Article

Heterosis and inbreeding depression of epigenetic Arabidopsis hybrids

  • Nature Plants 1, Article number: 15092 (2015)
  • doi:10.1038/nplants.2015.92
  • Download Citation
Received:
Accepted:
Published online:

Abstract

We have addressed the possible epigenetic contribution to heterosis using epigenetic inbred lines (epiRILs) with varying levels and distributions of DNA methylation. One line consistently displayed parent-of-origin heterosis for growth-related traits. Genome-wide transcription profiling followed by a candidate gene approach revealed 33 genes with altered regulation in crosses of this line that could contribute to the observed heterosis. Although none of the candidate genes could explain hybrid vigour, we detected intriguing, hybrid-specific transcriptional regulation of the RPP5 gene, encoding a growth suppressor. RPP5 displayed intermediate transcript levels in heterotic hybrids; surprisingly however, with global loss of fitness of their F2 progeny, we observed striking under-representation of the hybrid-like intermediate levels. Thus, in addition to genetic factors contributing to heterosis, our results strongly suggest that epigenetic diversity and epigenetic regulation of transcription play a role in hybrid vigour and inbreeding depression, and also in the absence of parental genetic diversity.

  • Subscribe to Nature Plants for full access:

    $62

    Subscribe

Additional access options:

Already a subscriber?  Log in  now or  Register  for online access.

References

  1. 1.

    & Towards the molecular basis of heterosis. Trends Plant Sci. 12, 428–432 (2007).

  2. 2.

    The Effects of Cross and Self-fertilization in the Vegetable Kingdom (John Murray, 1876).

  3. 3.

    Heterosis. Genetics 21, 375–397 (1936).

  4. 4.

    , , , & Heterosis. Plant Cell Online 22, 2105–2112 (2010).

  5. 5.

    & Progress toward understanding heterosis in crop plants. Annu. Rev. Plant Biol. 64, 71–88 (2013).

  6. 6.

    et al. Altered circadian rhythms regulate growth vigour in hybrids and allopolyploids. Nature 457, 327–331 (2009).

  7. 7.

    , & Epigenetic variations in plant hybrids and their potential roles in heterosis. J. Genet. Genomics 40, 205–210 (2013).

  8. 8.

    , , , & Heterosis: emerging ideas about hybrid vigour. J. Exp. Bot. 63, 6309–6314 (2012).

  9. 9.

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

  10. 10.

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

  11. 11.

    et al. Trans chromosomal methylation in Arabidopsis hybrids. Proc. Natl Acad. Sci. USA 109, 3570–3575 (2012).

  12. 12.

    et al. Transcriptome and methylome interactions in rice hybrids. Proc. Natl Acad. Sci. USA 109, 12040–12045 (2012).

  13. 13.

    , , , & Extraordinary transgressive phenotypes of hybrid tomato are influenced by epigenetics and small silencing RNAs. EMBO J. 31, 257–266 (2012).

  14. 14.

    et al. Compromised stability of DNA methylation and transposon immobilization in mosaic Arabidopsis epigenomes. Genes Dev. 23, 939–950 (2009).

  15. 15.

    , & Maintenance of CpG methylation is essential for epigenetic inheritance during plant gametogenesis. Nature Genet. 34, 65–69 (2003).

  16. 16.

    , , , & Genetic interactions among late-flowering mutants of Arabidopsis. Genetics 148, 885–892 (1998).

  17. 17.

    et al. PHENOPSIS, an automated platform for reproducible phenotyping of plant responses to soil water deficit in Arabidopsis thaliana permitted the identification of an accession with low sensitivity to soil water deficit. New Phytol. 169, 623–635 (2006).

  18. 18.

    et al. Growth stage-based phenotypic analysis of Arabidopsis: a model for high throughput functional genomics in plants. Plant Cell 13, 1499–1510 (2001).

  19. 19.

    , , , & Separating parental environment from seed size effects on next generation growth and development in Arabidopsis. Plant Cell Environ. 34, 291–301 (2011).

  20. 20.

    et al. Increased leaf size: different means to an end. Plant Physiol. 153, 1261–1279 (2010).

  21. 21.

    & Induced instability of two Arabidopsis constitutive pathogen-response alleles. Proc. Natl Acad. Sci. USA 99, 7792–7796 (2002).

  22. 22.

    , & Epigenetic variation in Arabidopsis disease resistance. Genes Dev. 16, 171–182 (2002).

  23. 23.

    & Phenotypic instability of Arabidopsis alleles affecting a disease resistance gene cluster. BMC Plant Biol. 8, 36–46 (2008).

  24. 24.

    & A cluster of disease resistance genes in Arabidopsis is coordinately regulated by transcriptional activation and RNA silencing. Plant Cell. 19, 2929–2939 (2007).

  25. 25.

    & Gene duplication and hypermutation of the pathogen resistance gene SNC1 in the Arabidopsis bal variant. Genetics 183, 1227–1234 (2009).

  26. 26.

    et al. Patterns of population epigenomic diversity. Nature 495, 193–198 (2013).

  27. 27.

    , & A test for a metastable epigenetic component of heterosis using haploid induction in maize. Theor. Appl. Genet. 108, 1017–1023 (2004).

  28. 28.

    , , & Heterosis for biomass yield and related traits in five hybrids of Arabidopsis thaliana L. Heynh. Heredity 91, 36–42 (2003).

  29. 29.

    , , & Heterosis of biomass production in Arabidopsis. Establishment during early development 1. Plant Physiol. 134, 1813–1823 (2004).

  30. 30.

    et al. Selective epigenetic control of retrotransposition in Arabidopsis. Nature 461, 427–430 (2009).

  31. 31.

    et al. A role for CHH methylation in the parent-of-origin effect on altered circadian rhythms and biomass heterosis in Arabidopsis intraspecific hybrids. Plant Cell 1, 1–12 (2014).

  32. 32.

    et al. Heterosis manifestation during early Arabidopsis seedling development is characterized by intermediate gene expression and enhanced metabolic activity in the hybrids. Plant J. 71, 669–683 (2012).

  33. 33.

    et al. Energy use efficiency is characterized by an epigenetic component that can be directed through artificial selection to increase yield. Proc. Natl Acad. Sci. USA 106, 20109–20114 (2009).

  34. 34.

    Genomic and epigenetic insights into the molecular bases of heterosis. Nature Rev. Genet. 14, 471–482 (2013).

  35. 35.

    et al. Comparative transcriptional profiling and preliminary study on heterosis mechanism of super-hybrid rice. Mol. Plant 3, 1012–1025 (2010).

  36. 36.

    et al. Reprogramming of DNA methylation in pollen guides epigenetic inheritance via small RNA. Cell 151, 194–205 (2012).

  37. 37.

    et al. A structural-maintenance-of-chromosomes hinge domain-containing protein is required for RNA-directed DNA methylation. Nature Genet. 40, 670–675 (2008).

  38. 38.

    et al. MOM1 and Pol-IV/V interactions regulate the intensity and specificity of transcriptional gene silencing. EMBO J. 29, 340–351 (2010).

  39. 39.

    & Heat-induced release of epigenetic silencing reveals the concealed role of an imprinted plant gene. PLoS Genet. 10, e1004806 (2014).

Download references

Acknowledgements

We thank all members of the Paszkowski and the LEPSE laboratory, as well as Patrick Descombes for expression profiling assistance and P. King for editing the manuscript. This work was supported by EVOBREED ERC grant 322621 and Gatsby Fellowship AT3273/GLE.

Author information

Author notes

    • Jon Reinders
    •  & Etienne Bucher

    Present addresses: DuPont Pioneer, Johnston, Iowa, USA (J.R.); Université d'Angers, UMR1345 Institut de Recherche en Horticulture et Semences, Beaucouzé 49071, France (E.B.).

Affiliations

  1. Department of Plant Biology, University of Geneva, Sciences III, Geneva 4 CH-1211, Switzerland

    • Mélanie Dapp
    • , Jon Reinders
    • , Etienne Bucher
    • , Gregory Theiler
    •  & Jerzy Paszkowski
  2. LEPSE unit, Campus INRA/Montpellier SupAgro, Montpellier 34060, France

    • Alexis Bédiée
    • , Crispulo Balsera
    •  & Christine Granier
  3. The Sainsbury Laboratory, University of Cambridge, Cambridge CB2 1LR, UK

    • Jerzy Paszkowski

Authors

  1. Search for Mélanie Dapp in:

  2. Search for Jon Reinders in:

  3. Search for Alexis Bédiée in:

  4. Search for Crispulo Balsera in:

  5. Search for Etienne Bucher in:

  6. Search for Gregory Theiler in:

  7. Search for Christine Granier in:

  8. Search for Jerzy Paszkowski in:

Contributions

M.D., J.R. and J.P. designed the research, with the help of C.G. for the design of the phenotyping experimentations. M.D. performed the experiments, with the help of A.B., C.B. and C.G. for the phenotyping, G.T. for the statistical tests on phenotyping, and J.R. and E.B. for genome-wide annotation, expression and in silico DNA methylation analyses. M.D. and J.P. wrote the manuscript.

Competing interests

The authors declare no competing financial interests.

Corresponding author

Correspondence to Jerzy Paszkowski.

Supplementary information