Abstract
Genome methylation plays a key role in regulating gene expression, but limited knowledge exists concerning the link between DNA methylation and economic traits in forest trees. We measured photosynthetic characteristics and growth traits in 130 intraspecific hybrids of Chinese white poplar (Populus tomentosa Carr.) and detected their genome methylation. The phenotypic data were normally distributed, and each trait had a significant difference among the hybrids. The net photosynthetic rate (Pn, 14.83 ± 3.76 μmol m−2 s−1), stomatal conductance (Gs, 0.29 ± 0.09 mol m−2 s−1), and intercellular CO2 concentration (Ci, 264.50 ± 30.94 μmol mol−1) showed similar trends. Positive correlations were found between Pn and height (H, 133.59 ± 50.44 cm) and basal diameter (D, 16.29 ± 5.20 mm), respectively. Using methylation-sensitive amplification polymorphism (MSAP) analysis, 32 primer-pair combinations generated 715 polymorphic markers. Positive correlations between photosynthetic characteristics, such as Pn and Gs, and total relative methylation level and relative hemimethylation (CNG methylation) level were investigated. Eighty-one candidate markers were associated with Pn, Gs, or Ci, 13 of which were also associated with growth traits using single MSAP molecular marker association. Sequencing and BLAST analysis showed that candidate markers were linked to genes encoding protochlorophyllide reductase and proteins of cytochrome P450 CYP4/CYP19/CYP26 subfamilies, and linked to genes taking part in, e.g., photosystem II. Therefore, the regions defined by the MSAP candidate markers are linked to genes that are essential for photosynthetic characteristics that respond to DNA methylation and subsequently affect growth traits.
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References
Assaad FF, Tucker KL, Signer ER (1993) Epigenetic repeat-induced gene silencing (RIGS) in Arabidopsis. Plant Mol Biol 22:1067–1085
Bassman JH, Zwier JC (1991) Gas exchange characteristics of Populus trichocarpa, Populus deltoides and Populus trichocarpa × P. deltoides clones. Tree Physiol 2:145–159
Bender J, Fink GR (1995) Epigenetic control of an endogenous gene family is revealed by a novel blue fluorescent mutant of Arabidopsis. Cell 83:725–734
Berry J, Downton WJS (1982) Environmental regulation of photosynthesis. In: Govindjee R (ed) Photosynthesis, vol II. Academia Press, New York, pp 163–343
Bowes G (1993) Facing the inevitable: plants and increasing atmospheric CO2. Annu Rev Plant Physiol Mol Biol 44:309–332
Causevic A, Delaunay A, Ounnar S, Righezza M, Delmotte F, Brignolas F, Hagège D, Maury S (2005) DNA methylating and demethylating treatments modify phenotype and cell wall differentiation state in sugarbeet cell lines. Plant Physiol Biochem 43:681–691
Cervera MT, Ruiz-Garcia L, Martinez-Zapater JM (2002) Analysis of DNA methylation in Arabidopsis thaliana based on methylation-sensitive AFLP markers. Mol Genet Genomics 268:543–552
Ceulemans R, Impens U, Steenackers V (1987) Variations in photosynthetic, anatomical, and enzymatic leaf traits and correlations with growth in recently selected Populus hybrids. Can J For Res 17:273–283
Cubas P, Vincent C, Coen E (1999) An epigenetic mutation responsible for natural variation in floral symmetry. Nature 401:157–161
Farquhar GD, Sharkey TD (1982) Stomatal conductance and photosynthesis. Annu Rev Plant Physiol 33:317–345
Faville MJ, Silvester WB, Allan Green TG, Jermyn WA (1999) Photosynthetic characteristics of three asparagus cultivars differing in yield. Crop Sci 39:1070–1077
Finnegan EJ, Peacock WJ, Dennis ES (1996) Reduced DNA methylation in Arabidopsis thaliana results in abnormal plant development. Proc Natl Acad Sci USA 93:8449–8454
Geiman TM, Robertson KD (2002) Chromatin remodeling, histone modifications, and DNA methylation-how does it all fit together? J Cell Biochem 87:117–125
Goubely C, Arnaud P, Tatout C, Heslop-Harrison JS, Deragon JM (1999) S1 SINE retroposons are methylated at symmetrical and non-symmetrical positions in Brassica napus: identification of a preferred target site for asymmetrical methylation. Plant Mol Biol 39:243–255
Gourcilleau D, Bogeat-Triboulot M, Thiec DL, Lafon-Placette C, Delaunay A, El-Soud WA, Brignolas F, Maury S (2010) DNA methylation and histone acetylation: genotypic variations in hybrid poplars, impact of water deficit and relationships with productivity. Ann For Sci 67:208
Gruenbaum Y, Naveh-Many T, Cedar H, Razin A (1981) Sequence specificity of methylation in higher plant DNA. Nature 292:860–862
Hanai LR, Floh EIS, Fungaro MHP, Santa-Catarina C, Matias de Paula F, Viana AM, Vieira MLC (2010) Methylation patterns revealed by MSAP profiling in genetically stable somatic embryogenic cultures of Ocotea catharinensis (Lauraceae). In Vitro Cell Dev Biol Plant 46:368–377
Hauben M, Haesendonckx B, Standaert E, Kelen KVD, Azmi A, AkpoH BFV, Guisez Y, Bots M, Lambert B, Laga B, Block MD (2009) Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield. Proc Natl Acad Sci USA 106:20109–20114
Idso SB (1991) A general relationship between CO2-induced increases in net photosynthesis and concomitant reductions in stomatal conductance. Environ Exp Bot 31:381–383
Ingelbrecht I, Houdt HV, Montagu MV, Depicker A (1994) Posttranscriptional silencing of reporter transgenes in tobacco correlates with DNA methylation. Proc Natl Acad Sci USA 91:10502–10506
Isebrands JG, Ceulemans R, Wiard BM (1988) Genetics variation in photosynthetic traits among Populus clones in relation to yield. Plant Physiol Biochem 26:427–437
Jablonka E, Goiten R, Marcus M, Cedar H (1985) DNA hypomethylation causes an increase in DNase I sensitivity and advance in the timing of replication of the entire X chromosome. Chromosoma 93:152–156
Jacobsen SE, Meyerowitz EM (1997) Hypermethylated SUPERMAN epigenetic alleles in Arabidopsis. Science 277:1100–1103
Kinoshita T, Miura A, Choi Y, Kinoshita Y, Cao X, Jacobsen SE, Fischer RL, Kakutani T (2004) One-way control of FWA imprinting in Arabidopsis endosperm by DNA methylation. Science 303:521–523
Kovarik A, Matyásek R, Leitch A, Gazdová B, Fulnecek J, Bezdek M (1997) Variability in CpNpG methylation in higher plant genomes. Gene 204:25–33
Lira-Medeiros CF, Parisod C, Fernandes RA, Mata CS, Cardoso MA, Ferreira PCG (2010) Epigenetic variation in mangrove plants occurring in contrasting natural environment. PLoS One 5:e10326
Long Y, Xia W, Li RY, Wang J, Shao MQ, Feng J, King GJ, Meng JL (2011) Epigenetic QTL mapping in Brassica napus. Genetics Published Articles Ahead of Print:111.131615
McClelland M (1983) The frequency and distribution of methylatable DNA sequences in leguminous plant protein coding genes. J Mol Evol 19:346–354
Messeguer R, Ganal MW, Steffens JC, Tanksley SD (1991) Characterization of the level, target sites and inheritance of cytosine methylation in tomato nuclear DNA. Plant Mol Biol 16:753–777
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4325
Nakao M (2001) Epigenetics: interaction of DNA methylation and chromatin. Gene 278:25–31
Ngernprasirtsiri J, Kobayashi H, Akazawa T (1989) Transcriptional regulation and DNA methylation of nuclear genes for photosynthesis in nongreen plant cells. Proc Natl Acad Sci USA 86:7919–7923
Ngernprasirtsiri J, Kobayashi H, Akazawa T (1990) DNA Methylation is a determinative element of photosynthesis gene expression in amyloplasts from liquid-cultured cells of sycamore (Acer pseudoplatanus L.). Cell Struct Funct 15:285–293
Noormets A, Sôber A, Pell EJ, DicksonI RE, Podila GK, Sôber J, Isebrands JG, Karnosky DF (2001) Stomatal and non-stomatal limitation to photosynthesis in two trembling aspen (Populus tremuloides Michx.) clones exposed to elevated CO2 and/or O3. Plant Cell Environ 24:327–336
Pan Q, Wang Z, Quebedeaux B (1998) Responses of the apple plant to CO2 enrichment: changes in photosynthesis, sorbitol, other soluble sugars, and starch. Aust J Plant Physiol 25:293–297
Pavlopoulou A, Kossida S (2007) Plant cytosine-5 DNA methyltransferases: structure, function, and molecular evolution. Genomics 90:530–541
Reyna-López GE, Simpson J, Ruiz-Herrera J (1997) Differences in DNA methylation patterns are detectable during the dimorphic transition of fungi by amplification of restriction polymorphisms. Mol Gen Genet 253:703–710
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 (MSAP) analysis. Mol Genet Genomics 273:484–490
Shikawa I (2001) Surveying CpG methylation at 5′-CCGG in the genomes of rice cultivars. Plant Mol Biol 45:31–39
Tan MP (2010) Analysis of DNA methylation of maize in response to osmotic and salt stress based on methylation-sensitive amplified polymorphism. Plant Physiol Biochem 48:21–26
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
Tsaftaris AS, Kafka M, Polidoros A, Tani W (1997) Epigenetic changes in maize DNA and heterosis. In: CIMMYT. Abstract. The genetics and exploitation of heterosis in crops. International Symposium, Mexico City, pp 112–113
Xiong LZ, Xu CG, Maroof MA, Zhang QF (1999) Patterns of cytosine methylation in an elite rice hybrid and its parental lines, detected by a methylation-sensitive amplification polymorphism technique. Mol Gen Genet 261:439–446
Yang MS, Lang HY, Gao BJ, Wang JM, Zheng JB (2003) Insecticidal activity and transgene expression stability of transgenic hybrid poplar clone 741 carrying two insect-resistant genes. Silvae Genetica 52:5–6
Zhang ZY, Li FL (1992) Studies on chromosome doubling triploid breeding of white poplar (І). J Beijing For Univ 14:52–58
Zhang D, Zhang Z, Yang K, Li B (2004) Genetic mapping in (Populus tomentosa × Populus bolleana) and P. tomentosa Carr. using AFLP markers. Theor Appl Genet 108:657–662
Zhang DQ, Zhang ZY, Yang K (2006a) QTL analysis of growth and wood chemical content traits in an interspecific backcross family of white poplar (Populous tomentosa × P.bolleana) × P. tomentosa. Can J For Res 36:2015–2023
Zhang XY, Yazaki J, Sundaresan A, Cokus S, Chan SWL, Chen H, Henderson IR, Shinn P, Pellegrini M, Jacobsen SE, Ecker JR (2006b) Genome-wide high-resolution mapping and functional analysis of DNA methylation in Arabidopsis. Cell 126:1189–1201
Zhang D, Zhang Z, Yang K (2007a) Identification of AFLP markers associated with embryonic root development in Populus tomentosa Carr. Silvae Genetica 56:27–31
Zhang MS, Yan HY, Zhao N, Lin XY, Pang JS, Xu KZ, Liu LX, Liu B (2007b) Endosperm-specific hypomethylation, and meiotic inheritance and variation of DNA methylation level and pattern in sorghum (Sorghum bicolor L.) inter-strain hybrids. Theor Appl Genet 115:195–207
Zhang X, Shiu S, Cal A, Borevitz JO (2008) Global analysis of genetic, epigenetic and transcriptional polymorphisms in Arabidopsis thaliana using whole genome tiling arrays. PLoS Genet 4:e1000032
Zhao XX, Chai Y, Liu B (2007) Epigenetic inheritance and variation of DNA methylation level and pattern in maize intra-specific hybrids. Plant Sci 172:930–938
Zhao Y, Yu S, Xing C, Fan S, Song M (2008) Analysis of DNA methylation in cotton hybrids and their parents. Mol Biol 42:169–178
Zhao XY, Ma KF, Zhang M, Bian JL, Jiao WY, Zhang ZY (2011) Comparative analysis of the photosynthetic characteristics of three-year-old Populus tomentosa clones. For Res 24:370–378
Acknowledgments
This work was supported by grants from the following sources: State Key Basic Research Program of China (no. 2012CB114506) and Project of the National Natural Science Foundation of China (no. 31170622, 30872042).
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Sequence data from this article have been deposited with the GenBank Data Library under the accession nos. JX041655–JX041698 and JX065417–JX065431.
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Communicated by A. Brunner
Zhiyi Zhang: Deceased
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Ma, K., Song, Y., Jiang, X. et al. Photosynthetic response to genome methylation affects the growth of Chinese white poplar. Tree Genetics & Genomes 8, 1407–1421 (2012). https://doi.org/10.1007/s11295-012-0527-2
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DOI: https://doi.org/10.1007/s11295-012-0527-2