Skip to main content
Log in

Heterosis in root development and differential gene expression between hybrids and their parental inbreds in wheat (Triticum aestivum L.)

  • Original Paper
  • Published:
Theoretical and Applied Genetics Aims and scope Submit manuscript

Abstract

In spite of commercial use of heterosis in agriculture, the molecular basis of heterosis is poorly understood. In this study, heterosis was estimated for eight root traits in 20 wheat hybrids derived from a NC Design II mating scheme. Positive mid-parent heterosis was detected in 96 of 160 hybrid–trait combinations, and positive high-parent heterosis was detected in 79 of 160 hybrid-trait combinations. Improved differential display was used to analyze alterations in gene expression between hybrids and their parents in roots at the jointing stage. More than 990 fragments were repeatedly displayed, among which 27.52% were differentially expressed between hybrids and their parents. Four differential expression patterns were observed. Thirty differentially expressed cDNA fragments and three genes with open reading frames were cloned, and their expression patterns were confirmed by reverse-northern blot and semi-quantitative RT-PCR analysis, respectively. We concluded that these differentially expressed genes, though mostly with unknown function, could play important roles for hybrids to demonstrate heterosis in root system traits.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aeschbacher RA, Schiefelbein KW, Benfey PN (1994) The genetic and molecular basis of root development. Annu Rev Plant Physiol Plant Mol Biol 45:25–45

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Broughton WT, Dilworth MJ (1971) Control of leghaemoglobin synthesis in snake beans. Biochem J 125:1075–1080

    PubMed  CAS  Google Scholar 

  • Brouwer R (1983) Functional equilibrium, sense or nonsense? Neth J Agric Sci 31:335–348

    Google Scholar 

  • Bruce AB (1910) The Mendelian theory of heredity and the augmentation of vigor. Science 32:627–628

    Article  PubMed  CAS  Google Scholar 

  • Carroll AD, Moyen C, Van Kesteren P, Tooke F, Battey NH, Brownlee C (1998) Ca, annexins, and GTP modulate exocytosis from maize root cap protoplasts. Plant Cell 10:1267–1276

    Article  PubMed  CAS  Google Scholar 

  • Chen NH, Yang JS, Gao YP, Xiao ML Qian M (1996) Differential display of mRNA between hybrid F1 and its parental inbred lines. Chin Sci Bull 41:939–943

    Google Scholar 

  • Chen NH, Gao YP, Yang JS, Qian M, Ge KL (1997) Alteration of gene expression in rice hybrid F1 and its parental seedlings. Acta Bot Sin 39:379–382

    Google Scholar 

  • Clark GB, Sessions A, Eastburn DJ, Roux SJ (2001) Differential expression of members of the annexin family in Arabidopsis. Plant Physiol 126:1072–1084

    Google Scholar 

  • Cook-Johnson RJ, Zhang Q, Wiskich JT, Soole KL (1999) The nuclear origin of the non-phosphorylating NADH dehydrogenases of plant mitochondria. FEBS Letters 454:37–41

    Article  PubMed  CAS  Google Scholar 

  • Davenport CB (1908) Degeneration, albinism and inbreeding. Science 28:454–455

    Article  PubMed  CAS  Google Scholar 

  • Diaz I, Vicente-Carbajosa J, Abraham Z, Martinez M, Moneda II-L, Carbonero P (2002) The GAMYB protein from barley interacts with the DOF transcription factor BPBF and activates endosperm-specific genes during seed development. Plant J 29(4):453–464

    Article  PubMed  CAS  Google Scholar 

  • Duvick DN (1997) Heterosis: feeding people and protecting natural resources. In: Coors JG, Pandey S (eds) Genetics and exploitation of heterosis in crops. American Society of Agronomy, Madison, pp 19–29

    Google Scholar 

  • East EM (1908) Inbreeding in corn. Reports of the Connecticut Agricultural Experiment Station for years 1907–1908, pp 419–428

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics, 4th edn. Prentice Hall, Harlow, UK

    Google Scholar 

  • Favery B, Ryan E, Foreman J, Linstead P, Boudonck K, Steer M, Shaw P, Dolan L (2001) KOJAK encodes a cellulose synthase-like protein required for root hair cell morphogenesis in Arabidosis. Genes Dev 15(1):79–89

    Article  PubMed  CAS  Google Scholar 

  • Fohse D, Claassen N, Jungk A (1988) Phosphorus efficiency of plants I: external and internal P requirement and P uptake efficiency of different plant species. Plant Soil 110:101–109

    Article  Google Scholar 

  • Frahm MA, Foster EF, Kelly JD (2003) Indirect screening techniques for drought resistance in dry bean. Annu Rep Bean Improv Coop 46:87–88

    Google Scholar 

  • Gaedeke N, Klein M, Kolukisaoglu U, Forestier C, Müller A, Ansorge M, Becker D, Mamnun Y, Kuchler K, Schulz B, Mueller-Roeber B, Martinoia E (2001) The Arabidopsis thaliana ABC transporter AtMRP5 controls root development and stomata movement. EMBO J 20(8):1875–1887

    Article  PubMed  CAS  Google Scholar 

  • Harris GA, Campbell GS (1989) Automated quantification of roots using a simple image analyzer. Agron J 81:935–938

    Article  Google Scholar 

  • Hauser MT, Morikami A, Benfey PN (1995) Conditional root expansion mutants of Arabidopsis. Development 121:1237–1252

    PubMed  CAS  Google Scholar 

  • Hua JP, Xing YZ, Wu WR, Xu CG, Sun XL, Yu SB, Zhang QF (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

    Article  PubMed  CAS  Google Scholar 

  • Jackson RB, Mooney HA, Schulze ED (1997) A global budget for fine root biomass, surface area and nutrient contents. Proc Natl Acad Sci USA 94:7362–7366

    Article  PubMed  CAS  Google Scholar 

  • von der Kammer H, Albrecht C, Mayhans M, Hoffman B, Stanke G, Nitsch RM (1999) Identification of genes regulated by muscarinic acetylcholine receptors: application of an improved and statistically comprehensive mRNA differential display technique. Nucleic Acids Res 27:2211–2218

    Article  PubMed  Google Scholar 

  • Keller B, Lamb CJ (1989) Specific expression of a novel cell-wall hydroxyproline-rich glycoprotein gene in lateral root initiation. Genes Dev 3:1639–1646

    PubMed  CAS  Google Scholar 

  • Kieliszewski ME, Lamport DTA (1994) Extensin: repetitive motifs, functional sites, post-translational codes, and phylogeny. Plant J 5:157–172

    Article  PubMed  CAS  Google Scholar 

  • Kovacs I, Ayaydin F, Oberschall A, Ipacs I, Bottka S, Dudits D, Toth EC (1998) Immunolocalization of a novel annexin-like protein encode by a stress and abscisic acid responsive gene in alfalfa. Plant J 15:185–197

    Article  PubMed  CAS  Google Scholar 

  • Leuchter R, Wolf K, Zimmermann M (1998) Isolation of an Arabidopsis cDNA complementing a Schizosaccharomyces pombe mutant deficient in phytochelatin synthesis. Plant Physiol 117:1526

    Google Scholar 

  • Li ZK, Luo LJ, Mei HW, Wang DL, Shu QY, Tabien R, Zhong DB, Ying CS, Stansel JW, Ghush WS, Paterson AH (2001) Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. I. Biomass and grain yield. Genetics 158:1737–1753

    CAS  Google Scholar 

  • Li YH, Qian Q, Zhou YH, Yan MX, Sun L, Zhang M, Fu ZM, Wang YH, Han B, Pang XM, Chen MS, Li JY (2003) BRITTLE CULM1, which encodes a COBRA-like protein, affects the mechanical properties of rice plants. Plant Cell 15:2020–2031

    Article  PubMed  CAS  Google Scholar 

  • Liu LX, Huang TC, Liu GT, Zhang SZ (1992) Stability analysis of yield and quality characters of hybrid and pureline winter wheat cultivars. Acta Agronomic Sin 181:38–49

    Google Scholar 

  • Luo LJ, Li ZK, Mei HW, Shu QY, Tabien R, Zhong DB, Ying CS, Stansel JW, Ghush WS, Paterson AH (2001) Overdominant epistatic loci are the primary genetic basis of inbreeding depression and heterosis in rice. II. Grain yield components. Genetics 158:1755–1771

    PubMed  CAS  Google Scholar 

  • Mena M, Vicente-Carbajosa J, Schmidt RJ, Carbonero P (1998) An endosperm-specific DOF protein from barley, highly conserved in wheat, binds to and cativates transcription from the prolamin-box of a native Bhordein promoter in barley endosperm. Plant J 16:53–62

    Article  PubMed  CAS  Google Scholar 

  • Mena M, Cejudo FJ, Isabel-Lamoneda I, Carbonero P (2002) A role for the DOF transcription factor BPBF in the regulation of gibberellin-responsive genes in barley aleurone. Plant Physiol 130:111–119

    Article  PubMed  CAS  Google Scholar 

  • Merkouropoulos G, Barnett DC, Shirsat AH (1999) The Arabidopsis extensin gene is developmentally regulated, is induced by wounding, methyl jasmonate, abscisic and salicylic acid, and codes for a protein with unusual motifs. Planta 208:212–219

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Perrin RM (2001) Cellulose:how many cellulose synthases to make a plant? Curr Biol 11(6):213–216

    Article  Google Scholar 

  • Plaumann M, Pelzer-Reith B, Martin WF, Schnarrenberger C (1997) Multiple recruitment of class-I aldolase to chloroplasts and eubacterial origin of eukaryotic class- II ldolases revealed by cDNAs from Euglena gracilis. Curr Genet 31:430–438

    Article  PubMed  CAS  Google Scholar 

  • Reiter Wolf-Dieter (1998) The molecular analysis of cell wall components. Trends Plant Sci 3 (1):27–32

    Article  Google Scholar 

  • Romagnoli S, Maddaloni M, Livini C, Motto M (1990) Relationship between gene expression and hybrid vigor in primary root tips of young maize Zea mays L. plantlets. Theor Appl Genet 80:767–775

    Article  Google Scholar 

  • Roudier F, Schindelman G, DeSalle R, Benfey PN (2002) The COBRA family of putative GPI-anchored proteins in Arabidopsis, a new fellowship in expansion. Plant Physiol 130:538–548

    Article  PubMed  CAS  Google Scholar 

  • Samad MA, Meisner CA, Rahman A, Rahman M, Duxbury JM, Lauren JG (2002) Wheat root growth in phosphorus depleted soils. In: Symposium of the 17th international soil science congress for August 2002, Thailand, pp. 14–21

  • SAS Institute (1999) SAS statistical package for Windows, v. 8.0. SAS Institute, Cary

  • Schiefelbein JW, Masucci JD, Wang H (1997) Building a root: the control of patterning and morphogenesis during root development. Plant Cell 9:1089–1098

    Article  PubMed  CAS  Google Scholar 

  • Schindelman G, Morikami A, Jung J, Baskin TI, Carpita NC, Derbyshire P, McCann MC, Benfey PN (2001) COBRA encodes a putative GPI-anchored protein, which is polarly localized and necessary for oriented cell expansion in Arabidopsis. Genes Dev 15:1115–1127

    Article  PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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 diallel cross. Plant Sci 166:651–657

    Article  CAS  Google Scholar 

  • Tam YY, Epstein E, Normanly J (2000) Characterization of auxin conjugates in Arabidopsis. Low steady-state levels of indole-3-acetylaspartate, indole-3-acetyl-glutamate, indole-3-acetyl-glucose. Plant Physiol 123:589–596

    Article  PubMed  CAS  Google Scholar 

  • Tsaftaris SA (1995) Molecular aspects of heterosis in plants. Physiol Plant 94:362–370

    Article  CAS  Google Scholar 

  • Tsaftaris SA, Kafka M (1998) Mechanisms of heterosis in crop plants. J Crop Prod 1:95–111

    Article  Google Scholar 

  • Wang ZK, Ni ZF, Meng FR, Wu LM, Xie XD, Sun QX (2003) Relationship between differential gene expression patterns in the root of jointing stage and heterosis in agronomic traits in a wheat diallel cross. Sci Agric Sin 365:473–479

    Google Scholar 

  • Wu LM, Ni ZF, Wang ZK, Lin Z, Sun QX (2001) Relationship between differential gene expression patterns of multigene families and heterosis in a wheat diallel crosses. Acta Genet Sin 28:256–266

    PubMed  CAS  Google Scholar 

  • Wu LM, Ni ZF, Meng FR, Lin Z, Sun QX (2003) Cloning and characterization of leaf cDNAs that are differentially expressed between wheat hybrids and their parents. Mol Genet Genomics 270:281–286

    Article  PubMed  CAS  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

    PubMed  CAS  Google Scholar 

  • Xiong LZ, Yang GP, Xu CG, Zhang QF, Maroof MAS (1998) Relationships of differential gene expression in leaves with heterosis and heterozygosity in a rice diallel cross. Mol Breed 4:129–136

    Article  CAS  Google Scholar 

  • Yabba MD, Foster EF (2003) Common bean root response to abscisic acid treatment. Annu Rep Bean Improv Coop 46:85–86

    Google Scholar 

  • Yanagisawa S (2002) The Dof family of plant transcription factors. Trends Plant Sci 7:555–560

    Article  PubMed  CAS  Google Scholar 

  • Yu S, Li JX, Xu CG, Tan YF, Gao YJ, Li XH, Zhang QF, Maroof MAS (1997) Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 94:9226–9231

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

Assistance from Prof. Zhang Fusuo (CAU) for root quantification is greatly appreciated. This work was financially supported by the State Key Basic Research and Development Plan of China (2001CB1088), National Science Fund for Distinguished Young Scholars (39925026) and National Natural Science Foundation of China (30270824).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Qixin Sun.

Additional information

Communicated by D. Mather

Z. Wang and Z. Ni contributed to this article equally.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wang, Z., Ni, Z., Wu, H. et al. Heterosis in root development and differential gene expression between hybrids and their parental inbreds in wheat (Triticum aestivum L.). Theor Appl Genet 113, 1283–1294 (2006). https://doi.org/10.1007/s00122-006-0382-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00122-006-0382-3

Keywords

Navigation