Evidence for pre-climacteric activation of AOX transcription during cold-induced conditioning to ripen in European pear (Pyrus communis L.)

Autoři: Christopher Hendrickson aff001;  Seanna Hewitt aff001;  Mark E. Swanson aff003;  Todd Einhorn aff004;  Amit Dhingra aff001
Působiště autorů: Department of Horticulture, Washington State University, Pullman, WA, United States of America aff001;  Molecular Plant Sciences Program, Washington State University, Pullman, WA, United States of America aff002;  School of the Environment, Washington State University, Pullman, WA, United States of America aff003;  Department of Horticulture, Michigan State University, East Lansing, MI, United States of America aff004
Vyšlo v časopise: PLoS ONE 14(12)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0225886


European pears (Pyrus communis L.) require a range of cold-temperature exposure to induce ethylene biosynthesis and fruit ripening. Physiological and hormonal responses to cold temperature storage in pear have been well characterized, but the molecular underpinnings of these phenomena remain unclear. An established low-temperature conditioning model was used to induce ripening of ‘D’Anjou’ and ‘Bartlett’ pear cultivars and quantify the expression of key genes representing ripening-related metabolic pathways in comparison to non-conditioned fruit. Physiological indicators of pear ripening were recorded, and fruit peel tissue sampled in parallel, during the cold-conditioning and ripening time-course experiment to correlate gene expression to ontogeny. Two complementary approaches, Nonparametric Multi-Dimensional Scaling and efficiency-corrected 2-(ΔΔCt), were used to identify genes exhibiting the most variability in expression. Interestingly, the enhanced alternative oxidase (AOX) transcript abundance at the pre-climacteric stage in ‘Bartlett’ and ‘D’Anjou’ at the peak of the conditioning treatments suggests that AOX may play a key and a novel role in the achievement of ripening competency. There were indications that cold-sensing and signaling elements from ABA and auxin pathways modulate the S1-S2 ethylene transition in European pears, and that the S1-S2 ethylene biosynthesis transition is more pronounced in ‘Bartlett’ as compared to ‘D’Anjou’ pear. This information has implications in preventing post-harvest losses of this important crop.

Klíčová slova:

Auxins – Biosynthesis – Conditioned response – Ethylene – Fruits – Gene expression – Pears – Ethylene signaling cascade


1. White PJ. Recent advances in fruit development and ripening: an overview. Journal of Experimental Botany. 2002;53(377):1995–2000. doi: 10.1093/jxb/erf105 12324524

2. Anwar R, Mattoo AK, Handa AK. Ripening and Senescence of Fleshy Fruits. Paliyath G, Subramanian J., Lim L., Subramanian K., Handa AK, Mattoo AK, editors2018. 15–51 p.

3. Karlova R, Chapman N, David K, Angenent GC, Seymour GB, de Maagd RA. Transcriptional control of fleshy fruit development and ripening. Journal of Experimental Botany. 2014;65(16):4527–41. doi: 10.1093/jxb/eru316 25080453

4. Granell A, Rambla José L. Biosynthesis of Volatile Compounds. The Molecular Biology and Biochemistry of Fruit Ripening. 2013. doi: 10.1002/9781118593714.ch6

5. Cherian S, Figueroa CR, Nair H. ‘Movers and shakers’ in the regulation of fruit ripening: a cross-dissection of climacteric versus non-climacteric fruit. Journal of Experimental Botany. 2014;65(17):4705–22. doi: 10.1093/jxb/eru280 24994760

6. S F Yang a, Hoffman NE. Ethylene Biosynthesis and its Regulation in Higher Plants. Annual Review of Plant Physiology. 1984;35(1):155–89. doi: 10.1146/annurev.pp.35.060184.001103

7. Tatsuki M. Ethylene Biosynthesis and Perception in Fruit. Journal of the Japanese Society for Horticultural Science. 2010;79(4):315–26. WOS:000283277200001.

8. Barry CS, Giovannoni JJ. Ethylene and fruit ripening. Journal of Plant Growth Regulation. 2007;26(2):143–59. doi: 10.1007/s00344-007-9002-y WOS:000248582800006.

9. Barry CS, Llop-Tous MI, Grierson D. The Regulation of 1-Aminocyclopropane-1-Carboxylic Acid Synthase Gene Expression during the Transition from System-1 to System-2 Ethylene Synthesis in Tomato. Plant Physiology. 2000;123(3):979. doi: 10.1104/pp.123.3.979 10889246

10. Tucker G, Yin XR, Zhang AD, Wang MM, Zhu QG, Liu XF, et al. Ethylene and fruit softening. Food Quality & Safety. 2017;1(4):253–67. doi: 10.1093/fqsafe/fyx024 WOS:000424579100002.

11. Han Y, Kuang J, Chen J, Liu X, Xiao Y, Fu C, et al. Banana Transcription Factor MaERF11 Recruits Histone Deacetylase MaHDA1 and Represses the Expression of MaACO1 and Expansins during Fruit Ripening. Plant Physiology. 2016;168(1):357–76. http://dx.doi.org/10.1104/pp.16.00301.

12. Liu M, Pirrello J, Kesari R, Mila I, Roustan JP, Li Z, et al. A dominant repressor version of the tomato Sl‐ERF. B3 gene confers ethylene hypersensitivity via feedback regulation of ethylene signaling and response components. The Plant Journal, 76(3), 406–419. The Plant Journal. 2013;73(6):406–19. doi: 10.1111/tpj.12305 23931552

13. 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. Journal of experimental botany, 64(8), 2499–2510. Journal of Experimental Botany. 2013;64(8). doi: 10.1093/jxb/ert108 23599278

14. Zhou M, Guo S, Zhang J, Zhang H, Li C, Tang X, et al. Comparative dynamics of ethylene production and expression of the ACS and ACO genes in normal-ripening and non-ripening watermelon fruits. Acta Physiologiae Plantarum. 2016;38(9). doi: 10.1007/s11738-016-2248-x

15. El-Sharkawy I, Sherif S, Mahboob A, Abubaker K, Bouzayen M, Jayasankar S. Expression of auxin-binding protein1 during plum fruit ontogeny supports the potential role of auxin in initiating and enhancing climacteric ripening. Plant Cell Reports. 2012;31(10):1911–21. doi: 10.1007/s00299-012-1304-2 22739723

16. Leng P, Yuan B, Guo YD. The role of abscisic acid in fruit ripening and responses to abiotic stress. Journal of Experimental Botany. 2014;65(16):4577–88. doi: 10.1093/jxb/eru204 WOS:000342928000008. 24821949

17. Soto A, Ruiz K. B., Ravaglia D., Costa G., & Torrigiani P. ABA may promote or delay peach fruit ripening through modulation of ripening-and hormone-related gene expression depending on the developmental stage. Plant Physiology and Biochemistry. 2013;64:11–24. Plant Physiology and Biochemistry. doi: 10.1016/j.plaphy.2012.12.011 23337357

18. Weng L, Zhao F, Li R, Xu C, Chen K, Xiao H. The Zinc Finger Transcription Factor SlZFP2 Negatively Regulates Abscisic Acid Biosynthesis and Fruit Ripening in Tomato. Plant Physiology. 2015;167(3):931–49. doi: 10.1104/pp.114.255174 25637453

19. Jia H, Jiu S, Zhang C, Wang C, Tariq P, Liu Z, et al. Abscisic acid and sucrose regulate tomato and strawberry fruit ripening through the abscisic acid-stress-ripening transcription factor. Plant Biotechnology Journal. 2016;14(10):2045–65. doi: 10.1111/pbi.12563 27005823

20. Dai S, Li P, Chen P, Li Q, Pei Y, He S, et al. Transcriptional regulation of genes encoding ABA metabolism enzymes during the fruit development and dehydration stress of pear 'Gold Nijisseiki'. Plant Physiology and Biochemistry. 2014;82:299–308. doi: 10.1016/j.plaphy.2014.06.013 25038474

21. Pons C, Martí C, Forment J, Crisosto CH, Dandekar AM, Granell A. A bulk segregant gene expression analysis of a peach population reveals components of the underlying mechanism of the fruit cold response. PLoS One. 2014;9(3). https://doi.org/10.1371/journal.pone.0090706.

22. Rahman A. Auxin: a regulator of cold stress response. Physiol Plantarum. 2013;147(1):28–35. doi: 10.1111/j.1399-3054.2012.01617.x 22435366

23. Ashraf MA, Rahman A. Hormonal Regulation of Cold Stress Response. In: Wani SH, Herath V, editors. Cold Tolerance in Plants: Physiological, Molecular and Genetic Perspectives. Cham: Springer International Publishing; 2018. p. 65–88.

24. El-Sharkawy I, Sherif S, Mila I, Bouzayen M, Jayasankar S. Molecular characterization of seven genes encoding ethylene-responsive transcriptional factors during plum fruit development and ripening. Journal of Experimental Botany. 2009;60(3):907–22. doi: 10.1093/jxb/ern354 19213809

25. Tatsuki M, Nakajima N, Fujii H, Shimada T, Nakano M, Hayashi K-I, et al. Increased levels of IAA are required for system 2 ethylene synthesis causing fruit softening in peach (Prunus persica L. Batsch). Journal of Experimental Botany. 2013;64(6):1049–59. https://doi.org/10.1093/jxb/ers381.

26. Yang Y, Wu Y, Pirrello J, Regad F, Bouzayen M, Deng W, et al. Silencing Sl-EBF1 and Sl-EBF2 expression causes constitutive ethylene response phenotype, accelerated plant senescence, and fruit ripening in tomato. Journal of Experimental Botany. 2009;61(3):697–708. doi: 10.1093/jxb/erp332 19903730

27. Choudhury SR, Roy S, Sengupta DN. Characterization of transcriptional profiles of MA-ACS1 and MA-ACO1 genes in response to ethylene, auxin, wounding, cold and different photoperiods during ripening in banana fruit. J Plant Physiol. 2008;165(18):1865–78. doi: 10.1016/j.jplph.2008.04.012 18554749

28. Fujisawa M, Nakano T, Shima Y, Ito Y. A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. The Plant Cell. 2013;25(3):371–86. http://dx.doi.org/10.1105/tpc.112.108118.

29. Ito Y, Nishizawa-Yokoi A, Endo M, Mikami M, Shima Y, Nakamura N, et al. Re-evaluation of the rin mutation and the role of RIN in the induction of tomato ripening. Nature plants. 2017;3(11):866. doi: 10.1038/s41477-017-0041-5 29085071

30. Elitzur T, Yakir E, Quansah L, Zhangjun F, Vrebalob JT, Khayat E, et al. Banana MaMADS transcription factors are necessary for fruit ripening and molecular tools to promote shelf-life and food security. Plant Physiology. 2016. http://dx.doi.org/10.1104/pp.15.01866.

31. Osorio S, Scossa F, Fernie AR. Molecular regulation of fruit ripening. Front Plant Sci. 2013;4. https://doi.org/10.3389/fpls.2013.00198.

32. Nham NT, Macnish AJ, Zakharov F, Mitcham EJ. ‘Bartlett’ pear fruit (Pyrus communis L.) ripening regulation by low temperatures involves genes associated with jasmonic acid, cold response, and transcription factors. Plant Science. 2017;260:8–18. doi: 10.1016/j.plantsci.2017.03.008 28554478

33. Berkowitz O, De Clercq I, Van Breusegem F, Whelan J. Interaction between hormonal and mitochondrial signalling during growth, development and in plant defence responses. Plant, Cell and Environment. 2016;39(5):1127–39. doi: 10.1111/pce.12712 26763171

34. Perotti VE, Moreno AS, Podestá FE. Physiological aspects of fruit ripening: the mitochondrial connection. Mitochondrion. 2014;17:1–6. doi: 10.1016/j.mito.2014.04.010 24769052

35. Dhingra A, Hendrickson C, inventorsControl of ripening and senescence in pre-harvest and post-harvest plants and plant materials by manipulating alternative oxidase activity. USA patent 9,591,847. 2017.

36. Szal B, Rychter A. Alternative oxidase-never ending story. Postepy biochemii. 2016;62(2):138–48. 28132465

37. Sewelam N, Kazan K, Schenk PM. Global plant stress signaling: reactive oxygen species at the cross-road. Frontiers in plant science. 2016;7:187. doi: 10.3389/fpls.2016.00187 26941757

38. Considine MJ, Daley DO, Whelan J. The expression of alternative oxidase and uncoupling protein during fruit ripening in mango. Plant Physiol. 2001;126(4):1619–29. doi: 10.1104/pp.126.4.1619 11500560

39. Duque P, Arrabaca JD. Respiratory metabolism during cold storage of apple fruit. II. Alternative oxidase is induced at the climacteric. Physiol Plantarum. 1999;107(1):24–31. doi: 10.1034/j.1399-3054.1999.100104.x ISI:000083523200004.

40. Holtzapffell RC, M Finnegan P, Millar A, R Badger M, Day D. Mitochondrial protein expression in tomato fruit during on-vine ripening and cold storage2002. 827–34 p.

41. Lei T, Feng H, Sun X, Dai Q-L, Zhang F, Liang H-G, et al. The alternative pathway in cucumber seedlings under low temperature stress was enhanced by salicylic acid. Plant Growth Regul. 2009;60(1):35. doi: 10.1007/s10725-009-9416-6

42. Yang Q-S, Wu J-H, Li C-Y, Wei Y-R, Sheng O, Hu C-H, et al. Quantitative proteomic analysis reveals that antioxidation mechanisms contribute to cold tolerance in plantain (Musa paradisiaca L.; ABB Group) seedlings. Molecular & cellular proteomics: MCP. 2012;11(12):1853–69. doi: 10.1074/mcp.M112.022079 22982374

43. Jobling JJ, McGlasson WB. A comparison of ethylene production, maturity and controlled atmosphere storage life of Gala, Fuji and Lady Williams apples (Malus domestica, Borkh.). Postharvest Biol Tec. 1995;6(3):209–18. https://doi.org/10.1016/0925-5214(94)00002-A.

44. Knee M, Looney NE, Hatfield SGS, Smith SM. Initiation of Rapid Ethylene Synthesis by Apple and Pear Fruits in Relation to Storage Temperature. Journal of Experimental Botany. 1983;34(146):1207–12.

45. Hershkovitz V, Friedman H, Goldschmidt EE, Feygenberg O, Pesis E. Induction of ethylene in avocado fruit in response to chilling stress on tree. J Plant Physiol. 2009;166(17):1855–62. Epub 2009/07/14. doi: 10.1016/j.jplph.2009.05.012 19592132.

46. Mworia EG, Yoshikawa T, Salikon N, Oda C, Asiche WO, Yokotani N, et al. Low-temperature-modulated fruit ripening is independent of ethylene in ‘Sanuki Gold’ kiwifruit. Journal of Experimental Botany. 2012;63(2):963–71. doi: 10.1093/jxb/err324 PMC3254691. 22058408

47. Lelievre JM, Tichit L, Dao P, Fillion L, Nam YW, Pech JC, et al. Effects of chilling on the expression of ethylene biosynthetic genes in Passe-Crassane pear (Pyrus communis L.) fruits. Plant Mol Biol. 1997;33(5):847–55. Epub 1997/03/01. doi: 10.1023/a:1005750324531 9106508.

48. Hartmann C, Drouet A, Morin F. Ethylene and ripenig of apple, pear and cherry fruit. Plant Physiology and Biochemistry. 1987;25(4):505–12.

49. Sugar D, Einhorn TC. Conditioning temperature and harvest maturity influence induction of ripening capacity in ‘d’Anjou’pear fruit. Postharvest Biol Tec. 2011;60(2):121–4. http://doi.org/10.1016/j.postharvbio.2010.12.005.

50. Sugar D, Basile SR. Integrated ethylene and temperature conditioning for induction of ripening capacity in ‘Anjou’and ‘Comice’pears. Postharvest Biol Tec. 2013;83:9–16. http://doi.org/10.1016/j.postharvbio.2013.03.010.

51. Sugar D, Basile SR. Integrated ethylene and temperature conditioning for inducing pear ripening capacity. 2015:567–72. doi: 10.17660/ActaHortic.2015.1094.76

52. Chiriboga MA, Schotsmans WC, Larrigaudière C, Dupille E, Recasens I. Responsiveness of ‘Conference’pears to 1‐methylcyclopropene: the role of harvest date, orchard location and year. Journal of Science of Food and Agriculture. 2013;93(3):619–25. doi: 10.1002/jsfa.5853 22936181

53. Zucoloto M, Antoniolli LR, Squeira DL, Czermainski ABC, Salomao LCC. Conditioning temperature for inducing uniform ripening of ‘Abate Fetel’ pears. Revista Ciência Agronômica. 2016;47(2):344–50. doi: 10.5935/1806-6690.20160040

54. Smékalová V, Doskočilová A, Komis G, Šamaj J. (2014). Crosstalk between secondary messengers, hormones and MAPK modules during abiotic stress signalling in plants., 32(1), 2–11. Biotechnology Advances. 2014;32(1):2–11. doi: 10.1016/j.biotechadv.2013.07.009 23911976

55. Nham NT, Willits N, Zakharov F, Mitcham EJ. A model to predict ripening capacity of ‘Bartlett’ pears (Pyrus communis L.) based on relative expression of genes associated with the ethylene pathway. Postharvest Biol Tec. 2017;128:138–43. https://doi.org/10.1016/j.postharvbio.2017.02.006.

56. Nham NT, de Fretas ST, Macnish AJ, Carr KM, Kietikul T, Guilatco AJ, et al. A transcriptome approach towards understanding the development of ripening capacity in ‘Bartlett’ pears (Pyrus communis L.). Bmc Genomics. 2015;16(1). doi: 10.1186/s12864-015-1939-9 26452470

57. Paul V, Pandey R, Srivastava GC. The fading distinctions between classical patterns of ripening in climacteric and non-climacteric fruit and the ubiquity of ethylene—an overview. Journal of Food Science and Technology. 2012;49(1):1–21. doi: 10.1007/s13197-011-0293-4 23572821

58. Catala R, Medina J, Salinas J. Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proceeding of National Academy of Sciences, USA. 2011;108(39):16475–80. doi: 10.1073/pnas.1107161108 21930922

59. Kondo S, Meemak S, Ban Y, Moriguchi T, Harada T. Effects of auxin and jasmonates on 1-aminocyclopropane-1-carboxylate (ACC) synthase and ACC oxidase gene expression during ripening of apple fruit. Postharvest Biol Tec. 2009;51(2):281–4. http://doi.org/10.1016/j.postharvbio.2008.07.012.

60. Tacken EJ, Ireland HS, Wang YY, Putterill J, Schaffer RJ. Apple EIN3 BINDING F-box 1 inhibits the activity of three apple EIN3-like transcription factors. AoB Plants. 2012. https://doi.org/10.1093/aobpla/pls034.

61. McCune B, Grace J. Analysis of ecological communities. MJM Software Design, Gleneden Beach, OR2002.

62. Donoho D. High-Dimensional Data Analysis: The Curses and Blessings of Dimensionality. AMS Math Challenges Lecture2000.

63. Val J, Monge E, Risco D, Blanco A. Effect of Pre-Harvest Calcium Sprays on Calcium Concentrations in the Skin and Flesh of Apples. Journal of Plant Nutrition. 2008;31(11):1889–905. 10.1080/01904160802402757

64. Gasic K, Hernandez A, Korban SS. RNA extraction from different apple tissues rich in polyphenols and polysaccharides for cDNA library construction. Plant Molecular Biology Reporter. 2004;22(4):437–8. doi: 10.1007/BF02772687

65. Dhingra A. Pre-publication Release of Rosaceae Genome Information https://genomics.wsu.edu/research/ Washington State University; 2013 [cited 2016 December 10]. Available from: https://genomics.wsu.edu/research/

66. Velasco R, Zharkikh A, Affourtit J, Dhingra A, Cestaro A, Kalyanaraman A, et al. The genome of the domesticated apple (Malus [times] domestica Borkh.). Nature Genetics. 2010;42(10):833–9. doi: 10.1038/ng.654 20802477

67. Ramakers C, Ruijter JM, Deprez RHL, Moorman AF. Assumption-free analysis of quantitative real-time polymerase chain reaction (PCR) data. Neuroscience Letters. 2003;339(1):62–6. doi: 10.1016/s0304-3940(02)01423-4 12618301

68. 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

69. Pfaffl MW. A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res. 2001;29(9):e45–e. doi: 10.1093/nar/29.9.e45 11328886

70. Andersen CL, Ledet-Jensen J., T. Ø. Normalization of real-time quantitative RT-PCR data: a model based variance estimation approach to identify genes suited for normalization—applied to bladder- and colon-cancer data-sets. Cancer Research. 2004;64:5245–50. doi: 10.1158/0008-5472.CAN-04-0496 15289330

71. Imai T, Ubi BE, Saito T, Moriguchi T. Evaluation of reference genes for accurate normalization of gene expression for real time-quantitative PCR in Pyrus pyrifolia using different tissue samples and seasonal conditions. PLoS One. 2014;9(1). https://doi.org/10.1371/journal.pone.0086492.

72. Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, et al. Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biology. 2002;3(7). doi: 10.1186/gb-2002-3-7-research0034 12184808

73. 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

74. Gish W, States DJ. Identification of protein coding regions by database similarity search. Nat Genet. 1993;3(3):266–72. Epub 1993/03/01. doi: 10.1038/ng0393-266 8485583.

75. Rieu I, Powers SJ. Real-time quantitative RT-PCR: design, calculations, and statistics. Plant Cell. 2009;21(4):1031–3. Epub 2009/04/28. doi: 10.1105/tpc.109.066001 19395682; PubMed Central PMCID: PMC2685626.

76. Kruskal JB. Nonmetric multidimensional scaling: A numerical method. Psychometrika. 1964;29(2):115–29. doi: 10.1007/bf02289694

77. Oksanen J. Multivariate analysis of ecological communities in R: vegan tutorial. R Package version. 2011;1(7):11–2.

78. Krzywinski M, Altman N. Points of significance: Nonparametric tests. Nature Methods. 2014;11(5):467–8. doi: 10.1038/nmeth.2937 24820360

79. 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.

80. Morpheus. Broad Institute https://software.broadinstitute.org/morpheus2019.

81. USDA. Agricultural Statistics 2016. USDA NASS; 2016.

82. Elkins R, Bell R, Einhorn TC. Needs Assessment for Future US Pear Rootstock Research Directions Based on the Current State of Pear Production and Rootstock Research. J Am Pom Soc. 2012;66(3):153–63.

83. Guzman D, Dhingra A. Challenges and Opportunities in Pear Breeding. In: Lang G, editor. Achieving sustainable cultivation of temperate zone tree fruits and berries. 2. Cambridge, UK: Burleigh Dodd Science Publishing Limited; 2019.

84. Minas IS, Tanou G, Molassiotis A. Environmental and orchard bases of peach fruit quality. Scientia Horticulturae. 2018;235:307–22. https://doi.org/10.1016/j.scienta.2018.01.028.

85. Serra S, Sullivan N, Mattheis JP, Musacchi S, Rudell DR. Canopy attachment position influences metabolism and peel constituency of European pear fruit. BMC Plant Biology. 2018;18(1):364. doi: 10.1186/s12870-018-1544-6 30563450

86. Agar IT, Biasi WV, Mitcham EJ. Temperature and exposure time during ethylene conditioning affect ripening of Bartlett pears. J Agric Food Chem. 2000;48(2):165–70. Epub 2000/02/26. doi: 10.1021/jf990458o 10691611.

87. Sugar D, Mitcham E, Kupferman G. Rethinking the chill requirement for pear ripening. Good Fruit Grower. 2009.

88. Villalobos-Acuna M, Mitcham EJ. Ripening of European pears: the chilling dilemma. Postharvest biology and technology. 2008;49(2):187–200.

89. Wayland M. A Practical Approach to Microarray Data Analysis. Briefings in Functional Genomics & Proteomics. 2003;2(1):82–4. https://doi.org/10.1093/bfgp/2.1.82.

90. Young FW. Nonmetric multidimensional scaling: Recovery of metric information. Psychometrika. 1970;35(4):455–73. doi: 10.1007/BF02291820

91. McCarthy DJ, Smyth GK. Testing significance relative to a fold-change threshold is a TREAT. Bioinformatics. 2009;25(6):765–71. doi: 10.1093/bioinformatics/btp053 19176553

92. Dalman MR, Deeter A, Nimishakavi G, Duan Z-H. Fold change and p-value cutoffs significantly alter microarray interpretations. BMC Bioinformatics. 2012;13(2):S11. doi: 10.1186/1471-2105-13-s2-s11 22536862

93. Ho J, Tumkaya T, Aryal S, Choi H, Claridge-Chang A. Moving beyond P values: Everyday data analysis with estimation plots. bioRxiv. 2019:377978. doi: 10.1101/377978

94. Jajo A, Rahim MA, Serra S, Gagliardi F, Jajo NK, Musacchi S, et al. Impact of tree training system, branch type and position in the canopy on the ripening homogeneity of ‘Abbé Fétel’ pear fruit. Tree Genetics & Genomes. 2014;10(5):1477–88. doi: 10.1007/s11295-014-0777-2

95. Rudell DR, Serra S, Sullivan N, Mattheis JP, Musacchi S. Survey of ‘d’Anjou’ Pear Metabolic Profile Following Harvest from Different Canopy Positions and Fruit Tissues. 2017;52(11):1501. doi: 10.21273/hortsci12375-17

96. Olsvik PA, Søfteland L, Lie KK. Selection of reference genes for qRT-PCR examination of wild populations of Atlantic cod Gadus morhua. BMC Research Notes. 2008;1(1):47. doi: 10.1186/1756-0500-1-47 18710500

97. Liu M, Udhe-Stone C, Goudar CT. Progress curve analysis of qRT-PCR reactions using the logistic growth equation. Biotechnology progress. 2011;27(5):1407–14. Epub 2011/07/19. doi: 10.1002/btpr.666 21766473.

98. Nham NT, Macnish AJ, Zakharov F, Mitcham EJ. ‘Bartlett’pear fruit (Pyrus communis L.) ripening regulation by low temperatures involves genes associated with jasmonic acid, cold response, and transcription factors. Plant Science. 2017;260:8–18. doi: 10.1016/j.plantsci.2017.03.008 28554478

99. Sharkawy IE-S, Jones B, Gentzbittel L, Lelièvre J-M. Differential regulation of ACC synthase genes in cold-dependent and -independent ripening in pear fruit. Plant, Cell & Environ. 2004;27(10):1197–210. doi: 10.1111/j.1365-3040.2004.01218.x

100. El-Sharkawy E-I, Jones B, Gentzbittel L, Lelivre JM, Pech JC, Latché A. Differential regulation of ACC synthase genes in cold‐dependent and‐independent ripening in pear fruit. Plant, Cell & Environ. 2004;27(10):1197–210. doi: 10.1111/j.1365-3040.2004.01218.x

101. Liu M, Pirrello J, Chervin C, Roustan J-P, Bouzayen M. Ethylene Control of Fruit Ripening: Revisiting the Complex Network of Transcriptional Regulation. Plant Physiology. 2015;169(4):2380–90. doi: 10.1104/pp.15.01361 26511917

102. Shan W, Kuang JF, Lu WJ, Chen JY. Banana fruit NAC transcription factor MaNAC1 is a direct target of MaICE1 and involved in cold stress through interacting with MaCBF1. Plant, Cell and Environment. 2014;37(9):2116–27. doi: 10.1111/pce.12303 24548087

103. Sivankalyani V, Geetha M, Subramanyam K, Girija S. Ectopic expression of Arabidopsis RCI2A gene contributes to cold tolerance in tomato. Transgenic Research. 2015;24(2):237–51. doi: 10.1007/s11248-014-9840-x 25260337

104. Shi Y, Yang S. ABA Regulation of the Cold Stress Response in Plants. In: Zhang D-P, editor. Abscisic Acid: Metabolism, Transport and Signaling. Dordrecht: Springer Netherlands; 2014. p. 337–63.

105. Eremina M, Rozhon W, Poppenberger B. Hormonal control of cold stress responses in plants. Cellular and Molecular Life Sciences. 2016;73(4):797–810. doi: 10.1007/s00018-015-2089-6 26598281

106. Tian MS, Prakash S, Zhang N, Ross GS. Chilling-induced ethylene biosynthesis in Braeburn apples. Plant Growth Regul. 2002;38(3):249–57. doi: 10.1023/a:1021552002676

107. Chang J, Clay JM, Chang C. Association of cytochrome b5 with ETR1 ethylene receptor signaling through RTE1 in Arabidopsis. The Plant journal: for cell and molecular biology. 2014;77(4):558–67. doi: 10.1111/tpj.12401 24635651.

108. Ma Q, Du W, Brandizzi F, Giovannoni JJ, Barry CS. Differential control of ethylene responses by GREEN-RIPE and GREEN-RIPE LIKE1 provides evidence for distinct ethylene signaling modules in tomato. Plant Physiology. 2012;160(4):1968–84. doi: 10.1104/pp.112.205476 23043080

109. Qiu L, Xie F, Yu J, Wen CK. Arabidopsis RTE1 is essential to ethylene receptor ETR1 amino-terminal signaling independent of CTR1. Plant Physiol. 2012;159(3):1263–76. Epub 2012/05/09. doi: 10.1104/pp.112.193979 22566492; PubMed Central PMCID: PMC3387708.

110. Binder BM, Rodríguez FI, Bleecker AB. The copper transporter RAN1 is essential for biogenesis of ethylene receptors in Arabidopsis. Journal of Biological Chemistry. 2010;285(48):37263–70. doi: 10.1074/jbc.M110.170027 20876528

111. Resnick JS, Wen C-K, Shockey JA, Chang C. REVERSION-TO-ETHYLENE SENSITIVITY 1, a conserved gene that regulates ethylene receptor function in Arabidopsis. Proceedings of the National Academy of Sciences. 2006;103(20):7917–22. doi: 10.1073/pnas.0602239103 16682642

112. Zhang M-Y, Xue C, Xu L, Sun H, Qin M-F, Zhang S, et al. Distinct transcriptome profiles reveal gene expression patterns during fruit development and maturation in five main cultivated species of pear (Pyrus L.). Scientific Reports. 2016;6:28130. doi: 10.1038/srep28130 https://www.nature.com/articles/srep28130#supplementary-information. 27305967

113. Catalá R, López-Cobollo R, Castellano MM, Angosto T, Alonso JM, Ecker JR, et al. The Arabidopsis 14-3-3 protein RARE COLD INDUCIBLE 1A links low-temperature response and ethylene biosynthesis to regulate freezing tolerance and cold acclimation. The Plant Cell. 2014;26(8):3326–42. doi: 10.1105/tpc.114.127605 25122152

114. Obsilova V, Kopecka M, Kosek D, Kacirova M, Kylarova S, Rezabkova L, et al. Mechanisms of the 14-3-3 protein function: regulation of protein function through conformational modulation. Physiol Res. 2014;63 Suppl 1:S155–64. Epub 2014/02/26. 24564655.

115. Medina J, Rodríguez-Franco M, Peñalosa A, Carrascosa MJ, Neuhaus G, Salinas J. Arabidopsis mutants deregulated in RCI2A expression reveal new signaling pathways in abiotic stress responses. The Plant Journal. 2005;42(4):586–97. doi: 10.1111/j.1365-313X.2005.02400.x 15860016

116. Pattison RJ, Csukasi F., & Catalá C. (2014). Mechanisms regulating auxin action during fruit development. Physiol Plantarum. 2014;151(1):62–72. doi: 10.1111/ppl.12142 24329770

117. El-Sharkawy I, Sherif SM, Jones B, Mila I, Kumar PP, Bouzayen M, et al. TIR1-like auxin-receptors are involved in the regulation of plum fruit development. Journal of Experimental Botany. 2014;65(18):5205–15. doi: 10.1093/jxb/eru279 24996652

118. Robles LM, Deslauriers SD, Alvarez AA, Larsen PB. A loss-of-function mutation in the nucleoporin AtNUP160 indicates that normal auxin signalling is required for a proper ethylene response in Arabidopsis. Journal of experimental botany. 2012;63(5):2231–41. Epub 2012/01/11. doi: 10.1093/jxb/err424 22238449.

119. Schaffer RJ, Ireland HS, Ross JJ, Ling TJ, David KM. SEPALLATA1/2-suppressed mature apples have low ethylene, high auxin and reduced transcription of ripening-related genes. AoB Plants. 2013;5:pls047. doi: 10.1093/aobpla/pls047 23346344; PubMed Central PMCID: PMC3551604.

120. Tacken EJ, Ireland HS, Wang YY, Putterill J, Schaffer RJ. Apple EIN3 BINDING F-box 1 inhibits the activity of three apple EIN3-like transcription factors. AoB Plants. 2012;2012:pls034. doi: 10.1093/aobpla/pls034 23585922; PubMed Central PMCID: PMC3624930.

121. Breitel DA, Chappell-Maor L, Meir S, Panizel I, Puig CP, Hao Y, et al. AUXIN RESPONSE FACTOR 2 Intersects Hormonal Signals in the Regulation of Tomato Fruit Ripening. PLoS genetics. 2016;12(3). https://doi.org/10.1371/journal.pgen.1005903.

122. Dong T, Hu Z, Deng L, Wang Y, Zhu M, Zhang J, et al. A tomato MADS-box transcription factor, SlMADS1, acts as a negative regulator of fruit ripening. Plant Physiology. 2013;163(2):1026–36. doi: 10.1104/pp.113.224436 24006286

123. Bemer M, Karlova R, Ballester AR, Tikunov YM, Bovy AG, Wolters-Arts M, et al. The Tomato FRUITFULL Homologs TDR4/FUL1 and MBP7/FUL2 Regulate Ethylene-Independent Aspects of Fruit Ripening. The Plant Cell. 2012;24(11):4437–51. doi: 10.1105/tpc.112.103283 23136376

124. Shima Y, Fujisawa M, Kitagawa M, Nakano T, Kimbara J, Nakamura N, et al. Tomato FRUITFULL homologs regulate fruit ripening via ethylene biosynthesis. Bioscience, Biotechnology and Biochemistry. 2014;78(2):231–7. http://dx.doi.org/10.1080/09168451.2014.878221.

125. Xu F, Yuan S, Zhang DW, Lv X, Lin HH. The role of alternative oxidase in tomato fruit ripening and its regulatory interaction with ethylene. J Exp Bot. 2012;63(15):5705–16. Epub 2012/08/24. ers226 [pii] doi: 10.1093/jxb/ers226 22915749.

126. Borecký J, Nogueira F. T., De Oliveira K. A., Maia I. G., Vercesi A. E., & Arruda P. (2006). The plant energy-dissipating mitochondrial systems: depicting the genomic structure and the expression profiles of the gene families of uncoupling protein and alternative oxidase in monocots and dicots. Journal of Experimental Botany. 2006;57(4):849–64. doi: 10.1093/jxb/erj070 16473895

127. Feng H, Guan D, Sun K, Wang Y, Zhang T, Wang R. Expression and signal regulation of the alternative oxidase genes under abiotic stresses. Acta Biochimica et Biophysica Sinica. 2013;45(12):985–94. doi: 10.1093/abbs/gmt094 24004533

128. Xu F, Yuan S, Zhang D-W, Lv X, Lin H-H. The role of alternative oxidase in tomato fruit ripening and its regulatory interaction with ethylene. J Exp Bot. 2012;63(15):5707–16. https://doi.org/10.1093/jxb/ers226.

129. Xu F, Yuan S, Zhang DW, Lv X, Lin HH. The role of alternative oxidase in tomato fruit ripening and its regulatory interaction with ethylene. Journal of Experimental Botany. 2012;63(15):5705–16. doi: 10.1093/jxb/ers226 22915749

130. Wagner AM. A role for active oxygen species as second messengers in the induction of alternative oxidase gene expression in Petunia hybrida cells. FEBS Lett. 1995;368(2):339–42. Epub 1995/07/17. doi: 10.1016/0014-5793(95)00688-6 7628633.

131. Vanlerberghe GC. Alternative Oxidase: A Mitochondrial Respiratory Pathway to Maintain Metabolic and Signaling Homeostasis during Abiotic and Biotic Stress in Plants. International Journal of Molecular Sciences. 2013;14(4):6805–47. doi: 10.3390/ijms14046805 PMC3645666. 23531539

132. Zhang X, Ivanova A, Vandepoele K, Radomilijac JD, Van de Velde J, Berkowitz O, et al. The transcription factor MYB29 is a regulator of ALTERNATIVE OXIDASE 1. Plant Physiology. 2017. http://dx.doi.org/10.1104/pp.16.01494.

133. Fan ZQ, Ba LJ, Shan W, Xiao YY, Lu WJ, Kuang JF, et al. A banana R2R3-MYB transcription factor MaMYB3 is involved in fruit ripening through modulation of starch degradation by repressing starch degradation-related genes and MabHLH6. Plant J. 2018;96(6):1191–205. Epub 2018/09/23. doi: 10.1111/tpj.14099 30242914.

134. Yao F, Zhu H, Yi C, Qu H, Jiang Y. MicroRNAs and targets in senescent litchi fruit during ambient storage and post-cold storage shelf life. BMC plant biology. 2015;15:181–. doi: 10.1186/s12870-015-0509-2 26179282.

135. Antoniou C, Savvides A, Christou A, Fotopoulos V. Unravelling chemical priming machinery in plants: the role of reactive oxygen–nitrogen–sulfur species in abiotic stress tolerance enhancement. Current Opinion in Plant Biology. 2016;33:101–7. doi: 10.1016/j.pbi.2016.06.020 27419886

136. Wawrzynska A, Moniuszko G, Sirko A. Links Between Ethylene and Sulfur Nutrition—A Regulatory Interplay or Just Metabolite Association? Front Plant Sci. 2015;6. doi: 10.3389/fpls.2015.01053 26648954

137. Ziogas V, Molassiotis A, Fotopoulos V, Tanou G. Hydrogen Sulfide: A Potent Tool in Postharvest Fruit Biology and Possible Mechanism of Action. Front Plant Sci. 2018;9(1375). doi: 10.3389/fpls.2018.01375 30283483

138. Moniuszko G. Ethylene signaling pathway is not linear, however its lateral part is responsible for sensing and signaling of sulfur status in plants. Plant Signal Behav. 2015;10(11):e1067742. Epub 2015/09/05. doi: 10.1080/15592324.2015.1067742 26340594; PubMed Central PMCID: PMC4883965.

Článek vyšel v časopise


2019 Číslo 12
Nejčtenější tento týden