Crossing different plant varieties to improve yield and fertility is common practice. A dissection of the genomic architecture that underlies such hybrid vigour might help to inform future crop-improvement strategies. See Article p.629
The progeny of crosses between different varieties of a plant species usually exhibit greater biomass and fertility than either parent. This phenomenon, called heterosis or hybrid vigour, is capitalized on to produce superior yields for many crop species (Fig. 1), and so is crucial for global food security. However, the genomic and molecular basis of heterosis has long been elusive1. On page 629, Huang et al.2 map the genomic regions associated with yield traits in elite rice lines and examine the genomic architecture of heterosis — a tour de force study in the field.
Starting from 17 representative elite rice hybrid lines, the authors bred first and second generations to produce more than 10,000 hybrid rice lines, which they characterized for quantitative traits — most importantly, grain yield, flowering time and plant architecture. They also performed DNA sequencing for each line, to map the genomic regions associated with yield-related traits. They classified these lines into three main groups on the basis of hybrid-breeding strategies.
Huang et al. did not find any universally shared genomic regions that contribute to heterosis, but they did find several regions within each group that are associated with heterotic effects for grain-yield traits. Although the authors could not resolve these regions to individual genes or variants, they do highlight several candidate genes. Further work is needed to resolve the new genetic associations and confirm functions for these candidate genes in heterosis.
The genomic regions associated with heterotic effects behave largely as would be expected for quantitative traits. In general, mutations that regulate qualitative traits such as colour do not exert their effect on this trait unless the mutation is present in both copies of the gene — one inherited from each parent. In other words, a reduction in the amount of protein or RNA produced by a particular gene variant (owing to its presence as one instead of two copies) does not alter the characteristic that it affects. By contrast, the quantitative characteristics of progeny are often, to some degree, an intermediate of the parents.
If a quantitative trait in progeny is an exact intermediate between parents, the genetic variants regulating that trait are said to be additive. If the presence of one copy of a variant has no discernible effect in the hybrid, that gene is said to exhibit complete dominance (as with qualitative characteristics). The continuum between the two is referred to as partial negative or positive dominance — whereby traits are quantified, respectively, as having a lesser or greater effect in progeny than would occur in an exact intermediate between parents. In some cases, a characteristic of the progeny is superior to both parents: this is referred to as overdominance. Most of the genomic regions identified by Huang et al. exhibited partial positive dominance, with a set of variants in one region showing overdominance. Thus, the superior performance of the progeny plants compared with either parent can be explained by the collective effect of partial positive dominance across genomic regions that affect different traits.
A version3 of a popular, century-old4 theory of heterosis posits that parent strains, which are inbred and so tend to have two identical copies of most genes, often harbour slightly deleterious genetic variants. However, the mutations in each parent have no effect when each is present in only one copy in the hybrid. This effect is cumulative across many genes, leading to hybrid vigour. Although such complementation certainly does occur, this simple concept has long been known5 to provide an inadequate explanation for heterosis. The idea relies on complete dominance, and Huang et al. identified no genomic regions that exhibit this characteristic. Evidently, a more complicated process is in operation.
The partial dominance and overdominance seen by Huang et al. suggest that the quantity of proteins produced by the genes affects the plant's characteristics to some degree — a phenomenon called dosage sensitivity. It seems no coincidence that the candidate genes highlighted by the authors encode transcription factors, chromatin modifiers and related regulatory proteins, which are typically dosage sensitive6. Huang and colleagues' work adds to the evidence that there is a dosage-sensitive component to heterosis, as indicated by previous work in tobacco5, alfalfa7, tomato8, oil palm9 and maize (corn)10.
But despite this emerging pattern, the role of each candidate gene in improving plant performance is clearly also context dependent. For instance, the genomic regions identified by the authors as linked to heterosis were distinct in each of the three breeding groups. For example, a candidate gene identified in one group has a relative in tomato8 that has been implicated in heterosis; however, this gene does not show an involvement in hybrid vigour in the other rice groups studied. Perhaps what is observed as a difference in dominance under different circumstances actually reflects different points on a continuum of dosage sensitivity, in which the impact of any one gene product depends on interactions of the corresponding gene with other regulatory gene products and their targets11. Furthermore, the lack of strict additivity indicates that there is not a strong correlation between the amount of gene product and that product's effect on the plant's characteristics. Any attempt to manipulate heterosis for crop improvement would need to take this consideration into account.
Interestingly, the study found little indication of genomic regions that showed negative partial dominance or underdominance (in which a hybrid characteristic falls below the parental average). If the major genetic determinants of heterosis act in a context-dependent, dosage-sensitive manner, why does their action seem to be more often positive than negative? One possible explanation is that previous selection favoured lines that promote heterosis in hybrids. But it seems doubtful that such selection alone could explain the effect, given that hybrids between different, but related, species that have not been subjected to breeding regimes also tend to produce exuberant growth. Understanding this aspect of heterosis is an imperative, albeit challenging, future direction for the field.
Huang and colleagues' insights into heterosis, when followed up by studies to resolve the genes and functional variants involved, will give researchers the potential to contemplate manipulating hybrid vigour through molecular breeding, genetic engineering and gene editing. Specific modifications could be introduced and examined in different genetic backgrounds to attain the best performance. Manipulating the quantities of dosage-sensitive regulatory genes might be a path towards a directed mimicking of hybrid vigour12,13. However, with this idea comes the caveat that each case is likely to be context-dependent and to depend on relative stoichiometries among many regulatory gene products. Footnote 1
Chen, Z. J. Nature Rev. Genet. 14, 471–482 (2013).
Huang, X. et al. Nature 537, 629–633 (2016).
Schnable, P. S. & Springer, N. M. Annu. Rev. Plant Biol. 64, 71–88 (2013).
Jones, D. F. Genetics 2, 466–479 (1917).
East, E. M. Genetics 21, 375–397 (1936).
Birchler, J. A. & Veitia, R. A. Proc. Natl Acad. Sci. USA 109, 14746–14753 (2012).
Busbice, T. H. & Wilsie, C. P. Euphytica 15, 52–67 (1966).
Krieger, U., Lippman, Z. B. & Zamir, D. Nature Genet. 42, 459–463 (2010).
Singh, R. et al. Nature 500, 340–344 (2013).
Yao, H., Dogra Gray, A., Auger, D. L. & Birchler, J. A. Proc. Natl Acad. Sci. USA 110, 2665–2669 (2013).
Birchler, J. A., Johnson, A. F. & Veitia, R. A. Plant Sci. 245, 128–134 (2016).
Jiang, K. et al. PLoS Genet. 9, e1004043 (2013).
Park, S. J. et al. Nature Genet. 46, 1337–1342 (2014).
About this article
Journal of Integrative Plant Biology (2020)
Plant Biotechnology Journal (2020)
Interspecies hybrids of Panax ginseng Meyer new line 0837 and Panax quinquefolius generated superior F1 hybrids with greater biomass and ginsenoside contents
Horticulture, Environment, and Biotechnology (2019)
Reinventing heterosis phenomenon through deployment of alien introgression lines in rice ( Oryza sativa L.)
Plant Breeding (2019)