Dosage and parent-of-origin effects shaping aneuploid swarms in A. thaliana

Abstract

Changes in chromosome number have a critical role in the evolution and formation of plant species. Triploids, which carry three complete sets of chromosomes, in particular produce offspring with different chromosome numbers, including diploid and tetraploid progeny, as well as a swarm of aneuploid progeny, which carry incomplete chromosome sets. In this study, we investigated the mechanisms shaping these swarms at the population level through a detailed characterization of the progeny of triploid Arabidopsis thaliana. We report that triploid meiosis predominately produced aneuploid gametes, most of which were viable. We performed reciprocal crosses between triploid and either diploid or tetraploid plants and karyotyped all surviving individuals. This allowed us to dissect the parent-of-origin (cross-direction) effects and also the effect of the dosage of the crossing partner on the inheritance of each chromosome type. Overall, our data indicate that the chromosomal composition of the swarms produced by the triploid A. thaliana were strongly influenced by selection acting against specific gamete combinations, but not necessarily associated with aneuploidy. Finally, each of the five chromosome types responded differently to this selection, suggesting the presence of dosage-sensitive factor(s) critical for viability and encoded on different chromosomes.

Phenotypic Consequences of Aneuploidy inArabidopsis thaliana

“…All simple trisomics of A. thaliana have been previously isolated and phenotypically characterized (Steinitz-Sears 1962; Lee-Chen and Steinitz-Sears 1967;Steinitz-Sears and Lee-Chen 1970;Koornneef and Van der Veen 1983), demonstrating that they are tolerated in A. thaliana. We previously reported that aneuploid swarmspopulations of aneuploid individuals of varying aneuploid karyotypes-could be obtained from the progeny of triploid A. thaliana individuals (Henry et al 2005(Henry et al , 2009. Using a combination of a quantitative PCR-based method and flow cytometry, we were able to derive the full aneuploid karyotype of each of these individuals (Henry et al 2006).…”

“…It contains diploid, triploid, and tetraploid individuals and a swarm of aneuploid individuals of intermediate genome content. Four pseudo-backcross populations (pBCs) were generated by crossing the CWW triploid as pollen parent or egg parent to either diploid Col-0 or tetraploid 4x-Col (Henry et al 2006(Henry et al , 2009. All individuals in the CWW F 2 , CCWW F 1 , and pBC populations were analyzed for genome content using flow cytometric analysis of nuclear DNA content.…”

“…More complex aneuploids, i.e., individuals carrying more than one additional chromosome, can be viable as well and have been observed in many plants species, especially among the progeny of triploid individuals (McClintock 1929;Levan 1942;Johnsson 1945;Khush 1973). Some species appear to be more tolerant of complex aneuploidies than others, suggesting a genetic basis for aneuploidy tolerance (Satina and Blakeslee 1938;Khush 1973;Ramsey and Schemske 2002;Henry et al 2009). Aneuploid individuals frequently appear spontaneously within polyploid plant populations, presumably due to a failure to equally partition the multiple chromosome sets at meiosis (Randolph 1935;Doyle 1986).…”

Pairing analysis and in situ Hybridisation reveal autopolyploid-like behaviour in Solanum commersonii × S. tuberosum (potato) interspecific hybrids

“…It is not clear yet what factors determine EBN or where they are mapped in the potato genome. Aneuploid gametes with extra chromosomes bearing the EBN controlling factors might be positively selected for compatible crosses and thus favour the formation of genotypes with complements higher than the expected 2n = 5x = 60 (Carputo 1999;Henry et al 2009). For the BC 2 plants Carputo et al (2003) observed a narrower range of chromosome number variation, with a tendency towards tetraploid (2n = 4x = 48) numbers.…”

Arabidopsisand relatives as models for the study of genetic and genomic incompatibilities

“…A. thaliana triploids retain some fertility and give rise to aneuploid swarms, resolving eventually into stable diploids and tetraploids. In one such swarm, a single locus was shown to be selected in tetraploid and aneuploid derivatives, but not in diploids, suggesting that it contributes to aneuploid survivorship or fertility (Henry et al 2007(Henry et al , 2009. Seed viability in A. thaliana interploidy crosses also varies in different genetic backgrounds.…”