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Heterosis in early seed development: a comparative study of F1 embryo and endosperm tissues 6 days after fertilization

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Abstract

Heterosis specifies the superior performance of heterozygous individuals and although used in plant breeding the underlying molecular mechanisms still remain largely elusive. In this study, we demonstrate the manifestation of heterosis in hybrid maize embryo and endosperm tissue 6 days after fertilization in crosses of several inbred lines. We provide a comparative analysis of heterosis-associated gene expression in these tissues by a combined approach of suppression subtractive hybridization and microarray hybridizations. Non-additive expression pattern indicated a trans-regulatory mechanism to act early after fertilization in hybrid embryo and endosperm although the majority of genes showed mid-parental expression levels in embryo and dosage dependent expression levels in endosperm. The consistent expression pattern within both tissues and both inbred line genotype combinations of genes coding for chromatin related proteins pointed to heterosis-related epigenetic processes. These and genes involved in other biological processes, identified in this study, might provide entry points for the investigation of regulatory networks associated with the specification of heterosis.

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References

  • Achard P, Cheng H, De Grauwe L, Decat J, Schoutteten H, Moritz T, Van Der Straeten D, Peng J, Harberd NP (2006) Integration of plant responses to environmentally activated phytohormonal signals. Science 311:91–94

    Article  CAS  PubMed  Google Scholar 

  • Achard P, Liao L, Jiang C, Desnos T, Bartlett J, Fu X, Harberd NP (2007) DELLAs contribute to plant photomorphogenesis. Plant Physiol 143:1163–1172

    Article  CAS  PubMed  Google Scholar 

  • Adams KL, Cronn R, Percifield R, Wendel JF (2003) Genes duplicated by polyploidy shows unequal contributions to the transcriptome and organ-specific reciprocal silencing. PNAS 100:4649–4654

    Article  CAS  PubMed  Google Scholar 

  • Alleman M, Doctor J (2000) Genomic imprinting in plants: observations and evolutionary implications. Plant Mol Biol 43:147–161

    Article  CAS  PubMed  Google Scholar 

  • Auger DL, Gray AD, Ream TS, Kato A, Coe EH Jr, Birchler JA (2005) Non-additive gene expression in diploid and triploid hybrids of maize. Genetics 169:389–397

    Article  CAS  PubMed  Google Scholar 

  • Baroux C, Spillane C, Grossniklaus U (2002) Genomic imprinting during seed development. Adv Genet 46:165–214

    Article  CAS  PubMed  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc 57:289–300

    Google Scholar 

  • Berger F (1999) Endosperm development. Curr Opin Plant Biol 2:28–32

    Article  CAS  PubMed  Google Scholar 

  • Birchler JA (1993) Dosage analysis of maize endosperm development. Annu Rev Genet 27:181–204

    Article  CAS  PubMed  Google Scholar 

  • Birchler JA, Auger DL, Riddle NC (2003) In search of the molecular basis of heterosis. Plant Cell 15:2236–2239

    Article  CAS  PubMed  Google Scholar 

  • Brink RA, Cooper DC (1947) The endosperm in seed development. Bot Rev 13:423–541

    Article  Google Scholar 

  • Chandler V, Stam M (2004) Chromatin conversations: mechanisms and implications of paramutation. Nat Rev Gen 5:532–544

    Article  CAS  Google Scholar 

  • Chinnusamy V, Gong Z, Zhu JK (2008) Abscisic acid-mediated epigenetic processes in plant development and stress responses. J Integr Plant Biol 50:1187–1195

    Article  CAS  PubMed  Google Scholar 

  • Costa LM, Gutièrrez-Marcos JF, Dickinson HG (2004) More than a yolk: the short life and complex times of the plant endosperm. Trends Plant Sci 9:507–514

    Article  CAS  PubMed  Google Scholar 

  • Drews GN, Lee D, Christensen CA (1998) Genetic analysis of female gametophyte development and function. Plant Cell 10:5–17

    Article  CAS  PubMed  Google Scholar 

  • Fransz PF, de Jong FH (2002) Chromatin dynamics in plants. Curr Opin Plant Biol 5:560–567

    Article  CAS  PubMed  Google Scholar 

  • Fu X, Harberd NP (2003) Auxin promotes Arabidopsis root growth by modulating gibberellin response. Nature 421:740–743

    Article  CAS  PubMed  Google Scholar 

  • Gao XH, Huang XZ, Xiao SL, Fu XD (2008) Evolutionarily conserved DELLA-mediated gibberellin signaling in plants. J Integr Plant Biol 50:825–834

    Article  CAS  PubMed  Google Scholar 

  • Goldberg RB, de Paiva G, Yadegari R (1994) Plant embryogenesis: zygote to seed. Science 266:605–614

    Article  CAS  PubMed  Google Scholar 

  • Grant-Downton R, Dickinson H (2004) Plants, pairing and phenotypes: two’s company? Trends Genet 20:188–195

    Article  CAS  PubMed  Google Scholar 

  • Groenewald JH, Botha FC (2008) Down-regulation of pyrophosphate: fructose 6-phosphate 1-phosphotransferase (PFP) activity in sugarcane enhances sucrose accumulation in immature internodes. Transgenic Res 17:85–92

    Article  CAS  PubMed  Google Scholar 

  • 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

    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. TAG 113:831–845

    Article  CAS  PubMed  Google Scholar 

  • Hämmerle B, Ferrus R (2003) Expression of enhancers is altered in Drosophila melanogaster hybrids. Evol Dev 5:221–230

    Article  PubMed  Google Scholar 

  • Henikoff S, Ahmad K (2005) Assembly of variant histones into chromatin. Annu Rev Cell Dev Biol 21:133–153

    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, Piepho H-P, Hochholdinger F (2005) Manifestation of heterosis during early maize (Zea mays L.) root development. TAG 12:421–429

    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 nonadditive gene expression and conserved expression trends. Genetics 179:1275–1283

    Article  CAS  PubMed  Google Scholar 

  • Hong SK, Kitano H, Satoh H, Nagato Y (1996) How is the embryo size genetically regulated in rice? Development 122:2051–2058

    CAS  PubMed  Google Scholar 

  • Huang Y, Zhang L, Zhang J, Yuan D, Xu C, Li X, Zhou D, Wang S, Zhang Q (2006) Heterosis and polymorphisms of gene expression in an elite rice hybrid as revealed by microarray analysis of 9198 unique ESTs. Plant Mol Biol 62:579–591

    Article  CAS  PubMed  Google Scholar 

  • Laux T, Jürgens G (1997) Embryogenesis: a new start in life. Plant Cell 9:989–1000

    Article  CAS  PubMed  Google Scholar 

  • Le Q, Gutiérrez-Marcos JF, Costa LM, Meyer S, Dickinson HG, Lörz H, Kranz E, Scholten S (2005) Construction and screening of subtracted cDNA libraries from limited populations of plant cells: a comparative analysis of gene expression between maize egg cells and central cells. Plant J 44:167–178

    Article  CAS  PubMed  Google Scholar 

  • Lin BY (1984) Ploidy barrier to endosperm development in maize. Genetics 107:103–115

    PubMed  Google Scholar 

  • Lopes MA, Larkins BA (1993) Endosperm origin, development, and function. Plant Cell 5:1383–1399

    Article  CAS  PubMed  Google Scholar 

  • Melchinger AE (1999) Genetic diversity and heterosis. In: International symposium on genetics and exploitation of heterosis in crop plants, Mexico City, 17–22 August 1997, pp 99–118

  • Mertens E (1991) Pyrophosphate-dependent phosphofructokinase, an anaerobic glycolytic enzyme? FEBS Lett 285:1–5

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Michalak P, Noor MAF (2003) Genome-wide patterns of expression in Drosophila pure species and hybrid males. Mol Biol Evol 20:1070–1076

    Article  CAS  PubMed  Google Scholar 

  • Okamoto T, Scholten S, Lörz H, Kranz E (2005) Identification of genes that are up- or down-regulated in the apical or basal cell of maize two-celled embryos and monitoring their expression during zygote development by a cell manipulation- and PCR-based approach. Plant Cell Physiol 46:332–833

    Article  CAS  PubMed  Google Scholar 

  • Olsen OA (1998) Endosperm development. Plant Cell 10:485–488

    Article  CAS  PubMed  Google Scholar 

  • Olsen OA (2001) Endosperm development: cellularization and cell fate specification. Annu Rev Plant Physiol Plant Mol Biol 52:233–267

    Article  CAS  PubMed  Google Scholar 

  • Olsen OA (2004) Nuclear endosperm development in cereals and Arabidopsis thaliana. Plant Cell 16:214–227

    Article  Google Scholar 

  • Pang SZ, DeBoer DL, Wan Y, Ye G, Layton JG, Neher MK, Armstrong CL, Fry JE, Hinchee MA, Fromm ME (1996) An improved green fluorescent protein gene as a vital marker in plants. Plant Physiol 112:893–900

    Article  CAS  PubMed  Google Scholar 

  • Peng J, Carol P, Richards DE, King KE, Cowling RJ, Murphy GP, Harberd NP (1997) The Arabidopsis GAI gene defines a signalling pathway that negatively regulates gibberellin response. Genes Dev 11:3194–3205

    Article  CAS  PubMed  Google Scholar 

  • Peng J, Richards DE, Hartley NM, Murphy GP, Devos KM, Flintham JE, Beales J, Fish LJ, Worland AJ, Pelica F, Sudhakar D, Christou P, Snape JW, Gale MD, Harberd NP (1999) ‘Green revolution’ genes encode mutant gibberellin response modulators. Nature 400:256–261

    Article  CAS  PubMed  Google Scholar 

  • Piepho H-P (2005) Optimal allocation in designs for assessing heterosis from cDNA gene expression data. Genetics 171:359–364

    Article  CAS  PubMed  Google Scholar 

  • Rhoades MM, Dempsey E (1966) Induction of chromosome doubling at meiosis by the elongate gene in maize. Genetics 54:505–522

    PubMed  Google Scholar 

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

  • Rood SB, Buzzell RI, Mander LN, Pearce D, Pharis RP (1988) Gibberellins: a phytohormonal basis for heterosis in maize. Science 241:1216–1218

    Article  CAS  PubMed  Google Scholar 

  • Russel SD (1992) Double fertilization. Int Rev Cytol 140:357–390

    Article  Google Scholar 

  • Sabelli PA, Larkins BA (2009) The development of endosperm in grasses. Plant Physiol 149:14–26

    Article  CAS  PubMed  Google Scholar 

  • Scott RJ, Spielman M, Bailey J et al (1998) Parent-of-origin effects on seed development in Arabidopsis thaliana. Development 125:3329–3341

    CAS  PubMed  Google Scholar 

  • Shull GH (1908) The composition of a field of maize. Proc Am Breeders Assoc 4:296–301

    Google Scholar 

  • Shull GH (1952) Beginning of the heterosis concept. In: Gowen JW (ed) Heterosis. Iowa State College Press, Ames, pp 14–48

    Google Scholar 

  • Smith OS, Smith JSC, Bowen SL, Tenborg RA, Wall SJ (1990) Similarities among a group of elite maize inbreds as measured by pedigree, F1 grain yield, heterosis, and RFLPs. TAG 80:833–840

    Google Scholar 

  • Song R, Messing J (2003) Gene expression of a gene family in maize based on noncollinear haplotypes. PNAS 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 

  • 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, Hermanson PJ, Springer NM (2007) Nonadditive expression and parent-of-origin effects identified by microarray and allele-specific expression profiling of maize endosperm. Plant Physiol 145:411–425

    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 8:33

    Article  PubMed  Google Scholar 

  • Swanson-Wagner RA, Jia Y, DeCook R, Borsuk LA, Nettelton 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. PNAS 103:6805–6810

    Article  CAS  PubMed  Google Scholar 

  • 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 Mol Biol 63:21–34

    Article  CAS  PubMed  Google Scholar 

  • Vuylsteke M, van Eeuwijk F, Van Hummelen P, Kuiper M, Zabeau M (2005) Genetic analysis of variation in gene expression in Arabidopsis thaliana. Genetics 171:1267–1275

    Article  CAS  PubMed  Google Scholar 

  • Wang FH (1947) Embryological development of inbred and hybrid Zea mays L. Am J Bot 34:113–125

    Article  Google Scholar 

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Acknowledgments

For providing seeds of the inbred lines used in this study we thank Prof. Dr. A. Melchinger (University of Hohenheim) and his co-workers. We thank T. Okamoto for allocating cDNAs of zygotes and two-celled embryos and André Schützenmeister for data processing for GEO submission. Furthermore we are especially grateful to Petra von Wiegen, Marlis Nissen and Sabina Miaskowska for excellent technical help with embryo and endosperm isolation and microarray hybridization. For assisting the glass house work we are thankful to Bärbel Hagemann. We thank Prof. Dr. Erhard Kranz and Prof. Dr. Horst Lörz for providing working space and support. This work was financially supported by the Deutsche Forschungsgemeinschaft (DFG) grant SCHO746/2 within the framework program “heterosis in plants” and by the Eiselen-Foundation (Ulm).

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Correspondence to Stefan Scholten.

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Communicated by T. Luebberstedt.

Contribution to the special issue “Heterosis in Plants”.

The microarray data of this study were deposited in Gene Expression Omnibus (GEO) at the National Centre for Biotechnology Information (NCBI) with the series entry GSE17754.

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Jahnke, S., Sarholz, B., Thiemann, A. et al. Heterosis in early seed development: a comparative study of F1 embryo and endosperm tissues 6 days after fertilization. Theor Appl Genet 120, 389–400 (2010). https://doi.org/10.1007/s00122-009-1207-y

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