Abstract
The andromonoecious poplar is an exceptional model system for studying sex-specific flower development in dioecious plants. There is increasing evidence that epigenetic regulation, particularly DNA methylation, is an important regulatory factor during flower development. Here, methylation-sensitive amplified polymorphism (MSAP) was used to screen for sex-specific DNA methylation alterations in the andromonoecious poplar. The sequences of 27 sex-specific amplified fragments were obtained from DNA prepared from sex-specific flower tissues. PtGT2, PtPAL3, and PtCER4, which are homologous to MF26, MF29, and MF35, respectively, were cloned as candidate genes. Expression analysis and DNA methylation pattern profiling of the three candidate genes revealed that gene expression upregulation was always associated with gene body methylation. The results suggested that DNA methylation sites have the potential to regulate the genes’ transcript levels. These three genes were shown to play important roles during different phases of flower development. This study will help to provide candidates for future experiments aimed at understanding the mechanism, whereby DNA methylation regulates gene expression in poplar.
Key messages
We report the first screen for sex-specific DNA methylation alterations in the andromonoecious poplar. 27 sex-specific methylation sites were identified. The gene expression levels and DNA methylation patterns were detected for three candidate genes.
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References
Aarts MG, Hodge R, Kalantidis K, Florack D, Wilson ZA, Mulligan BJ, Stiekema WJ, Scott R, Pereira A (1997) The Arabidopsis MALE STERILITY 2 protein shares similarity with reductases in elongation/condensation complexes. Plant J 12:615–623
Chan SW, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6:351–360
Cokus SJ, Feng S, Zhang X, Chen Z, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE (2008) Shotgun bisulphate sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–219
Elkind Y, Edwards R, Mavandad M, Hedrick SA, Ribak O, Dixon RA, Lamb CJ (1990) Abnormal plant development and down-regulation of phenylpropanoid biosynthesis in transgenic tobacco containing a heterologous phenylalanine ammonia-lyase gene. Proc Natl Acad Sci USA 87:9057–9061
Garcia ME, Lynch T, Peeters J, Snowden C, Finkelstein R (2008) A small plant-specific protein family of ABI five binding proteins (AFPs) regulates stress response in germinating Arabidopsis seeds and seedlings. Plant Mol Biol 67:643–658
Herman JG, Graff JR, Myohanen S, Nelkin BD, Baylin SB (1996) Methylation-specific PCR: a novel PCR assay for methylation status of CpG islands. Proc Natl Acad Sci USA 93:9821–9826
Lamb CJ, Lawton MA, Dron M, Dixon RA (1989) Signals and transduction mechanisms for activation of plant defenses against microbial attack. Cell 56:215–224
Leljak-Levanić D, Bauer ND, Mihaljević S, Jelaska S (2004) Changes in DNA methylation during somatic embryogenesis in Cucurbita pepo L. Plant Cell Rep 23:120–127
Li R, Moore M, Bonham-Smith PC, King J (2002) Overexpression of formate dehydrogenase in Arabidopsis thaliana resulted in plants tolerant to high concentrations of formate. J Plant Physiol 159:1069–1076
Li X, Qin GJ, Chen ZL, Gu HY, Qu LJ (2008) A gain-of-function mutation of transcriptional factor PTL results in curly leaves, dwarfism and male sterility by affecting auxin homeostasis. Plant Mol Biol 66:315–327
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 461:1135–1139
Ni M, Dehesh K, Tepperman JM, Quail PH (1996) GT-2: in vivo transcriptional activation activity and definition of novel twin DNA binding domains with reciprocal target sequence selectivity. Plant Cell 8:1041–1059
Peredo EL, Revilla MA, Arroyo-Garcýa R (2006) Assessment of genetic and epigenetic variation in hop plants regenerated from sequential subcultures of organogenic calli. J Plant Physiol 163:1071–1079
Rapp RA, Wendel JF (2005) Epigenetics and plant evolution. New Phytol 168:81–91
Ruiz-Garcia L, Cervera MT, Martinez-Zapater JM (2005) DNA methylation increases throughout Arabidopsis development. Planta 222:301–306
Schimd M, Davison TS, Henz SR, Pape UJ, Demar M, Vingron M, Scholkopf B, Weigel D, Lohmann JU (2005) A gene expression map of Arabidopsis thaliana development. Nat Genet 37:501–506
Sha AH, Lin XH, Huang JB, Zhang DP (2005) Analysis of DNA methylation related to rice adult plant resistance to bacterial blight based on methylation-sensitive AFLP. Mol Genet Genomics 273:484–490
Sheppard LA, Brunner AM, Krutovskii KV, Rottmann WH, Skinner JS, Vollmer SS, Strauss SH (2000) A DEFICIENS homolog from the dioecious tree black cottonwood is expressed in female and male floral meristems of the two-whorled, unisexual flowers. Plant Physiol 124:627–639
Stettler RF (1971) Variation in sex expression in black cottonwood and related hybrids. Silvae Genet 20:42–46
Teyssier E, Bernacchia G, Maury S, How Kit A, Stammitti-Bert L, Rolin D, Gallusci P (2008) Tissue dependent variations of DNA methylation and endoreduplication levels during tomato fruit development and ripening. Planta 228:391–399
Tixier MH, Sourdille RM, Leroy P, Bernard M (1997) Detection of wheat microsatellites using a non-radioactive silver-nitrate staining method. J Genet Breed 51:175–177
Verhoeven KJF, Jansen JJ, van Dijk PJ, Biere A (2010) Stress-induced DNA methylation changes and their heritability in asexual dandelions. New Phytol 185:1108–1118
Wang WX, Vinocur B, Shoseyov O, Altman A (2004) Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9:244–252
Wassenegger M (2000) RNA-directed DNA methylation. Plant Mol Biol 43:203–220
Zhang XY, Yazaki J, Sundaresan A, Cokus S, Chan SW, Chen HM, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR (2006) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201
Zhang WL, Wang XE, Yu QY, Ming R, Jiang JM (2008) DNA methylation and heterochromatinization in the male-specific region of the primitive Y chromosome of papaya. Genome Res 18:1938–1943
Zhang DQ, Du QZ, Xu BH, Zhang ZY, Li BL (2010) The actin multigene family in Populus: organization, expression and phylogenetic analysis. Mol Genet Genomics 284:105–119
Zluvova J, Zak J, Janousek B, Vyskot B (2010) Dioecious Silene latifolia plants show sexual dimorphism in the vegetative stage. BMC Plant Biol 10:208
Acknowledgments
This work was supported by grants from the following sources: the Specific Programs in Graduate Science and Technology Innovation of Beijing Forestry University (No. BLYJ201202) and Project of the National Natural Science Foundation of China (No. 30872042, 31170622).
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Communicated by J. S. Shin.
Sequence data from this article has been deposited with the GenBank Data Library under the accession nos. JN315780–JN315782 (PtPAL3, PtCER4, PtGT2).
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Song, Y., Ma, K., Bo, W. et al. Sex-specific DNA methylation and gene expression in andromonoecious poplar. Plant Cell Rep 31, 1393–1405 (2012). https://doi.org/10.1007/s00299-012-1255-7
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DOI: https://doi.org/10.1007/s00299-012-1255-7