Physiological and transcriptomic responses of Lanzhou Lily (Lilium davidii, var. unicolor) to cold stress

English version

Autoři: Xuehui Tian ^aff001; Jianming Xie ^aff001; Jihua Yu ^aff001
Působiště autorů: College of Horticulture, Gansu Agricultural University, Lanzhou, Gansu, China ^aff001; Department of Ecological Environment and Engineering, Yangling Vocational and Technical College, Yangling, Shanxi, China ^aff002
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pone.0227921

Souhrn

Low temperature induces changes in plants at physiological and molecular levels, thus affecting growth and development. The Lanzhou lily (Lilium davidii, var. unicolor) is an important medicinal plant with high economic value. However, the molecular mechanisms underlying its photosynthetic and antioxidation responses to low temperature still remain poorly understood. This study subjected the Lanzhou lily to the two temperatures of 20°C (control) and 4°C (low temperature) for 24 h. Physiological parameters related to membrane integrity, photosynthesis, antioxidant system, and differentially expressed genes were investigated. Compared with control, low temperature increased the relative electrical conductivity by 43.2%, while it decreased net photosynthesis rate, ratio of variable to maximal fluorescence, and catalase activity by 47.3%, 10.1%, and 11.1%, respectively. In addition, low temperature significantly increased the content of soluble protein, soluble sugar, and proline, as well as the activity of superoxide dismutase and peroxidase. Comparative transcriptome profiling showed that a total of 238,109 differentially expressed genes were detected. Among these, 3,566 were significantly upregulated while 2,982 were significantly downregulated in response to low temperature. Gene Ontology enrichment analysis indicated that in response to low temperature, the mostly significantly enriched differentially expressed genes were mainly involved in phosphorylation, membrane and protein kinase activity, as well as photosynthesis, light harvesting, light reaction, and alpha,alpha-trehalose-phosphate synthase activity. Kyoto Encyclopedia of Genes and Genomes enrichment analysis also indicated that the most significantly enriched pathways involved ribosome biogenesis in eukaryotes, phenylalanine metabolism, circadian rhythm, porphyrin and chlorophyll metabolism, photosynthesis of antenna proteins, photosynthesis, and carbon fixation in photosynthetic organisms. Moreover, the expression patterns of 10 randomly selected differentially expressed genes confirmed the RNA-Seq results. These results expand the understanding of the physiological and molecular mechanisms underlying the response of the Lanzhou lily to low temperature stress.

Klíčová slova:

Antioxidants – Gene expression – Gene ontologies – Photosynthesis – Plant physiology – Thermal stresses – Transcriptome analysis – Lily

Zdroje

1. Gomes FP, Oliva MA, Mielke MS, Almeida AAF, Aquino LA. Osmotic adjustment, proline accumulation and cell membrane stability in leaves of cocos nucifera submitted to drought stress. Sci Hortic. 2010; 126(3): 379–384. https://doi.org/10.1016/j.scienta.2010.07.036

2. Sapeta H, Costa JM, Lourenco T, Maroco J, Linde PVD, Oliveira MM. Drought stress response in jatropha curcas: growth and physiology. Environ Exp Bot. 2013; 85: 76–84. https://doi.org/10.1016/j.envexpbot.2012.08.012

3. Tominaga J, Inafuku S, Coetzee T, Kawamitsu Y. Diurnal regulation of photosynthesis in jatropha curcas under drought during summer in a semi-arid region. Biomass Bioenerg. 2014; 67: 279–287. https://doi.org/10.1016/j.biombioe.2014.05.010

4. Wang JM, Yang Y, Liu XH, Huang J, Wang Q, Gu JH, et al. Transcriptome profiling of the cold response and signaling pathways in Lilium lancifolium. BMC Genomics. 2014; 15(1): 203. doi: 10.1186/1471-2164-15-203 24636716

5. Zhu ZJ, Wei GQ, Li J, Qian QQ, Yu JQ. Silicon alleviates salt stress and increases antioxidant enzymes activity in leaves of salt-stressed cucumber (cucumis sativus L.). Plant Sci. 2004; 167(3): 527–533. https://doi.org/10.1016/j.plantsci.2004.04.020

6. Roh MS. Effect of high temperature on bud blast in asiatic hybrid lily. Acta Hortic. 1990; 266: 141–146. https://doi.org/10.17660/actahortic.1990.266.17

7. Klerk d GJM. A cold treatment promotes both sprouting and sink strength of lily bulblets. Propag Ornam Plants. 2009; 9(2): 102–106. https://doi.org/10.1016/j.postharvbio.2009.01.006

8. Prisa D, Burchi G, van Doorn WG. Effects of low temperature storage and sucrose pulsing on the vase life of Lilium cv. Brindisi inflorescences. Postharvest Biol Technol. 2013; 79: 39–46. https://doi.org/10.1016/j.postharvbio.2012.12.018

9. Yang TW, Zhang LJ, Zhang TG, Zhang H, Xu SJ, An LZ. Transcriptional regulation network of cold-responsive genes in higher plants. Plant Sci. 2005;169(6): 987–995. https://doi.org/10.1016/j.plantsci.2005.07.005

10. Janská A, Maršík P, Zelenková S, Ovesná J. Cold stress and acclimation–what is important for metabolic adjustment? Plant Biol. 2010; 12(3): 395–405. doi: 10.1111/j.1438-8677.2009.00299.x 20522175

11. Barrero-Gil J, Huertas R, Rambla JL, Granell A, Salinas J. Tomato plants increase their tolerance to low temperature in a chilling acclimation process entailing comprehensive transcriptional and metabolic adjustments. Plant Cell Environ. 2016; 39(10): 2303–2318. doi: 10.1111/pce.12799 27411783

12. Thomashow MF. Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol. 1999; 50: 571–599. doi: 10.1146/annurev.arplant.50.1.571 15012220

13. Nievola CC, Carvalho CP, Carvalho V, Rodrigues E. Rapid responses of plants to temperature changes. Temperature. 2017; 8940: 1–35. https://doi.org/10.1080/23328940.2017.1377812

14. Shi YT, Ding YL, Yang SH. Cold signal transduction and its interplay with phytohormones during cold acclimation. Plant Cell Physiol. 2014; 56(1): 7–15. doi: 10.1093/pcp/pcu115 25189343

15. Nie HT, Jiang LW, Huo ZM, Liu L, Yang F, Yan X. Transcriptomic responses to low temperature stress in the manila clam, Ruditapes philippinarum. Fish Shellfish Immunol. 2016; 55: 358–366. doi: 10.1016/j.fsi.2016.06.008 27288255

16. Yamaguchi-Shinozaki K, Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol. 2006; 57:781–803. doi: 10.1146/annurev.arplant.57.032905.105444 16669782

17. Joanna TD, Anna B, Jan F, Piotr Z, Emilia J, Marlena R, et al. Global analysis of gene expression in maize leaves treated with low temperature: i. moderate chilling (14°C). Plant Sci. 2019; 177(6): 648–658. https://doi.org/10.1016/j.plantsci.2009.09.001

18. Shin KS, Chakrabarty D, Paek KY. Sprouting rate, change of carbohydrate contents and related enzymes during cold treatment of lily bulblets regenerated in vitro. Sci Hortic. 2002; 96(1–4): 195–204. https://doi.org/10.1016/s0304-4238(02)00087-0

19. Ranwala AP, Miller WB. Preventive mechanisms of gibberellin4+7 and light on low-temperature-induc- -ed leaf senescence in Lilium cv. Stargazer. Postharvest Biol Tec. 2000; 19(1): 85–92. https://doi.org/10.1016/S0925-5214(00)00072-7

20. Weiss J, Egeacortines M. Transcriptomic analysis of cold response in tomato fruits identifies dehydrin as a marker of cold stress. J Appl Genet. 2009; 50(4): 311–319. doi: 10.1007/BF03195689 19875881

21. Kim SI, Tai TH. Evaluation of seedling cold tolerance in rice cultivars: a comparison of visual ratings and quantitative indicators of physiological changes. Euphytica. 2011; 178: 437–447. https://doi.org/10.1007/s10681-010-0343-4

22. Berghage RD, Flore JA, Heins RD, Erwin JE. The relationship between day and night temperature influences photosynthesis but not light compensation point or flower longevity of easter lily, lilium longiflorum thunb. Acta Horticulturae. 1990; (272): 91–96. https://doi.org/10.17660/ActaHortic.1990.272.12

23. Guidi L, Landi M, Lo Piccolo E. Chlorophyll fluorescence, photoinhibition and abiotic stress: does it make any difference the fact to be a C3 or C4 species? Front Plant Sci. 2019; 10: 174. doi: 10.3389/fpls.2019.00174 30838014

24. Sorrentino G, Cerio L, Alvino A. Effect of shading and air temperature on leaf photosynthesis, fluorescence and growth in lily plants. Sci Hortic. 1997; 69(3–4): 259–273. https://doi.org/10.1016/s0304-4238(97)00016-2

25. Kalisz A, Jezdinsky A, Pokluda R, SeKara A, Grabowska A, Gil J. Impacts of chilling on photosynthesis and chlorophyll pigment content in juvenile basil cultivars. Hortic Environ Biotechnol. 2016; 57(4): 330–339. https://doi.org/10.1007/s13580-016-0095-8

26. Devacht S, Lootens P, Baert J, Waes JV, Bockstaele EV, Roldán-Ruiz I. Evaluation of cold stress of young industrial chicory (cichorium intybus L.) plants by chlorophyllafluorescence imaging. i. light induction curve. Photosynthetica. 2011; 49(2): 161–171. https://doi.org/10.1007/s11099-011-0025-z

27. Lootens P, Van Waes J, Carlier L. Effect of a short photoinhibition stress on photosynthesis, chlorophyll a fluorescence, and pigment contents of different maize cultivars. Can a rapid and objective stress indicator be found? Photosynthetica. 2004; 42(2): 187–192. https://doi.org/10.1023/b:phot.0000040589.09614.a0

28. Petrić M, Jevremović S, Trifunović M, Tadić V, Milošević S, Dragićević M, et al. The effect of low temperature and GA3, treatments on dormancy breaking and activity of antioxidant enzymes in Fritillaria meleagris, bulblets cultured in vitro. Acta Physiol Plant. 2013; 35(11): 3223–3236. https://doi.org/10.1007/s11738-013-1357-z

29. Knight MR, Knight H. Low-temperature perception leading to gene expression and cold tolerance in higher plants. New Phytol. 2012; 195: 737–51. doi: 10.1111/j.1469-8137.2012.04239.x 22816520

30. Li NN, Chen L, Li XH, Li Q, Zhang WB, Takechi K, et al. Overexpression of UDP-glucose dehydrogenase from Larix gmelinii enhances growth and cold tolerance in transgenic Arabidopsis thaliana. Biol Plantarum. 2017; 61 (1): 95–105. https://doi.org/10.1007/s10535-016-0657-8

31. 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

32. Mhamdi A, Han Y, Noctor G. Glutathione-dependent phytohormone responses: teasing apart signaling and antioxidant functions. Plant Signal Behav. 2013; 8(5): e24181. doi: 10.4161/psb.24181 23470721

33. Eremina M, Rozhon W, Poppenberger B. Hormonal control of cold stress responses in plants. Cell Mol Life Sci. 2016; 73: 797–810. doi: 10.1007/s00018-015-2089-6 26598281

34. Puyaubert J, Baudouin E. New clues for a cold case: nitric oxide response to low temperature. Plant Cell Environ. 2014; 37: 2623–30. doi: 10.1111/pce.12329 24720833

35. Zhao BT, Zhang J, Guo X, Wang JL. Microwave-assisted extraction, chemical characterization of polysaccharides from Lilium davidii var. unicolor Salisb and its antioxidant activities evaluation. Food Hydrocolloid. 2013; 31(2): 346–356. https://doi.org/10.1016/j.foodhyd.2012.11.021

36. Zhao LH, Liu HM, Cai GZ, Xia MZ. Assessment of the genetic diversity and genetic relationships of Lilium in China using ISSR markers. Biochem Syst Ecol. 2014; 55: 184–189. https://doi.org/10.1016/j.bse.2014.03.024

37. Hu ZH, Tang B, Wu Q, Zheng J, Leng PS, Zhang KZ. Transcriptome sequencing analysis reveals a difference in monoterpene biosynthesis between scented Lilium ‘Siberia’and unscented Lilium ‘Novano’. Front Plant Sci. 2017; 8: 1351. doi: 10.3389/fpls.2017.01351 28824685

38. Xu LF, Ma FW, Liang D. Plant regeneration from in vitro cultured leaves of Lanzhou lily (Lilium davidii var. unicolor). Sci Hortic. 2009; 119(4): 458–461. https://doi.org/10.1016/j.scienta.2008.08.026

39. Toker C. Preliminary screening and selection for cold tolerance in annual wild Cicer species. Genet Resour Crop Ev. 2005; 52: 1–5. https://doi.org/10.1007/s10722-005-1743-5

40. Chakrabarty D, Verma AK, Datta SK. Oxidative stress and antioxidant activity as the basis of senescence in Hemerocallis (day lily) flowers. J Hortic Fores. 2009; 1(7): 113–119. https://doi.org/101016/s0168-9452(01)00462-9

41. Villacorta-Martin C, de Cáceres González FFN, de Haan J, Huijben K, Passarinho P, Hamo MLB, et al. Whole transcriptome profiling of the vernalization process in Lilium longiflorum (cultivar White Heaven) bulbs. BMC Genomics. 2015; 16(1): 550. doi: 10.1186/s12864-015-1675-1 26216467

42. Li WQ, Liu XH, Lu YM. Transcriptome comparison reveals key candidate genes in response to vernalization of oriental lily. BMC Genomics. 2016; 17(1): 664. doi: 10.1186/s12864-016-2955-0 27549794

43. Wang W, Su XX, Tian ZP, Liu Y, Zhou YW, He M. Transcriptome profiling provides insights into dormancy release during cold storage of Lilium pumilum. BMC Genomics. 2018; 19(S2): 196. https://doi.org/10.1186/s12864-018-4536-x 29703130

44. Yong YB, Li WQ, Wang JM, Zhang Y, Lu YM. Identification of gene co-expression networks involved in cold resistance of Lilium lancifolium. Biol Plantarum. 2018; 62(2): 287–298. https://doi.org/10.1007/s10535-017-0767-y

45. Rees T, Dixon WL, Pollock CJ, Franks F. Low temperature sweetening of higher plants. In: Friend J., Rhodes M.J.C. (Eds.), Recent Advances in the Biochemistry of Fruits and Vegetables. Academic Press, New York, 1981; pp. 41–61.

46. Liu XH, Wang Q, Gu JH, Lü Yingmin. Vernalization of oriental hybrid lily ‘sorbonne’: changes in physiology metabolic activity and molecular mechanism. Mol Biol Rep. 2014; 41(10): 6619–6634. doi: 10.1007/s11033-014-3545-3 24990697

47. Langens-Gerrits MM, Miller WB, Croes AF, De Klerk GJ. Effect of low temperature on dormancy breaking and growth after planting in lily bulblets regenerated in vitro. Plant Growth Regul. 2003; 40(3): 267–275. https://doi.org/10.1023/a:1025018728178

48. Xue J, Bao YY, Li B, Cheng YB, Peng ZY. Transcriptome analysis of the brown planthopper Nilaparvata lugens. Plos One. 2010; 5(12): e14233. doi: 10.1371/journal.pone.0014233 21151909

49. Huang LY, Zhang F, Wang WS, Zhou YL, Fu BY, Li ZK. Comparative transcriptome sequencing of tolerant rice introgression line and its parents in response to drought stress. BMC Genomics. 2014; 15(1): 1026. doi: 10.1186/1471-2164-15-1026 25428615

50. Xie ZY, Zhou ZL, Li HM, Yu JJ, Jiang JJ, Tang ZH, et al. High throughput sequencing identifies chilling responsive genes in sweetpotato (Ipomoea batatas Lam.) during storage. Genomics. 2018; S0888754318303008. doi: 10.1016/j.ygeno.2018.05.014 29792923

51. He XF, Shenkute AG, Wang WH, Xu SF. Characterization of conserved and novel microRNAs in Lilium lancifolium Thunb. by high-throughput sequencing. Sci Rep. 2018; 8(1): 2880. doi: 10.1038/s41598-018-21193-4 29440670

52. Pérez-Bueno ML, Pineda M, Díaz-Casado E, Barón M. Spatial and temporal dynamics of primary and secondary metabolism in Phaseolus vulgaris challenged by Pseudomonas syringae. Physiol Plant. 2015; 153(1): 161–74. doi: 10.1111/ppl.12237 24871330

53. Bates L, Waldren RP, Teare ID. Rapid determination of free proline for water-stress studies. Plant Soil. 1973; 39: 205–207. https://doi.org/10.1007/BF00018060

54. Pan TH, Ding JJ, Qin GG, Wang YL, Xi LJ, Yang JW, et al. Interaction of supplementary light and CO2 enrichment improves growth, photosynthesis, yield, and quality of tomato in autumn through spring greenhouse production. HortSci. 2019; 54(2): 246–252. https://doi.org/10.21273/HORTSCI13709-18

55. Giannopolitis CN, Ries SK. Superoxide dismutases I. Occurrence in higher plants. Plant Physiol. 1977; 59: 309–14. doi: 10.1104/pp.59.2.309 16659839

56. Yang QZ, Rao JP, Yi SC, Meng K, Wu JF, Hou YL. Antioxidant enzyme activity and chilling injury during low-temperature storage of Kiwifruit cv. Hongyang exposed to gradual postharvest cooling. Hort Environ Biotechnol. 2012; 53(6): 505–512. https://doi.org/10.1007/s13580-012-0101-8.

57. Liu T, Hu XH, Zhang J, Zhang JH, Du QJ, Li JM. H2O2 mediates ALA-induced glutathione and ascorbate accumulation in the perception and resistance to oxidative stress in Solanum lycopersicum at low temperatures. BMC Plant Biol. 2018; 18(1): 34. doi: 10.1186/s12870-018-1254-0 29448924

58. Meng L, Feldman L. A rapid trizol-based two-step method for dna-free rna extraction from arabidopsis siliques and dry seeds. Biotech J. 2010; 5(2): 183–186. doi: 10.1002/biot.200900211 20108272

59. Li H, Durbin R. Fast and accurate short read alignment with Burrows-Wheeler transform. Bioinforma tics. 2009; 25 (14): 1754–1760. doi: 10.1093/bioinformatics/btp324 19451168

60. Schmittgen TD, Livak KJ. Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc. 2008; 3 (6): 1101e1108. doi: 10.1038/nprot.2008.73 18546601

61. Rui HJ, Cao SF, Shang HT, Jin P, Wang KT, Zheng YH. Effects of heat treatment on internal browning and membrane fatty acid in loquat fruit in response to chilling stress. J Sci Food Agric. 2010; 90: 1557–1561. doi: 10.1002/jsfa.3993 20549812

62. Yang J, Kong QS, Xiang CP. Effects of low night temperature on pigments, chlafluorescence and energy allocation in two bitter gourd (Momordica charantia L.) genotypes. Acta Physiol Plant. 2009; 31(2): 285–293. https://doi.org/10.1007/s11738-008-0231-x.

63. Miller WB, Langhans RW. Low temperature alters carbohydrate metabolism in Easter lily bulbs. Hortsci. 1990; 25(4): 463–465. https://doi.org/10.1007/BF00027226.

64. Ashraf M, Foolad MR. Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot. 2007; 59: 206–216. https://doi.org/10.1016/j.envexpbot.2005.12.006.

65. Moellering ER, Muthan B, Benning C. Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science. 2010; 330: 226–228. doi: 10.1126/science.1191803 20798281

Physiological and transcriptomic responses of Lanzhou Lily (Lilium davidii, var. unicolor) to cold stress

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