Abstract
Novel hybrid-specific/heterotic gene expression patterns observed from expression studies suggest the need to characterize the underlying regulatory mechanism(s) to reveal the biological basis of heterosis in crop plants. To gain an insight into the molecular basis of heterosis in rice, we investigated the inheritance pattern and level of cytosine methylation, a major epigenetic regulatory mechanism, in the leaf tissue of an elite Indian rice hybrid KRH2 and its parents at three stages (15 day-old, 35 day-old seedling and flag leaf) and their correlation with heterosis using methylation-sensitive amplification polymorphism (MSAP) technique. In contrast to parents, the level of methylation was high during initial growth stages and reduced as the hybrid grew. Even though, a majority of cytosine methylation profiles were transmitted to hybrid at all stages, a considerable level (25.4%) of cytosine methylation pattern was observed to be novel in hybrid and some of these altered loci were identified to code for known/hypothetical proteins. It was also observed that demethylation events occurred more predominantly during early stages than hypermethylation while the frequency of demethylation events decreased in flag leaf with a remarkable increase in hypermethylation in the hybrid. These bi-directional events in methylation in KRH2 were validated in six hybrids with different levels of grain yield heterosis and the level of cytosine methylation in the hybrid was observed to be significantly correlated with heterosis.
Similar content being viewed by others
References
Bergman Y, Mostoslavsky R (1998) DNA demethylation: turning genes on. Biol Chem 379:401–407
Bestor TH (1998) The host defense function of genomic methylation patterns. Novartis Found Symp 214:187–195
Birchler JA, Auger DL, Riddle NC (2003) In search of the molecular basis of heterosis. Plant Cell 15:2236–2239
Bourc’his D, Bestor TH (2004) Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431:96–99
Cao X, Jacobsen SE (2002) Role of the Arabidopsis DRM methyltransferases in de novo DNA methylation and gene silencing. Curr Biol 12:1138–1144
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
Chan SW, Henderson IR, Jacobsen SE (2005) Gardening the genome: DNA methylation in Arabidopsis thaliana. Nat Rev Genet 6:351–360
Colot V, Rossignol JL (1999) Eukaryotic DNA methylation as an evolutionary device. BioEssays 21:402–411
Diequez MJ, Vaucheret H, Paszkowski J, Scheid OM (1998) Cytosine methylation at CG and CNG sites is not a prerequisite for the initiation of transcriptional gene silencing in plants, but it is required for its maintenance. Mol Gen Genet 259:207–215
Dong ZY, Wang YM, Zhang ZJ, Shen Y, Lin XY, Ou XF, Han FP, Liu B (2006) Extent and pattern of DNA methylation alteration in rice lines derived from introgressive hybridization of rice and Zizania latifolia Griseb. Theor Appl Genet 113:196–205
Fang JG, Chao CT (2007) Methylation-sensitive amplification polymorphism in date palms (Phoenix dactylifera L.) and their off-shoots. Plant Biol 9:526–533
Finnegan EJ, Peacock WJ, Dennis ES (2000) DNA methylation, a key regulator of plant development and other processes. Curr Opin Genet Dev 10:217–223
Frascaroli E, Cane MA, Landi P, Pea G, Gianfranceschi L, Villa M, Morgante M, Pe ME (2007) Classical genetic and quantitative trait loci analyses of heterosis in a maize hybrid between two elite inbred lines. Genetics 176:625–644
Guo M, Rupe MA, Danilevskaya ON, Yang X, Hu Z (2003) Genome-wide mRNA profiling reveals heterochronic allelic variation and a new imprinted gene in hybrid maize endosperm. Plant J 36:30–44
Guo M, Rupe MA, Yang XF, Crasta O, Zinselmeier C, Smith OS, Bowen B (2006) Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis. Theor Appl Genet 113:831–845
Hayes HK, Immer FF, Smith DC (1955) Methods of plant breeding. McGraw Hill Book Co. Inc., New York
Hua JP, Xing YZ, Xu CG, Sun XL, Yu SB, Zhang Q (2002) Genetic dissection of an elite rice hybrid revealed that heterozygotes are not always advantageous for performance. Genetics 162:1885–1895
Hua J, Xing Y, Wu W, Xu C, Sun X, Yu S, Zhang Q (2003) Single-locus heterotic effects and dominance by dominance interactions can adequately explain the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 100:2574–2579
Huang Y, Zhang L, Zhang J, Yuan D, Xu CG, Li XG, Zhou D, Wang S, Zhang Q (2006) Heterosis and polymorphisms of gene expression in an elite rice hybrid as revealed by a microarray analysis of 9198 unique ESTs. Plant Mol Biol 62:579–581
Joel AJ, Zhang Q (2001a) Differential cytosine methylation in rice. In: Book of Abstracts of 8th National Rice Biotechnology Network Meeting, Aurangabad, pp 226-230
Joel AJ, Zhang Q (2001b) Direction of methylation and its effect on heterosis in rice. In: Book of Abstracts of 8th National Rice Biotechnology Network Meeting, Aurangabad, pp 231-237
Khush GS (1997) Origin, dispersal, cultivation and variation of rice. Plant Mol Biol 35:25–34
Klein BC, Coasta M (1997) DNA methylation, heterochromatin and epigenetic carcinogens. Mut Res 386:163–180
Li ZK, Luo LJ, Mei HW, Wang DL, Shu QY (2001) Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield. Genet 158:1737–1753
Li Y, Shan X, Liu X, Hu L, Guo W, Liu B (2008) Utility of the methylation-sensitive amplified polymorphism (MSAP) marker for detection of DNA methylation polymorphism and epigenetic population structure in a wild barley species (Hordeum brevisubulatum). Ecol Res DOI 10.1007/s11284-007-0459-8
Lippman ZB, Zamir Dani (2006) Heterosis: revisiting the magic. Trends Genet 23:60–66
Liu DJ, Zhao MF, Li XH, Yang JB, Xu CG, Zhang Q (1998) SSR heterogenic patterns for marking and predicting heterosis in rice breeding. Mol Br 4:263–268
Luo LJ, Li ZK, Mei HW, Shu QY, Tabien R (2001) Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. II. Grain yield components. Genet 158:1755–1771
Matzke MA, Mette MF, Aufsatz W, Jakowitsch J, Matzke AJM (1999) Host defenses to parasitic sequences and the evolution of epigenetic control mechanisms. Genetica 107:271–287
Meyer S, Pospisil H, Scholten S (2007) Heterosis associated gene expression in maize embryos 6 days after fertilization exhibits additive, dominant and overdominant pattern. Plant Mol Biol 63:381–391
Murray MG, Thompson WF (1980) Rapid isolation of high molecular weight plant DNA. Nucleic Acids Res 8:4321–4326
Panaud O, Chen X, McCouch SR (1996) Development of microsatellite markers and characterization of simple sequence length polymorphism (SSLP) in rice (Oryza sativa L.). Mol Gen Genet 252:597–607
Panse VG, Sukhatme PV (1967) In: Statistical methods for Agricultural workers. 3rd Edn., ICAR, New Delhi
Portis E, Acquadro A, Comino C, Lanteri S (2004) Analysis of DNA methylation during germination of pepper (Capsicum annuum L.) seeds using methylation-sensitive amplification polymorphism (MSAP). Plant Sci 166:169–178
Rangwala SH, Richards EJ (2004) The value-added genome: building and maintaining genomic cytosine methylation landscapes. Curr Opin Genet Dev 14:686–691
Rapp RA, Wendel JF (2005) Epigenetics and plant evolution. New Phytol 168:81–91
Rasmusson DC, Phillips RL (1997) Plant breeding progress and genetic diversity from de nova variation and elevated epistasis. Crop Sci 37:303–310
Saghai Maroof MA, Yang GP, Zhang Q, Gravors KA (1997) Correlation between molecular marker distance and hybrid performance in U.S Southern long grain rice. Crop Sci 37:145–150
Salmon A, Clotault J, Jenczewski E, Chable V, Manzanares-Dauleux MJ (2008) Brassica oleracea displays a high level of DNA methylation polymorphism. Plant Sci 174:61–70
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
Springer NM, Stupar RM (2007) Allelic variation and heterosis in maize: how do two halves make more than a whole? Genome Res 17:264–275
Stupar RM, Springer NM (2006) Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genet 173:2199–2210
Sun QX, Wu LM, Ni ZF, Meng FR, Wang ZK, Lin Z (2004) Differential gene expression patterns in leaves between hybrids and their parental inbreds are correlated with heterosis in a wheat diallel cross. Plant Sci 166:651–657
Swanson-Wagner RA, Jia Y, DeCook R, Borsuk LA, Nettleton D, Schnable PS (2006) All possible modes of gene action are observed in a global comparison of gene expression in a maize F1 hybrid and its inbred parents. Proc Natl Acad Sci USA 103:6805–6810
Tariq M, Paszkowski J (2004) DNA and histone methylation in plants. Trends Genet 20:244–251
Tsaftaris AS, Polidoros A (2000) DNA methylation and Plant breeding. Pl Breed Rev 18:87–177
Tsaftaris AS, Kafka M, Polidoros A, Tani E (1997) Epigenetic changes in maize DNA and heterosis. In: Abstracts of the international symposium on “The genetics and exploitation of heterosis in crops”, Mexico City, pp 112-113
Turner JH (1953) A study of heterosis in upland cotton I. Yield of hybrids compared with varieties 2. Combining ability and inbreeding effect. Agronomy J 45:485–490
Varshney RK, Graner A, Sorrells ME (2005) Genomics-assisted breeding for crop improvement. Trends Plant Sci 10:621–630
Vos P, Hogers R, Bleeker M, Reijans M, Van de Lee T, Horness M, Fijiters A, Pot J, Peleman J, Kuiper M, Zabeau M (1995) AFLP : A new technique for DNA fingerprinting. Nucleic Acids Res 23:4407–4414
Vuylsteke M, Van Eeuwijk F, Van Hummelen P, Kuiper M, Zabeau M (2005) Genetic analysis of variation in gene expression in Arabidopsis thaliana. Genet 171:1267–1275
Wynne JC, Emery A, Rice PW (1970) Combining ability estimates in Arachis hypogaea L. II. Field performance of F1 hybrids. Crop Sci 10:713–715
Xiao J, Li J, Yuan L, Tanksley SD (1995) Dominance is the major genetic basis of heterosis in rice as revealed by QTL analysis using molecular markers. Genet 140:745–754
Xing YZ, Tan YF, Hua JP, Sun XL, Xu CG (2002) Characterization of the main effects, epistatic effects and their environmental interactions of QTLs in the genetic basis of yield traits in rice. Theor Appl Genet 105:248–257
Xiong LZ, Yang GP, Xu CG, Zhang Q, Maroof Saghai (1998) Relationships of differential gene expression in leafs with heterosis and heterozygosity in a rice diallel cross. Mol Br 4:129–136
Xiong LZ, Xu CG, Maroof Saghai, Zhang Q (1999) Patterns of cytosine methylation in an elite rice hybrid and its parental lines detected by methylation sensitive amplification polymorphism technique. Mol Gen Genet 261:439–446
Yu SB, Li JX, Xu CG, Tan YF, Gao YJ, Li XH, Zhang Qifa, Saghai Maroof MA (1997) Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 94:9226–9231
Zhang Q, Gao YJ, Yang S, Ragab R, Saghai Maroof MA, Li ZB (1994) A diallel analysis of heterosis in elite hybrid rice based on RFLPs and microsatellites. Theor Appl Genet 89:185–192
Zhang Q, Gao YJ, Saghai Maroof MA, Yang SH, Li JX (1995) Molecular divergence and hybrid performance in rice. Mol Br 1:133–142
Zhang Q, Zhou ZQ, Yang GP, Xu CG, Liu KD, Saghai Maroof MA (1996) Molecular marker heterozygosity and hybrid performance in indica and japonica rice. Theor Appl Genet 93:1218–1224
Zhang Q, Hua JP, Yu SB, Xiong L, Xu CG (2001) Genetic and molecular basis of heterosis in rice. In: Khush GS (ed) Rice Genetics IV. IRRI Publications, Phillippines, pp 173–188
Zhang MS, Yan HY, Zhao N, Lin XY, Pang JS, Xu KZ, Liu LX, Liu B (2007) 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 HY, He H, Chen LB, Li L, Liang MZ, Wang XF, Liu XG, He GM, Chen RS, Ma LG, Deng XW (2008a) A genome-wide transcription analysis reveals a close correlation of promoter INDEL polymorphism and heterotic gene expression in rice hybrids. Mol Plant 1:720–731
Zhang Y, Liu ZH, Liu C, Yang ZJ, Deng KJ, Peng JH, Zhou JP, Li GR, Tang ZX, Ren ZL (2008b) Analysis of DNA methylation variation in wheat genetic background after alien chromatin introduction based on methylation-sensitive amplification polymorphism. Chin Sci Bull 53:58–69
Zhao MF, Li XH, Yang JB, Xu CG, Hu RY, Liu DJ, Zhang Q (1999) Relationship between molecular marker heterozygosity and hybrid performance in intra- and inter- subspecific crosses of rice. Pl Breed 118:139–144
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
Acknowledgments
The fellowship and facilities provided to K.S. by Barwale foundation are gratefully acknowledged. The authors thank Dr Amalraj John Joel for useful discussion and Mahyco Life Science Research Center, Jalna for sequencing facility. Seed material supplied by IRRI, Philippines and DRR, Hyderabad is thankfully acknowledged. We also thank R. M. Sundaram and P. Rajendrakumar for their useful suggestions which helped to improve the manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Sakthivel, K., Girishkumar, K., Ramkumar, G. et al. Alterations in inheritance pattern and level of cytosine DNA methylation, and their relationship with heterosis in rice. Euphytica 175, 303–314 (2010). https://doi.org/10.1007/s10681-010-0167-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10681-010-0167-2