Molecular mechanisms of polyploidy and hybrid vigor

doi:10.1016/j.tplants.2009.12.003

Trends in Plant Science

Volume 15, Issue 2, February 2010, Pages 57-71

https://doi.org/10.1016/j.tplants.2009.12.003 Get rights and content

Hybrids such as maize (Zea mays) or domestic dog (Canis lupus familiaris) grow bigger and stronger than their parents. This is also true for allopolyploids such as wheat (Triticum spp.) or frog (i.e. Xenopus and Silurana) that contain two or more sets of chromosomes from different species. The phenomenon, known as hybrid vigor or heterosis, was systematically characterized by Charles Darwin (1876). The rediscovery of heterosis in maize a century ago has revolutionized plant and animal breeding and production. Although genetic models for heterosis have been rigorously tested, the molecular bases remain elusive. Recent studies have determined the roles of nonadditive gene expression, small RNAs, and epigenetic regulation, including circadian-mediated metabolic pathways, in hybrid vigor, which could lead to better use and exploitation of the increased biomass and yield in hybrids and allopolyploids for food, feed, and biofuels.

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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Trends in Plant Science

ReviewFeature ReviewMolecular mechanisms of polyploidy and hybrid vigor

Section snippets

Polyploidy and hybrid vigor – a general view

Hybrids, allopolyploids, and hybrid vigor – a historical perspective

Modern view of hybrids, allopolyploids, and hybrid vigor

Genetic models for hybrid vigor

Nonadditive gene expression in the hybrids and allotetraploids

A molecular clock model for growth vigor in hybrids and allopolyploids

Roles for small RNAs in hybrid vigor and incompatibility in allotetraploids

Future perspectives

Acknowledgements

Glossary

Trends Ecol. Evolu.

Adv. Agron.

Curr. Biol.

Curr. Biol.

Dev. Cell

Cell

Trends Plant Sci.

The Effects of Cross- and Self-fertilization in the Vegetable Kingdom

The composition of a field of maize

Amer. Breeders Assoc. Rep.

Inbreeding in corn. In Reports of the Connecticut Agricultural Experiment Station for Years 1907–1908

Biotechnology in the 1930s: the development of hybrid maize

Nat. Rev. Genet.

90 years ago: the beginning of hybrid maize

Genetics

Progress in research and development on hybrid rice: a super-domesticate in China

Ann. Bot. (Lond.)

Polyploid hybrids of Raphanus sativus L. × Brassica oleracea L

Bull. Appl. Bot.

Interspecific hybridization in Nicotiana. II. a tetraploid GLUTINOSA-TABACUM hybrid, an experimental verification of Winge's hypothesis

Genetics

Chromosome number and morphology in Nicotiana VI: Chromosome numbers of forty species

Proc. Natl. Acad. Sci. U. S. A.

Cytogenetics of triticale

Bot. Rev.

Triticale: Today and Tomorrow

Hybridization as an invasion of the genome

Trends Ecol. Evol.

The frequency of polyploid speciation in vascular plants

Proc. Natl. Acad. Sci. U. S. A.

Stomatal size in fossil plants: evidence for polyploidy in majority of angiosperms

Science

Plant Speciation

Polyploidy in arctic plants

Biol. J. Linn. Soc.

Molecular investigations in populations of Spartina anglica C.E. Hubbard (Poaceae) invading coastal Brittany (France)

Mol. Ecol.

Origins, establishment and evolution of new polyploid species: Senecio cambrensis and S. eboracensis in the British Isles

Biol. J. Linn. Soc.

Genetics and geography of wild cereal domestication in the near east

Nat. Rev. Genet.

Chloroplast DNA indicates a single origin of the allotetraploid Arabidopsis suecica

J. Evol. Biol.

Genome plasticity a key factor in the success of polyploid wheat under domestication

Science

Heterosis of biomass production in Arabidopsis. Establishment during early development

Plant Physiol.

Heterosis in the freezing tolerance of crosses between two Arabidopsis thaliana accessions (Columbia-0 and C24) that show differences in non-acclimated and acclimated freezing tolerance

Plant J.

Natural allelic variation at seed size loci in relation to other life history traits of Arabidopsis thaliana

Proc. Natl. Acad. Sci. U. S. A.

Pleiotropic effects of the Arabidopsis cryptochrome 2 allelic variation underlie fruit trait-related QTL

Plant Biol. (Stuttg.)

A unique recent origin of the allotetraploid species Arabidopsis suecica: Evidence from nuclear DNA markers

Mol. Biol. Evol.

FISH analysis of meiosis in Arabidopsis allopolyploids

Chromosome Res.

The basis of natural and artificial postzygotic hybridization barriers in Arabidopsis species

Plant Cell

The genetic basis of inbreeding depression

Genet. Res.

Why polyploidy is rarer in animals than in plants

Amer. Nat.

‘Why polyploidy is rarer in animals than in plants’: myths and mechanisms

Biol. J. Linn. Soc.

The role of hybridization and introgression in the diversification of animals

Annu. Rev. Ecol. Syst.

Review
Feature Review
Molecular mechanisms of polyploidy and hybrid vigor