Concomitant phytonutrient and transcriptome analysis of mature fruit and leaf tissues of tomato (Solanum lycopersicum L. cv. Oregon Spring) grown using organic and conventional fertilizer


Autoři: Richard M. Sharpe aff001;  Luke Gustafson aff001;  Seanna Hewitt aff001;  Benjamin Kilian aff001;  James Crabb aff001;  Christopher Hendrickson aff001;  Derick Jiwan aff001;  Preston Andrews aff001;  Amit Dhingra aff001
Působiště autorů: Department of Horticulture, Washington State University,Pullman, WA, United States of America aff001;  Molecular Plant Sciences Graduate Program, Washington State University, Pullman, WA, United States of America aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: 10.1371/journal.pone.0227429

Souhrn

Enhanced levels of antioxidants, phenolic compounds, carotenoids and vitamin C have been reported for several crops grown under organic fertilizer, albeit with yield penalties. As organic agricultural practices continue to grow and find favor it is critical to gain an understanding of the molecular underpinnings of the factors that limit the yields in organically farmed crops. Concomitant phytochemical and transcriptomic analysis was performed on mature fruit and leaf tissues derived from Solanum lycopersicum L. ‘Oregon Spring’ grown under organic and conventional fertilizer conditions to evaluate the following hypotheses. 1. Organic soil fertilizer management results in greater allocation of photosynthetically derived resources to the synthesis of secondary metabolites than to plant growth, and 2. Genes involved in changes in the accumulation of phytonutrients under organic fertilizer regime will exhibit differential expression, and that the growth under different fertilizer treatments will elicit a differential response from the tomato genome. Both these hypotheses were supported, suggesting an adjustment of the metabolic and genomic activity of the plant in response to different fertilizers. Organic fertilizer treatment showed an activation of photoinhibitory processes through differential activation of nitrogen transport and assimilation genes resulting in higher accumulation of phytonutrients. This information can be used to identify alleles for breeding crops that allow for efficient utilization of organic inputs.

Klíčová slova:

Fertilizers – Fruits – Gene expression – Gene ontologies – Leaves – Nitrates – Tomatoes – Vitamin C


Zdroje

1. Aune JB. Conventional, Organic and Conservation Agriculture: Production and Environmental Impact. Lichtfouse E, editor2012. 149–65 p.

2. Seufert V, Ramankutty N, Foley JA. Comparing the yields of organic and conventional agriculture. Nature. 2012;485(7397):229–32. http://www.nature.com/nature/journal/v485/n7397/abs/nature11069.html#supplementary-information. doi: 10.1038/nature11069 22535250

3. Reganold JP, Wachter JM. Organic agriculture in the twenty-first century. Nature Plants. 2016;2(2). doi: 10.1038/nplants.2015.221 WOS:000375393200007. 27249193

4. Kravchenko AN, Snapp SS, Robertson GP. Field-scale experiments reveal persistent yield gaps in low-input and organic cropping systems. Proceedings of the National Academy of Sciences. 2017;114(5):926–31. doi: 10.1073/pnas.1612311114 28096409

5. Barański M, Średnicka-Tober D, Volakakis N, Seal C, Sanderson R, Stewart GB, et al. Higher antioxidant and lower cadmium concentrations and lower incidence of pesticide residues in organically grown crops: a systematic literature review and meta-analyses. British Journal of Nutrition. 2014;112(5):794–811. doi: 10.1017/S0007114514001366 24968103

6. Smith-Spangler C, Brandeau ML, Hunter GE, et al. Are organic foods safer or healthier than conventional alternatives?: A systematic review. Annals of Internal Medicine. 2012;157(5):348–66. doi: 10.7326/0003-4819-157-5-201209040-00007 22944875

7. Dangour AD, Dodhia SK, Hayter A, Allen E, Lock K, Uauy R. Nutritional quality of organic foods: a systematic review. Am J Clin Nutr. 2009;90(3):680–5. Epub 2009/07/31. doi: 10.3945/ajcn.2009.28041 19640946.

8. Asami DK, Hong YJ, Barrett DM, A.E. M. Comparison of the total phenolic and ascorbic acid content of freeze-dried and air-dried marionberry, strawberry, and corn grown using conventional, organic, and sustainable agricultural practices. J Agr Food Chem. 2003;51(5):1237–41.

9. Reganold JP, Andrews PK, Reeve JR, Carpenter-Boggs L, Schadt CW, Alldredge JR, et al. Fruit and Soil Quality of Organic and Conventional Strawberry Agroecosystems. PLoS ONE. 2010;5:e12346. doi: 10.1371/journal.pone.0012346 20824185

10. Peck GM, Andrews PK, Reganold JP, Fellman JK. Apple Orchard Productivity and Fruit Quality under Organic, Conventional, and Integrated Management. Hortscience. 2006;41:99–107.

11. Desjardins Y. Are organically grown fruits and vegetables nutritionally better than conventional ones? Revisiting the question with new eyes. In: Bellon S, Granatstein D, Urban L, editors. International Symposium on Innovation in Integrated and Organic Horticulture. Acta Horticulturae. 11372016. p. 187–99.

12. Kiiski H, Dittmar H, Drach M, Vosskamp R, Trenkel ME, Gutser R, et al. Fertilizers, 2. Types. Ullmann's Encyclopedia of Industrial Chemistry: Wiley-VCH Verlag GmbH & Co. KGaA; 2000.

13. Lammerts van Bueren ET, Jones SS, Tamm L, Murphy KM, Myers JR, Leifert C, et al. The need to breed crop varieties suitable for organic farming, using wheat, tomato and broccoli as examples: A review. NJAS—Wageningen Journal of Life Sciences. 2011;58(3):193–205. https://doi.org/10.1016/j.njas.2010.04.001.

14. Hartmann M, Frey B, Mayer J, Mäder P, Widmer F. Distinct soil microbial diversity under long-term organic and conventional farming. The ISME Journal. 2015;9(5):1177–94. doi: 10.1038/ismej.2014.210 PMC4409162. 25350160

15. van Dijk JP, Cankar K, Scheffer SJ, Beenen HG, Shepherd LVT, Stewart D, et al. Transcriptome Analysis of Potato Tubers—Effects of Different Agricultural Practices. J Agr Food Chem. 2009;57(4):1612–23. doi: 10.1021/jf802815d 19173602

16. van Dijk JP, Cankar K, Hendriksen PJ, Beenen HG, Zhu M, Scheffer S, et al. The identification and interpretation of differences in the transcriptomes of organically and conventionally grown potato tubers. J Agr Food Chem. 2012;60(9):2090–101.

17. Tenea GN, Cordeiro Raposo F, Maquet A. Comparative Transcriptome Profiling in Winter Wheat Grown under Different Agricultural Practices. J Agr Food Chem. 2012;60(44):10970–8. doi: 10.1021/jf302705p 23039160

18. Connor DJ. Organic agriculture cannot feed the world. Field Crop Res. 2008;2008 v.106 no.2(no. 2):pp. 187–90. doi: 10.1016/j.fcr.2007.11.010 PMID: 723091.

19. Muller A, Schader C, El-Hage Scialabba N, Brüggemann J, Isensee A, Erb K-H, et al. Strategies for feeding the world more sustainably with organic agriculture. Nature Communications. 2017;8(1):1290. doi: 10.1038/s41467-017-01410-w 29138387

20. Hewitt S, Kilian B, Hari R, Koepke T, Sharpe R, Dhingra A. Evaluation of multiple approaches to identify genome-wide polymorphisms in closely related genotypes of sweet cherry (Prunus avium L.). Computational and Structural Biotechnology Journal. 2017. Epub March 18. http://dx.doi.org/10.1016/j.csbj.2017.03.002.

21. Conesa A, Gotz S. Blast2GO: A comprehensive suite for functional analysis in plant genomics. Int J Plant Genomics. 2008;2008:619832. Epub 2008/05/17. doi: 10.1155/2008/619832 18483572.

22. Conesa A, Gotz S, Garcia-Gomez JM, Terol J, Talon M, Robles M. Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics. 2005;21(18):3674–6. doi: 10.1093/bioinformatics/bti610 ISI:000231694600016. 16081474

23. Bellieny-Rabelo D, De Oliveira EAG, da Silva Ribeiro E, Costa EP, Oliveira AEA, Venancio TM. Transcriptome analysis uncovers key regulatory and metabolic aspects of soybean embryonic axes during germination. Scientific reports. 2016;6:36009. doi: 10.1038/srep36009 27824062

24. Hoff MLM, Fabrizius A, Czech-Damal NU, Folkow LP, Burmester T. Transcriptome Analysis Identifies Key Metabolic Changes in the Hooded Seal (Cystophora cristata) Brain in Response to Hypoxia and Reoxygenation. PLOS ONE. 2017;12(1):e0169366. doi: 10.1371/journal.pone.0169366 28046118

25. Ye J, Hu T, Yang C, Li H, Yang M, Ijaz R, et al. Transcriptome Profiling of Tomato Fruit Development Reveals Transcription Factors Associated with Ascorbic Acid, Carotenoid and Flavonoid Biosynthesis. PLOS ONE. 2015;10(7):e0130885. doi: 10.1371/journal.pone.0130885 26133783

26. Zhang S, Xu M, Qiu Z, Wang K, Du Y, Gu L, et al. Spatiotemporal transcriptome provides insights into early fruit development of tomato (Solanum lycopersicum). Scientific Reports. 2016;6:23173. doi: 10.1038/srep23173 https://www.nature.com/articles/srep23173#supplementary-information. 26988970

27. Zhang C, Zhang H, Zhan Z, Liu B, Chen Z, Liang Y. Transcriptome Analysis of Sucrose Metabolism during Bulb Swelling and Development in Onion (Allium cepa L.). Front Plant Sci. 2016;7(1425). doi: 10.3389/fpls.2016.01425 27713754

28. Matas AJ, Yeats TH, Buda GJ, Zheng Y, Chatterjee S, Tohge T, et al. Tissue- and Cell-Type Specific Transcriptome Profiling of Expanding Tomato Fruit Provides Insights into Metabolic and Regulatory Specialization and Cuticle Formation. The Plant Cell. 2011;23(11):3893–910. doi: 10.1105/tpc.111.091173 PMC3246317. 22045915

29. Oliveira AB, Moura CFH, Gomes-Filho E, Marco CA, Urban L, Miranda MRA. The Impact of Organic Farming on Quality of Tomatoes Is Associated to Increased Oxidative Stress during Fruit Development. PLoS ONE. 2013;8:e56354. doi: 10.1371/journal.pone.0056354 23437115

30. Zushi K, Matsuzoe N, Kitano M. Developmental and tissue-specific changes in oxidative parameters and antioxidant systems in tomato fruits grown under salt stress. Scientia Horticulturae. 2009;122(3):362–8. https://doi.org/10.1016/j.scienta.2009.06.001.

31. Britto DT, Kronzucker HJ. NH4 + toxicity in higher plants: a critical review. J Plant Physiol. 2002;159(6):567–84. doi: 10.1078/01761610222260815

32. Magalhaes JR, Wilcox GE. Ammonium toxicity development in tomato plants relative to nitrogen form and light intensity. Journal of Plant Nutrition. 1984;7(10):1477–96. doi: 10.1080/01904168409363295

33. Galpaz N, Ronen G, Khalfa Z, Zamir D, Hirschberg J. A chromoplast-specific carotenoid biosynthesis pathway is revealed by cloning of the tomato white-flower locus. Plant Cell. 2006;18(8):1947–60. doi: 10.1105/tpc.105.039966 16816137; PubMed Central PMCID: PMCPMC1533990.

34. Apel W, Bock R. Enhancement of carotenoid biosynthesis in transplastomic tomatoes by induced lycopene-to-provitamin A conversion. Plant Physiol. 2009;151(1):59–66. Epub 2009/07/10. doi: 10.1104/pp.109.140533 19587100; PubMed Central PMCID: PMCPMC2735999.

35. Giorio G, Yildirim A, Stigliani AL, D'Ambrosio C. Elevation of lutein content in tomato: a biochemical tug-of-war between lycopene cyclases. Metab Eng. 2013;20:167–76. Epub 2013/10/22. doi: 10.1016/j.ymben.2013.10.007 24141052.

36. Wheeler GL, Jones MA, Smirnoff N. The biosynthetic pathway of vitamin C in higher plants. Nature. 1998;393:365. doi: 10.1038/30728 9620799

37. Foyer CH, Noctor G. Ascorbate and Glutathione: The Heart of the Redox Hub. Plant Physiology. 2011;155(1):2–18. doi: 10.1104/pp.110.167569 PMC3075780. 21205630

38. Mellidou I, Kanellis AK. Genetic Control of Ascorbic Acid Biosynthesis and Recycling in Horticultural Crops. Frontiers in Chemistry. 2017;5:50. doi: 10.3389/fchem.2017.00050 PMC5504230. 28744455

39. Bulley SM, Rassam M, Hoser D, Otto W, Schunemann N, Wright M, et al. Gene expression studies in kiwifruit and gene over-expression in Arabidopsis indicates that GDP-L-galactose guanyltransferase is a major control point of vitamin C biosynthesis. J Exp Bot. 2009;60(3):765–78. doi: 10.1093/jxb/ern327 19129165; PubMed Central PMCID: PMCPMC2652059.

40. Ioannidi E, Kalamaki MS, Engineer C, Pateraki I, Alexandrou D, Mellidou I, et al. Expression profiling of ascorbic acid-related genes during tomato fruit development and ripening and in response to stress conditions. J Exp Bot. 2009;60(2):663–78. doi: 10.1093/jxb/ern322 19129160; PubMed Central PMCID: PMCPMC2651456.

41. Bulley S, Wright M, Rommens C, Yan H, Rassam M, Lin-Wang K, et al. Enhancing ascorbate in fruits and tubers through over-expression of the L-galactose pathway gene GDP-L-galactose phosphorylase. Plant Biotechnol J. 2012;10(4):390–7. doi: 10.1111/j.1467-7652.2011.00668.x 22129455.

42. Foyer CH, Halliwell B. The presence of glutathione and glutathione reductase in chloroplasts: A proposed role in ascorbic acid metabolism. Planta. 1976;133(1):21–5. doi: 10.1007/BF00386001 24425174.

43. Massot C, Bancel D, Lopez Lauri F, Truffault V, Baldet P, Stevens R, et al. High Temperature Inhibits Ascorbate Recycling and Light Stimulation of the Ascorbate Pool in Tomato despite Increased Expression of Biosynthesis Genes. PLoS ONE. 2013;8(12):e84474. doi: 10.1371/journal.pone.0084474 PMC3868655. 24367665

44. Gautier H, Massot C, Stevens R, Sérino S, Génard M. Regulation of tomato fruit ascorbate content is more highly dependent on fruit irradiance than leaf irradiance. Annals of Botany. 2009;103(3):495–504. doi: 10.1093/aob/mcn233 PMC2707328. 19033285

45. Amorati R, Valgimigli L. Advantages and limitations of common testing methods for antioxidants. Free radical research. 2015;49(5):633–49. doi: 10.3109/10715762.2014.996146 25511471

46. Ainsworth EA, Gillespie KM. Estimation of total phenolic content and other oxidation substrates in plant tissues using Folin–Ciocalteu reagent. Nature Protocols. 2007;2:875. doi: 10.1038/nprot.2007.102 17446889

47. Singleton VL, Orthofer R, Lamuela-Raventós RM. [14] Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods in Enzymology. 299: Academic Press; 1999. p. 152–78.

48. Plaxton WC, Tran HT. Metabolic Adaptations of Phosphate-Starved Plants. Plant Physiology. 2011;156(3):1006. doi: 10.1104/pp.111.175281 21562330

49. Poirier Y, Thoma S, Somerville C, Schiefelbein J. Mutant of Arabidopsis deficient in xylem loading of phosphate. Plant Physiol. 1991;97(3):1087–93. Epub 1991/11/01. doi: 10.1104/pp.97.3.1087 16668493; PubMed Central PMCID: PMCPMC1081126.

50. Hamburger D, Rezzonico E, MacDonald-Comber Petetot J, Somerville C, Poirier Y. Identification and characterization of the Arabidopsis PHO1 gene involved in phosphate loading to the xylem. Plant Cell. 2002;14(4):889–902. Epub 2002/04/24. doi: 10.1105/tpc.000745 11971143; PubMed Central PMCID: PMCPMC150690.

51. González E, Solano R, Rubio V, Leyva A, Paz-Ares J. PHOSPHATE TRANSPORTER TRAFFIC FACILITATOR1 Is a Plant-Specific SEC12-Related Protein That Enables the Endoplasmic Reticulum Exit of a High-Affinity Phosphate Transporter in Arabidopsis. The Plant Cell. 2005;17(12):3500–12. doi: 10.1105/tpc.105.036640 PMC1315384. 16284308

52. Miura K, Rus A, Sharkhuu A, Yokoi S, Karthikeyan AS, Raghothama KG, et al. The Arabidopsis SUMO E3 ligase SIZ1 controls phosphate deficiency responses. Proc Natl Acad Sci U S A. 2005;102(21):7760–5. Epub 2005/05/17. doi: 10.1073/pnas.0500778102 15894620; PubMed Central PMCID: PMCPMC1140425.

53. Stefanovic A, Ribot C, Rouached H, Wang Y, Chong J, Belbahri L, et al. Members of the PHO1 gene family show limited functional redundancy in phosphate transfer to the shoot, and are regulated by phosphate deficiency via distinct pathways. Plant J. 2007;50(6):982–94. Epub 2007/04/28. doi: 10.1111/j.1365-313X.2007.03108.x 17461783.

54. Hsieh LC, Lin SI, Shih AC, Chen JW, Lin WY, Tseng CY, et al. Uncovering small RNA-mediated responses to phosphate deficiency in Arabidopsis by deep sequencing. Plant Physiol. 2009;151(4):2120–32. Epub 2009/10/27. doi: 10.1104/pp.109.147280 19854858; PubMed Central PMCID: PMCPMC2785986.

55. Nunes-Nesi A, Fernie AR, Stitt M. Metabolic and Signaling Aspects Underpinning the Regulation of Plant Carbon Nitrogen Interactions. Molecular Plant. 2010;3(6):973–96. https://doi.org/10.1093/mp/ssq049. 20926550

56. Stitt M. Nitrate regulation of metabolism and growth. Curr Opin Plant Biol. 1999;2(3):178–86. Epub 1999/06/22. doi: 10.1016/S1369-5266(99)80033-8 10375569.

57. Wang YH, Garvin DF, Kochian LV. Nitrate-induced genes in tomato roots. Array analysis reveals novel genes that may play a role in nitrogen nutrition. Plant Physiol. 2001;127(1):345–59. Epub 2001/09/13. doi: 10.1104/pp.127.1.345 11553762; PubMed Central PMCID: PMCPMC117990.

58. Masclaux-Daubresse C, Daniel-Vedele F, Dechorgnat J, Chardon F, Gaufichon L, Suzuki A. Nitrogen uptake, assimilation and remobilization in plants: challenges for sustainable and productive agriculture. Annals of Botany. 2010;105:1141–57. doi: 10.1093/aob/mcq028 20299346

59. Ono F, Frommer WB, Wirén N. Coordinated Diurnal Regulation of Low- and High-Affinity Nitrate Transporters in Tomato. Plant Biology. 2000;2(1):17–23. doi: 10.1055/s-2000-297

60. Remans T, Nacry P, Pervent M, Girin T, Tillard P, Lepetit M, et al. A central role for the nitrate transporter NRT2.1 in the integrated morphological and physiological responses of the root system to nitrogen limitation in Arabidopsis. Plant Physiol. 2006;140(3):909–21. Epub 2006/01/18. doi: 10.1104/pp.105.075721 16415211; PubMed Central PMCID: PMCPMC1400583.

61. Buchanan B, Gruissem W, Jones R, editors. Biochemistry & Molecular Biology of Plants. Rockville, MD: American Society of Plant Biologists; 2005.

62. Schjoerring JK, Husted S, Mäck G, Mattsson M. The regulation of ammonium translocation in plants. Journal of Experimental Botany. 2002;53(370):883–90. doi: 10.1093/jexbot/53.370.883 11912231

63. Tegeder M, Rentsch D. Uptake and partitioning of amino acids and peptides. Mol Plant. 2010;3(6):997–1011. Epub 2010/11/18. doi: 10.1093/mp/ssq047 21081651.

64. Gilsenan C, Burke RM, Barry-Ryan C. Do Organic Cherry Vine Tomatoes Taste Better Than Conventional Cherry Vine Tomatoes? A Sensory and Instrumental Comparative Study from Ireland. Journal of Culinary Science & Technology. 2012;10(2):154–67. doi: 10.1080/15428052.2012.679232

65. Lindahl M, Spetea C, Hundal T, Oppenheim AB, Adam Z, Andersson B. The thylakoid FtsH protease plays a role in the light-induced turnover of the photosystem II D1 protein. Plant Cell. 2000;12(3):419–31. Epub 2000/03/15. doi: 10.1105/tpc.12.3.419 10715327; PubMed Central PMCID: PMCPMC139841.

66. Caffarri S, Tibiletti T, Jennings RC, Santabarbara S. A Comparison Between Plant Photosystem I and Photosystem II Architecture and Functioning. Current Protein & Peptide Science. 2014;15(4):296–331. doi: 10.2174/1389203715666140327102218 PMC4030627. 24678674

67. Lorimer GH. The Carboxylation and Oxygenation of Ribulose 1,5-Bisphosphate: The Primary Events in Photosynthesis and Photorespiration. Annual Review of Plant Physiology. 1981;32(1):349–82. doi: 10.1146/annurev.pp.32.060181.002025

68. Esser C, Kuhn A, Groth G, Lercher MJ, Maurino VG. Plant and animal glycolate oxidases have a common eukaryotic ancestor and convergently duplicated to evolve long-chain 2-hydroxy acid oxidases. Mol Biol Evol. 2014;31(5):1089–101. Epub 2014/01/11. doi: 10.1093/molbev/msu041 24408912.

69. Quan L-J, Zhang B, Shi W-W, Li H-Y. Hydrogen Peroxide in Plants: a Versatile Molecule of the Reactive Oxygen Species Network. Journal of Integrative Plant Biology. 2008;50(1):2–18. doi: 10.1111/j.1744-7909.2007.00599.x 18666947

70. Gururani MA, Venkatesh J, Tran LS. Regulation of Photosynthesis during Abiotic Stress-Induced Photoinhibition. Mol Plant. 2015;8(9):1304–20. Epub 2015/05/23. doi: 10.1016/j.molp.2015.05.005 25997389.

71. Alscher RG, Erturk N, Heath LS. Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. J Exp Bot. 2002;53(372):1331–41. Epub 2002/05/09. 11997379.

72. Feng K, Yu J, Cheng Y, Ruan M, Wang R, Ye Q, et al. The SOD Gene Family in Tomato: Identification, Phylogenetic Relationships, and Expression Patterns. Front Plant Sci. 2016;7:1279. Epub 2016/09/15. doi: 10.3389/fpls.2016.01279 27625661; PubMed Central PMCID: PMCPMC5003820.

73. Jimenez A, Creissen G, Kular B, Firmin J, Robinson S, Verhoeyen M, et al. Changes in oxidative processes and components of the antioxidant system during tomato fruit ripening. Planta. 2002;214(5):751–8. Epub 2002/03/08. doi: 10.1007/s004250100667 11882944.

74. Neubauer C, Yamamoto HY. Mehler-peroxidase reaction mediates zeaxanthin formation and zeaxanthin-related fluorescence quenching in intact chloroplasts. Plant Physiol. 1992;99(4):1354–61. Epub 1992/08/01. doi: 10.1104/pp.99.4.1354 16669044; PubMed Central PMCID: PMCPMC1080632.

75. Igamberdiev AU, Eprintsev AT. Organic Acids: The Pools of Fixed Carbon Involved in Redox Regulation and Energy Balance in Higher Plants. Front Plant Sci. 2016;7(1042). doi: 10.3389/fpls.2016.01042 27471516

76. Choi K, Lee G, J. Han Y, M. Bunn J. Tomato Maturity Evaluation Using Color Image Analysis. Transactions of the ASAE. 1995;38(1):171. https://doi.org/10.13031/2013.27827.

77. Nagata M, Yamashita I. Simple Method for Simultaneous Determination of Chlorophyll and Carotenoids in Tomato Fruit. NIPPON SHOKUHIN KOGYO GAKKAISHI. 1992;39(10):925–8. doi: 10.3136/nskkk1962.39.925

78. Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods. 2008;5(7):621–8. Epub 2008/06/03. nmeth.1226 [pii] doi: 10.1038/nmeth.1226 18516045.

79. Fernandez-Pozo N, Menda N, Edwards JD, Saha S, Tecle IY, Strickler SR, et al. The Sol Genomics Network (SGN)—from genotype to phenotype to breeding. Nucleic Acids Res. 2015;43(Database issue):D1036–41. doi: 10.1093/nar/gku1195 25428362; PubMed Central PMCID: PMCPMC4383978.

80. Altschul S, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215. doi: 10.1016/s0022-2836(05)80360-2

81. O’Neil ST, Emrich SJ. Assessing De Novo transcriptome assembly metrics for consistency and utility. Bmc Genomics. 2013;14(1):465. doi: 10.1186/1471-2164-14-465 23837739

82. Ruijter JM, Pfaffl MW, Zhao S, Spiess AN, Boggy G, Blom J, et al. Evaluation of qPCR curve analysis methods for reliable biomarker discovery: bias, resolution, precision, and implications. Methods (San Diego, Calif). 2013;59(1):32–46. Epub 2012/09/15. doi: 10.1016/j.ymeth.2012.08.011 22975077.

83. Ruijter JM, Ramakers C, Hoogaars WM, Karlen Y, Bakker O, van den Hoff MJ, et al. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 2009;37(6):e45. doi: 10.1093/nar/gkp045 19237396

84. Pfaffl MW, Horgan GW, Dempfle L. Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acid Research. 2002;30(9). https://doi.org/10.1093/nar/30.9.e36.

85. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008;3(6):1101–8. Epub 2008/06/13. doi: 10.1038/nprot.2008.73 18546601.


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