Lachance D, Pelletier G (2001a) Regeneration of transgenic Picea glauca, P. mariana, and P. abies after cocultivation of embryogenic tissue with Agrobacteriumtumefaciens. In Vitro Cell Dev Biol Plant 37: 748-755.
30. Klimaszewska KK, Park YS, Overton C, MacEacheron I, Bonga JM (2001b) Optimized somatic embryogenesis in Pinus strobus L. In Vitro Cell Dev Biol Plant 37: 392-399.
31. Lara-Chavez A, Egertsdotter U, Flinn BS (2012) Comparison of gene expression markers during zygotic and somatic embryogenesis in pine. In Vitro Cell Dev Biol Plant 48: 341-354.
32. Li Q-F, Sun SSM, Yuan D-Y, Yu H-X, Gu M-H, Liu Q-Q (2010) Validation of candidate reference genes for the accurate normalization of real-time quantitative RT-PCR data in rice during seed development. Plant Mol Biol Rep 28: 49-57.
33. Lin Y, Lai Z (2010) Reference gene selection for qPCR analysis during somatic embryogenesis in longan tree. Plant Sci 178: 359-365.
34. Litvay JD, Verma DC, Johnson MA (1985) Influence of loblolly pine (Pinus taeda L.) culture medium and its components on growth and somatic embryogenesis of the wild carrot (Daucus carota L.). Plant Cell Rep 4: 325-328.
35. Liu J-J, Zamani A, Ekramoddoullah AKM (2010) Expression profiling of a complex thaumatin-like protein family in western white pine. Planta 231: 637-651.
36. Livak K, Schmittgen T (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-[Delta][Delta] CT method. Methods 25: 402-408.
37. Marum L, Estêvão C, Oliveira MM, Amâncio S, Rodrigues L, Miguel C (2004) Recovery of cryopreserved embryogenic cultures of maritime pine: effect of cryoprotectant and suspension density. Cryo Lett 25: 363-374.
38. Marum L, Rocheta M, Maroco J, Oliveira MM, Miguel C (2009) Analysis of genetic stability at SSR loci during somatic embryogenesis in maritime pine (Pinus pinaster). Plant Cell Rep 28: 673-682.
39. Marum L, Miguel A, Ricardo CP, Miguel C (2012) Reference gene selection for quantitative real-time PCR normalization in Quercus suber. PLoS One 7: e35113.
40. Meinke DW (1995) Molecular genetics of plant embryogenesis. Annu Rev Plant Physiol Plant Mol Biol 46: 369-394.
41. Miguel C, Gonçalves S, Tereso S, Marum L, Maroco J, Oliveira MM (2004) Somatic embryogenesis from 20 open-pollinated families of Portuguese plus trees of maritime pine. Plant Cell Tiss Org Cult 76: 121-130.
42. Nolan T, Bustin SA (2004) Pitfalls of quantitative real-time reverse-transcription polymerase chain reaction. J Biomol Tech 15: 155.
43. Nolan T, Hands RE, Bustin SA (2006) Quantification of mRNA using real-time RT-PCR. Nat Protoc 1: 1559-1582.
44. Nordgård O, Kvaløy JT, Farmen RK, Heikkilä R (2006) Error propagation in relative real-time reverse transcription polymerase chain reaction quantification models: the balance between accuracy and precision. Anal biochem 356: 182-193.
45. Paim RM, Pereira MH, Di Ponzio R, Rodrigues JO, Guarneri AA, Gontijo NF, Araújo RN (2012) Validation of reference genes for expression analysis in the salivary gland and the intestine of Rhodnius prolixus (Hemiptera, Reduviidae) under different experimental conditions by quantitative real-time PCR. BMC Res Notes 5: 128.
46. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45.
47. Pfaffl MW, Tichopad A, Prgomet C, Neuvians TP (2004) Determination of stable housekeeping genes, differentially regulated target genes and sample integrity: BestKeeper-Excel-based tool using pair-wise correlations. Biotechnol Lett 26: 509-515.
48. Ramakers C, Ruijter J, Deprez R, Moorman A (2003) Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neurosci Lett 339: 62-66.
49. Ratnaparkhe S, Egertsdotter E, Flinn B (2009) Identification and characterization of a matrix metalloproteinase (Pta1-MMP) expressed during Loblolly pine (Pinus taeda) seed development, germination completion, and early seedling establishment. Planta 230: 339-354.
50. Ruijter J, Ramakers C, Hoogaars W, Karlen Y, Bakker O, van den Hoff M, Moorman A (2009) Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res 37(6): e45.
51. Schmittgen T, Livak K (2008) Analyzing real-time PCR data by the comparative CT method. Nat Protoc 3: 1101-1108.
52. Schmittgen TD, Zakrajsek BA (2000) Effect of experimental treatment on housekeeping gene expression: validation by real-time, quantitative RT-PCR. J Biochem Biophys Methods 46: 69-81.
53. Simões M, Lorenz WW, Alba R, Gonçalves S, Maroco J, Dean J, Miguel CM (2009) Embryogenesis in maritime pine: a transcriptomics approach. In: IUFRO tree biotechnology conference, Jun 28-Jul 2, Whistler, Canada (Poster).
54. Spencer MWB, Grene R, Lindsey K (2007) Transcriptional profiling of the Arabidopsis embryo. Plant Physiol 143: 924-940.
55. Suzuki M, Wang HHY, McCarty DR (2006) Repression of the LEAFY COTYLEDON 1/B3 regulatory network in plant embryo development by VP1/ABSCISIC ACID INSENSITIVE 3-LIKE B3 genes. Plant Physiol 143: 902-911.
56. Tereso S, Miguel C, Zoglauer K, Valle-Piquera C (2006) Stable Agrobacterium-mediated transformation of embryogenic tissues from Pinus pinaster Portuguese genotypes. Plant Growth Regul 50: 57-68.
57. Thellin O, ElMoualij B, Heinen E, Zorzi W (2009) A decade of improvements in quantification of gene expression and internal standard selection. Biotechnol Adv 27: 323-333.
58. Tong Z, Gao Z, Wang F, Zhou J, Zhang Z (2009) Selection of reliable reference genes for gene expression studies in peach using real-time PCR. BMC Mol Biol 10: 71.
59. Trontin J, Walter C, Klimaszewska K, Park Y, Lelu-Walter M (2007) Recent progress in genetic transformation of four Pinus spp. Transgenic Plant J 1: 314-329.
60. Trontin JF, Debille S, Canlet F, Harvengt L, Lelu-Walter MA, Label P, Teyssier C, Lesage-Descauses MC, Le Metté C, Miguel C et al (2013) Somatic embryogenesis as an effective regeneration support for reverse genetics in maritime pine: the Sustainpine collaborative project as a case study. In: Proceedings of the IUFRO Working Party 2. 09. 02, integrating vegetative propagation, biotechnology and genetic improvement for tree production and sustainable forest management.
61. Tu L, Zhang X, Liu D, Jin S, Cao J, Zhu L, Deng F, Tan J, Zhang C (2007) Suitable internal control genes for qRT-PCR normalization in cotton fiber development and somatic embryogenesis. Chin Sci Bull 52: 3110-3117.
62. Uddenberg D, Valladares S, Abrahamsson M, Sundström JF, Sundås-Larsson A, von Arnold S (2011) Embryogenic potential and expression of embryogenesis-related genes in conifers are affected by treatment with a histone deacetylase inhibitor. Planta 234: 527-539.
63. Vandesompele J, de Preter K, Pattyn F, Poppe B, van Roy N, de Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol 3(7): research0034.
64. Vandesompele J, Kubista M, Pfaffl M (2009) Reference gene validation software for improved normalization. In: Logan J, Edwards K, Saunders N (eds) Real-time PCR: current technology and applications. Caister Academic Press, London, pp 47-64.
65. Vásquez-Robinet C, Watkinson JI, Sioson AA, Ramakrishnan N, Heath LS, Grene R (2010) Differential expression of heat shock protein genes in preconditioning for photosynthetic acclimation in water-stressed loblolly pine. Plant Physiol Biochem 48: 256-264.
66. Vestman D, Larsson E, Uddenberg D, Cairney J, Clapham D, Sundberg E, von Arnold S (2011) Important processes during differentiation and early development of somatic embryos of Norway spruce as revealed by changes in global gene expression. Tree Genet Genomes 7: 347-362.
67. von Arnold S, Clapham D (2008) Spruce embryogenesis. In: Suarez MF, Bozhkov PV (eds) Plant embryogenesis methods in molecular biology. Humana, Totowa, pp 31-47.
68. von Arnold S, Sabala I, Bozhkov P, Dyachok J, Filonova L (2002) Developmental pathways of somatic embryogenesis. Plant Cell Tiss Organ Cult 69: 233-249.
69. von Arnold S, Bozhkov P, Clapham D, Dyachok J, Filonova L, Hogberg K-A, Ingouff M, Wiweger M (2005) Propagation of Norway spruce via somatic embryogenesis. Plant Cell Tiss Organ Cult 81: 323-329.
70. West M, Harada JJ (1993) Embryogenesis in higher plants: an overview. Plant Cell Online 5: 1361-1369.
71. Xu M, Zhang B, Su X, Zhang S, Huang M (2011) Reference gene selection for quantitative real-time polymerase chain reaction in Populus. Anal Biochem 408: 337-339.
72. Yan J, Yuan F, Long G, Qin L, Deng Z (2012) Selection of reference genes for quantitative real-time RT-PCR analysis in citrus. Mol Biol Rep 39: 1831-1838.