Allopolyploidization Lays the Foundation for Evolution of Distinct Populations: Evidence From Analysis of SyntheticArabidopsisAllohexaploids

Abstract

Polyploidization is an important mechanism for introducing diversity into a population and promoting evolutionary change. It is believed that most, if not all, angiosperms have undergone whole genome duplication events in their evolutionary history, which has led to changes in genome structure, gene regulation, and chromosome maintenance. Previous studies have shown that polyploidy can coincide with meiotic abnormalities and somatic cytogenetic mosaics in Arabidopsis allotetraploids, but it is unclear whether this phenomenon can contribute to novel diversity or act as a mechanism for speciation. In this study we tested the hypothesis that mosaic aneuploidy contributes to the formation of incipient diversity in neoallopolyploids. We generated a population of synthesized Arabidopsis allohexaploids and monitored karyotypic and phenotypic variation in this population over the first seven generations. We found evidence of sibling line-specific chromosome number variations and rapidly diverging phenotypes between lines, including flowering time, leaf shape, and pollen viability. Karyotypes varied between sibling lines and between cells within the same tissues. Cytotypic variation correlates with phenotypic novelty, and, unlike in allotetraploids, remains a major genomic destabilizing factor for at least the first seven generations. While it is still unclear whether new stable aneuploid lines will arise from these populations, our data are consistent with the notion that somatic aneuploidy, especially in higher level allopolyploids, can act as an evolutionary relevant mechanism to induce rapid variation not only during the initial allopolyploidization process but also for several subsequent generations. This process may lay the genetic foundation for multiple, rather than just a single, new species. P OLYPLOIDY is a major force in shaping angiosperm evolution and plant biodiversity (Ohno 1970;Stebbins 1971;Hegarty and Hiscock 2008;Leitch and Leitch 2008;Buggs et al. 2011). Polyploids are organisms with two or more complete sets of chromosomes. Polyploidy is frequent in nature and evidence shows that most, if not all, angiosperms have undergone at least one ancient genome doubling event in their evolutionary history (Bowers et al. 2003;Blanc and Wolfe 2004;Cui et al. 2006;Soltis and Soltis 2009;Jiao et al. 2011). Two major forms of polyploidy exist: autopolyploidy, which describes multiple genomes derived from a single species, and allopolyploidy, which refers to species in which genome doubling occurred concomitantly with the hybridization of two or more species.Newly formed allopolyploids (neoallopolyploids) are subject to multiple changes from their progenitors in response to genome duplication, including structural chromosomal change, aneuploidy, genome rearrangement, epigenetic remodeling, and transcriptional change (Madlung et al. 2002;Henry et al. 2005;Huettel et al. 2008;Lim et al. 2008;Wright et al. 2009;Salmon et al. 2010;Chen 2010). Plants are generally quite plastic and can tolerate variation in the...

Persistent whole-chromosome aneuploidy is generally associated with nascent allohexaploid wheat

“…The frequencies of aneuploidy varied from approximately 20-100% among the plants from each line, with chromosome numbers ranging from 39 to 45 (Dataset S1). All aneuploidy occurred in a per plant basis; that is, no plant contained two or more types of aneuploid cells, which is in contrast with synthesized Arabidopsis allohexaploids (9). Surprisingly, we did not identify any unambiguous chromosomal translocation/inversion or duplication/deletion in any of the 580 plants, although we cannot exclude the presence of submicroscopic chromosomal rearrangements.…”

Environmental Regulation of Heterosis in the Allopolyploid Arabidopsis suecica

“…Briefly, diploids were treated with colchicine, and ploidy levels were measured in the offspring of the treated plants using flow cytometry. Both 2x and 4x plants were recovered from the same treated parent plant and thus considered a "matched pair" (Pignatta et al, 2010 were ascertained by fluorescent in situ hybridization as described before (Wright et al, 2009;Matsushita et al, 2012). Seeds for diploid/autotetraploid matched pairs were deposited with the ABRC and accession numbers are provided in Supplemental Table S1.…”

“…However, allopolyploidy adds another complication in that organisms with genomic contributions from two or more species do not exhibit exclusively additive or predictably changing gene expression (Madlung et al, 2002;Wang et al, 2004;Chen, 2010;Matsushita et al, 2012). This could potentially lead to variation in levels of enzymes involved in the biochemical aspects of photosynthesis between allopolyploids and their progenitors or even among allopolyploid siblings or lineages.…”

Global Analysis of Gene Expression in Response to Whole-Chromosome Aneuploidy in Hexaploid Wheat

“…For still mysterious reasons, plants in general are more tolerant to aneuploidy than animals. For example, in Arabidopsis (Arabidopsis thaliana), selfed progeny of a triploid mother plant generates a swarm of diverse types of aneuploid plants that are viable and fertile (Henry et al, 2007;Huettel et al, 2008;Henry et al, 2010;Matsushita et al, 2012). Moreover, many plant species are polyploids, which in theory have a much greater capacity to buffer the dosage imbalance of individual chromosome gain or loss and, therefore, are more permissive to the occurrence of whole-chromosome aneuploidy than diploids, especially for chromosome loss.…”