Skip to main content

Abstract

Heterosis refers to improved or altered performance observed in F1 hybrid organisms when compared to their parents. Heterosis has revolutionized agriculture by improving key agronomic traits in crop plants. However, even after decades of research in this area a unifying molecular theory of heterosis remains somewhat elusive. For many years the dominant, overdominant, and epistasis models have prevailed for explaining multigenic heterosis. The use of whole transcriptome, proteome, metabolome, and epigenome profiling approaches can further generate and inform hypotheses regarding heterosis. This chapter reviews the models that have been used to explain heterosis. We also review the mechanistic basis of epigenetic pathways in plants and describe how they may also be considered in relation to understanding heterosis. There are number of findings that support potential links between epigenetic regulation and heterosis in model and crop plants, including the potential for DNA methylation, histone modification, and small RNAs to influence heterotic effects in F1 hybrids. Overall, we assess some opportunities and challenges for epigenetic research to advance the molecular understanding of heterosis.

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

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 139.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Hardcover Book
USD 179.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

References

  • Baranwal VK, Mikkilineni V, Zehr UB et al (2012) Heterosis: emerging ideas about hybrid vigour. J Exp Bot 63:6309–6314

    Article  CAS  PubMed  Google Scholar 

  • Barber WT, Zhang W, Win H et al (2012) Repeat associated small RNAs vary among parents and following hybridization in maize. Proc Natl Acad Sci USA 109:10444–10449

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bartel DP (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell 116:281–297

    Article  CAS  PubMed  Google Scholar 

  • Basunanda P, Radoev M, Ecke W et al (2010) Comparative mapping of quantitative trait loci involved in heterosis for seedling and yield traits in oilseed rape (Brassica napus L.). Theor Appl Genet 120:271–281

    Article  CAS  PubMed  Google Scholar 

  • Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    Article  CAS  PubMed  Google Scholar 

  • Berger SL (2007) The complex language of chromatin regulation during transcription. Nature 447:407–412

    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  PubMed Central  Google Scholar 

  • Birchler JA, Riddle NC, Auger DL et al (2005) Dosage balance in gene regulation: biological implications. Trends Genet 21:219–226

    Article  CAS  PubMed  Google Scholar 

  • Birchler JA, Yao H, Chudalayandi S et al (2010) Heterosis. Plant Cell 22:2105–2112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boutet S, Vazquez F, Liu J et al (2003) Arabidopsis HEN1: a genetic link between endogenous miRNA controlling development and siRNA controlling transgene silencing and virus resistance. Curr Biol 13:843–848

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burkart-Waco D, Ngo K, Dilkes B et al (2013) Early disruption of maternal–zygotic interaction and activation of defense-like responses in Arabidopsis interspecific crosses. Plant Cell 25:2037–2055

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burke JM, Arnold ML (2001) Genetics and the fitness of hybrids. Annu Rev Genet 35:31–52

    Article  CAS  PubMed  Google Scholar 

  • Calarco JP, Borges F, Donoghue MT et al (2012) Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151:194–205

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao X, Jacobsen SE (2002) Locus-specific control of asymmetric and CpNpG methylation by the DRM and CMT3 methyltransferase genes. Proc Natl Acad Sci USA 99:16491–16498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Castel SE, Martienssen RA (2013) RNA interference in the nucleus: roles for small RNAs in transcription, epigenetics and beyond. Nat Rev Genet 14:100–112

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

    Article  Google Scholar 

  • Charlesworth D, Willis JH (2009) The genetics of inbreeding depression. Nat Rev Genet 10:783–796

    Article  CAS  PubMed  Google Scholar 

  • Chen HM, Chen LT, Patel K et al (2010) 22-nuleotide RNAs trigger secondary siRNA biogenesis in plants. Proc Natl Acad Sci USA 107:15269–15274

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen ZJ (2010) Molecular mechanisms of polyploidy and hybrid vigor. Trends Plant Sci 15:57–71

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen ZJ (2013) Genomic and epigenetic insights into the molecular bases of heterosis. Nat Rev Genet 14:471–482

    Article  CAS  PubMed  Google Scholar 

  • Chodavarapu RK, Feng S, Ding B et al (2012) Transcriptome and methylome interactions in rice hybrids. Proc Natl Acad Sci USA 109:12040–12045

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crow JF (1952) Dominance and over-dominance. In: Gowen JW (ed) Heterosis. Iowa State College Press, Ames, pp 282–297

    Google Scholar 

  • Crow JF (1998) 90 years ago: the beginning of hybrid maize. Genetics 148:923–928

    CAS  PubMed  PubMed Central  Google Scholar 

  • Darwin CR (1876) The effects of cross- and self-fertilisation in the Vegetable Kingdom. John Murray, London

    Book  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Ding D, Wang YJ, Han MS et al (2012) MicroRNA transcriptomic analysis of heterosis during maize seed germination. PLoS One 7:e39578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dodd AN, Salathia N, Hall A et al (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633

    Article  CAS  PubMed  Google Scholar 

  • Duszynska D, Mckeown PC, Juenger TE et al (2013) Gamete fertility and ovule number variation in selfed reciprocal F1 hybrid triploid plants are heritable and display epigenetic parent-of-origin effects. New Phytol 198:71–78

    Article  PubMed  Google Scholar 

  • 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, Madison, pp 19–29

    Google Scholar 

  • Duvick DN (2001) Biotechnology in the 1930s: the development of hybrid maize. Nat Rev Genet 2:69–74

    Article  CAS  PubMed  Google Scholar 

  • East EM, Jones DF (1919) Inbreeding and outbreeding: their genetic and sociological significance. Lippincott, Philadelphia

    Book  Google Scholar 

  • Feng S, Jacobsen SE, Reik W (2010) Epigenetic reprogramming in plant and animal development. Science 330:622–627

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fu H, Dooner HK (2002) Intraspecific violation of genetic colinearity and its implications in maize. Proc Natl Acad Sci USA 99:9573–9578

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuchs J, Demidov D, Houben A et al (2006) Chromosomal histone modification patterns–from conservation to diversity. Trends Plant Sci 11:199–208

    Article  CAS  PubMed  Google Scholar 

  • Gendrel A-V, Lippman Z, Martienssen R et al (2005) Profiling histone modification patterns in plants using genomic tiling microarrays. Nat Methods 2:213–218

    Article  CAS  PubMed  Google Scholar 

  • Gernand D, Rutten T, Varshney A et al (2005) Uniparental chromosome elimination at mitosis and interphase in wheat and pearl millet crosses involves micronucleus formation, progressive heterochromatinization, and DNA fragmentation. Plant Cell 17:2431–2438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goff SA (2011) A unifying theory for general multigenic heterosis: energy efficiency, protein metabolism, and implications for molecular breeding. New Phytol 189:923–937

    Article  CAS  PubMed  Google Scholar 

  • Goff SA, Zhang Q (2013) Heterosis in elite hybrid rice: speculation on the genetic and biochemical mechanisms. Curr Opin Plant Biol 16:221–227

    Article  CAS  PubMed  Google Scholar 

  • Good R, Hallauer AR (1977) Inbreeding depression in maize by selfing and full-sibbing. Crop Sci 17:935–940

    Article  Google Scholar 

  • Greaves IK, Groszmann M, Ying H et al (2012) Trans chromosomal methylation in Arabidopsis hybrids. Proc Natl Acad Sci USA 109:3570–3575

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greaves IK, Groszmann M, Wang A et al (2014) Inheritance of trans chromosomal methylation patterns from Arabidopsis F1 hybrids. Proc Natl Acad Sci USA 111:2017–2022

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groszmann M, Greaves IK, Albertyn ZI et al (2011) Changes in 24-nt siRNA levels in Arabidopsis hybrids suggest an epigenetic contribution to hybrid vigor. Proc Natl Acad Sci USA 108:2617–2622

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Groszmann M, Greaves IK, Fujimoto R et al (2013) The role of epigenetics in hybrid vigour. Trends Genet 29:684–690

    Article  CAS  PubMed  Google Scholar 

  • Ha M, Lu J, Tian L et al (2009) Small RNAs serve as a genetic buffer against genomic shock in Arabidopsis interspecific hybrids and allopolyploids. Proc Natl Acad Sci USA 106:17835–17840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Han Z, Mtango NR, Patel BG et al (2008) Hybrid vigor and transgenerational epigenetic effects on early mouse embryo phenotype. Biol Reprod 79:638–648

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He G, Zhu X, Elling AA et al (2010) Global epigenetic and transcriptional trends among two rice subspecies and their reciprocal hybrids. Plant Cell 22:17–33

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • He G, He H, Deng XW (2013) Epigenetic variations in plant hybrids and their potential roles in heterosis. J Genet Genomics 40:205–210

    Article  CAS  PubMed  Google Scholar 

  • Hsieh T-F, Ibarra CA, Silva P et al (2009) Genome-wide demethylation of Arabidopsis endosperm. Science 324:1451–1454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hua J, Xing Y, Wu W et al (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  CAS  PubMed  PubMed Central  Google Scholar 

  • Hufford KM, Mazer SJ (2003) Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18:147–155

    Article  Google Scholar 

  • Jahnke S, Sarholz B, Thiemann A et al (2010) Heterosis in early seed development: a comparative study of F1 embryo and endosperm tissues 6 days after fertilization. Theor Appl Genet 120:389–400

    Article  PubMed  Google Scholar 

  • Jenuwein T, Allis CD (2001) Translating the histone code. Science 293:1074–1080

    Article  CAS  PubMed  Google Scholar 

  • Jones DF (1917) Dominance of linked factors as a means of accounting for heterosis. Genetics 2:466–479

    CAS  PubMed  PubMed Central  Google Scholar 

  • Kenan-Eichler M, Leshkowitz D, Tal L et al (2011) Wheat hybridization and polyploidization results in deregulation of small RNAs. Genetics 188:263–272

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kooter JM, Matzke MA, Meyer P (1999) Listening to the silent genes: transgene silencing, gene regulation and pathogen control. Trends Plant Sci 4:340–347

    Article  CAS  PubMed  Google Scholar 

  • Krieger U, Lippman ZB, Zamir D (2010) The flowering gene SINGLE FLOWER TRUSS drives heterosis for yield in tomato. Nat Genet 42:459–463

    Article  CAS  PubMed  Google Scholar 

  • Leamy L, Thorpe RS (1984) Morphometric studies in inbred and hybrid house mice. Heterosis, homeostasis and heritability of size and shape. Biol J Linn Soc Lond 22:233–241

    Article  Google Scholar 

  • Lewontin RC (1964) The interaction of selection and linkage. I. General considerations; heterotic models. Genetics 49:49–67

    CAS  PubMed  PubMed Central  Google Scholar 

  • Li W, Zhu H, Challa GS et al (2013) A non-additive interaction in a single locus causes a very short root phenotype in wheat. Theor Appl Genet 126:1189–1200

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Varala K, Moose SP et al (2012) The inheritance pattern of 24 nt siRNA clusters in arabidopsis hybrids Is influenced by proximity to transposable elements. PLoS One 7:e47043

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lippman Z, Gendrel A-V, Black M et al (2004) Role of transposable elements in heterochromatin and epigenetic control. Nature 430:471–476

    Article  CAS  PubMed  Google Scholar 

  • Lisch D, Carey CC, Dorweiler JE et al (2002) A mutation that prevents paramutation in maize also reverses Mutator transposon methylation and silencing. Proc Natl Acad Sci USA 99:6130–6135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mckeown PC, Spillane C (2014) Landscaping plant epigenetics. Methods Mol Biol 1112:1–24

    Google Scholar 

  • Mckeown PC, Fort A, Duszynska D et al (2013a) Emerging molecular mechanisms for biotechnological harnessing of heterosis in crops. Trends Biotechnol 31:549–551

    Article  CAS  PubMed  Google Scholar 

  • Mckeown PC, Keshavaiah C, Fort A et al (2013b) Genomics in agriculture and food processing. In: Panesar PS, Marwaha SS (eds) Biotechnology in agriculture and food processing: opportunities and challenges. CRC Press, Boca Raton, pp 45–70

    Chapter  Google Scholar 

  • Mendoza H, Haynes F (1974) Genetic basis of heterosis for yield in the autotetraploid potato. Theor Appl Genet 45:21–25

    Article  CAS  PubMed  Google Scholar 

  • Meyer RC, Kusterer B, Lisec J et al (2010) QTL analysis of early stage heterosis for biomass in Arabidopsis. Theor Appl Genet 120:227–237

    Article  PubMed  Google Scholar 

  • Miller M, Zhang C, Chen ZJ (2012) Ploidy and hybridity effects on growth vigor and gene expression in Arabidopsis thaliana hybrids and their parents. G3 (Bethesda) 2:505–513

    Article  CAS  Google Scholar 

  • Neufeld Arce RO (2006) Evaluation of heterosis and heterosis retention in Bos taurus-Bos indicus crossbred cattle for reproductive and maternal traits in cows. Dissertation, Texas A&M University

    Google Scholar 

  • Ni Z, Kim E-D, Ha M et al (2008) Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457:327–331

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Penterman J, Zilberman D, Huh JH et al (2007) DNA demethylation in the Arabidopsis genome. Proc Natl Acad Sci USA 104:6752–6757

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfluger J, Wagner D (2007) Histone modifications and dynamic regulation of genome accessibility in plants. Curr Opin Plant Biol 10:645–652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qi B, Huang W, Zhu B et al (2012) Global transgenerational gene expression dynamics in two newly synthesized allohexaploid wheat (Triticum aestivum) lines. BMC Biol 10:3

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Reed HS (1942) A short history of the plant sciences. Chronica Botanica, Waltham

    Google Scholar 

  • Rice J, Dudley J (1974) Gene effects responsible for inbreeding depression in autotetraploid maize. Crop Sci 14:390–393

    Article  Google Scholar 

  • Richards EJ (2006) Inherited epigenetic variation--revisiting soft inheritance. Nat Rev Genet 7:395–401

    Article  CAS  PubMed  Google Scholar 

  • Riedelsheimer C, Czedik-Eysenberg A, Grieder C et al (2012) Genomic and metabolic prediction of complex heterotic traits in hybrid maize. Nat Genet 44:217–220

    Article  CAS  PubMed  Google Scholar 

  • Schnable PS, Springer NM (2013) Progress toward understanding heterosis in crop plants. Annu Rev Plant Biol 64:71–88

    Article  CAS  PubMed  Google Scholar 

  • Schön C, Dhillon B, Utz HF et al (2010) High congruency of QTL positions for heterosis of grain yield in three crosses of maize. Theor Appl Genet 120:321–332

    Article  PubMed  Google Scholar 

  • Shen H, He H, Li J et al (2012) Genome-wide analysis of DNA methylation and gene expression changes in two Arabidopsis ecotypes and their reciprocal hybrids. Plant Cell 24:875–892

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shull GH (1908) The composition of a field of maize. J Hered 4:296–301

    Article  Google Scholar 

  • Simon SA, Meyers BC (2011) Small RNA-mediated epigenetic modifications in plants. Curr Opin Plant Biol 14:148–155

    Article  CAS  PubMed  Google Scholar 

  • Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8:272–285

    Article  CAS  PubMed  Google Scholar 

  • Slotkin RK, Vaughn M, Borges F et al (2009) Epigenetic reprogramming and small RNA silencing of transposable elements in pollen. Cell 136:461–472

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Smith LM, Bomblies K, Weigel D (2011) Complex evolutionary events at a tandem cluster of Arabidopsis thaliana genes resulting in a single-locus genetic incompatibility. PLoS Genet 7:e1002164

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Springer NM, Stupar RM (2007) Allele-specific expression patterns reveal biases and embryo-specific parent-of-origin effects in hybrid maize. Plant Cell 19:2391–2402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swanson-Wagner RA, Jia Y, Decook R et al (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  PubMed Central  Google Scholar 

  • Troyer AF (2006) Adaptedness and heterosis in corn and mule hybrids. Crop Sci 46:528–543

    Article  Google Scholar 

  • Vance V, Vaucheret H (2001) RNA silencing in plants--defense and counterdefense. Science 292:2277–2280

    Article  CAS  PubMed  Google Scholar 

  • Vaucheret H (2006) Post-transcriptional small RNA pathways in plants: mechanisms and regulations. Genes Dev 20:759–771

    Article  CAS  PubMed  Google Scholar 

  • Vilkaitis G, Plotnikova A, KlimaÅ¡auskas S (2010) Kinetic and functional analysis of the small RNA methyltransferase HEN1: the catalytic domain is essential for preferential modification of duplex RNA. RNA 16:1935–1942

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wallace J, Larsson S, Buckler E (2014) Entering the second century of maize quantitative genetics. Heredity 112:30–38

    Article  CAS  PubMed  Google Scholar 

  • Wang Z, Ni Z, Wu H et al (2006) Heterosis in root development and differential gene expression between hybrids and their parental inbreds in wheat (Triticum aestivum L.). Theor Appl Genet 113:1283–1294

    Article  CAS  PubMed  Google Scholar 

  • Waterhouse PM, Wang M-B, Lough T (2001) Gene silencing as an adaptive defence against viruses. Nature 411:834–842

    Article  CAS  PubMed  Google Scholar 

  • Williams W, Gilbert N (1960) Heterosis and the inheritance of yield in the tomato. Heredity 14:133–149

    Article  Google Scholar 

  • Yao H, Gray AD, Auger DL et al (2013) Genomic dosage effects on heterosis in triploid maize. Proc Natl Acad Sci USA 110:2665–2669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yu S, Li J, Xu C et al (1997) Importance of epistasis as the genetic basis of heterosis in an elite rice hybrid. Proc Natl Acad Sci USA 94:9226–9231

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao XX, Chai Y, Liu B (2007) Epigenetic inheritance and variation of DNA methylation level and pattern in maize intra-specific hybrids. Plant Sci 172:930–938

    Article  CAS  Google Scholar 

  • Zhu JK (2009) Active DNA demethylation mediated by DNA glycosylases. Annu Rev Genet 43:143–166

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Charles Spillane .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2019 Springer Nature Switzerland AG

About this chapter

Check for updates. Verify currency and authenticity via CrossMark

Cite this chapter

Ryder, P., McKeown, P.C., Fort, A., Spillane, C. (2019). Epigenetics and Heterosis in Crop Plants. In: Alvarez-Venegas, R., De-la-Peña, C., Casas-Mollano, J. (eds) Epigenetics in Plants of Agronomic Importance: Fundamentals and Applications. Springer, Cham. https://doi.org/10.1007/978-3-030-14760-0_4

Download citation

Publish with us

Policies and ethics