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Correlation between parental transcriptome and field data for the characterization of heterosis in Zea mays L.

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Abstract

Heterosis is widely exploited in plant breeding, although its molecular basis is still not fully understood. For the characterization of this phenomenon and the development of transcriptome-based methods to predict hybrid performance (HP), we applied a microarray (46k) analysis of 21 European maize (Zea mays L.), 14 dent and 7 flint parental inbred lines. Expression profiles of the parental inbreds at the seedling stage were correlated with grain yield (GY) and grain dry matter content (GDMC) of 98 flint × dent factorial crosses at six locations. We observed highly significant correlations of the parental expression levels of certain differentially expressed genes with heterosis and HP for GY and also with HP for GDMC. This strong correlation provided first evidence toward a prediction potential of the genes and their expression levels. The identified gene set based on the parental transcriptome data revealed functional characteristics of HP and heterosis. Gene ontology (GO) analyses were performed to compare genes correlated with their expression pattern to HP for GY and GDMC, respectively. Between these gene groups, mostly different functional classes of genes were found to be enriched or underrepresented. The phenomenon of heterosis was characterized by the over- and underrepresentation of specific GO terms among heterosis-correlated genes.

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References

  • Alexa A, Rahnenführer J, Lengauer T (2006) Improved scoring of functional groups from gene expression data by decorrelating GO graph structure. Bioinformatics 22:1600–1607

    Article  CAS  PubMed  Google Scholar 

  • Bernardo R (1996) Best linear unbiased prediction of maize single-cross performance. Crop Sci 36:50–56

    Google Scholar 

  • Birchler JA, Bhadra U, Bhadra MP, Auger DL (2001) Dosage-dependent gene regulation in multicellular eukaryotes: Implications for dosage compensation, aneuploid syndromes, and quantitative traits. Dev Biol 234:275–288

    Article  CAS  PubMed  Google Scholar 

  • Clark RM, Wagler TN, Quijada P, Doebley J (2006) A distant upstream enhancer at the maize domestication gene tb1 has pleiotropic effects on plant and inflorescent architecture. Nat Genet 38:594–597

    Article  CAS  PubMed  Google Scholar 

  • East EM (1936) Heterosis. Genetics 21:375–397

    CAS  PubMed  Google Scholar 

  • Frisch M, Thiemann A, Fu J, Schrag TA, Scholten S, Melchinger AE (2010) Transcriptome-based distance measures for grouping of germplasm and performance prediction in hybrid breeding. Theor Appl Genet (this issue)

  • Gene Ontology Consortium (2000) Gene ontology: tool for the unification of biology. Nat Genet 25:25–29

    Article  CAS  Google Scholar 

  • Gentleman RC, Carey VJ, Bates DM et al (2004) Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 5(10):R80

    Article  PubMed  Google Scholar 

  • Guarente L, Mason T (1983) Heme regulates transcription of the CYC1 gene of S. cerevisiae via an upstream activation site. Cell 32:1279–1286

    Article  CAS  PubMed  Google Scholar 

  • Guo M, Rupe MA, Zinselmeier C, Habben J, Bowen BA, Smith OS (2004) Allelic variation of gene expression in maize hybrids. Plant Cell 16:1707–1716

    Article  CAS  PubMed  Google Scholar 

  • Guo M, Rupe MA, Yang X, 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

    Article  CAS  PubMed  Google Scholar 

  • Harwood JL (1980) Plant acyl lipids. In: Stumpf PK, Conn EE (eds) Biochemistry of plants, vol 4. Academic Press, New York, pp 1–55

    Google Scholar 

  • Herbers K, Meuwly P, Frommer WB, Metraux JP, Sonnewald U (1996) Systemic acquired resistance mediated by the ectopic expression of invertase: possible hexose sensing in the secretory pathway. Plant Cell 8:793–803

    Article  CAS  PubMed  Google Scholar 

  • Hochholdinger F, Hoecker N (2007) Towards the molecular basis of heterosis. Trends Plant Sci 12:427–432

    Article  CAS  PubMed  Google Scholar 

  • Hoecker N, Keller B, Muthreich N, Chollet D, Descombes P, Piepho HP, Hochholdinger F (2008) Comparison of maize (Zea mays L.) F1-hybrid and parental inbred line primary root transcriptomes suggests organ-specific patterns of non-additive gene expression and conserved expression trends. Genetics 179:1275–1283

    Article  CAS  PubMed  Google Scholar 

  • Inoue N, Kasuga S (1989) Agronomic traits and nutritive value of stover in brown midrib-3 maize hybrids. Grassl Sci 35:220–227

    Google Scholar 

  • Jabrin S, Ravanel S, Gambonnet B, Douce R, Rébeillé F (2003) One-carbon metabolism in plants. Regulation of tetrahydrofolate synthesis during germination and seedling development. Plant Physiol 131:1431–1439

    Article  CAS  PubMed  Google Scholar 

  • Jiménez-Bremont JF, Ruiz OA, Rodríguez-Kessler M (2007) Modulation of spermidine and spermine levels in maize seedlings subjected to long-term salt stress. Plant Physiol Biochem 45:812–821

    Article  PubMed  CAS  Google Scholar 

  • Kendziorski C, Irizarry RA, Chen KS, Haag JD, Gould MN (2005) On the utility of pooling biological samples in microarray experiments. Proc Natl Acad Sci USA 102(12):4252–4257

    Article  CAS  PubMed  Google Scholar 

  • Kerr KM, Churchill GA (2001) Experimental design for gene expression microarrays. Biostatistics 2:183–201

    Article  PubMed  Google Scholar 

  • Kim GT, Shoda K, Tsuge T, Cho KH, Uchimiya H, Yokoyama R, Nishitani K, Tsukaya H (2002) The ANGUSTIFOLIA gene of Arabidopsis, a plant CtBP gene, regulates leaf-cell expansion, the arrangement of cortical microtubules in leaf cells and expression of a gene involved in cell-wall formation. EMBO J 21:1267–1279

    Article  CAS  PubMed  Google Scholar 

  • Kinney AJ, Clarkson DT, Loughman BC (1987) The regulation of phosphatidylcholine biosynthesis in rye (Secale cereale) roots. Stimulation of the nucleotide pathway by low temperature. Biochem J 242:755–759

    CAS  PubMed  Google Scholar 

  • Koch KE (1996) Carbohydrate-modulated gene expression in plants. Annu Rev Plant Physiol Plant Mol Biol 47:509–540

    Article  CAS  PubMed  Google Scholar 

  • Lu H, Romero-Severson J, Bernardo R (2003) Genetic basis of heterosis explored by simple sequence repeat markers in a random-mated maize population. Theor Appl Genet 107:494–502

    Article  CAS  PubMed  Google Scholar 

  • Mason SC, D’Croz-Mason NE (2002) Agronomic practices influence maize grain quality. J Crop Prod 5(1):75–91

    Article  CAS  Google Scholar 

  • McDermitt DK, Loomis RS (1981) Elemental composition of biomass and its relation to energy content, growth efficiency, and growth yield. Ann Bot 48:275–290

    CAS  Google Scholar 

  • Melchinger AE (1999) Genetic diversity and heterosis. In: Coors JG, Pandey S (eds) The genetics and exploitation of heterosis in crops. Madison, Wisconsin, pp 99–118

    Google Scholar 

  • Meyer RC, Törjék O, Becher M, Altmann T (2004) Heterosis of biomass production in Arabidopsis. Establishment during early development. Plant Physiol 134:1813–1823

    Article  CAS  PubMed  Google Scholar 

  • Meyer S, Pospisil H, Scholten S (2007) Heterosis associated gene expression in maize embryos 6 days after fertilization exhibits additive, dominant and overdominant patterns. Plant Mol Biol 63:381–391

    Article  CAS  PubMed  Google Scholar 

  • Pical C, Westergren T, Dove SK, Larsson C, Sommarin M (1999) Salinity and hyperosmotic stress induce rapid increases in phosphatidylinositol 4, 5-bisphosphate, diacylglycerol pyrophosphate, and phosphatidylcholine in Arabidopsis thaliana cells. J Biol Chem 274:38232–38240

    Article  CAS  PubMed  Google Scholar 

  • Rédei GP (1962) Single locus heterosis. Z Vererbungsl 93:164–170

    Google Scholar 

  • Römisch-Margl L, Spielbauer G, Schützenmeister A, Schwab W, Piepho H-P, Genschel U, Gierl A (2010) Heterotic patterns of sugar and amino acid components in developing maize kernels. Theor Appl Genet (this issue)

  • Sarkissian IV, McDaniel RG (1967) Mitochondrial polymorphism in maize. I. Putative evidence for de novo origin of hybrid-specific mitochondria. Proc Natl Acad Sci USA 57:1262

    Article  Google Scholar 

  • Sarkissian IV, Srivastava HK (1971) Mitochondrial polymorphism. III. Heterosis, complementation, and spectral properties of purified cytochrome oxidase of wheat. Biochem Genet 5(1):57–63

    Article  CAS  PubMed  Google Scholar 

  • Sarkissian IV, Kessinger MA, Harris W (1964) Differential rates of development of heterotic and non-heterotic young seedlings. I. Correlation of differential morphological development with physiological differences in germinating seeds. Proc Natl Acad Sci USA 51:212

    Article  CAS  PubMed  Google Scholar 

  • Schrag TA, Melchinger AE, Sørensen AP, Frisch M (2006) Prediction of single-cross hybrid performance for grain yield and grain dry matter content in maize using AFLP markers associated with QTL. Theor Appl Genet 113:1037–1047

    Article  CAS  PubMed  Google Scholar 

  • Schrag TA, Maurer HP, Melchinger AE, Piepho HP, Peleman J, Frisch M (2007) Prediction of single-cross hybrid performance in maize using haplotype blocks associated with QTL for grain yield. Theor Appl Genet 114:1345–1355

    Article  PubMed  Google Scholar 

  • Schrag TA, Möhring J, Maurer HP, Dhillon BS, Melchinger AE, Piepho HP, Sørensen AP, Frisch M (2009) Molecular marker-based prediction of hybrid performance in maize using unbalanced data from multiple experiments with factorial crosses. Theor Appl Genet 118:741–751

    Article  CAS  PubMed  Google Scholar 

  • Schrag A, Möhring J, Kusterer B, Dhillon BS, Melchinger AE, Piepho H-P, Frisch M (2010) Hybrid performance prediction in maize using molecular markers and joint analyses of hybrids and parental inbreds. Theor Appl Genet (this issue)

  • Semel Y, Nissenbaum J, Menda N, Zinder M, Krieger U, Issman N, Pleban T, Lippman Z, Gur A, Zamir D (2006) Overdominant quantitative trait loci for yield and fitness in tomato. Proc Natl Acad Sci USA 103(35):12981–12986

    Article  CAS  PubMed  Google Scholar 

  • Shpak ED, Berthiaume CT, Hill EJ, Torii KU (2004) Synergistic interaction of three ERECTA-family receptor-like kinases controls Arabidopsis organ growth and flower development by promoting cell proliferation. Development 131:1491–1501

    Article  CAS  PubMed  Google Scholar 

  • Shull GH (1908) The composition of a world of maize. Rep Am Breed Assoc 4:296–301

    Google Scholar 

  • Sikorska E, Kacperska-Palacz A (1980) Frost-induced phospholipid changes in cold-acclimated and non-acclimated rape leaves. Physiol Plant 48:201–206

    Article  CAS  Google Scholar 

  • Smeekens S, Rook F (1997) Sugar sensing and sugar-mediated signal transduction in plants. Plant Physiol 115:7–13

    CAS  PubMed  Google Scholar 

  • Song R, Messing J (2003) Gene expression of a gene family in maize based on noncollinear haplotypes. Proc Natl Acad Sci USA 100:9055–9060

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Stam M, Belele C, Dorweiler JE, Chandler VL (2002) Differential chromatin structure within a tandem array 100 kb upstream of the maize b1 locus is associated with paramutation. Genes Dev 16:1906–1918

    Article  CAS  PubMed  Google Scholar 

  • Steinfath M, Gärtner T, Lisec J, Meyer RC, Altmann T, Willmitzer L, Selbig J (2010) Prediction of hybrid biomass in Arabidopsis thaliana by selected parental SNP and metabolic markers. Theor Appl Genet (this issue)

  • Stuber CW, Lincoln SE, Wolff DW, Helentjaris T, Lander ES (1992) Identification of genetic factors contributing to heterosis in a hybrid from two elite maize inbred lines using molecular markers. Genetics 132:823–839

    CAS  PubMed  Google Scholar 

  • Stupar RM, Springer NM (2006) Cis-transcriptional variation in maize inbred lines B73 and Mo17 leads to additive expression patterns in the F1 hybrid. Genetics 173:2199–2210

    Article  CAS  PubMed  Google Scholar 

  • Stupar RM, Gardiner JM, Oldre AG, Haun WJ, Chandler VL, Springer NM (2008) Gene expression analyses in maize inbreds and hybrids with varying levels of heterosis. BMC Plant Biol 10(8):33

    Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Tasseva G, Richard L, Zachowski A (2004) Regulation of phosphatidylcholine biosynthesis under salt stress involves choline kinases in Arabidopsis thaliana. FEBS Lett 566:115–120

    Article  CAS  PubMed  Google Scholar 

  • Tollenaar M, Ahmadzadeh A, Lee EA (2004) Physiological basis of heterosis for grain yield in maize. Crop Sci 44:2086–2094

    Article  Google Scholar 

  • Uzarowska A, Keller B, Piepho HP, Schwarz G, Ingvardsen C, Wenzel G, Lübberstedt T (2006) Comparative expression profiling in meristems of inbred-hybrid triplets of maize based on morphological investigations of heterosis for plant height. Plant Mol Biol 63:21–34

    Article  PubMed  CAS  Google Scholar 

  • Vuylsteke M, Kuiper M, Stam P (2000) Chromosomal regions involved in hybrid performance and heterosis: their AFLP-based identification and practical use in prediction models. Heredity 85:208–218

    Article  CAS  PubMed  Google Scholar 

  • Wittkopp PJ, Haerum BK, Clark AG (2004) Evolutionary changes in cis and trans gene regulation. Nature 430:85–88

    Article  CAS  PubMed  Google Scholar 

  • 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. Genetics 140:745–754

    CAS  PubMed  Google Scholar 

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Acknowledgments

We thank the staff of the Plant Breeding Research Station at Eckartsweiler and Hohenheim for conducting the field experiments. We thank Sabina Miaskowska and Nadine Petersen for technical assistance. We are grateful to Heike Pospisil for helpful discussion. This project was supported by the German Research Foundation (DFG) within the priority program SPP 1149 “Heterosis in Plants” (Grant no. FR 1615/4-1).

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Correspondence to Stefan Scholten.

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Communicated by M. Xu.

A. Thiemann and J. Fu contributed equally to this work.

Contribution to the special issue “Heterosis in Plants”.

The microarray data of this work were deposited in GEO at NCBI with the accession number GSE17754.

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Thiemann, A., Fu, J., Schrag, T.A. et al. Correlation between parental transcriptome and field data for the characterization of heterosis in Zea mays L.. Theor Appl Genet 120, 401–413 (2010). https://doi.org/10.1007/s00122-009-1189-9

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