When is polyploidy useful

The masking of deleterious alleles, that may arise from induced mutation, by their dominant forms cushions polyploids from lethal conditions often associated with inbred diploid crops Gaul, This concept has been instrumental in the evolution of polyploids during bottlenecks where there is enforced inbreeding Comai, Mutation breeding exploits the concept of gene redundancy and mutation tolerance in polyploid crop improvement in two ways.

First, polyploids are able to tolerate deleterious allele modifications post-mutation, and secondly, they have increased mutation frequency because of their large genomes resulting from duplicated condition of their genes Gaul, The high mutation frequencies observed with polyploids may be exploited when trying to induce mutations in diploid cultivars that do not produce enough genetic variation after a mutagenic treatment.

This approach has been used in mutation breeding of Achimenes sp. In this study, the autotetraploids were found to have times higher mutation frequency than the corresponding diploid cultivar due to the large genome Broertjes, The seedless trait of triploids has been desirable especially in fruits.

Commercial use of triploid fruits can be found in crops such as watermelons and are produced artificially by first developing tetraploids which are then crossed with diploid watermelon. In order to set fruit, the triploid watermelon is crossed with a desirable diploid pollen donor. Another breeding strategy that utilizes the reproductive superiority of polyploids is bridge crossing. When sexual incompatibilities between two species are due to ploidy levels, transitional crosses can be carried out followed by chromosome doubling to produce fertile bridge hybrids.

This method has been used to breed for superior tall fescue grass F. The same principle has been applied in fixing heterozygosity in hybrids by doubling the chromosomes in the superior progeny Comai, One of the immediate and obvious consequences of polyploidy in plants is an increase in cell size which in turn leads to enlarged plant organs, a phenomenon termed gigas effect Fig 5.

For example, the volume of tetraploid cells usually is about twice that of their diploid progenitors Acquaah, ; Emsweller and Ruttle, ; Levin, ; Schepper et al. The increase in cell volume however is mainly attributed to increased water and not biomass. Therefore, its application is limited for breeding agronomically important crops such as cereals. Although chromosome doubling may result in significantly larger seeds and increased seed-protein content in cereal crops, this advantage is offset by low seed set Dhawan and Lavania, In contrast, the gigas effect has been explored in tree, ornamental, forage crop and fruit breeding Emsweller and Ruttle, ; Schepper et al.

For example, through induced polyploidy, breeders have developed Bouschet tetraploid grapes with more yield and juice content than the diploid progenitor Alicante Olmo, Ornamental crops such as snapdragons and marigolds have been bred through chromosome doubling to improve the quality and size of their blossoms Emsweller and Ruttle, A strong inverse correlation between DNA content and development rates in plants has been reported by several authors Levin, ; Smith and Bennett, It has been attributed to lower auxin levels, reduced surface to volume ratio and altered nuclear surface to cell volume ratio Acquaah, ; Levin, The slower growth rate of polyploids allows them to flower later and for a longer period of time than their diploid progenitors Levin, This quality may be of interest especially in ornamental breeding.

Apomixis provides another avenue for use of polyploids in breeding. Apomixis provides an avenue for the production of seeds asexually through parthenogenesis. Most apomictic plants are polyploid but most polyploid plants are not apomictic Otto and Whitton, In plants capable of both sexual and asexual reproduction, polyploidy promotes the latter Dhawan and Lavania, ; Levin, Obligate apomicts are the most desired of hybrids but little gain has been realized towards their development.

However, it has been suggested that obligate apomicts may be induced through development of very high ploidy plants Levin, An example of an obligate apomict achieved at high ploidy level is the octoploid of the grass, Themeda triandra Levin, Aneuploidy has been applied in breeding to develop disease resistant plants through the addition of an extra chromosome into the progeny genome. An example is the transfer of leaf rust resistance to Tricum aestivum from Aegilops umbellulata through backcrossing.

In addition, other breeding strategies utilizing aneuploidy have been explored including chromosome deletion, chromosome substitution and supernumerary chromosomes Acquaah, Chromosome doubling is reported to have an apparent effect on many physiological properties of a plant.

The most discernable of these has been the increase in secondary as well as primary metabolism Levin, In vitro secondary metabolite production systems that exploit polyploidism have also been developed. The production of the antimalarial sesquiterpene artemisinin has been enhanced six fold by inducing tetraploids of the wild diploid Artemisia annua L. In addition, commercial synthesis of sex hormones and corticosteroids has been improved significantly by artificial induction of tetraploids from diploid Dioscorea zingiberensis , native to China Heping et al.

Attempts have been made to improve the production of pyrethrin, a botanical insecticide, by chromosome doubling of Chrysanthemum cinerariifolium Liu and Gao, Other plants whose production of terpenes has increased following artificial chromosome doubling include Carum cari, Ocimum kilmandscharicum and Mentha arvensis Bose and Choudhury, ; Levin, The enhanced production of secondary metabolites such as alkaloids and terpenes in polyploids may concurrently offer resistance to pests and pathogens.

Similar results were observed while comparing resistance to insects and the clover eel nematode between Trifolium pratense red clover tetraploids and diploids Mehta and Swaminathan, Andrus C. Bellostas N. Journal of the Science of Food and Agriculture Bingham E.

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Publication types Research Support, Non-U. Gov't Review. It is considered an ecosystem engineer that expands its habitat by enhancing sediment accretion Boumat et al. Spartina anglica has deliberately been introduced in several parts of the world, where it rapidly expanded, and is listed as one of the IUCN's worst invasive alien species Lowe et al.

Spartina anglica represents an excellent model system for investigating the immediate consequences of hybridization and genome duplication when it comes to ecological success and invasiveness, being of recent origin, with all parental species still extant, and with historical records that track the timing of events.

Molecular studies show low genetic diversity in the species, suggesting that S. The genetic diversity of the species relies mainly on the subsequent dynamics of its hybrid genome Ainouche et al. Hybridization appears to have triggered both genetic and epigenetic changes in the homoploid hybrid S.

This leads to the suggestion that the most important genetic and epigenetic changes in the genome of the S. However, considerable changes to the transcriptome have also accompanied the formation of both S. These changes most probably explain the phenotypic plasticity and other morphological and physiological traits Thompson, that characterize S. The extensive and rapid spread both through seed production and via vegetative means of the fertile allopolyploid S. We have described several examples of how intra- and interspecific genome duplication may enhance the success of introduced plant species and provided a mechanistic explanation of how polyploidy may affect invasiveness see Figs 1 and 2.

On the one hand, the direct effects of polyploidization might predispose species to be better adapted to harsher conditions in novel environments. This flexibility might also counteract the reduced fertility that is often found in polyploids. Moreover, when a polyploid is introduced into a new environment in the absence of the diploid progenitor, one of its main challenges, i.

Several consequences of genome duplication, such as lower growth rates or larger seed mass, may also clearly reduce invasiveness. However, these traits are not necessarily disadvantageous to plants in general. This raises the question of how to quantify the success of an invasive plant. Should this be related to abundance or to the extent of its geographic range?

The life history attributes usually associated with polyploids suggest that polyploidy often favours successful establishment and subsequent persistence, rather than the achievement of the high local densities that are often associated with successful invasive species and that lead to negative impacts on biodiversity and ecosystem services Parker et al.

Therefore, it is likely that polyploid plants have a higher chance of becoming naturalized, but not necessarily invasive. There are also many examples of polyploid invaders that can become extremely dominant. For example, among woody plants: Ailanthus altissima , Chromolaena odorata , Cytisus scoparius , Fallopia japonica , Lantana camara , Leucaena leucocephala , Psidium cattleianum , Rosa rubiginosa , Salix fragilis , Schinus terebinthifolius and Ulex europaeus are all major transformer species sensu Richardson et al.

Among the many herbaceous polyploids that can qualify as transformer species, S. It has been proposed that broad ecological tolerance may predispose polyploid lineages to successful colonization in novel environments, i. Even though this hypothesis remains controversial Soltis et al. For example, the invasion success of tetraploid Centaurea stoebe in North America has been partly attributed to pre-adaptation of native European tetraploids to wider climate ranges compared with diploids and, following the initial introduction, tetraploids may have further adapted to drier continental conditions Treier et al.

Similarly, introductions of pre-adapted highland tetraploids from southern Africa that are more cold tolerant than lowland diploid populations have been suggested as an explanation for the invasion success of Senecio inaequidens in Europe Lafuma et al. Other examples include the invasion of tetraploid Rubus alceifolius on islands in the Indian Ocean Amsellem et al. These examples are all characterized by the dominance or sole occurrence of one invasive polyploid cytotype.

In addition to the explanation that the polyploid lineage is pre-adapted and therefore more successful in the new habitat than diploid lineages, there are several other explanations for this phenomenon. Strong founder effects may favour the cytotype with the most effective reproduction and, hence, highest fitness, and cause shifts in cytotype frequency or even exclusion of other cytotypes Kliber and Eckert, ; Bakker et al.

Alternatively, different introduction pathways could also influence the presence of one or more ploidal levels in the new range. For example, a single introduction of a species might by chance cause a polyploid to establish, whereas in the case of multiple introductions the mixing of cytotypes could be expected.

Accidental or deliberate introductions also play an important role. Deliberate introductions of crops and ornamental plants have been recognized as a major pathway of plant invasions Dehnen-Schmutz et al. Ploidy manipulation triploid production has also been proposed to produce sterile, non-invasive cultivars in invasive ornamental plants, such as Lantana camara Czarnecki and Deng, It is generally accepted that the stochasticity typically associated with biological invasions will greatly influence the pace of contemporary evolution, i.

Clear evidence for rapid evolutionary change in invasive plants has been repeatedly found when intraspecific hybridization admixture between previously allopatric lineages occurs in the invasive range s e. Hurka et al. Admixed individuals often show broader ecological tolerance, increased levels of phenotypic plasticity and increased vigour compared with parental lineages.

It is therefore not surprising that allopolyploids show similar but more pronounced changes, combining the complete genomes of two divergent species. The link between invasiveness and autopolyploidization is less clear. However, given that numerous genomic processes are profoundly influenced by genome doubling, it is conceivable that autopolyploidy can contribute to invasion success e. It is, however, important to distinguish the immediate evolutionary effects of polyploidy from effects that arose following polyploidization Soltis et al.

Recently, Ramsey reported on historical and contemporary evolutionary effects of polyploidization using field transplants of tetraploid and hexaploid Achillea borealis with a parallel experiment on neohexaploids — first-generation autopolyploid mutants. The use of neohexaploid cytotypes provides a direct measure of the phenotypic effects of genome duplication per se , whereas the comparison of neopolyploids with established polyploids reveals post-polyploidization evolution such as allele substitutions and gene silencing.

These results suggest that genome duplication can immediately facilitate ecological differentiation in plants. Insights from studies on neopolyploids are otherwise limited e. Bretagnolle and Lumerat, ; Husband et al. This observation of greater polyploid survival generates two questions that are essential for our understanding of the role of polyploidy in species success. We hope to have made clear in this review that due to lower growth rates, higher seed mass, increased drought and temperature tolerance, flexible breeding behaviour, etc.

Further evidence for this comes from the observation that the production of unreduced gametes increases with increasing environmental stress, e. This suggests that natural environmental variation, as well as large-scale climate change, could substantially alter the dynamics of polyploid evolution and subsequent species success.

Unfortunately, however, data on unreduced gamete formation in natural systems are few Ramsey and Schemske, Various approaches have been used to address the question of whether polyploidy mediates ecological differentiation, adaptation and, ultimately, range expansion. Observational studies that describe the distribution of and habitat differentiation between different ploidal levels within a single species or between closely related species e.

Baldwin, ; Lumaret et al. Large-scale correlative studies comparing the flora of certain regions Stebbins, ; Brochmann et al. Ultimately, experimental studies of diploid—polyploid systems, such as field transplant e.

However, relatively few experimental studies have been undertaken considering the amount of efforts that have been put into polyploidy research in recent years.

Many more studies, especially combining observations and experimentation, are needed in the years to come to test rigorously the hypothesis that polyploidy provides plants with novel features that allow them to invade new environments or expand their geographic range.

Alternatively, polyploidization may play an important role by restoring sexual reproduction after hybridization, as, for example, in Spartina anglica or, conversely, allowing for asexual reproduction in the absence of suitable mates, as, for example, in Oxalis pes-caprae. We have shown that polyploidy might be an important factor in species invasion success and suggest that ploidy must be considered in any general model that seeks to explain why some species are more successful than others as invaders.

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Volume Article Contents Abstract. The more the better? The role of polyploidy in facilitating plant invasions. E-mail mariskatebeest hotmail.

Oxford Academic. Johannes J. Le Roux. David M. Anne K. Jan Suda. Revision requested:. Select Format Select format. Permissions Icon Permissions. Abstract Background. Biological invasions , genome size , invasiveness , invasion ecology , polyploidy , whole genome duplication.

Box 1. Methods for determining ploidal levels. Open in new tab Download slide. Table 1. Native range. Introduced range. Reference s. Open in new tab. Google Scholar Crossref. Search ADS. Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing.

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