Transcriptome dynamics in mango fruit peel reveals mechanisms of chilling stress

Frontiers in Plant Science

Volumn 7, Issue OCTOBER2016, 2016, Pages

  Sivankalyani, Velu ^a   Sela, Noa ^a   Feygenberg, Oleg ^a   Zemach, Hanita ^a   Maurer, Dalia ^a   Alkan, Noam ^a  

^a VOLCANI CENTER   (Israel)

Author keywords

Chilling injury; Cold storage; Fruit response; Lenticel discoloration; Lipid peroxidation; Mango fruit; Transcriptome

Indexed keywords

EID: 84992498996     PISSN: None     EISSN: 1664462X     Source Type: Journal    
DOI: 10.3389/fpls.2016.01579     Document Type: Article

References (87)

1. Achard, P., Gong, F., Cheminant, S., Alioua, M., Hedden, P., and Genschik, P. (2008). The cold-inducible CBF1 factor-dependent signaling pathway modulates the accumulation of the growth-repressing DELLA proteins via its effect on gibberellin metabolism. Plant Cell 20, 2117-2129. doi: 10.1105/tpc.108.058941
2. Agarwal, P. K., Agarwal, P., Reddy, M., and Sopory, S. K. (2006). Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep. 25, 1263-1274. doi: 10.1007/s00299-006-0204-8
3. Alkan, N., and Fortes, A. M. (2015). Insights into molecular and metabolic events associated with fruit response to postharvest fungal pathogens. Front. Plant Sci. 6:889. doi: 10.3389/fpls.2015.00889
4. Alonso-Ramires, A., Rodriguez, D., Reyes, D., Jimenez, J. A., Nicolas, G., Lopez-Climent, M., et al. (2009). Evidence for a role of gibberellins in salicylic acid-modulated early plant responses to abiotic stress in Arabidopsis seeds. Plant Physiol. 150, 1335-1344. doi: 10.1104/pp.109.139352
5. Altschul, S. F., Gish, W., Miller, W., Myers, E. W., and Lipman, D. J. (1990). Basic local alignment search tool. J. Mol. Biol. 215, 403-410. doi: 10.1016/S0022-2836(05)80360-2
6. Anderson, J. V., Li, Q. B., Haskell, D. W., and Guy, C. L. (1994). Structural organization of the spinach endoplasmic reticulum-luminal 70-kilodalton heat-shock cognate gene and expression of 70-kilodalton heat-shock genes during cold acclimation. Plant Physiol. 104, 1359-1370. doi: 10.1104/pp.104.4.1359
7. Bell, E., and Mullet, J. E. (1993). Characterization of an Arabidopsis lipoxygenase gene responsive to methyl jasmonate and wounding. Plant Physiol. 103, 1133-1137. doi: 10.1104/pp.103.4.1133
8. Bezuidenhout, J., Robbertse, P., and Kaiser, C. (2005). Anatomical investigation of lenticel development and subsequent discolouration of ‘Tommy Atkins’ and ‘Keitt’ mango (Mangifera indica L.) fruit. J. Hortic. Sci. Biotechnol. 80, 18-22. doi: 10.1080/14620316.2005.11511884
9. Birtic, S., Ksas, B., Genty, B., Mueller, M. J., Triantaphylid�s, C., and Havaux, M. (2011). Using spontaneous photon emission to image lipid oxidation patterns in plant tissues. Plant J. 67, 1103-1115. doi: 10.1111/j.1365-313X.2011.04646.x
10. Bolger, A. M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114-2120. doi: 10.1093/bioinformatics/btu170
11. Cao, S., Zheng, Y., Wang, K., Jin, P., and Rui, H. (2009). Methyl jasmonate reduces chilling injury and enhances antioxidant enzyme activity in postharvest loquat fruit. Food Chem. 115, 1458-1463. doi: 10.1016/j.foodchem.2009.01.082
12. Carpaneto, A., Ivashikina, N., Levchenko, V., Krol, E., Jeworutzki, E., Zhu, J. K., et al. (2007). Cold transiently activates calcium-permeable channels in Arabidopsis mesophyll cells. Plant Physiol. 143, 487-494. doi: 10.1104/pp.106.090928
13. Chaplin, G. R., Cole, S. P., Landrigan, M., Nuevo, P. A., Lam, P. F., and Graham, D. (1991). Chilling injury and storage of mango (mangifera indica l.) fruit held under low temperatures. Acta Hortic. 291, 461-471. doi: 10.17660/ActaHortic.1991.291.52
14. Conesa, A., G�tz, S., Garc�a-G�mez, J. M., Terol, J., Tal�n, M., and Robles, M. (2005). Blast2GO: a universal tool for annotation, visualization and analysis in functional genomics research. Bioinformatics 21, 3674-3676. doi: 10.1093/bioinformatics/bti610
15. Consortium, G.O. (2013). Gene ontology annotations and resources. Nucleic Acids Res. 41, D530-D535. doi: 10.1093/nar/gks1050
16. Crif�, T., Puglisi, I., Petrone, G., Recupero, G. R., and Lo Piero, A. R. (2011). Expression analysis in response to low temperature stress in blood oranges: implication of the flavonoid biosynthetic pathway. Gene 476, 1-9. doi: 10.1016/j.gene.2011.02.005
17. Dautt-Castro, M., Ochoa-Leyva, A., Contreras-Vergara, C. A., Pacheco-Sanchez, M. A., Casas-Flores, S., Sanchez-Flores, A., et al. (2015). Mango (Mangifera indica L.) cv. Kent fruit mesocarp de novo transcriptome assembly identifies gene families important for ripening. Front. Plant Sci. 6:62. doi: 10.3389/fpls.2015.00062
18. Dixon, R. A., and Paiva, N. L. (1995). Stress-induced phenylpropanoid metabolism. Plant Cell 7, 1085-1097. doi: 10.2307/3870059
19. Djami-Tchatchou, A. T., and Straker, C. J. (2012). The isolation of high quality RNA from the fruit of avocado (Persea americana Mill.). S. Afr. J. Bot. 78, 44-46. doi: 10.1016/j.sajb.2011.04.009
20. Du Plooy, G., Combrinck, S., Regnier, T., and Botha, B. (2009). Linking lenticel discolouration of mango (Mangifera indica L.) fruit to reversed-phase HPLC profiles of phenolic compounds. J. Hortic. Sci. Biotechnol. 84, 421-426. doi: 10.1080/14620316.2009.11512543
21. Du Plooy, W., Combrinck, S., Botha, B., Van Der Merwe, C., and Regnier, T. (2006). Development of discolouration in mango lenticels. Acta Hortic. 820, 665-672.
22. Echeverria, E., and Valich, J. (1989). Enzymes of sugar and acid metabolism in stored Valencia oranges. J. Am. Soc. Hortic. Sci. 114, 445-449.
23. Farooqi, W., Sattar, A. Jr., Daud, K., and Hussain, M. (1985). Studies on the postharvest chilling sensitivity of mango fruit (Mangifera indica L.). Proc. Annu. Meet. Fla. State Hort. Soc. 98, 220-221.
24. Ferguson, I., Volz, R., and Woolf, A. (1999). Preharvest factors affecting physiological disorders of fruit. Postharvest Biol. Technol. 15, 255-262. doi: 10.1016/S0925-5214(98)00089-1
25. Gentleman, R. C., Carey, V. J., Bates, D. M., Bolstad, B., Dettling, M., Dudoit, S., et al. (2004). Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5:R80. doi: 10.1186/gb-2004-5-10-r80
26. Gonz�lez-Aguilar, G. A., Buta, J. G., and Wang, C. Y. (2001). Methyl jasmonate reduces chilling injury symptoms and enhances colour development of ’Kent’ mangoes. J. Sci. Food Agric. 81, 1244-1249. doi: 10.1002/jsfa.933
27. Gonzalez-Aguilar, G. A., Fortiz, J., Cruz, R., Baez, R., and Wang, C. Y. (2000). Methyl jasmonate reduces chilling injury and maintains postharvest quality of mango fruit. J. Agric. Food Chem. 48, 515-519. doi: 10.1021/jf9902806
28. Grassmann, J., Hippeli, S., and Elstner, E. F. (2002). Plant’s defence and its benefits for animals and medicine: role of phenolics and terpenoids in avoiding oxygen stress. Plant Physiol. Biochem. 40, 471-478. doi: 10.1016/S0981-9428(02)01395-5
29. Hausman, J. F., Evers, D., Thiellement, H., and Jouve, L. (2000). Compared responses of poplar cuttings and in vitro raised shoots to short-term chilling treatments. Plant Cell Rep. 19, 954-960. doi: 10.1007/s002990000229
30. Hodges, D. M., Delong, J. M., Forney, C. F., and Prange, R. K. (1999). Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207, 604-611. doi: 10.1007/s004250050524
31. Hunter, S., Apweiler, R., Attwood, T. K., Bairoch, A., Bateman, A., Binns, D., et al. (2009). InterPro: the integrative protein signature database. Nucleic Acids Res. 37, D211-D215. doi: 10.1093/nar/gkn785
32. Janas, K. M., Cvikrov�, M., Pałągiewicz, A., and Eder, J. (2000). Alterations in phenylpropanoid content in soybean roots during low temperature acclimation. Plant Physiol. Biochem. 38, 587-593. doi: 10.1016/S0981-9428(00)00778-6
33. Jones, J. D., and Dangl, J. L. (2006). The plant immune system. Nature 444, 323-329. doi: 10.1038/nature05286
34. Kane, O., Boulet, M., and Castaigne, F. (1982). Effect of chilling-injury on texture and fungal rot of Mangoes (Mangifera indica L.). J. Food Sci. 47, 992-995. doi: 10.1111/j.1365-2621.1982.tb12762.x
35. Kaniuga, Z. (2008). Chilling response of plants: importance of galactolipase, free fatty acids and free radicals*. Plant Biol. 10, 171-184. doi: 10.1111/j.1438-8677.2007.00019.x
36. Karashima, Y., Talavera, K., Everaerts, W., Janssens, A., Kwan, K. Y., Vennekens, R., et al. (2009). TRPA1 acts as a cold sensor in vitro and in vivo. Proc. Natl. Acad. Sci. U.S.A. 106, 1273-1278. doi: 10.1073/pnas.0808487106
37. Kawasaki, T., Nam, J., Boyes, D. C., Holt, B. F., Hubert, D. A., Wiig, A., et al. (2005). A duplicated pair of Arabidopsis RING-finger E3 ligases contribute to the RPM1-and RPS2-mediated hypersensitive response. Plant J. 44, 258-270. doi: 10.1111/j.1365-313X.2005.02525.x
38. Kim, C. Y., and Zhang, S. (2004). Activation of a mitogen-activated protein kinase cascade induces WRKY family of transcription factors and defense genes in tobacco. Plant J. 38, 142-151. doi: 10.1111/j.1365-313X.2004.02033.x
39. Knight, H., Trewavas, A. J., and Knight, M. R. (1996). Cold calcium signaling in Arabidopsis involves two cellular pools and a change in calcium signature after acclimation. Plant Cell 8, 489-503. doi: 10.1105/tpc.8.3.489
40. Langmead, B., and Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nat. Methods 9, 357-359. doi: 10.1038/nmeth.1923
41. Laxalt, A. M., and Munnik, T. (2002). Phospholipid signalling in plant defence. Curr. Opin. Plant Biol. 5, 332-338. doi: 10.1016/S1369-5266(02)00268-6
42. Le, S., Josse, J., and Husson, F. (2008). FactoMineR: an R package for multivariate analysis. J. Stat. Softw. 25, 1-18. doi: 10.18637/jss.v025.i01
43. Lederman, I. E., Zauberman, G., Weksler, A., Rot, I., and Fuchs, Y. (1997). Ethylene-forming capacity during cold storage and chilling injury development in ‘Keitt’ mango fruit. Postharvest Biol. Technol. 10, 107-112. doi: 10.1016/S0925-5214(96)00060-9
44. Lee, S. H., Ahn, S. J., Im, Y. J., Cho, K., Chung, G.-C., Cho, B.-H., et al. (2005). Differential impact of low temperature on fatty acid unsaturation and lipoxygenase activity in figleaf gourd and cucumber roots. Biochem. Biophys. Res. Commun. 330, 1194-1198. doi: 10.1016/j.bbrc.2005.03.098
45. Li, B., and Dewey, C. N. (2011). RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics 12:323. doi: 10.1186/1471-2105-12-323
46. Liu, J.-X., and Howell, S. H. (2010). Endoplasmic reticulum protein quality control and Its relationship to environmental stress responses in plants. Plant Cell 22, 2930-2942. doi: 10.1105/tpc.110.078154
47. Loveys, B., Robinson, S., Brophy, J., and Chacko, E. (1992). Mango sapburn: components of fruit sap and their role in causing skin damage. Funct. Plant Biol. 19, 449-457.
48. Lukatkin, A. S., Brazaityte, A., Bobinas, C., and Duchovskis, P. (2012). Chilling injury in chilling-sensitive plants: a review. Zemdirbyste 99, 111-124.
49. Luria, N., Sela, N., Yaari, M., Feygenberg, O., Kobiler, I., Lers, A., et al. (2014). De-novo assembly of mango fruit peel transcriptome reveals mechanisms of mango response to hot water treatment. BMC Genomics 15:957. doi: 10.1186/1471-2164-15-957
50. Lyons, J. M. (1973). Chilling injury in plants. Annu. Rev. Plant Physiol. 24, 445-466. doi: 10.1146/annurev.pp.24.060173.002305
51. Manolopoulou-Lambrinou, M., and Papadopoulou, P. (1995). Effect of storage temperature on encore mandarin quality. Acta Hort. 379, 475-482. doi: 10.17660/ActaHortic.1995.379.59
52. Martiniere, A., Shvedunova, M., Thomson, A. J. W., Evans, N. H., Penfield, S., Runions, J., et al. (2011). Homeostasis of plasma membrane viscosity in fluctuating temperatures. New Phytol. 192, 328-337. doi: 10.1111/j.1469-8137.2011.03821.x
53. McGlasson, W., Scott, K., and Mendoza, D. Jr. (1979). The refrigerated storage of tropical and subtropical products. Int. J. Refrig. 2, 199-206. doi: 10.1016/0140-7007(79)90083-5
54. Miller, G., Shulaev, V., and Mittler, R. (2008). Reactive oxygen signaling and abiotic stress. Physiol. Plant. 133, 481-489. doi: 10.1111/j.1399-3054.2008.01090.x
55. Mortazavi, A., Williams, B. A., Mccue, K., Schaeffer, L., and Wold, B. (2008). Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat. Methods 5, 621-628. doi: 10.1038/nmeth.1226
56. Moura, J. C., Bonine, C. A., De Oliveira Fernandes Viana, J., Dornelas, M. C., and Mazzafera, P. (2010). Abiotic and biotic stresses and changes in the lignin content and composition in plants. J. Integr. Plant Biol. 52, 360-376. doi: 10.1111/j.1744-7909.2010.00892.x
57. Mukherjee, P., and Smock, R. (1958). Cold storage of mango. Hortic. Adv. 2:44.
58. Nair, S., and Singh, Z. (2003). Pre-storage ethrel dip reduces chilling injury, enhances respiration rate, ethylene production and improves fruit quality of ‘Kensington’ mango. J. Food Agric. Environ. 1, 93-97.
59. Oufir, M., Legay, S., Nicot, N., Van Moer, K., Hoffmann, L., Renaut, J., et al. (2008). Gene expression in potato during cold exposure: changes in carbohydrate and polyamine metabolisms. Plant Sci. 175, 839-852. doi: 10.1016/j.plantsci.2008.08.010
60. Parkin, K. L., and Kuo, S.-J. (1989). Chilling-induced lipid degradation in Cucumber (Cucumis sativa L. cv Hybrid C) fruit. Plant Physiol. 90, 1049-1056. doi: 10.1104/pp.90.3.1049
61. Peier, A. M., Moqrich, A., Hergarden, A. C., Reeve, A. J., Andersson, D. A., Story, G. M., et al. (2002). A TRP channel that senses cold stimuli and menthol. Cell 108, 705-715. doi: 10.1016/S0092-8674(02)00652-9
62. Peleg, Z., and Blumwald, E. (2011). Hormone balance and abiotic stress tolerance in crop plants. Curr. Opin. Plant Biol. 14, 290-295. doi: 10.1016/j.pbi.2011.02.001
63. 2 and ethanol vapours. Acta Hortic. 455, 629-634. doi: 10.17660/ActaHortic.1997.455.81
64. Phakawatmongkol, W., Ketsa, S., and Van Doorn, W. G. (2004). Variation in fruit chilling injury among mango cultivars. Postharvest Biol. Technol. 32, 115-118. doi: 10.1016/j.postharvbio.2003.11.011
65. Ramamoorthy, R., Jiang, S.-Y., Kumar, N., Venkatesh, P. N., and Ramachandran, S. (2008). A Comprehensive transcriptional profiling of the WRKY gene family in rice under various abiotic and phytohormone treatments. Plant Cell Physiol. 49, 865-879. doi: 10.1093/pcp/pcn061
66. Rapisarda, P., Bellomo, S. E., and Intelisano, S. (2001). Storage temperature effects on blood orange fruit quality. J. Agric. Food Chem. 49, 3230-3235. doi: 10.1021/jf010032l
67. Robinson, M. D., Mccarthy, D. J., and Smyth, G. K. (2010). edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140. doi: 10.1093/bioinformatics/btp616
68. Ruzin, S. E. (1999). Plant Microtechnique and Microscopy. Cambridge: Oxford University Press.
69. Sagi, M., and Fluhr, R. (2006). Production of reactive oxygen species by plant NADPH oxidases. Plant Physiol. 141, 336-340. doi: 10.1104/pp.106.078089
70. 2 levels. Postharvest Biol. Technol. 46, 29-35. doi: 10.1016/j.postharvbio.2007.04.001
71. Scandalios, J. G. (1993). Oxygen stress and superoxide dismutases. Plant Physiol. 101, 7-12.
72. Sevillano, L., Sanchez-Ballesta, M. T., Romojaro, F., and Flores, F. B. (2009). Physiological, hormonal and molecular mechanisms regulating chilling injury in horticultural species. Postharvest technologies applied to reduce its impact. J. Sci. Food Agric. 89, 555-573.
73. Sherman, A., Rubinstein, M., Eshed, R., Benita, M., Ish-Shalom, M., Sharabi-Schwager, M., et al. (2015). Mango (Mangifera indica L.) germplasm diversity based on single nucleotide polymorphisms derived from the transcriptome. BMC Plant Biol. 15:277. doi: 10.1186/s12870-015-0663-6
74. Sivakumar, D., Jiang, Y., and Yahia, E. M. (2011). Maintaining mango (Mangifera indica L.) fruit quality during the export chain. Food Res. Int. 44, 1254-1263. doi: 10.1016/j.foodres.2010.11.022
75. Sivankalyani, V., Feygenberg, O., Diskin, S., Wright, B., and Alkan, N. (2016). Increased anthocyanin and flavonoids in mango fruit peel are associated with cold and pathogen resistance. Postharvest Biol. Technol. 111, 132-139. doi: 10.1016/j.postharvbio.2015.08.001
76. Sivankalyani, V., Feygenberg, O., Maorer, D., Zaaroor, M., Fallik, E., and Alkan, N. (2015). Combined treatments reduce chilling injury and maintain fruit quality in avocado fruit during cold quarantine. PLoS ONE 10:e0140522. doi: 10.1371/journal.pone.0140522
77. Tamjinda, B., Siriphanich, J., and Nobuchi, T. (1992). Anatomy of lenticels and the occurrence of their discolouration in mangoes (Mangifera indica cv. Namdokmai). Kasetsart J. 26, 57-64.
78. Teige, M., Scheikl, E., Eulgem, T., Doczi, F., Ichimura, K., Shinozaki, K., et al. (2004). The MKK2 pathway mediates cold and salt stress signaling in Arabidopsis. Mol. Cell 15, 141-152. doi: 10.1016/j.molcel.2004.06.023
79. Testerink, C., and Munnik, T. (2005). Phosphatidic acid: a multifunctional stress signaling lipid in plants. Trends Plant Sci. 10, 368-375. doi: 10.1016/j.tplants.2005.06.002
80. Tharanathan, R. N., Yashoda, H. M., and Prabha, T. N. (2006). Mango (Mangifera indica L.), “The king of fruits”—an overview. Food Rev. Int. 22, 95-123. doi: 10.1080/87559120600574493
81. Thomashow, M. F. (1999). Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu. Rev. Plant Physiol. Plant Mol. Biol. 50, 571-599. doi: 10.1146/annurev.arplant.50.1.571
82. Vogt, T. (2010). Phenylpropanoid biosynthesis. Mol. Plant 3, 2-20. doi: 10.1093/mp/ssp106
83. Wang, B., Wang, J., Liang, H., Yi, J., Zhang, J., Lin, L., et al. (2008). Reduced chilling injury in mango fruit by 2,4-dichlorophenoxyacetic acid and the antioxidant response. Postharvest Biol. Technol. 48, 172-181. doi: 10.1016/j.postharvbio.2007.10.005
84. Wise, R. R., and Naylor, A. W. (1987). Chilling-enhanced photooxidation-the peroxidative destruction of lipids during chilling Injury to photosynthesis and ultrastructure. Plant Physiol. 83, 272-277. doi: 10.1104/pp.83.2.272
85. Xue, H., Chen, X., and Li, G. (2007). Involvement of phospholipid signaling in plant growth and hormone effects. Curr. Opin. Plant Biol. 10, 483-489. doi: 10.1016/j.pbi.2007.07.003
86. Zhu, A., Li, W., Ye, J., Sun, X., Ding, Y., Cheng, Y., et al. (2011). Microarray expression profiling of postharvest Ponkan mandarin (Citrus reticulata) fruit under cold storage reveals regulatory gene candidates and implications on soluble sugars metabolism. J. Integr. Plant Biol. 53, 358-374. doi: 10.1111/j.1744-7909.2011.01035.x
87. Zhu, Y.-N., Shi, D.-Q., Ruan, M.-B., Zhang, L.-L., Meng, Z.-H., Liu, J., et al. (2013). Transcriptome analysis reveals crosstalk of responsive genes to multiple abiotic stresses in Cotton (Gossypium hirsutum L.). PloS ONE 8:e80218. doi: 10.1371/journal.pone.0080218