Transgenerationally Precipitated Meiotic Chromosome Instability Fuels Rapid Karyotypic Evolution and Phenotypic Diversity in an Artificially Constructed Allotetraploid Wheat (AADD)

Abstract

Although a distinct karyotype with defined chromosome number and structure characterizes each biological species, it is intrinsically labile. Polyploidy or whole-genome duplication has played a pervasive and ongoing role in the evolution of all eukaryotes, and is the most dramatic force known to cause rapid karyotypic reconfiguration, especially at the initial stage. However, issues concerning transgenerational propagation of karyotypic heterogeneity and its translation to phenotypic diversity in nascent allopolyploidy, at the population level, have yet to be studied in detail. Here, we report a large-scale examination of transgenerationally propagated karyotypic heterogeneity and its phenotypic manifestation in an artificially constructed allotetraploid with a genome composition of AADD, that is, involving two of the three progenitor genomes of polyploid wheat. Specifically, we show that 1) massive organismal karyotypic heterogeneity is precipitated after 12 consecutive generations of selfing from a single euploid founder individual, 2) there exist dramatic differences in aptitudes between subgenomes and among chromosomes for whole-chromosome gain and/or loss and structural variations, 3) majority of the numerical and structural chromosomal variations are concurrent due to mutual contingency and possible functional constraint, 4) purposed and continuous selection and propagation for euploidy over generations did not result in enhanced karyotype stabilization, and 5) extent of karyotypic variation correlates with variability of phenotypic manifestation. Together, our results document that allopolyploidization catalyzes rampant and transgenerationally heritable organismal karyotypic heterogeneity that drives population-level phenotypic diversification, which lends fresh empirical support to the still contentious notion that whole-genome duplication enhances organismal evolvability.

The causes and consequences of subgenome dominance in hybrids and recent polyploids

“…Not only were numerous HEs identified between individuals, but HEs showed a significant subgenome bias, resulting in more C subgenome regions replaced with A subgenome regions than A subgenome regions being replaced with C subgenome regions (Chalhoub et al ., ). These findings were supported by subsequent studies in B. napus and other allopolyploid crops (He et al ., ; Samans et al ., ), including similar subgenome biased patterns in natural cotton allopolyploids (Guo et al ., ), octoploid strawberry (Tennessen et al ., ), and synthetic AADD wheat tetraploids (Gou et al ., ).…”

Paleogenomics: reconstruction of plant evolutionary trajectories from modern and ancient DNA

“…The access to ancient DNA (aDNA) sequences from extinct diploid and polyploid ancestors contemporary to past polyploidization events will further expand our understanding of this major phenomenon driving plant evolutionary dynamics, making it possible to characterize the driving molecular mechanisms that have potential for use in breeding. In that regard, nascent polyploids (particularly in wheat and Brassicaceae) provide opportunities for testing the hypothesis that polyploidization accelerates evolutionary adaptation to environmental changes [56].…”

DNA methylation repatterning accompanying hybridization, whole genome doubling and homoeolog exchange in nascent segmental rice allotetraploids

“…Consequently, multivalents and univalents occur due to compromised pairing fidelity, resulting in homoeologous exchanges (HEs) and aneuploidy (Pecinka et al ., ; Higgins et al ., ; Lloyd et al ., ). Conceivably, while most aneuploidies that cause deficiency and/or chromosome‐wide dosage imbalance will be rapidly purged due to lethality or lack of fitness, many progenies with HEs may remain and be transgenerationally persistent due to the frequent (Gou et al ., ), but not ever‐present (Zhang et al ., ; Gong et al ., ; Lloyd et al ., ), mutual functional compensation of homoeologs (Xiong et al ., ; Chester et al ., ). HEs generate alterations of the otherwise 2 : 2 homoeolog ratio, and hence may impact epigenetic stabilities (e.g.…”