Correlation analysis of cold-related gene expression with physiological and biochemical indicators under cold stress in oil palm

Autoři: Jing Li aff001;  Yaodong Yang aff001;  Amjad Iqbal aff001;  Rashad Qadri aff001;  Peng Shi aff001;  Yong Wang aff001;  Yi Wu aff001;  Haikuo Fan aff001;  Guojiang Wu aff002
Působiště autorů: Hainan Key Laboratory of Tropical Oil Crops Biology/Coconut Research Institute, Chinese Academy of Tropical Agricultural Sciences, Wenchang, Hainan, China aff001;  Key Laboratory of Plant Resource Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, China aff002
Vyšlo v časopise: PLoS ONE 14(11)
Kategorie: Research Article
doi: 10.1371/journal.pone.0225768


Oil palm (Elaeis guineensis Jacq.) is a representative tropical oil crop that is sensitive to low temperature. Oil palm can experience cold damage when exposed to low temperatures for a long period. During these unfavorable conditions, a series of gene induction/repression and physico-chemical changes occur in oil palm. To better understand the link between these events, we investigated the expression levels of various genes (including COR410, COR413, CBF1, CBF2, CBF3, ICE1-1, ICE1-2, ICE1-4, SIZ1-1, SIZ1-2, ZAT10, ZAT12) and the accumulation of osmolytes (proline, malondialdehyde and sucrose). Likewise, the activity of superoxide dismutase (SOD) in oil palm under cold stress (4°C, 8°C and 12°C) was examined. The results showed a clear link among the expression of CBFs (especially CBF1 and CBF3) and the all genes examined under cold stress (12°C). The expression of CBF1 and CBF2 also exhibited a positive link with the accumulation of sucrose and proline under cold stress in oil palm. At 4°C, the proline content exhibited a very significant correlation with electrolyte leakage in oil palm. The results of this study provide necessary information regarding the mechanism of the response and adaption of oil palm to cold stress. Additionally, they offer clues for the selection or development of cold-tolerant cultivars from the available germplasms of oil palm.

Klíčová slova:

Electrolytes – Gene expression – Leaves – Oil palm – Plant resistance to abiotic stress – Proline – Superoxide dismutase – Thermal stresses


1. Singh R, Ong-Abdullah M, Low E-TL, Manaf MAA, Rosli R, Nookiah R, et al. Oil palm genome sequence reveals divergence of interfertile species in Old and New worlds. Nature. 2013;500(7462):335. doi: 10.1038/nature12309 23883927

2. Corley R. How much palm oil do we need? Environmental Science & Policy. 2009;12(2):134–9.

3. Verheye W. Growth and production of oil palm. Land use, land cover and soil sciences: UNESCO-EOLSS Publishers; 2010.

4. Thomashow MF. Molecular basis of plant cold acclimation: insights gained from studying the CBF cold response pathway. Plant Physiol. 2010;154(2):571–7. doi: 10.1104/pp.110.161794 20921187; PubMed Central PMCID: PMC2948992.

5. Lei X, Xiao Y, Xia W, Mason AS, Yang Y, Ma Z, et al. RNA-seq analysis of oil palm under cold stress reveals a different C-repeat binding factor (CBF) mediated gene expression pattern in Elaeis guineensis compared to other species. PloS one. 2014;9(12):e114482. doi: 10.1371/journal.pone.0114482 25479236; PubMed Central PMCID: PMC4257668.

6. Alvim PdT, Kozlowski TT. Ecophysiology of tropical crops: Elsevier; 2013.

7. Corley R, Tinker P. Vegetative propagation and biotechnology. The oil palm. 2003;4:201–15.

8. Shi Y, Ding Y, Yang S. Molecular Regulation of CBF Signaling in Cold Acclimation. Trends in Plant Science. 2018;23(7):623–37. doi: 10.1016/j.tplants.2018.04.002 29735429

9. Janmohammadi M. Metabolomic analysis of low temperature responses in plants. Current Opinion in Agriculture. 2012;1(1):1–6.

10. Pamplona R. Advanced lipoxidation end-products. Chemico-biological interactions. 2011;192(1):14–20.

11. Rütten D, Santarius KA. Relationship between frost tolerance and sugar concentration of various bryophytes in summer and winter. Oecologia. 1992;91(2):260–5. doi: 10.1007/BF00317794 28313467

12. Ma YZ, Lu Y., Shao J., H. Roles of plant soluble sugars and their responses to plant cold stress. African Journal of Biotechnology. 2009;Vol. 8, (10): pp. 2004–10.

13. Shah K, Dubey RS. Effect of cadmium on proline accumulation and ribonuclease activity in rice seedlings: role of proline as a possible enzyme protectant. Biologia Plantarum. 1997;40(1):121–30. doi: 10.1023/a:1000956803911

14. Thomashow MF. PLANT COLD ACCLIMATION: Freezing Tolerance Genes and Regulatory Mechanisms. Annual Review of Plant Physiology and Plant Molecular Biology. 1999;50(1):571–99. doi: 10.1146/annurev.arplant.50.1.571 15012220.

15. Novillo F, Alonso JM, Ecker JR, Salinas J. CBF2/DREB1C is a negative regulator of CBF1/DREB1B and CBF3/DREB1A expression and plays a central role in stress tolerance in Arabidopsis. Proceedings of the National Academy of Sciences of the United States of America. 2004;101(11):3985–90. doi: 10.1073/pnas.0303029101 15004278

16. Novillo F, Medina J, Salinas J. Arabidopsis CBF1 and CBF3 have a different function than CBF2 in cold acclimation and define different gene classes in the CBF regulon. Proceedings of the National Academy of Sciences. 2007;104(52):21002–7. doi: 10.1073/pnas.0705639105 18093929

17. Kim YS, Lee M, Lee J-H, Lee H-J, Park C-M. The unified ICE–CBF pathway provides a transcriptional feedback control of freezing tolerance during cold acclimation in Arabidopsis. Plant molecular biology. 2015;89(1):187–201. doi: 10.1007/s11103-015-0365-3 26311645

18. Ding Y, Li H, Zhang X, Xie Q, Gong Z, Yang S. OST1 Kinase Modulates Freezing Tolerance by Enhancing ICE1 Stability in Arabidopsis. Developmental Cell. 2015;32(3):278–89. doi: 10.1016/j.devcel.2014.12.023 25669882

19. Miura K, Jin JB, Lee J, Yoo CY, Stirm V, Miura T, et al. SIZ1-mediated sumoylation of ICE1 controls CBF3/DREB1A expression and freezing tolerance in Arabidopsis. The Plant cell. 2007;19(4):1403–14. doi: 10.1105/tpc.106.048397 17416732.

20. Liu Y, Dang P, Liu L, He C. Cold acclimation by the CBF–COR pathway in a changing climate: Lessons from Arabidopsis thaliana. Plant cell reports. 2019;38(5):511–9. doi: 10.1007/s00299-019-02376-3 30652229

21. Xiao Y, Zhou L, Lei X, Cao H, Wang Y, Dou Y, et al. Genome-wide identification of WRKY genes and their expression profiles under different abiotic stresses in Elaeis guineensis. PLOS ONE. 2017;12(12):e0189224. doi: 10.1371/journal.pone.0189224 29228032

22. Byun MY, Cui LH, Lee J, Park H, Lee A, Kim WT, et al. Identification of Rice Genes Associated With Enhanced Cold Tolerance by Comparative Transcriptome Analysis With Two Transgenic Rice Plants Overexpressing DaCBF4 or DaCBF7, Isolated From Antarctic Flowering Plant Deschampsia antarctica. Frontiers in plant science. 2018;9:601. Epub 2018/05/19. doi: 10.3389/fpls.2018.00601 29774046; PubMed Central PMCID: PMC5943562.

23. Shan DP, Huang JG, Yang YT, Guo YH, Wu CA, Yang GD, et al. Cotton GhDREB1 increases plant tolerance to low temperature and is negatively regulated by gibberellic acid. New Phytologist. 2007;176(1):70–81. doi: 10.1111/j.1469-8137.2007.02160.x 17803642

24. Feng Z, Pang J, Kobayashi K, Zhu J, Ort DR. Differential responses in two varieties of winter wheat to elevated ozone concentration under fully open‐air field conditions. Global Change Biology. 2011;17(1):580–91.

25. Karimi M, Ebadi A, Mousavi SA, Salami SA, Zarei A. Comparison of CBF1, CBF2, CBF3 and CBF4 expression in some grapevine cultivars and species under cold stress. Scientia horticulturae. 2015;197:521–6. doi: 10.1016/j.scienta.2015.10.011 26973374.

26. Xiao Y, Yang Y, Cao H, Fan H, Ma Z, Lei X, et al. Efficient isolation of high quality RNA from tropical palms for RNA-seq analysis. Plant Omics. 2012;5(6):584.

27. Miura K, Furumoto T. Cold signaling and cold response in plants. International journal of molecular sciences. 2013;14(3):5312–37. doi: 10.3390/ijms14035312 23466881.

28. Chinnusamy V, Zhu J, Zhu JK. Cold stress regulation of gene expression in plants. Trends Plant Sci. 2007;12(10):444–51. doi: 10.1016/j.tplants.2007.07.002 17855156.

29. Hayat S, Hayat Q, Alyemeni MN, Wani AS, Pichtel J, Ahmad A. Role of proline under changing environments: a review. Plant signaling & behavior. 2012;7(11):1456–66. Epub 09/05. doi: 10.4161/psb.21949 22951402.

30. Fu J, Miao Y, Shao L, Hu T, Yang P. De novo transcriptome sequencing and gene expression profiling of Elymus nutans under cold stress. BMC genomics. 2016;17(1):870–. doi: 10.1186/s12864-016-3222-0 27814694.

31. Maruyama K, Sakuma Y, Kasuga M, Ito Y, Seki M, Goda H, et al. Identification of cold-inducible downstream genes of the Arabidopsis DREB1A/CBF3 transcriptional factor using two microarray systems. The Plant Journal. 2004;38(6):982–93. doi: 10.1111/j.1365-313X.2004.02100.x 15165189

32. Karimi M, Ebadi A, Mousavi SA, Salami SA, Zarei A. Comparison of CBF1, CBF2, CBF3 and CBF4 expression in some grapevine cultivars and species under cold stress. Sci Hortic (Amsterdam). 2015;197:521–6. doi: 10.1016/j.scienta.2015.10.011 26973374; PubMed Central PMCID: PMC4784723.

33. Chinnusamy V, Zhu JK, Sunkar R. Gene regulation during cold stress acclimation in plants. Methods Mol Biol. 2010;639:39–55. doi: 10.1007/978-1-60761-702-0_3 20387039; PubMed Central PMCID: PMC3064467.

34. Verbruggen N, Hermans C. Proline accumulation in plants: a review. Amino acids. 2008;35(4):753–9. doi: 10.1007/s00726-008-0061-6 18379856

35. Yang A, Dai X, Zhang W-H. A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. Journal of experimental botany. 2012;63(7):2541–56. doi: 10.1093/jxb/err431 22301384

36. Szabados L, Savouré A. Proline: a multifunctional amino acid. Trends in plant science. 2010;15(2):89–97. doi: 10.1016/j.tplants.2009.11.009 20036181

37. Yoon Y-E, Kuppusamy S, Cho KM, Kim PJ, Kwack Y-B, Lee YB. Influence of cold stress on contents of soluble sugars, vitamin C and free amino acids including gamma-aminobutyric acid (GABA) in spinach (Spinacia oleracea). Food Chemistry. 2017;215:185–92. doi: 10.1016/j.foodchem.2016.07.167 27542466

38. Savitch LV, Harney T, Huner NPA. Sucrose metabolism in spring and winter wheat in response to high irradiance, cold stress and cold acclimation. Physiologia Plantarum. 2000;108(3):270–8. doi: 10.1034/j.1399-3054.2000.108003270.x

39. Crespi MD, Zabaleta EJ, Pontis HG, Salerno GL. Sucrose Synthase Expression during Cold Acclimation in Wheat. Plant physiology. 1991;96(3):887–91. doi: 10.1104/pp.96.3.887 16668270.

40. Kaur S, Gupta AK, Kaur N, Sandhu JS, Gupta SK. Antioxidative Enzymes and Sucrose Synthase Contribute to Cold Stress Tolerance in Chickpea. Journal of Agronomy and Crop Science. 2009;195(5):393–7. doi: 10.1111/j.1439-037X.2009.00383.x

41. Pasquali G, Biricolti S, Locatelli F, Baldoni E, Mattana M. Osmyb4 expression improves adaptive responses to drought and cold stress in transgenic apples. Plant Cell Rep. 2008;27(10):1677–86. doi: 10.1007/s00299-008-0587-9 18679687.

42. Ma Q, Dai X, Xu Y, Guo J, Liu Y, Chen N, et al. Enhanced tolerance to chilling stress in OsMYB3R-2 transgenic rice is mediated by alteration in cell cycle and ectopic expression of stress genes. Plant physiology. 2009;150(1):244–56. doi: 10.1104/pp.108.133454 19279197

43. Kong X, Pan J, Zhang M, Xing X, Zhou Y, Liu Y, et al. ZmMKK4, a novel group C mitogen‐activated protein kinase kinase in maize (Zea mays), confers salt and cold tolerance in transgenic Arabidopsis. Plant, cell & environment. 2011;34(8):1291–303.

44. Spinner JL, Seo KS, O'Loughlin JL, Cundiff JA, Minnich SA, Bohach GA, et al. Neutrophils are resistant to Yersinia YopJ/P-induced apoptosis and are protected from ROS-mediated cell death by the type III secretion system. PLoS One. 2010;5(2):e9279. doi: 10.1371/journal.pone.0009279 20174624

45. Marchi S, Giorgi C, Suski JM, Agnoletto C, Bononi A, Bonora M, et al. Mitochondria-ros crosstalk in the control of cell death and aging. Journal of signal transduction. 2011;2012.

46. Balakhnina T, Borkowska A. Effects of silicon on plant resistance to environmental stresses. International Agrophysics. 2013;27(2):225–32.

47. Jiang J, Su M, Chen Y, Gao N, Jiao C, Sun Z, et al. Correlation of drought resistance in grass pea (Lathyrus sativus) with reactive oxygen species scavenging and osmotic adjustment. Biologia. 2013;68(2):231–40.

48. Abreu IA, Cabelli DE. Superoxide dismutases—a review of the metal-associated mechanistic variations. Biochimica et Biophysica Acta (BBA)-Proteins and Proteomics. 2010;1804(2):263–74.

49. Liu W, Yu K, He T, Li F, Zhang D, Liu J. The low temperature induced physiological responses of Avena nuda L., a cold-tolerant plant species. The Scientific World Journal. 2013;2013.

50. An D, Yang J, Zhang P. Transcriptome profiling of low temperature-treated cassava apical shoots showed dynamic responses of tropical plant to cold stress. BMC Genomics. 2012;13:64. doi: 10.1186/1471-2164-13-64 22321773; PubMed Central PMCID: PMC3339519.

51. Zhang Q, Chen Q, Wang S, Hong Y, Wang Z. Rice and cold stress: methods for its evaluation and summary of cold tolerance-related quantitative trait loci. Rice (N Y). 2014;7(1):24. doi: 10.1186/s12284-014-0024-3 25279026; PubMed Central PMCID: PMC4182278.

52. Gill SS, Tuteja N. Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant physiology and biochemistry. 2010;48(12):909–30. doi: 10.1016/j.plaphy.2010.08.016 20870416

53. Miller G, Suzuki N, CIFTCI‐YILMAZ S, Mittler R. Reactive oxygen species homeostasis and signalling during drought and salinity stresses. Plant, cell & environment. 2010;33(4):453–67.

54. Chatgilialoglu C, Ferreri C, Hermetter A, Lacote E, Mihaljević B, Nicolaides A, et al. Lipidomics and free radical modifications of lipids. CHIMIA International Journal for Chemistry. 2008;62(9):713–20.

55. Bajji M, Kinet J-M, Lutts S. Osmotic and ionic effects of NaCl on germination, early seedling growth, and ion content of Atriplex halimus (Chenopodiaceae). Canadian Journal of Botany. 2002;80(3):297–304. doi: 10.1139/b02-008

56. Blum A, Ebercon A. Cell Membrane Stability as a Measure of Drought and Heat Tolerance in Wheat1. Crop Science. 1981;21(1):43–7. doi: 10.2135/cropsci1981.0011183X002100010013x

57. Dominguez T, Hernandez ML, Pennycooke JC, Jimenez P, Martinez-Rivas JM, Sanz C, et al. Increasing omega-3 desaturase expression in tomato results in altered aroma profile and enhanced resistance to cold stress. Plant Physiol. 2010;153(2):655–65. doi: 10.1104/pp.110.154815 20382895; PubMed Central PMCID: PMC2879794.

58. Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF. Arabidopsis CBF1 Overexpression Induces COR Genes and Enhances Freezing Tolerance. Science. 1998;280(5360):104–6. doi: 10.1126/science.280.5360.104 9525853

59. Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, et al. Two Transcription Factors, DREB1 and DREB2, with an EREBP/AP2 DNA Binding Domain Separate Two Cellular Signal Transduction Pathways in Drought- and Low-Temperature-Responsive Gene Expression, Respectively, in Arabidopsis. The Plant Cell. 1998;10(8):1391–406. doi: 10.1105/tpc.10.8.1391 9707537

60. J. GS, G. ZD, J. SE, P. SM, M. HJ, F. TM. Low temperature regulation of the Arabidopsis CBF family of AP2 transcriptional activators as an early step in cold-induced COR gene expression. The Plant Journal. 1998;16(4):433–42. doi: 10.1046/j.1365-313x.1998.00310.x 9881163

61. T. VJ, G. ZD, A. VBH, G. FS, F. TM. Roles of the CBF2 and ZAT12 transcription factors in configuring the low temperature transcriptome of Arabidopsis. The Plant Journal. 2005;41(2):195–211. doi: 10.1111/j.1365-313X.2004.02288.x 15634197

Článek vyšel v časopise


2019 Číslo 11