Paternity matters in polyploid plants

In the most basic definition, polyploidy is a numerical increase in whole chromosome number. The effects of this increase in genomic material often produce novel morphologies compared to parental species, and polyploids have become both a huge part of explaining the evolutionary history of biological diversity and a crucial aspect of agriculture.
However, polyploids are clearly not the result of simple math. Those genomes might be duplicates of one another or from two different species. There might be an odd number of genomes where one parental species dominates the other. There might be differing ploidy depending on tissue type.
The conflict between how many genomes an organism has (polyploidy) and where each of those genomes came from (hybridity) is a large confounding factor when trying to understand what genetic characteristics are most responsible a given phenotype. If you observe a difference in biomass between a diploid plant and an triploid plant hybrid, is that difference due to the extra genome, the heterozygosity contributed by the two parental genomes, or some combination of both?
A recent study by Fort et al. appearing in New Phytologist attempts to cleverly tease apart these factors. First, the authors acquired isogenic varieties of Arabidopsis that were either diploid and tetraploid. These plants were crossed and separated into those that were triploid with an additional paternal genome [3x(p)] or triploid with an additional maternal genome [3x(m)], producing a gradient of groups from 2N-4N that all have the same genetic background except for which parental donated a genome to the triploids. Second, the authors did the same with crosses between different genetic backgrounds, creating gradients of 2N-4N individuals with increased heterozygosity due to having divergent parents.
The authors show that the triploid plants with an additional paternal genome had the greatest increase in plant size when compared to diploids. The truly fascinating aspect of this result is that it didn’t matter whether those 3x(p) individuals were isogenic or hybrids.

Strikingly, our data indicate that paternal genome dosage increases in isogenic F1 triploid plants trigger positive heterosis outcomes, whereas maternal genome dosage increases in isogenic F1 triploid plants trigger negative heterosis outcomes. When paternal genome dosage is increased in an F1 hybrid context, the paternal genome dosage effect can act as an enhancer of hybridity-associated heterosis.

Plant size can be the result of multiple growth characteristics, and the authors indicate that increased seed size is mainly responsible for increased plant size, not growth rate. Hybrid individuals showed increased growth rates compared to diploids, but only early in development.

Figure 5 from Fort et al.

Figure 5 from Fort et al. (2015) that demonstrated the positive (black arrows), negative (gray arrows), and unknown (question marks) relationships between genome dosage and hybridity on phenotype.

The conclusion here is that genome dosage matters, even independent of the hybrid status of the genomes that make up a polyploid. However, the parental status of extra genomes produces different effects even when both parents are genetically similar, indicating that epigenetic effects are yet another layer to untangle among the complexity of polyploid genetics.
Fort, A., Ryder, P., McKeown, P. C., Wijnen, C., Aarts, M. G., Sulpice, R., & Spillane, C. (2015). Disaggregating polyploidy, parental genome dosage and hybridity contributions to heterosis in Arabidopsis thaliana. New PhytologistDOI: 10.1111/nph.13650

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