DNA methylation-mediated modulation of rapid desiccation tolerance acquisition and dehydration stress memory in the resurrection plant Boea hygrometrica


Autoři: Run-Ze Sun aff001;  Jie Liu aff002;  Yuan-Yuan Wang aff001;  Xin Deng aff001
Působiště autorů: Key Laboratory of Plant Resources, Institute of Botany, Chinese Academy of Sciences, Beijing, China aff001;  Facility Horticulture Laboratory of Universities in Shandong, Weifang University of Science and Technology, Shouguang, China aff002;  College of Life Sciences, University of Chinese Academy of Sciences, Beijing, China aff003
Vyšlo v časopise: DNA methylation-mediated modulation of rapid desiccation tolerance acquisition and dehydration stress memory in the resurrection plant Boea hygrometrica. PLoS Genet 17(4): e1009549. doi:10.1371/journal.pgen.1009549
Kategorie: Research Article
doi: https://doi.org/10.1371/journal.pgen.1009549

Souhrn

Pre-exposure of plants to various abiotic conditions confers improved tolerance to subsequent stress. Mild drought acclimation induces acquired rapid desiccation tolerance (RDT) in the resurrection plant Boea hygrometrica, but the mechanisms underlying the priming and memory processes remain unclear. In this study, we demonstrated that drought acclimation-induced RDT can be maintained for at least four weeks but was completely erased after 18 weeks based on a combination of the phenotypic and physiological parameters. Global transcriptome analysis identified several RDT-specific rapid dehydration-responsive genes related to cytokinin and phospholipid biosynthesis, nitrogen and carbon metabolism, and epidermal morphogenesis, most of which were pre-induced by drought acclimation. Comparison of whole-genome DNA methylation revealed dehydration stress-responsive hypomethylation in the CG, CHG, and CHH contexts and acclimation-induced hypermethylation in the CHH context of the B. hygrometrica genome, consistent with the transcriptional changes in methylation pathway genes. As expected, the global promoter and gene body methylation levels were negatively correlated with gene expression levels in both acclimated and dehydrated plants but showed no association with transcriptional divergence during the procedure. Nevertheless, the promoter methylation variations in the CG and CHG contexts were significantly associated with the differential expression of genes required for fundamental genetic processes of DNA conformation, RNA splicing, translation, and post-translational protein modification during acclimation, growth, and rapid dehydration stress response. It was also associated with the dehydration stress-induced upregulation of memory genes, including pre-mRNA-splicing factor 38A, vacuolar amino acid transporter 1-like, and UDP-sugar pyrophosphorylase, which may contribute directly or indirectly to the improvement of dehydration tolerance in B. hygrometrica plants. Altogether, our findings demonstrate the potential implications of DNA methylation in dehydration stress memory and, therefore, provide a molecular basis for enhanced dehydration tolerance in plants induced by drought acclimation.

Klíčová slova:

Dehydration (medicine) – DNA methylation – DNA transcription – Flowering plants – Gene expression – Leaves – Plant physiology – Transcriptome analysis


Zdroje

1. Lobell DB, Gourdji SM. The influence of climate change on global crop productivity. Plant Physiol. 2012; 160(4): 1686–1697. doi: 10.1104/pp.112.208298 23054565

2. Hasanuzzaman M, Nahar K, Gill SS, Fujita M. Drought stress responses in plants, oxidative stress, and antioxidant defense. In: Tuteja N, Gill SS, editors. Climate change and plant abiotic stress tolerance. Weinheim: John Wiley & Sons; 2013. pp. 209–250.

3. Kumar S, Sachdeva S, Bhat KV, Vats S. Plant responses to drought stress: physiological, biochemical and molecular basis. In: Vats S, editor. Biotic and abiotic stress tolerance in plants. Singapore: Springer; 2018. pp. 1–25.

4. Fang Y, Xiong L. General mechanisms of drought response and their application in drought resistance improvement in plants. Cell Mol Life Sci. 2015; 72(4): 673–689. doi: 10.1007/s00018-014-1767-0 25336153

5. Proctor MC, Pence VC. Vegetative tissues: bryophytes, vascular resurrection plants and vegetative propagules. In: Black M, Pritchard H, editors. Desiccation and plant survival. Wallingford: CABI; 2002. pp. 207–237.

6. Challabathula D, Bartels D. Desiccation tolerance in resurrection plants: new insights from transcriptome, proteome and metabolome analysis. Front Plant Sci. 2013; 4: 482. doi: 10.3389/fpls.2013.00482 24348488

7. Gaff DF, Oliver M. The evolution of desiccation tolerance in angiosperm plants: a rare yet common phenomenon. Funct Plant Biol. 2013; 40(4): 315–328. doi: 10.1071/FP12321 32481110

8. Chen P, Jung NU, Giarola V, Bartels D. The dynamic responses of cell walls in resurrection plants during dehydration and rehydration. Front Plant Sci. 2020; 10: 1698. doi: 10.3389/fpls.2019.01698 32038677

9. Oliver MJ, Farrant JM, Hilhorst HWM, Mundree S, Williams B, Bewley JD. Desiccation tolerance: avoiding cellular damage during drying and rehydration. Annu Rev Plant Biol. 2020; 71(1): 435–460. doi: 10.1146/annurev-arplant-071219-105542 32040342

10. Gechev TS, Dinakar C, Benina M, Toneva V, Bartels D. Molecular mechanisms of desiccation tolerance in resurrection plants. Cell Mol Life Sci. 2012; 69(19): 3175–3186. doi: 10.1007/s00018-012-1088-0 22833170

11. Li X, Liu F. Drought stress memory and drought stress tolerance in plants: biochemical and molecular basis. In: Hossain MA, Wani SH, Bhattacharjee S, Burritt DJ, Tran L-SP, editors. Drought stress tolerance in plants, Vol 1. Cham: Springer; 2016. pp. 17–44.

12. Crisp PA, Ganguly D, Eichten SR, Borevitz JO, Pogson BJ. Reconsidering plant memory: Intersections between stress recovery, RNA turnover, and epigenetics. Sci Adv. 2016; 2(2): e1501340. doi: 10.1126/sciadv.1501340 26989783

13. Chang YN, Zhu C, Jiang J, Zhang H, Zhu JK, Duan CG. Epigenetic regulation in plant abiotic stress responses. J Integr Plant Biol. 2020; 62(5): 563–580. doi: 10.1111/jipb.12901 31872527

14. Bruce TJA, Matthes MC, Napier JA, Pickett JA. Stressful “memories” of plants: Evidence and possible mechanisms. Plant Sci. 2007; 173(6): 603–608.

15. Kinoshita T, Seki M. Epigenetic memory for stress response and adaptation in plants. Plant Cell Physiol. 2014; 55(11): 1859–1863. doi: 10.1093/pcp/pcu125 25298421

16. Lämke J, Bäurle I. Epigenetic and chromatin-based mechanisms in environmental stress adaptation and stress memory in plants. Genome Biol. 2017; 18(1): 124. doi: 10.1186/s13059-017-1263-6 28655328

17. Grossniklaus U, Kelly WG, Ferguson-Smith AC, Pembrey M, Lindquist S. Transgenerational epigenetic inheritance: how important is it? Nat Rev Genet. 2013; 14(3): 228–235. doi: 10.1038/nrg3435 23416892

18. Chinnusamy V, Zhu JK. Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol. 2009; 12(2): 133–139. doi: 10.1016/j.pbi.2008.12.006 19179104

19. Ding Y, Fromm M, Avramova Z. Multiple exposures to drought ’train’ transcriptional responses in Arabidopsis. Nat Commun. 2012; 3(1): 740. doi: 10.1038/ncomms1732 22415831

20. Virlouvet L, Avenson TJ, Du Q, Zhang C, Liu N, Fromm M, et al. Dehydration stress memory: gene networks linked to physiological responses during repeated stresses of Zea mays. Front Plant Sci. 2018; 9: 1058. doi: 10.3389/fpls.2018.01058 30087686

21. Ding Y, Liu N, Virlouvet L, Riethoven J-J, Fromm M, Avramova Z. Four distinct types of dehydration stress memory genes in Arabidopsis thaliana. BMC Plant Biol. 2013; 13(1): 229. doi: 10.1186/1471-2229-13-229 24377444

22. Ding Y, Virlouvet L, Liu N, Riethoven J-J, Fromm M, Avramova Z. Dehydration stress memory genes of Zea mays; comparison with Arabidopsis thaliana. BMC Plant Biol. 2014; 14(1): 141.

23. de Freitas Guedes FA, Nobres P, Ferreira DCR, Menezes-Silva PE, Ribeiro-Alves M, Correa RL, et al. Transcriptional memory contributes to drought tolerance in coffee (Coffea canephora) plants. Environ Exp Bot. 2018; 147: 220–233.

24. Liu N, Ding Y, Fromm M, Avramova Z. Different gene-specific mechanisms determine the ‘revised-response’ memory transcription patterns of a subset of A. thaliana dehydration stress responding genes. Nucleic Acids Res. 2014; 42(9): 5556–5566. doi: 10.1093/nar/gku220 24744238

25. Li P, Yang H, Wang L, Liu H, Huo H, Zhang C, et al. Physiological and transcriptome analyses reveal short-term responses and formation of memory under drought stress in rice. Front Genet. 2019; 10: 55. doi: 10.3389/fgene.2019.00055 30800142

26. Forestan C, Farinati S, Zambelli F, Pavesi G, Rossi V, Varotto S. Epigenetic signatures of stress adaptation and flowering regulation in response to extended drought and recovery in Zea mays. Plant Cell Environ. 2020; 43(1): 55–75. doi: 10.1111/pce.13660 31677283

27. Mitra J, Xu G, Wang B, Li M, Deng X. Understanding desiccation tolerance using the resurrection plant Boea hygrometrica as a model system. Front Plant Sci. 2013; 4: 446. doi: 10.3389/fpls.2013.00446 24273545

28. Zhu Y, Wang B, Phillips J, Zhang Z-N, Du H, Xu T, et al. Global transcriptome analysis reveals acclimation-primed processes involved in the acquisition of desiccation tolerance in Boea hygrometrica. Plant Cell Physiol. 2015; 56(7): 1429–1441. doi: 10.1093/pcp/pcv059 25907569

29. Sun R-Z, Lin C-T, Zhang X-F, Duan L-X, Qi X-Q, Gong Y-H, et al. Acclimation-induced metabolic reprogramming contributes to rapid desiccation tolerance acquisition in Boea hygrometrica. Environ Exp Bot. 2018; 148: 70–84.

30. Xiao L, Yang G, Zhang L, Yang X, Zhao S, Ji Z, et al. The resurrection genome of Boea hygrometrica: A blueprint for survival of dehydration. Proc Natl Acad Sci USA. 2015; 112(18): 5833–5837. doi: 10.1073/pnas.1505811112 25902549

31. Sun R-Z, Zuo E-H, Qi J-F, Liu Y, Lin C-T, Deng X. A role of age-dependent DNA methylation reprogramming in regulating the regeneration capacity of Boea hygrometrica leaves. Funct Integr Genomic. 2020; 20(1): 133–149. doi: 10.1007/s10142-019-00701-3 31414312

32. Salehi-Lisar SY, Bakhshayeshan-Agdam H. Drought stress in plants: causes, consequences, and tolerance. In: Hossain MA, Wani SH, Bhattacharjee S, Burritt DJ, Tran L-SP, editors. Drought stress tolerance in plants, Vol 1. Cham: Springer; 2016. pp. 1–16.

33. Juenger TE. Natural variation and genetic constraints on drought tolerance. Curr Opin Plant Biol. 2013; 16(3): 274–281. doi: 10.1016/j.pbi.2013.02.001 23462639

34. Chen D, Wang S, Cao B, Cao D, Leng G, Li H, et al. Genotypic variation in growth and physiological response to drought stress and re-watering reveals the critical role of recovery in drought adaptation in maize seedlings. Front Plant Sci. 2016; 6: 1241. doi: 10.3389/fpls.2015.01241 26793218

35. Luo LJ. Breeding for water-saving and drought-resistance rice (WDR) in China. J Exp Bot. 2010; 61(13): 3509–3517. doi: 10.1093/jxb/erq185 20603281

36. Challabathula D, Puthur JT, Bartels D. Surviving metabolic arrest: photosynthesis during desiccation and rehydration in resurrection plants. Ann N Y Acad Sci. 2016; 1365(1): 89–99. doi: 10.1111/nyas.12884 26376004

37. Liu J, Moyankova D, Djilianov D, Deng X. Common and specific mechanisms of desiccation tolerance in two gesneriaceae resurrection plants. Multiomics evidences. Front Plant Sci. 2019; 10: 1067. doi: 10.3389/fpls.2019.01067 31552070

38. Mihailova G, Kocheva K, Goltsev V, Kalaji HM, Georgieva K. Application of a diffusion model to measure ion leakage of resurrection plant leaves undergoing desiccation. Plant Physiol Biochem. 2018; 125: 185–192. doi: 10.1016/j.plaphy.2018.02.008 29459287

39. Oliver MJ, Tuba Z, Mishler BD. The evolution of vegetative desiccation tolerance in land plants. Plant Ecol. 2000; 151(1): 85–100.

40. Harb A, Krishnan A, Ambavaram MMR, Pereira A. Molecular and physiological analysis of drought stress in Arabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol. 2010; 154(3): 1254–1271. doi: 10.1104/pp.110.161752 20807999

41. Walter J, Beierkuhnlein C, Jentsch A, Kreyling J. Ecological stress memory and cross stress tolerance in plants in the face of climate extremes. Environ Exp Bot. 2013; 94: 3–8.

42. Sakakibara H, Takei K, Hirose N. Interactions between nitrogen and cytokinin in the regulation of metabolism and development. Trends Plant Sci. 2006; 11(9): 440–448. doi: 10.1016/j.tplants.2006.07.004 16899391

43. Geβler A, Kopriva S, Rennenberg H. Regulation of nitrate uptake at the whole-tree level: interaction between nitrogen compounds, cytokinins and carbon metabolism. Tree Physiol. 2004; 24(12): 1313–1321. doi: 10.1093/treephys/24.12.1313 15465694

44. Gan Y, Liu C, Yu H, Broun P. Integration of cytokinin and gibberellin signalling by Arabidopsis transcription factors GIS, ZFP8 and GIS2 in the regulation of epidermal cell fate. Development. 2007; 134(11): 2073–2081. doi: 10.1242/dev.005017 17507408

45. Laplaze L, Benková E, Casimiro I, Maes L, Vanneste S, Swarup R, et al. Cytokinins act directly on lateral root founder cells to inhibit root initiation. Plant Cell. 2007; 19(12): 3889–3990. doi: 10.1105/tpc.107.055863 18065686

46. Zhang X, Xu Y, Huang B. Lipidomic reprogramming associated with drought stress priming-enhanced heat tolerance in tall fescue (Festuca arundinacea). Plant Cell Environ. 2019; 42(3): 947–958. doi: 10.1111/pce.13405 29989186

47. He X-J, Chen T, Zhu J-K. Regulation and function of DNA methylation in plants and animals. Cell Res. 2011; 21(3): 442–465. doi: 10.1038/cr.2011.23 21321601

48. Zhang H, Lang Z, Zhu J-K. Dynamics and function of DNA methylation in plants. Nat Rev Mol Cell Biol. 2018; 19(8): 489–506. doi: 10.1038/s41580-018-0016-z 29784956

49. Xu J, Zhou S, Gong X, Song Y, van Nocker S, Ma F, et al. Single-base methylome analysis reveals dynamic epigenomic differences associated with water deficit in apple. Plant Biotechnol J. 2018; 16(2): 672–687. doi: 10.1111/pbi.12820 28796917

50. Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, et al. Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature. 2008; 452(7184): 215–219. doi: 10.1038/nature06745 18278030

51. Li X, Zhu J, Hu F, Ge S, Ye M, Xiang H, et al. Single-base resolution maps of cultivated and wild rice methylomes and regulatory roles of DNA methylation in plant gene expression. BMC Genomics. 2012; 13: 300. doi: 10.1186/1471-2164-13-300 22747568

52. Song Q-X, Lu X, Li Q-T, Chen H, Hu X-Y, Ma B, et al. Genome-wide analysis of DNA methylation in soybean. Mol Plant. 2013; 6(6): 1961–1974. doi: 10.1093/mp/sst123 23966636

53. Gardiner L-J, Quinton-Tulloch M, Olohan L, Price J, Hall N, Hall A. A genome-wide survey of DNA methylation in hexaploid wheat. Genome Biol. 2015; 16(1): 273. doi: 10.1186/s13059-015-0838-3 26653535

54. Wang H, Beyene G, Zhai J, Feng S, Fahlgren N, Taylor NJ, et al. CG gene body DNA methylation changes and evolution of duplicated genes in cassava. Proc Natl Acad Sci USA. 2015; 112(44): 13729–13734. doi: 10.1073/pnas.1519067112 26483493

55. West PT, Li Q, Ji L, Eichten SR, Song J, Vaughn MW, et al. Genomic distribution of H3K9me2 and DNA methylation in a maize genome. PLoS One. 2014; 9(8): e105267. doi: 10.1371/journal.pone.0105267 25122127

56. Ausin I, Feng S, Yu C, Liu W, Kuo HY, Jacobsen EL, et al. DNA methylome of the 20-gigabase Norway spruce genome. Proc Natl Acad Sci USA. 2016; 113(50): E8106–E8113. doi: 10.1073/pnas.1618019113 27911846

57. Niederhuth CE, Bewick AJ, Ji L, Alabady MS, Kim KD, Li Q, et al. Widespread natural variation of DNA methylation within angiosperms. Genome Biol. 2016; 17(1): 194. doi: 10.1186/s13059-016-1059-0 27671052

58. Takuno S, Ran J-H, Gaut BS. Evolutionary patterns of genic DNA methylation vary across land plants. Nat Plants. 2016; 2(2): 15222. doi: 10.1038/nplants.2015.222 27249194

59. Wang W-S, Pan Y-J, Zhao X-Q, Dwivedi D, Zhu L-H, Ali J, et al. Drought-induced site-specific DNA methylation and its association with drought tolerance in rice (Oryza sativa L.). J Exp Bot. 2010; 62(6): 1951–1960. doi: 10.1093/jxb/erq391 21193578

60. Wang M, Qin L, Xie C, Li W, Yuan J, Kong L, et al. Induced and constitutive DNA Methylation in a salinity-tolerant wheat introgression line. Plant Cell Physiol. 2014; 55(7): 1354–1365. doi: 10.1093/pcp/pcu059 24793752

61. Fan HH, Wei J, Li TC, Li ZP, Guo N, Cai YP, et al. DNA methylation alterations of upland cotton (Gossypium hirsutum) in response to cold stress. Acta Physiol Plant. 2013; 35(8): 2445–2453.

62. Aina R, Sgorbati S, Santagostino A, Labra M, Ghiani A, Citterio S. Specific hypomethylation of DNA is induced by heavy metals in white clover and industrial hemp. Physiol Plant. 2004; 121(3): 472–480.

63. Zhang H, Zhu J-K. RNA-directed DNA methylation. Curr Opin Plant Biol. 2011; 14(2): 142–147. doi: 10.1016/j.pbi.2011.02.003 21420348

64. Matzke MA, Mosher RA. RNA-directed DNA methylation: an epigenetic pathway of increasing complexity. Nat Rev Genet. 2014; 15(6): 394–408. doi: 10.1038/nrg3683 24805120

65. Zhong S, Fei Z, Chen Y-R, Zheng Y, Huang M, Vrebalov J, et al. Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol. 2013; 31: 154–159. doi: 10.1038/nbt.2462 23354102

66. Stelpflug SC, Eichten SR, Hermanson PJ, Springer NM, Kaeppler SM. Consistent and heritable alterations of DNA methylation are induced by tissue culture in maize. Genetics. 2014; 198(1): 209–218. doi: 10.1534/genetics.114.165480 25023398

67. Yaish MW, Al-Lawati A, Al-Harrasi I, Patankar HV. Genome-wide DNA Methylation analysis in response to salinity in the model plant caliph medic (Medicago truncatula). BMC Genomics. 2018; 19(1): 78. doi: 10.1186/s12864-018-4484-5 29361906

68. Zilberman D, Coleman-Derr D, Ballinger T, Henikoff S. Histone H2A.Z and DNA methylation are mutually antagonistic chromatin marks. Nature. 2008; 456(7218): 125–129. doi: 10.1038/nature07324 18815594

69. Takuno S, Gaut BS. Body-methylated genes in Arabidopsis thaliana are functionally important and evolve slowly. Mol Biol Evol. 2011; 29(1): 219–227. doi: 10.1093/molbev/msr188 21813466

70. Xu W, Yang T, Dong X, Li D-Z, Liu A. Genomic DNA methylation analyses reveal the distinct profiles in castor bean seeds with persistent endosperms. Plant Physiol. 2016; 171(2): 1242–1258. doi: 10.1104/pp.16.00056 27208275

71. Ding C-J, Liang L-X, Diao S, Su X-H, Zhang B-Y. Genome-wide analysis of day/night DNA methylation differences in Populus nigra. PLoS One. 2018; 13(1): e0190299. doi: 10.1371/journal.pone.0190299 29293569

72. Watanabe S, Matsumoto M, Hakomori Y, Takagi H, Shimada H, Sakamoto A. The purine metabolite allantoin enhances abiotic stress tolerance through synergistic activation of abscisic acid metabolism. Plant Cell Environ. 2014; 37(4): 1022–1036. doi: 10.1111/pce.12218 24182190

73. Watanabe S, Nakagawa A, Izumi S, Shimada H, Sakamoto A. RNA interference-mediated suppression of xanthine dehydrogenase reveals the role of purine metabolism in drought tolerance in Arabidopsis. FEBS Lett. 2010; 584(6): 1181–1186. doi: 10.1016/j.febslet.2010.02.023 20153325

74. Fan X, Han W, Teng L, Jiang P, Zhang X, Xu D, et al. Single-base methylome profiling of the giant kelp Saccharina japonica reveals significant differences in DNA methylation to microalgae and plants. New Phytol. 2020; 225(1): 234–249. doi: 10.1111/nph.16125 31419316

75. Laloum T, Martín G, Duque P. Alternative splicing control of abiotic stress responses. Trends Plant Sci. 2018; 23(2): 140–150. doi: 10.1016/j.tplants.2017.09.019 29074233

76. Decker D, Kleczkowski LA. UDP-sugar producing pyrophosphorylases: distinct and essential enzymes with overlapping substrate specificities, providing de novo precursors for glycosylation reactions. Front Plant Sci. 2019; 9: 1822. doi: 10.3389/fpls.2018.01822 30662444

77. Kawano-Kawada M, Kakinuma Y, Sekito T. Transport of amino acids across the vacuolar membrane of yeast: its mechanism and physiological role. Biol Pharm Bull. 2018; 41(10): 1496–1501. doi: 10.1248/bpb.b18-00165 30270317

78. Lin C-T, Xu T, Xing S-L, Zhao L, Sun R-Z, Liu Y, et al. Weighted gene co-expression network analysis (WGCNA) reveals the hub role of protein ubiquitination in the acquisition of desiccation tolerance in Boea hygrometrica. Plant Cell Physiol. 2019; 60(12): 2707–2719. doi: 10.1093/pcp/pcz160 31410481

79. Boorse GC, Bosma TL, Ewers FW, Davis SD. Comparative methods of estimating freezing temperatures and freezing injury in leaves of chaparral shrubs. Int J Plant Sci. 1998; 159(3): 513–521.

80. Kim D, Langmead B, Salzberg SL. HISAT: a fast spliced aligner with low memory requirements. Nat Methods. 2015; 12(4): 357–360. doi: 10.1038/nmeth.3317 25751142

81. Trapnell C, Roberts A, Goff L, Pertea G, Kim D, Kelley DR, et al. Differential gene and transcript expression analysis of RNA-seq experiments with TopHat and Cufflinks. Nat Protoc. 2012; 7(3): 562–578. doi: 10.1038/nprot.2012.016 22383036

82. Pertea M, Pertea GM, Antonescu CM, Chang T-C, Mendell JT, Salzberg SL. StringTie enables improved reconstruction of a transcriptome from RNA-seq reads. Nat Biotechnol. 2015; 33(3): 290. doi: 10.1038/nbt.3122 25690850

83. Li B, Dewey CN. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinformatics. 2011; 12(1): 323.

84. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012; 9(4): 357. doi: 10.1038/nmeth.1923 22388286

85. Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014; 15(12): 550. doi: 10.1186/s13059-014-0550-8 25516281

86. Xi Y, Li W. BSMAP: whole genome bisulfite sequence MAPping program. BMC Bioinformatics. 2009; 10(1): 232. doi: 10.1186/1471-2105-10-232 19635165

87. Lai Y-S, Zhang X, Zhang W, Shen D, Wang H, Xia Y, et al. The association of changes in DNA methylation with temperature-dependent sex determination in cucumber. J Exp Bot. 2017; 68(11): 2899–2912. doi: 10.1093/jxb/erx144 28498935

88. Sun R, He F, Lan Y, Xing R, Liu R, Pan Q, et al. Transcriptome comparison of Cabernet Sauvignon grape berries from two regions with distinct climate. J Plant Physiol. 2015; 178: 43–54. doi: 10.1016/j.jplph.2015.01.012 25765362


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