The role of genetic and genomic attributes in the success of polyploids

Abstract

P olyploidy, the presence of more than two genomes per cell, is a significant mode of species formation in plants and was one of the topics closest to the heart of Ledyard Stebbins. In Variation and Evolution in Plants, Stebbins (1) devoted two chapters to polyploidy and addressed the following issues: the frequency, taxonomic distribution, and geographic distribution of polyploidy; the origins of polyploidy and factors promoting polyploidy; the direct effects of polyploidy; the polyploid complex; the success of polyploids in extreme habitats (including weeds); ancient polyploidy; and the role of polyploidy in the evolution and improvement of crops. He continued to explore these and other themes in his subsequent work, most notably in Chromosomal Evolution in Plants (2). In this paper we pay tribute to Ledyard, who was an inspiration and a friend, by exploring some of the questions that he asked about polyploids and by reviewing recent advances in the study of polyploidy.Estimates of the frequency of polyploid angiosperm species range from Ϸ30-35% (3) to as high as 80% (4); most estimates are near 50% (2, 5). Levels of polyploidy may be even higher in pteridophytes, with some estimates of polyploidy in ferns as high as 95% (5). Polyploids often occupy habitats different from those of their diploid parents, and have been proposed to be superior colonizers to diploids. Furthermore, most crop plants are of polyploid origin, as noted by Stebbins (1). In contrast, although genome doubling has been reported from other major groups of eukaryotes (reviewed in ref. 6), it is not nearly as common in these groups as it is in plants.The question often has arisen as to why polyploids are so common and so successful, and several possible explanations have been proposed. Stebbins (1) considered vegetative reproduction and the perennial habit to be important factors promoting the establishment of polyploids, along with an outcrossing mating system to allow for hybridization (between species, subspecies, races, populations, etc.) in the formation of the polyploid. Perhaps most important to Stebbins (1) was the availability of new ecological niches. Additional hypotheses for the success of polyploids include broader ecological amplitude of the polyploid relative to its diploid parents, better colonizing ability, higher selfing rates, and increased heterozygosity.In fact, many aspects of the genetic systems of polyploids may contribute to the success of polyploid plants. These characteristics range from the molecular level to the population level and include increased heterozygosity, reduced inbreeding depression and an associated increase in selfing rates, increased genetic diversity through multiple formations of a polyploid species, genome rearrangements, and ancient polyploidy and gene silencing. But what role, if any, do these factors really play in the success of polyploids? In this paper, we will explore the evidence for the role of these genetic attributes in the evolutionary success of polyploid plant species.

Meiotic aberrations during 2n pollen formation in Begonia

“…New methods for synthetic polyploidization of plants through the use of spindle inhibitors, such as colchicine or dinitroanilines (for example, oryzalin and trifluralin), have been developed and successfully used in several plants (Vaughn and Lehnen, 1991;Hancock, 1997;Zlesak et al, 2005;Dhooghe et al, 2009). However, synthetic polyploidization has contributed little to crop improvement, likely owing to fixed heterozygosity (Soltis and Soltis, 2000). Contrary to the assumption of Stebbins (1950), Harlan and De Wet (1975) showed that almost all plant species produce 2n gametes with some frequency.…”

PCR survey of hox genes in the goldfish Carassius auratus auratus

“…How is dosage balance achieved when the genome suddenly contains additional copies of a gene? Such questions have been explored in plants (Soltis and Soltis, 2000;Wendel, 2000;Chen et al, 2004;Comai, 2005). What are the mechanisms leading to retention or loss of a duplicated gene?…”

Diagnosing duplications – can it be done?

“…These observations led to the prediction that polyploidization will rarely be observed in animals but more frequently in plants. However, with the discovery of many additional polyploid species [35], the emergence of molecular methods in the 1980s and 1990s and the increasing availability of genomic sequence, much of the accepted pre-genomic lore concerning polyploids has been questioned [36][37][38]. This has led to a resurgence of studies of the mechanisms of polyploidization, the physiological conditions that enable polyploids to arise, positive and negative forces acting on neopolyploids and the extent to which polyploidization represents special evolutionary opportunities.…”