Theoretical and Applied Genetics

, Volume 120, Issue 2, pp 383–388 | Cite as

Molecular dissection of heterosis manifestation during early maize root development

  • Anja Paschold
  • Caroline Marcon
  • Nadine Hoecker
  • Frank Hochholdinger
Original Paper


Heterosis is of paramount agronomic importance and has been successfully exploited in maize hybrid breeding for decades. Nevertheless, the molecular basis of heterosis remains elusive. Heterosis is not only observed in adult traits like yield or plant height, but is already detected during embryo and seedling development. Hence, the maize (Zea mays L.) primary root which is the first organ that emerges after germination is a suitable model to study heterosis manifestation. Various seedling root traits including primary root length and lateral root density display heterosis. Microarray studies suggest organ specific patterns of nonadditive gene expression in maize hybrids. Moreover, such experiments support the notion that global expression trends in maize primary roots are conserved between different hybrids. Furthermore, nonadditive expression patterns of specific genes such as a SUPEROXIDE DISMUTASE 2 might contribute to the early manifestation of heterosis. Proteome profiling experiments of maize hybrid primary roots revealed nonadditive accumulation patterns that were distinct from the corresponding RNA profiles underscoring the importance of posttranscriptional processes such as protein modifications that might be related to heterosis. Finally, analysis of selected metabolites imply that a subtle regulation of particular biochemical pathways such as the phenylpropanoid pathway in hybrids might contribute to the manifestation of heterosis in maize primary roots. In the future, recently developed molecular tools will facilitate the analysis of the molecular principles underlying heterosis in maize roots.


  1. Andorf S, Gartner T, Steinfath M, Witucka-Wall H, Altmann T, Repsilber D (2009) Towards systems biology of heterosis: a hypothesis about molecular network structure applied for the Arabidopsis metabolome. EURASIP J Bioinform Syst Biol:147157Google Scholar
  2. Bi IV, McMullen MD, Sanchez-Villeda H, Schroeder S, Gardiner J, Polacco M, Soderlund C, Wing R, Fang Z, Coe EH (2006) Single nucleotide polymorphisms and insertion-deletions for genetic markers and anchoring the maize fingerprint contig physical map. Crop Sci 46:12–21CrossRefGoogle Scholar
  3. Brenner S, Johnson M, Bridgham J, Golda G, Lloyd DH, Johnson D, Luo SJ, McCurdy S, Foy M, Ewan M, Roth R, George D, Eletr S, Albrecht G, Vermaas E, Williams SR, Moon K, Burcham T, Pallas M, DuBridge RB, Kirchner J, Fearon K, Mao J, Corcoran K (2000) Gene expression analysis by massively parallel signature sequencing (MPSS) on microbead arrays. Nat Biotechnol 18:630–634CrossRefPubMedGoogle Scholar
  4. Brunner S, Fengler K, Morgante M, Tingey S, Rafalski A (2005) Evolution of DNA sequence nonhomologies among maize inbreds. Plant Cell 17:343–360CrossRefPubMedGoogle Scholar
  5. Candela H, Hake S (2008) The art and design of genetic screens: maize. Nat Rev Genet 9:192–203CrossRefPubMedGoogle Scholar
  6. Chang WWP, Huang L, Shen M, Webster C, Burlingame AL, Roberts JKM (2000) Patterns of protein synthesis and tolerance of anoxia in root tips of maize seedlings acclimated to a low-oxygen environment, and identification of proteins by mass spectrometry. Plant Physiol 122:295–317CrossRefPubMedGoogle Scholar
  7. Cokus SJ, Feng SH, Zhang XY, Chen ZG, Merriman B, Haudenschild CD, Pradhan S, Nelson SF, Pellegrini M, Jacobsen SE (2008) Shotgun bisulphite sequencing of the Arabidopsis genome reveals DNA methylation patterning. Nature 452:215–219CrossRefPubMedGoogle Scholar
  8. Dembinsky D, Woll K, Saleem M, Liu Y, Fu Y, Borsuk LA, Lamkemeyer T, Fladerer C, Madlung J, Barbazuk B, Nordheim A, Nettleton D, Schnable PS, Hochholdinger F (2007) Transcriptomic and proteomic analyses of pericycle cells of the maize primary root. Plant Physiol 145:575–588CrossRefPubMedGoogle Scholar
  9. Dixon RA, Achnine L, Kota P, Liu CJ, Reddy MSS, Wang LJ (2002) The phenylpropanoid pathway and plant defence—a genomics perspective. Mol Plant Pathol 3:371–390CrossRefPubMedGoogle Scholar
  10. Duvick DN (1999) Heterosis: feeding people and protecting natural resources. In: Coors JG, Pandey S (eds) The genetics and exploitation of heterosis in crops. American Society of Agronomy, Crop Science Society of America and Soil Science Society of America, pp 19–29Google Scholar
  11. Duvick DN (2001) Biotechnology in the 1930s: the development of hybrid maize. Nat Rev Genet 2:69–74CrossRefPubMedGoogle Scholar
  12. East EM (1908) Inbreeding in corn. Conn Agric Exp Stn 1907:419–428Google Scholar
  13. Ettenhuber C, Spielbauer G, Margl L, Hannah LC, Gierl A, Bacher A, Genschel U, Eisenreich W (2005) Changes in flux pattern of the central carbohydrate metabolism during kernel development in maize. Phytochemistry 66:2632–2642CrossRefPubMedGoogle Scholar
  14. Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Longman, HarlowGoogle Scholar
  15. Fu HH, Dooner HK (2002) Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci USA 99:9573–9578PubMedGoogle Scholar
  16. Guo M, Rupe MA, Danilevskaya ON, Yang XF, Hut ZH (2003) Genome-wide mRNA profiling reveals heterochronic allelic variation and a new imprinted gene in hybrid maize endosperm. Plant J 36:30–44CrossRefPubMedGoogle Scholar
  17. Guo M, Rupe MA, Zinselmeier C, Habben J, Bowen BA, Smith OS (2004) Allelic variation of gene expression in maize hybrids. Plant Cell 16:1707–1716CrossRefPubMedGoogle Scholar
  18. 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 113:831–845CrossRefPubMedGoogle Scholar
  19. Guo M, Yang S, Rupe M, Hu B, Bickel DR, Arthur L, Smith O (2008) Genome-wide allele-specific expression analysis using massively parallel signature sequencing (MPSS) reveals cis- and trans-effects on gene expression in maize hybrid meristem tissue. Plant Mol Biol 66:551–563CrossRefPubMedGoogle Scholar
  20. Haberer G, Young S, Bharti AK, Gundlach H, Raymond C, Fuks G, Butler E, Wing RA, Rounsley S, Birren B, Nusbaum C, Mayer KFX, Messing J (2005) Structure and architecture of the maize genome. Plant Physiol 139:1612–1624CrossRefPubMedGoogle Scholar
  21. Harbers M, Carninci P (2005) Tag-based approaches for transcriptome research and genome annotation. Nat Methods 2:495–502CrossRefPubMedGoogle Scholar
  22. Hochholdinger F, Hoecker N (2007) Towards the molecular basis of heterosis. Trends Plant Sci 12:427–432CrossRefPubMedGoogle Scholar
  23. Hochholdinger F, Guo L, Schnable PS (2004a) Lateral roots affect the proteome of the primary root of maize (Zea mays L.). Plant Mol Biol 56:397–412CrossRefPubMedGoogle Scholar
  24. Hochholdinger F, Park WJ, Sauer M, Woll K (2004b) From weeds to crops: genetic analysis of root development in cereals. Trends Plant Sci 9:42–48CrossRefPubMedGoogle Scholar
  25. Hochholdinger F, Woll K, Sauer M, Dembinsky D (2004c) Genetic dissection of root formation in maize (Zea mays L.) reveals root-type specific developmental programmes. Ann Bot 93:359–368CrossRefPubMedGoogle Scholar
  26. Hochholdinger F, Woll K, Guo L, Schnable PS (2005) The accumulation of abundant soluble proteins changes early in the development of the primary roots of maize (Zea mays L.). Proteomics 5:4885–4893CrossRefPubMedGoogle Scholar
  27. Hoecker N, Keller B, Piepho HP, Hochholdinger F (2006) Manifestation of heterosis during early maize (Zea mays L.) root development. Theor Appl Genet 112:421–429CrossRefPubMedGoogle Scholar
  28. Hoecker N, Keller B, Muthreich N, Chollet D, Descombes P, Piepho HP, Hochholdinger F (2008a) 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 179:1275–1283CrossRefPubMedGoogle Scholar
  29. Hoecker N, Lamkemeyer T, Sarholz B, Paschold A, Fladerer C, Madlung J, Wurster K, Stahl M, Piepho HP, Nordheim A, Hochholdinger F (2008b) Analysis of nonadditive protein accumulation in young primary roots of a maize (Zea mays L.) F1-hybrid compared to its parental inbred lines. Proteomics 8:3882–3894CrossRefPubMedGoogle Scholar
  30. Hollick JB (2008) Sensing the epigenome. Trends Plant Sci 13:398–404CrossRefPubMedGoogle Scholar
  31. Jones DF (1917) Dominance of linked factors as a means of accounting for heterosis. Genetics 2:466–479PubMedGoogle Scholar
  32. Kapranov P, Willingham AT, Gingeras TR (2007) Genome-wide transcription and the implications for genomic organization. Nat Rev Genet 8:413–423CrossRefPubMedGoogle Scholar
  33. Keller B, Emrich K, Hoecker N, Sauer M, Hochholdinger F, Piepho HP (2005) Designing a microarray experiment to estimate dominance in maize (Zea mays L.). Theor Appl Genet 111:57–64CrossRefPubMedGoogle Scholar
  34. Kempton JH, McLane JW (1942) Hybrid vigor aid weight of germs in the seeds of maize. J Agric Res 64:0065–0080Google Scholar
  35. Lamkey KR, Edwards JW (1998) Heterosis: theory and estimation.. Proceedings of the 34th Illinois Corn Breeders’ School, Urbana, pp 62–72Google Scholar
  36. Lippman ZB, Zamir D (2007) Heterosis: revisiting the magic. Trends Genet 23:60–66CrossRefPubMedGoogle Scholar
  37. Liu Y, Lamkemeyer T, Jakob A, Mi GH, Zhang FS, Nordheim A, Hochholdinger F (2006) Comparative proteome analyses of maize (Zea mays L.) primary roots prior to lateral root initiation reveal differential protein expression in the lateral root initiation mutant rum1. Proteomics 6:4300–4308CrossRefPubMedGoogle Scholar
  38. Mardis ER (2008) The impact of next-generation sequencing technology on genetics. Trends Genet 24:133–141PubMedGoogle Scholar
  39. Margulies M, Egholm M, Altman WE, Attiya S, Bader JS, Bemben LA, Berka J, Braverman MS, Chen YJ, Chen ZT, Dewell SB, Du L, Fierro JM, Gomes XV, Godwin BC, He W, Helgesen S, Ho CH, Irzyk GP, Jando SC, Alenquer MLI, Jarvie TP, Jirage KB, Kim JB, Knight JR, Lanza JR, Leamon JH, Lefkowitz SM, Lei M, Li J, Lohman KL, Lu H, Makhijani VB, McDade KE, McKenna MP, Myers EW, Nickerson E, Nobile JR, Plant R, Puc BP, Ronan MT, Roth GT, Sarkis GJ, Simons JF, Simpson JW, Srinivasan M, Tartaro KR, Tomasz A, Vogt KA, Volkmer GA, Wang SH, Wang Y, Weiner MP, Yu PG, Begley RF, Rothberg JM (2005) Genome sequencing in microfabricated high-density picolitre reactors. Nature 437:376–380PubMedGoogle Scholar
  40. 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 63:381–391CrossRefPubMedGoogle Scholar
  41. Morgante M, Brunner S, Pea G, Fengler K, Zuccolo A, Rafalski A (2005) Gene duplication and exon shuffling by helitron-like transposons generate intraspecies diversity in maize. Nat Genet 37:997–1002CrossRefPubMedGoogle Scholar
  42. Murdoch HA (1940) Hybrid vigor in maize embryos. J Hered 31:361–363Google Scholar
  43. Piepho HP, Keller B, Hoecker N, Hochholdinger F (2006) Combining signals from spotted cDNA microarrays obtained at different scanning intensities. Bioinformatics 22:802–807CrossRefPubMedGoogle Scholar
  44. Powers L (1945) Relative yields of inbred lines and F1-hybrids of tomato. Bot Gaz 106:247–268CrossRefGoogle Scholar
  45. Rose JKC, Bashir S, Giovannoni JJ, Jahn MM, Saravanan RS (2004) Tackling the plant proteome: practical approaches, hurdles and experimental tools. Plant J 39:715–733CrossRefPubMedGoogle Scholar
  46. Sauer M, Jakob A, Nordheim A, Hochholdinger F (2006) Proteomic analysis of shoot-borne root initiation in maize (Zea mays L.). Proteomics 6:2530–2541CrossRefPubMedGoogle Scholar
  47. Shull GF (1908) The composition of a field of maize. Am Breed Assoc Rep 4:296–301Google Scholar
  48. Song RT, Messing J (2003) Gene expression of a gene family in maize based on noncollinear haplotypes. Proc Natl Acad Sci USA 100:9055–9060CrossRefPubMedGoogle Scholar
  49. Spielbauer G, Margl L, Hannah LC, Romisch W, Ettenhuber C, Bacher A, Gierl A, Eisenreich W, Genschel U (2006) Robustness of central carbohydrate metabolism in developing maize kernels. Phytochemistry 67:1460–1475CrossRefPubMedGoogle Scholar
  50. Sprague GF (1936) Hybrid vigor and growth rates in a maize cross and its reciprocal. J Agricl Res 53:0819–0830Google Scholar
  51. Springer NM, Stupar RM (2007a) Allele-specific expression patterns reveal biases and embryo-specific parent-of-origin effects in hybrid maize. Plant Cell 19:2391–2402CrossRefPubMedGoogle Scholar
  52. Springer NM, Stupar RM (2007b) Allelic variation and heterosis in maize: how do two halves make more than a whole? Genome Res 17:264–275CrossRefPubMedGoogle Scholar
  53. Stuber CW (1999) Biochemistry, molecular biology and physiology of heterosis. In: Coors JG, Pandey S (eds) Genetics and exploitation of heterosis in crops. American Society of Agronomy, Crop Science Society of America, Madison, pp 173–184Google Scholar
  54. 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 173:2199–2210CrossRefPubMedGoogle Scholar
  55. 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 103:6805–6810CrossRefPubMedGoogle Scholar
  56. Uzarowska A, Keller B, Piepho HP, Schwarz G, Ingvardsen C, Wenzel G, Lubberstedt 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 63:21–34CrossRefPubMedGoogle Scholar
  57. Vega-Sanchez ME, Gowda M, Wang GL (2007) Tag-based approaches for deep transcriptome analysis in plants. Plant Sci 173:371–380CrossRefGoogle Scholar
  58. Velculescu VE, Zhang L, Vogelstein B, Kinzler KW (1995) Serial analysis of gene expression. Science 270:484–487CrossRefPubMedGoogle Scholar
  59. Wang FH (1947) Embryological development of inbred and hybrid Zea mays L. Am J Bot 34:113–125CrossRefGoogle Scholar
  60. Wang QH, Dooner HK (2006) Remarkable variation in maize genome structure inferred from haplotype diversity at the bz locus. Proc Natl Acad Sci USA 103:17644–17649CrossRefPubMedGoogle Scholar
  61. Wang ZK, Ni ZF, Wu HL, Nie XL, Sun QX (2006) Heterosis in root development and differential gene expression between hybrids and their parental inbreds in wheat (Triticum aestivum L.). Theor Appl Genet 113:1283–1294CrossRefPubMedGoogle Scholar
  62. Wen TJ, Hochholdinger F, Sauer M, Bruce W, Schnable PS (2005) The roothairless1 gene of maize encodes a homolog of sec3, which is involved in polar exocytosis. Plant Physiol 138:1637–1643CrossRefPubMedGoogle Scholar
  63. Woll K, Dressel A, Sakai H, Piepho HP, Hochholdinger F (2006) ZmGrp3: identification of a novel marker for root initiation in maize and development of a robust assay to quantify allele-specific contribution to gene expression in hybrids. Theor Appl Genet 113:1305–1315CrossRefPubMedGoogle Scholar

Copyright information

© Springer-Verlag 2009

Authors and Affiliations

  • Anja Paschold
    • 1
  • Caroline Marcon
    • 1
  • Nadine Hoecker
    • 1
  • Frank Hochholdinger
    • 1
  1. 1.Department of General Genetics, Center for Plant Molecular Biology (ZMBP)University of TuebingenTuebingenGermany

Personalised recommendations