Trends in Plant Science
ReviewFeature ReviewMolecular mechanisms of polyploidy and hybrid vigor
Section snippets
Polyploidy and hybrid vigor – a general view
Hybrids and polyploids (whole genome duplication) occur in many plants and some animals. Hybrids are formed by hybridizing different strains, varieties, or species. Although heterosis or hybrid vigor is evolutionarily defined as that the heterozygotes have higher fitness in a population than the homozygotes, heterosis generally refers to superior levels of biomass, stature, growth rate, and/or fertility in the hybrid offspring than in the parents. The latter definition is adopted in this
Hybrids, allopolyploids, and hybrid vigor – a historical perspective
“I raised close together two large beds of self-fertilised and crossed seedlings from the same plant of Linaria vulgaris. To my surprise, the crossed plants when fully grown were plainly taller and more vigorous than the self-fertilised ones.” – Charles Darwin (The Effects of Cross and Self Fertilisation in the Vegetable Kingdom, 1876).
In his book [1], Charles Darwin systematically documented the growth, development, and seed fertility of cross-pollinated plants compared with that plants for
Modern view of hybrids, allopolyploids, and hybrid vigor
Humans have simply replicated a few examples of these remarkable natural processes that have produced many hybrid and polyploid plants not recorded in literature. Estimates indicate that ∼10% of animal and ∼25% of plant species hybridize with at least one other species [12]. A recent study estimates that 15% of angiosperm and 31% of fern speciation events are accompanied by an increase in ploidy [13]. The proportion of polyploid flowering plants might be 70% or more [14], and the majority
Genetic models for hybrid vigor
The genetic basis for hybrid vigor or heterosis has been debated for over a century, but little consensus has been reached. Several hypotheses including dominance, overdominance, and pseudo-overdominance are available to explain the phenomenon of hybrid vigor. According to the dominance model 60, 61, inbred parents contain inferior or deleterious alleles in several loci that inhibit overall good performance, whereas in the hybrids these inferior alleles in one parent are complemented by the
Nonadditive gene expression in the hybrids and allotetraploids
At gene expression levels, the dominance model suggests that the expression of genes in the hybrids is a result of combined or additive expression of two alleles in the parents (e.g. 1 + 1 = 2) (Figure 2d), whereas the overdominance model indicates that allelic interactions in the hybrids lead to nonadditive expression of the alleles derived from the parents (1 + 1 ≠ 2) (Figure 2e and f). If the interactions lead to positive effects or gene activation, the outcome is expected to be 1 + 1 >2. If the
A molecular clock model for growth vigor in hybrids and allopolyploids
At the molecular levels, both dominance and overdominance models suggest nonadditive expression of alleles in the hybrids relative to the parents. The dominant mode of gene expression represents one extreme: monoallelic expression in the hybrids, whereas overdominant mode of gene expression indicates another: biallelic expression in the hybrids at levels either higher than the high-parent value or lower than the low-parent value. Neither the dominance nor the overdominance model can explain the
Roles for small RNAs in hybrid vigor and incompatibility in allotetraploids
The above models suggest that epigenetic and transcriptional regulation of key regulatory genes leads to heterosis. Nonadditive gene expression is also controlled by post-transcriptional mechanisms via RNA-mediated pathways 108, 122. Small RNAs, including microRNAs (miRNAs) [123], small interfering RNAs (siRNAs) [124], and trans-acting siRNAs (tasiRNAs) 125, 126, mediate post-transcriptional regulation, RNA-directed DNA methylation, and chromatin remodeling. miRNAs are produced from genetic
Future perspectives
Heterosis or hybrid vigor results from genome-wide changes and interactions between paternal and maternal alleles. Heterozygosity is a prerequisite to changes in gene expression and phenotypic variation in hybrids and allopolyploids. The heterotic effects on gene expression changes in the hybrids can be augmented in polyploids (e.g. diploid versus tetraploid hybrids). Expression alteration of the genes that encode transcription factors and chromatin proteins is expected to cause cascade effects
Acknowledgements
I thank many former and current members, including but not limited to Hyeon-Se Lee, Jianlin Wang, Lu Tian, Zhongfu Ni, Meng Chen, Erika Lackey, Misook Ha, Eun-Deok Kim, Danny Ng, Changqing Zhang, Gyoungju Nah, Jie Lu, Marisa Miller, and Dae Kwan Ko, for their invaluable contributions to the research program. I am grateful to Edward Buckler and an anonymous reviewer for their insightful and constructive suggestions to improve the manuscript. I apologize for not citing additional relevant
Glossary
- Allelic expression variation
- the expression pattern or level of the alleles in the hybrids is different from that in the parents. This can also refer to the expression of homoeologous loci in interspecific hybrids.
- Allopolyploid
- an organism or individual that contains two or more sets of genetically distinct chromosomes, usually by hybridization between different species.
- Amphidiploid
- synonymous to allopolyploid. Contains a diploid set of chromosomes derived from each parent. Strictly speaking, only
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