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| Genome-Wide Transcriptional Analysis of Yield and Heterosis-Associated Genes in Maize (Zea mays L.) |
| ZHANG Ti-fu, LI Bo, ZHANG Deng-feng, JIA Guan-qing, LI Zhi-yong, WANG Shou-cai |
| National Maize Improvement Center/Maize Breeding Engineering Center, Ministry of Education/Key Laboratory of Crop Genomics and Genetic Improvement, Ministry of Agriculture/College of Agriculture and Biotechnology, China Agricultural University, Beijing 100193, P.R.China |
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摘要 Heterosis has contributed greatly to yield in maize, but the nature of its contribution is not completely clear. In this study, two strategies using whole-genome oligonucleotide microarrays were employed to identify differentially expressed genes (DEGs) associated with heterosis and yield. The analysis revealed 1 838 heterosis-associated genes (HAGs), 265 yieldassociated genes (YAGs), and 85 yield heterosis-associated genes (YHAGs). 37.1% of HAGs and 22.4% of YHAGs expressed additively. The remaining genes expressed non-additively, including those with high/low-parent dominance and over/under dominance, which were prevalent in this research. Pathway enrichment analysis and quantitative trait locus (QTL) co-mapping demonstrated that the metabolic pathways for energy and carbohydrates were the two main enriched pathways influencing heterosis and yield. Therefore, the DEGs participating in energy and carbohydrate metabolism were considered to contribute to heterosis and yield significantly. The investigation of potential groups of HAGs, YAGs, and YHAGs might provide valuable information for exploiting heterosis to improve yield in maize breeding. In addition, our results support the view that heterosis is contributed by multiple, complex molecular mechanisms.
Abstract Heterosis has contributed greatly to yield in maize, but the nature of its contribution is not completely clear. In this study, two strategies using whole-genome oligonucleotide microarrays were employed to identify differentially expressed genes (DEGs) associated with heterosis and yield. The analysis revealed 1 838 heterosis-associated genes (HAGs), 265 yieldassociated genes (YAGs), and 85 yield heterosis-associated genes (YHAGs). 37.1% of HAGs and 22.4% of YHAGs expressed additively. The remaining genes expressed non-additively, including those with high/low-parent dominance and over/under dominance, which were prevalent in this research. Pathway enrichment analysis and quantitative trait locus (QTL) co-mapping demonstrated that the metabolic pathways for energy and carbohydrates were the two main enriched pathways influencing heterosis and yield. Therefore, the DEGs participating in energy and carbohydrate metabolism were considered to contribute to heterosis and yield significantly. The investigation of potential groups of HAGs, YAGs, and YHAGs might provide valuable information for exploiting heterosis to improve yield in maize breeding. In addition, our results support the view that heterosis is contributed by multiple, complex molecular mechanisms.
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Received: 28 April 2011
Accepted:
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| Fund: This work was supported by the National Basic Research Program of China (2007CB109000 and 2009CB118400). |
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Corresponding Authors:
Correspondence WANG Shou-cai, Tel/Fax: +86-10-62732409, E-mail: wangshoucai678@sina.com
E-mail: wangshoucai678@sina.com
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Cite this article:
ZHANG Ti-fu, LI Bo, ZHANG Deng-feng, JIA Guan-qing, LI Zhi-yong, WANG Shou-cai.
2012.
Genome-Wide Transcriptional Analysis of Yield and Heterosis-Associated Genes in Maize (Zea mays L.). Journal of Integrative Agriculture, 12(8): 1245-1256.
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| [1]Auger D L, Gray A D, Ream T S, Kato A, Coe Jr E H, Birchler J A. 2005. Nonadditive gene expression in diploid and triploid hybrids of maize. Genetics, 169, 389-397. [2]Benjamini Y, Hochberg Y. 1995. Controlling the false discovery rate: a practical and powerful approch to multiple testing. Journal of the Royal Statistical Society (Series B), 57, 289-300. [3]Bruce A B. 1910. The Mendelian theory of heredity and the argumentation of vigor. Science, 32, 627-628. [4]Chen F, He G, He H, Chen W, Zhu X P, Liang M Z, Chen L B, Deng X W. 2010. Expression analysis of miRNAs and highly-expressed small RNAs in two rice subspecies and their reciprocal hybrids. Journal of Integrative Plant Biology, 52, 971-980. [5]Cho Y, Fernandes J, Kim S H, Walbot V. 2002. Geneexpression profile comparisons distinguish seven organs of maize. Genome Biology, 3, research 0045.1-0045.16. [6]Cui X, Churchill G A. 2002. Statistical tests for differential expression in cDNA microarray experiments. Genome Biology, 4, 210. Davenport C B. 1908. Degeneration, albinism and inbreeding. Science, 28, 454-455. [7]Duvick D N. 1999. Heterosis: feeding people and protecting natural resources. In: Coors J D, Pandey S, eds., The Genetics and Exploitation of Heterosis in Crops. Madison, WI: ASA, CSSA and SSSA, USA. pp. 19-29. [8]East E M. 1908. Inbreeding in corn. In: Reports of the Connecticut Agricultural Experiment Station. USA. pp. 419-428. [9]Frick U B, Schaller A. 2002. cDNA microarray analysis of fusicoccin-induced changes in gene expression in tomato plants. Planta, 216, 83-94. [10]Furutani I, Sukegawa S, Kyozuka J. 2006. Genome-wide analysis of spatial and temporal gene expression in rice panicle development. The Plant Journal, 46, 503-511. [11]Ge X M, Chen W H, Song S H, Wang W W, Hu S N, Yu J. 2008. Transcriptomic profiling of mature embryo from an elite super-hybrid rice LYP9 and its parental lines. BMC Plant Biology, 8, 114. [12]Girke T, Todd J, Ruuska S, White J, Benning C, Ohlrogge J. 2000. Microarray analysis of developing arabidopsis seeds. Plant Physiology, 124, 1570-1581. [13]Gregersen P L, Brinch-Pedersen H, Holm P B. 2005. A microarray-based comparative analysis of gene expression profiles during grain development in transgenic and wild type wheat. Transgenic Research, 14, 887-905. [14]Guo M, Rupe M A, Danilevskaya O N, Yang X F, Hu Z H. 2003. Genome-wide mRNA profiling reveals heterochronic allelic variation and a new imprinted gene in hybrid maize endosperm. The Plant Journal, 36, 30-44. [15]Guo M, Rupe M A, Yang X, Crasta O, Zinselmeier C, Smith O S, Bowen B. 2006. Genome-wide transcript analysis of maize hybrids: allelic additive gene expression and yield heterosis. Theoretical and Applied Genetics, 113, 831-845. [16]Horton P. 2000. Prospects for crop improvement through the genetic manipulation of photosynthesis: morphological and biochemical aspects of light capture. Journal of Experimental Botany, 51, 475-485. [17]Huang Y, Zhang L D, Zhang J W, Yuan D J, Xu C G, Li X H, Zhou D X, Wang S P, Zhang Q F. 2006. Heterosis and polymorphisms of gene expression in an elite rice hybrid as revealed by a microarray analysis of 9198 unique ESTs. Plant Molecular Biology, 62, 579-591. [18]Hubner N, Wallace C A, Zimdahl H, Petretto E, Schulz H, Maciver F, Mueller M, Hummel O, Monti J, Zidek V, et al. 2005. Integrated transcriptional profiling and linkage analysis for identification of genes underlying disease. Nature Genetics, 37, 243-253. [19]Kim B H, von Arnim A G. 2006. The early dark-response in Arabidopsis thaliana revealed by cDNA microarray analysis. Plant Molecular Biology, 60, 321-342. [20]Krieger U, Lippman Z B, Zamir D. 2010. The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nature Genetics, 42, 459-463. [21]Lee M, Sharopova N, Beavis W D, Grant D, Katt M, Blair D. 2002. Expanding the genetic map of maize with the intermated B73×Mo17 (IBM) population. Plant Molecular Biology, 48, 453-461. [22]Li B, Zhang D F, Jia G Q, Dai J R, Wang S C. 2009. Genomewide comparisons of gene expression for yield heterosis in maize. Plant Molecular Biology Reporter, 27, 162-176. [23]Li L, Yan J B, Lei H Z. 2007. QTL-Finder: a bioinformatics tool for QTL integration, comparison and discovery candidate genes across genomes and experiments. In: Zhang Q F, ed., In: The Abstract of Plant Genomics Conference VIII. Shanghai, China. [24]Lian X M, Wang S P, Zhang J W, Feng Q, Zhang L D, Fan D L, Li X H, Yuan D J, Han B, Zhang Q F. 2006. Expression profiles of 10 422 genes at early stage of low nitrogen stress in rice assayed using a cDNA microarray. Plant Molecular Biology, 60, 617-631. [25]Lisec J, Meyer R C, Steinfath M, Redestig H, Becher M, Witucka-Wall H, Fiehn O, Törjék O, Selbig J, Altmann T, et al. 2008. Identification of metabolic and biomass QTL in Arabidopsis thalisna in a parallel analysis of RIL and IL populations. The Plant Journal, 53, 960-972. [26]Mao X Z, Cai T, Olyarchuk J G, Wei L P. 2005. Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics, 21, 3787-3793. [27]Marathe R, Guan Z, Anandalakshmi R, Zhao H Y, Dinesh-Kumar S. 2004. Study of Arabidopsis thaliana resistome in response to cucumber mosaic virus infection using whole genome microarray. Plant Molecular Biology, 55, 501-520. [28]Marcon C, Schützenmeister A, Schütz W, Madlung J, Piepho H P, Hochholdinger F. 2010. Nonadditive protein accumulation patterns in maize (Zea mays L.) hybrids during embryo development. Journal of Proteome Research, 9, 6511-6522. [29]Meyer R C, Kusterer B, Lisec J, Steinfath M, Becher M, Scharr H, Melchinger A E, Selbig J, Schurr U, Willmitzer L, et al. 2010. QTL analysis of early stage heterosis for biomass in Arabidopsis. Theoretical and Applied Genetics, 120, 227-237. [30]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 Molecular Biology, 63, 381-391. [31]Park S J, Huang Y, Ayoubi P. 2006. Identification of expression profiles of sorghum genes in response to greenbug phloemfeeding using cDNA subtraction and microarray analysis. Planta, 223, 932-947. [32]Pea G, Ferron S, Gianfranceschi L, Krajewski P, Pè M E. 2008. Gene expression non-additivity in immature ears of a heterotic F1 maize hybrid. Plant Science, 174, 17-24. [33]Richards R A. 2000. Selectable traits to increase crop photosynthesis and yield of grain crops. Journal of Experimental Botany, 51, 447-458. [34]Sachs T. 1969. Regeneration experiments on the determination of the form of leaves. Israel Journal of Botany, 18, 21-30. [35]Schauer N, Semel Y, Balbo I, Steinfath M, Repsilber D, Selbig J, Pleban T, Zamir D, Fernie A R. 2008. Mode of inheritance of primary metabolic traits in tomato. The Plant Cell, 20, 509-523. [36]Shull G H. 1908. The composition of a field of maize. Report of American Breeders’ Association, 4, 296-301. [37]Shull G H. 1952. Beginning of the heterosis concept. In: Gowen J W, ed., Heterosis. Iowa State College Press, USA. pp. 14-48. [38]Song G S, Zhai H L, Peng Y G, Zhang L, Wei G, Chen X Y, Xiao Y G, Wang L L, Chen Y J, Wu B, et al. 2010. Comparative transcriptional profiling and preliminary study on heterosis mechanism of super-hybrid rice. Molecular Plant, 3, 1012-1025. [39]Song R, Messing J. 2003. Gene expression of a gene family in maize based on noncollinear haplotypes. Proceedings of the National Academy of Sciences of the United States of America, 100, 9055-9060. [40]Stupar R M, Springer N M. 2006. Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genetics, 173, 2199-2210. [41]Swanson-Wagner R A, Jia Y, DeCook R, Borsuk L A, Nettleton D, Schnable P S. 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. Proceedings of the National Academy of Sciences of the United States of America, 103, 6805-6810. [42]Uzarowska A, Keller B, Piepho H P, Schwarz G, Ingvardsen C, Wenzel G, Lübberstedt T. 2007. Comparative expression profiling in meristems of inbred-hybrid triplets of maize based on morphological investigations of heterosis for plant height. Plant Molecular Biology, 63, 21-34. [43]Vuylsteke M, van Eeuwijk F, van Hummelen P, Kuiper M, Zabeau M. 2005. Genetic analysis of variation in gene expression in Arabidopsis thaliana. Genetics, 171, 1267-1175. [44]Wang Z, Liang Y, Li C j, Xu Y Y, Lan L F, Zhao D Z, Chen C B, Xu Z H, Xue Y B, Chong K. 2005. Microarray analysis of gene expression invovled in anther development in rice (Oryza sativa L.). Plant Molecular Biology, 58, 721-737. [45]Wei G, Tao Y, Liu G Z, Chen C, Luo R Y, Xia H A, Gan Q, Zeng H P, Lu Z K, Han Y N, et al. 2009. A transcriptomic analysis of superhybrid rice LYP9 and its parents. Proceedings of the National Academy of Sciences of the United States of America, 106, 7695-7701. [46]Wu H, Kerr M, Cui X Q, Churchill G. 2003. MAANOVA: a software package for the analysis of spotted cDNA microarray experiments. In: Parmigiani G, Garett E S, Irizarry R A, eds., The Analysis of Gene Expression Data: Methods and Software. Springer. pp. 313-341. [47]Yang X H, Chen X Y, Ge Q Y, Li B, Tong Y P, Li Z S, Kuang T Y, Lu C M. 2007. Characterization of photosynthesis of flag leaves in a wheat hybrid and its parents grown under field conditions. Journal of Plant Physiology, 164, 318-326. |
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