Understanding the classics: the unifying concepts of transgressive segregation, inbreeding depression and heterosis and their central relevance for crop breeding

Abstract

Transgressive segregation and heterosis are the reasons that plant breeding works. Molecular explanations for both phenomena have been suggested and play a contributing role. However, it is often overlooked by molecular genetic researchers that transgressive segregation and heterosis are most simply explained by dispersion of favorable alleles. Therefore, advances in molecular biology will deliver the most impact on plant breeding when integrated with sources of heritable trait variation - and this will be best achieved within a quantitative genetics framework. An example of the power of quantitative approaches is the implementation of genomic selection, which has recently revolutionized animal breeding. Genomic selection is now being applied to both hybrid and inbred crops and is likely to be the major source of improvement in plant breeding practice over the next decade. Breeders' ability to efficiently apply genomic selection methodologies is due to recent technology advances in genotyping and sequencing. Furthermore, targeted integration of additional molecular data (such as gene expression, gene copy number and methylation status) into genomic prediction models may increase their performance. In this review, we discuss and contextualize a suite of established quantitative genetics themes relating to hybrid vigour, transgressive segregation and their central relevance to plant breeding, with the aim of informing crop researchers outside of the quantitative genetics discipline of their relevance and importance to crop improvement. Better understanding between molecular and quantitative disciplines will increase the potential for further improvements in plant breeding methodologies and so help underpin future food security.

Keywords: crop breeding; crop genetics and genomics; genomic selection; heterosis; heterotic groups; hybrid vigour; molecular genetics; quantitative genetics; transgressive segregation.

Figure 1

Two sides of the same coin: transgressive segregation and heterosis. (a) The increase in wheat yields in the United Kingdom from 1885 to 2015. Data are taken from the UK Government Web Archive http://www.nationalarchives.gov.uk/webarchive/. (b) Schematic illustrating transgressive segregation in a cross between two elite lines: segregation among progeny (individuals or lines), some of which fall outside the range of trait value for the two parents. (c) Schematic illustrating a simple model for transgressive segregation. The letters a, A, b and B indicate alleles at two loci. Upper case letters increase the value of the trait, lower case letters decrease it. If the increasing alleles are dispersed among the parents of a cross, then segregating progeny can be found which have a higher or lower trait value than the parents. (d) Transgressive segregation for an exemplar trait, seed width, in the ‘NIAB Elite MAGIC wheat’ population (n founders = 8, n progeny = 643, Mackay et al., 2014). Founder trait values are indicated: A = Alchemy, B = Brompton, C = Claire, H = Hereward, Ri = Rialto, Ro = Robigus, S = Soissons, X = Xi19). (e) A simple model for heterosis. The letters a, A, b and B indicate alleles at two loci. Upper case letters are partially dominant. The contribution of each single locus genotype to the trait is AA = BB = 1, Aa = Bb = 0.75, aa = bb = 0. The increasing alleles are dispersed among the parents of a cross. The F₁ therefore has a higher value than either parent.

Figure 2

Comparison of heterosis in diploid (2n) and tetraploid (4n) inbred crops, and an explanation for progressive heterosis based on dispersion of dominant alleles. (a) Illustration of progressive heterosis where four inbred tetraploid lines (A, B, C, D) are crossed in pairs (AxB and CxD), and the resulting hybrids (E and F) subsequently crossed with each other to create double‐cross hybrids (G) that show greater heterosis on average than either of the single‐cross hybrids. (b) Possible genotypes at a single locus with two alleles in a diploid and tetraploid. (c) Illustration of progressive heterosis (PH) in a diploid and a tetraploid, based on four alleles, A1 A2 a3 a4 where Ax is partially dominant to ay.