Variations of Cytosine Methylation Patterns between Staminate and Perfect Flowers within Andromonoecious Taihangia rupestris (Rosaceae) Revealed by Methylation-Sensitive Amplification Polymorphism

Abstract

DNA methylation is an epigenetic modification that plays important roles in flower development through regulation of gene expression. Taihangia rupestris is an andromonoecious plant species, which can produce staminate and perfect flowers within the same individual. In this study, we employed methylation-sensitive amplified polymorphism (MSAP) to investigate cytosine methylation patterns in staminate and perfect flowers within the andromonoecious T. rupestris. Our data showed the cytosine methylation patterns varied in staminate and perfect flowers at early and late developmental stages. The level of cytosine methylation was slightly higher in perfect flowers than in staminate flowers, and an increase of cytosine methylation levels was found alongside developmental stages in both staminate and perfect flowers. Based on MSAP profiles, a total of 116 differentially methylated fragments (DMFs) were obtained and sequenced. Of these obtained DMFs, 42 fragments showed sequence similarity to functional genes involved in a wide range of biological processes such as flower development, signal transduction, and cell proliferation, and transcription regulation. By integrative analysis of MSAP and transcriptome data, we found transcript levels correlated with cytosine methylation patterns for majority of DMF-associated genes. This study revealed that DNA methylation could play important roles in regulation of gene expression during establishment and development of staminate and perfect flower within andromonoecious T. rupestris and would be helpful to shed light on the underlying molecular mechanisms responsible for flower formation at epigenetic scale in andromonoecious sexual system.

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References

  1. Abid G, Mingeot D, Muhovski Y, Mergeai G, Aouida M, Abdelkarim S, Aroua I, El Ayed M, M’hamdi M, Sassi K, Jebara M (2017) Analysis of DNA methylation patterns associated with drought stress response in faba bean (Vicia faba L.) using methylation-sensitive amplification polymorphism (MSAP). Environ Exp Bot 142:34–44. https://doi.org/10.1016/j.envexpbot.2017.08.004

    CAS  Article  Google Scholar 

  2. Airoldi CA, Rovere FD, Falasca G, Marino G, Kooiker M, Altamura MM, Citterio S, Kater MM (2010) The Arabidopsis BET bromodomain factor GTE4 is involved in maintenance of the mitotic cell cycle during plant development. Plant Physiol 152:1320–1334. https://doi.org/10.1104/pp.109.150631

    CAS  Article  PubMed  Google Scholar 

  3. Andres-Robin A, Reymond MC, Dupire A, Battu V, Dubrulle N, Mouille G, Lefebvre V, Pelloux J, Boudaoud A, Traas J, Scutt CP, Monéger F (2018) Evidence for the regulation of gynoecium morphogenesis by ETTIN via cell wall dynamics. Plant Physiol 178:1222–1232. https://doi.org/10.1104/pp.18.00745

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  4. Barrett SCH (2002) The evolution of plant sexual diversity. Nat Rev Genet 3:274–284. https://doi.org/10.1038/nrg776

    CAS  Article  PubMed  Google Scholar 

  5. Barrett SCH (2010) Understanding plant reproductive diversity. Philos T R Soc B 365:99–109. https://doi.org/10.1098/rstb.2009.0199

    Article  Google Scholar 

  6. Bi Z, Li X, Huang H, Hua Y (2016) Identification, functional study, and promoter analysis of HbMFT1, a homolog of MFT from rubber tree (Hevea brasiliensis). Int J Mol Sci 17:247. https://doi.org/10.3390/ijms17030247

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  7. Cheng Y, Wang J, Liu J, Zhao Y, Geng W, Zhang H (2015) Analysis of ovary DNA methylation during delayed fertilization in hazel using the methylation-sensitive amplification technique. Acta Physiol Plant 37:231. https://doi.org/10.1007/s11738-015-1984-7

    CAS  Article  Google Scholar 

  8. Chwialkowska K, Nowakowska U, Mroziewicz A, Szarejko I, Kwasniewski M (2016) Water-deficiency conditions differently modulate the methylome of roots and leaves in barley (Hordeum vulgare L.). J Exp Bot 67:1109–1121. https://doi.org/10.1093/jxb/erv552

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  9. Coen ES, Meyerowitz EM (1991) The war of the whorls: genetic interactions controlling flower development. Nature 353:31–37. https://doi.org/10.1038/353031a0

    CAS  Article  PubMed  Google Scholar 

  10. Colicchio JM, Miura F, Kelly JK, Ito T, Hileman LC (2015) DNA methylation and gene expression in Mimulus guttatus. BMC Genomics 16:507. https://doi.org/10.1186/s12864-015-1668-0

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  11. Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–161. https://doi.org/10.1038/43657

    CAS  Article  PubMed  Google Scholar 

  12. Finnegan EJ, Peacock WJ, Dennis ES (1996) Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. P Natl Acad Sci USA 93:8449–8454. https://doi.org/10.1073/pnas.93.16.8449

    CAS  Article  Google Scholar 

  13. Jang S, Lee B, Kim C, Kim S-J, Yim J, Han J-J, Lee S, Kim S-R, An G (2003) The OsFOR1 gene encodes a polygalacturonase-inhibiting protein (PGIP) that regulates floral organ number in rice. Plant Mol Biol 53:357–372. https://doi.org/10.1023/B:PLAN.0000006940.89955.f1

    CAS  Article  PubMed  Google Scholar 

  14. Janoušek B, Široký J, Vyskot B (1996) Epigenetic control of sexual phenotype in a dioecious plant, Melandrium album. Mol General Genet 250:483–490. https://doi.org/10.1007/BF02174037

    Article  Google Scholar 

  15. Ji G, Zhang J, Zhang H, Sun H, Gong G, Shi J, Tian S, Guo S, Ren Y, Shen H, Gao J, Xu Y (2016) Mutation in the gene encoding 1-aminocyclopropane-1-carboxylate synthase 4 (CitACS4) led to andromonoecy in watermelon. J Integr Plant Biol 58:762–765. https://doi.org/10.1111/jipb.12466

    CAS  Article  PubMed  Google Scholar 

  16. Khadka J, Yadav NS, Guy M, Grafi G, Golan-Goldhirsh A (2019) Epigenetic aspects of floral homeotic genes in relation to sexual dimorphism in the dioecious plant Mercurialis annua. J Exp Bot 70:6245–6259. https://doi.org/10.1093/jxb/erz379

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  17. Komivi D, Marie AM, Rong Z, Qi Z, Mei Y, Ndiaga C, Diaga D, Linhai W, Xiurong Z (2018) The contrasting response to drought and waterlogging is underpinned by divergent DNA methylation programs associated with transcript accumulation in sesame. Plant Sci 277:207–217. https://doi.org/10.1016/j.plantsci.2018.09.012

    CAS  Article  PubMed  Google Scholar 

  18. Kumar G, Rattan UK, Singh AK (2016) Chilling-mediated DNA methylation changes during dormancy and its release reveal the importance of epigenetic regulation during winter dormancy in apple (Malus x domestica Borkh). PLoS ONE 11:e0149934. https://doi.org/10.1371/journal.pone.0149934

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  19. Lai Y, Zhang X, Zhang W, Shen D, Wang H, Xia Y, Qiu Y, Song J, Wang C, Li X (2017) The association of changes in DNA methylation with temperature-dependent sex determination in cucumber. J Exp Bot 68:2899–2912. https://doi.org/10.1093/jxb/erx144

    CAS  Article  PubMed  Google Scholar 

  20. Lai Y, Shen D, Zhang W, Zhang X, Qiu Y, Wang H, Dou X, Li S, Wu Y, Song J, Ji G, Li X (2018) Temperature and photoperiod changes affect cucumber sex expression by different epigenetic regulations. BMC Plant Biol 18:268. https://doi.org/10.1186/s12870-018-1490-3

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  21. Law JA, Jacobsen SE (2010) Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11:204–220. https://doi.org/10.1038/nrg2719

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  22. Li W, Chen W, Qi X, Wang Q, Chen J (2013) Variation of cytosine methylation in response to water availability in two contrasting growth types of an amphibious plant Alternanthera philoxeroides. Biochem Syst Ecol 50:175–181. https://doi.org/10.1016/j.bse.2013.03.053

    CAS  Article  Google Scholar 

  23. Li W, Zhang L, Ding Z, Wang G, Zhang Y, Gong H, Chang T, Zhang Y (2017a) De novo sequencing and comparative transcriptome analysis of the male and hermaphroditic flowers provide insights into the regulation of flower formation in andromonoecious Taihangia rupestris. BMC Plant Biol 17:54. https://doi.org/10.1186/s12870-017-0990-x

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  24. Li W, Zhang L, Zhang Y, Wang G, Song D, Zhang Y (2017b) Selection and validation of appropriate reference genes for quantitative real-time PCR normalization in staminate and perfect flowers of andromonoecious Taihangia rupestris. Fronti Plant Sci 8:729. https://doi.org/10.3389/fpls.2017.00729

    Article  Google Scholar 

  25. Li Z, Jiang D, He Y (2018) FRIGIDA establishes a local chromosomal environment for FLOWERING LOCUS C mRNA production. Nat Plants 4:836–846. https://doi.org/10.1038/s41477-018-0250-6

    CAS  Article  PubMed  Google Scholar 

  26. Li Y, Zhao F, Yang X, Zhong S, Li F, Lin C, Wu H, Guo W, Liao F (2019) Cytosine methylation analysis of Pinus elliottii × Pinus caribaea var. hondurensis and their parental lines. J Plant Growth Regul 38:30–38. https://doi.org/10.1007/s00344-018-9804-0

    CAS  Article  Google Scholar 

  27. Lin Z, Liu M, Damaris NR, Nyong’a MT, Cao D, Ou K, Yang P (2019) Genome-wide DNA methylation profiling in the Lotus (Nelumbo nucifera) flower showing its contribution to the stamen petaloid. Plants 8:135. https://doi.org/10.3390/plants8050135

    CAS  Article  PubMed Central  Google Scholar 

  28. Liu J, Chatham L, Aryal R, Yu Q, Ming R (2018) Differential methylation and expression of HUA1 ortholog in three sex types of papaya. Plant Sci 272:99–106. https://doi.org/10.1016/j.plantsci.2018.04.001

    CAS  Article  PubMed  Google Scholar 

  29. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408. https://doi.org/10.1006/meth.2001.1262

    CAS  Article  Google Scholar 

  30. Lü S, Du X, Lu W, Chong K, Meng Z (2007) Two AGAMOUS-like MADS-box genes from Taihangia rupestris (Rosaceae) reveal independent trajectories in the evolution of class C and class D floral homeotic functions. Evol Dev 9:92–104. https://doi.org/10.1111/j.1525-142X.2006.00140.x

    Article  PubMed  Google Scholar 

  31. Lü S, Fan Y, Liu L, Liu S, Zhang W, Meng Z (2010) Ectopic expression of TrPI, a Taihangia rupestris (Rosaceae) PI ortholog, causes modifications of vegetative architecture inArabidopsis. J Plant Physiol 167:1613–1621. https://doi.org/10.1016/j.jplph.2010.06.028

    CAS  Article  PubMed  Google Scholar 

  32. Martin A, Troadec C, Boualem A, Rajab M, Fernandez R, Morin H, Pitrat M, Dogimont C, Bendahmane A (2009) A transposon-induced epigenetic change leads to sex determination in melon. Nature 461:1135–1138. https://doi.org/10.1038/nature08498

    CAS  Article  PubMed  Google Scholar 

  33. Murphy E, De Smet I (2014) Understanding the RALF family: a tale of many species. Trends Plant Sci 19:664–671. https://doi.org/10.1016/j.tplants.2014.06.005

    CAS  Article  PubMed  Google Scholar 

  34. Niederhuth CE, Bewick AJ, Ji L, Alabady MS, Kim KD, Li Q, Rohr NA, Rambani A, Burke JM, Udall JA, Egesi C, Schmutz J, Grimwood J, Jackson SA, Springer NM, Schmitz RJ (2016) Widespread natural variation of DNA methylation within angiosperms. Genome Biol 17:194. https://doi.org/10.1186/s13059-016-1059-0

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  35. Orlowska R, Bednarek PT (2020) Precise evaluation of tissue culture-induced variation during optimisation of in vitro regeneration regime in barley. Plant Mol Biol 103:33–50. https://doi.org/10.1007/s11103-020-00973-5

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  36. Park SY, Murthy HN, Chakrabarthy D, Paek KY (2009) Detection of epigenetic variation in tissue-culture-derived plants of Doritaenopsis by methylation-sensitive amplification polymorphism (MSAP) analysis. Vitro Cell Dev-PL 45:104–108. https://doi.org/10.1007/s11627-008-9166-6

    CAS  Article  Google Scholar 

  37. Reuther K, Claßen-Bockhoff R (2013) Andromonoecy and developmental plasticity in Chaerophyllum bulbosum (Apiaceae–Apioideae). Ann Bot 112:1495–1503. https://doi.org/10.1093/aob/mct073

    Article  PubMed  PubMed Central  Google Scholar 

  38. Rodríguez Lorenzo JL, Hobza R, Vyskot B (2018) DNA methylation and genetic degeneration of the Y chromosome in the dioecious plant Silene latifolia. BMC Genomics 19:540. https://doi.org/10.1186/s12864-018-4936-y

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  39. Song Y, Ma K, Bo W, Zhang Z, Zhang D (2012) Sex-specific DNA methylation and gene expression in andromonoecious poplar. Plant Cell Rep 31:1393–1405. https://doi.org/10.1007/s00299-012-1255-7

    CAS  Article  PubMed  Google Scholar 

  40. Song Y, Ma K, Ci D, Chen Q, Tian J, Zhang D (2013) Sexual dimorphic floral development in dioecious plants revealed by transcriptome, phytohormone, and DNA methylation analysis in Populus tomentosa. Plant Mol Biol 83:559–576. https://doi.org/10.1007/s11103-013-0108-2

    CAS  Article  PubMed  Google Scholar 

  41. Takeshima R, Nishio T, Komatsu S, Kurauchi N, Matsui K (2019) Identification of a gene encoding polygalacturonase expressed specifically in short styles in distylous common buckwheat (Fagopyrum esculentum). Heredity (Edinb) 123:492–502. https://doi.org/10.1038/s41437-019-0227-x

    CAS  Article  PubMed Central  Google Scholar 

  42. Theißen G, Melzer R, Rümpler F (2016) MADS-domain transcription factors and the floral quartet model of flower development: linking plant development and evolution. Development 143:3259. https://doi.org/10.1242/dev.134080

    CAS  Article  PubMed  Google Scholar 

  43. Wang Y, Zhao M, Xu Z, Qi S, Yu X, Han X (2019) MSAP analysis of epigenetic changes reveals the mechanism of bicolor petal formation in Paeonia suffruticosa ‘Shima Nishiki.’ 3 Biotech 9:313. https://doi.org/10.1007/s13205-019-1844-z

    Article  PubMed  PubMed Central  Google Scholar 

  44. Xi W, Liu C, Hou X, Yu H (2010) MOTHER OF FT AND TFL1 regulatesseed germination through a negative feedback loop modulating ABA signaling in Arabidopsis. Plant Cell 22:1733–1748. https://doi.org/10.1105/tpc.109.073072

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  45. Xiong LZ, Xu CG, Saghai Maroof MA, Zhang Q (1999) Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol General Genet 261:439–446. https://doi.org/10.1007/s004380050986

    CAS  Article  Google Scholar 

  46. Yaish MW, Colasanti J, Rothstein SJ (2011) The role of epigenetic processes in controlling flowering time in plants exposed to stress. J Exp Bot 62:3727–3735. https://doi.org/10.1093/jxb/err177

    CAS  Article  PubMed  Google Scholar 

  47. Yang H, Chang F, You C, Cui J, Zhu G, Wang L, Zheng Y, Qi J, Ma H (2015) Whole-genome DNA methylation patterns and complex associations with gene structure and expression during flower development in Arabidopsis. Plant J 81:268–281. https://doi.org/10.1111/tpj.12726

    CAS  Article  PubMed  Google Scholar 

  48. Yu T, Li C (1980) Taihangia- a new genus of Rosaceae from China. Acta Phytotaxon Sinica 18:469–472

    Google Scholar 

  49. Zang L, Zheng T, Chu Y, Ding C, Zhang W, Huang Q, Su X (2015) Genome-wide analysis of the Fasciclin-Like Arabinogalactan protein gene family reveals differential expression patterns, localization, and salt stress response in Populus. Front Plant Sci 6:1140. https://doi.org/10.3389/fpls.2015.01140

    Article  PubMed  PubMed Central  Google Scholar 

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

    CAS  Article  PubMed  Google Scholar 

  51. Zhou Q, Cai Q, Zheng Y, Wu Z, Mao J (2019) Floral development and the formation of functionally unisexual flowers in Xanthoceras sorbifolium (Sapindaceae), a morphologically andromonoecious tree endemic to northern China. Trees 33:1571–1582. https://doi.org/10.1007/s00468-019-01879-6

    Article  Google Scholar 

  52. Zhou P, Zhang X, Fatima M, Ma X, Fang H, Yan H, Ming R (2020) DNA methylome and transcriptome landscapes revealed differential characteristics of dioecious flowers in papaya. Horticulture Research 7:81. https://doi.org/10.1038/s41438-020-0298-0

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  53. Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2007) Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39:61–69. https://doi.org/10.1038/ng1929

    CAS  Article  PubMed  Google Scholar 

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Acknowledgements

The authors are grateful to Ms Shangtong Jiang and Mr Yiming Dong for assistance in experiment. The financial supports of this study were from the National Natural Science Foundation of China (31370434 and U1704241), and the Plan for Scientific Innovation Talent of Henan Province (194200510010).

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WL conceived and designed the work. YM and CZ performed experiments. WL and GL analyzed data. WL wrote the paper. All authors read and approved the manuscript.

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Correspondence to Weiguo Li.

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Li, W., Ma, Y., Zheng, C. et al. Variations of Cytosine Methylation Patterns between Staminate and Perfect Flowers within Andromonoecious Taihangia rupestris (Rosaceae) Revealed by Methylation-Sensitive Amplification Polymorphism. J Plant Growth Regul (2021). https://doi.org/10.1007/s00344-021-10308-3

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Keywords

  • DNA methylation pattern
  • MSAP
  • Staminate flower
  • Perfect flower
  • Taihangia rupestris
  • Gene expression