Mechanisms of genomic rearrangements and gene expression changes in plant polyploids

Abstract

Polyploidy is produced by multiplication of a single genome (autopolyploid) or combination of two or more divergent genomes (allopolyploid). The available data obtained from the study of synthetic (newly created or human-made) plant allopolyploids have documented dynamic and stochastic changes in genomic organization and gene expression, including sequence elimination, inter-chromosomal exchanges, cytosine methylation, gene repression, novel activation, genetic dominance, subfunctionalization and transposon activation. The underlying mechanisms for these alterations are poorly understood. To promote a better understanding of genomic and gene expression changes in polyploidy, we briefly review origins and forms of polyploidy and summarize what has been learned from genome-wide gene expression analyses in newly synthesized auto-and allopolyploids. We show transcriptome divergence between the progenitors and in the newly formed allopolyploids. We propose models for transcriptional regulation, chromatin modification and RNA-mediated pathways in establishing locus-specific expression of orthologous and homoeologous genes during allopolyploid formation and evolution.

Figure 1

Two models (“one-step” and “two-step”) for the formation of allopolyploids. A: An amphidiploid (synonymous with allotetraploid, combination of two divergent genomes) is formed by hybridization between two diploid progenitors followed by chromosome doubling (two-step model). For simplicity, each diploid species has one pair of chromosomes. P1 and P2 represent two progenitors. Here we considered allopolyploids and amphidiploids to be synonyms (R. C. King and W. D. Stansfield, A Dictionary of Genetics, 5^th edition, Oxford University Press, 1997), although they may be distinguished by chromosome behaviors during meiosis. Strictly speaking, only bivalents are formed in amphidiploids, whereas multivalents may be formed in allopolyploids. B: Fusion of unreduced male and female gemetes of two diploid progenitors leads to the production of an allotetraploid (one-step model). C: An allotetraploid is immediately formed by direct hybridization between two autotetraploid species (one-step model).

Figure 2

Types of genomic and gene expression changes documented in the polyploids. A: Genomic modification involves deletion, translocation and interstitial homoeologous exchanges (transposition),(55) and epigenetic modification (e.g. changes in DNA methylation). Blue and red colors represent two genomes or chromosomes from P1 and P2, respectively. B: Gene expression changes include genetic dominance, gene silencing, subfunctionalization and novel activation. In each case, the loci that display expression changes in allotetraploids (A1–A6) may be from either or both parents compared to the expression levels in the original parent (P1, red or P2, blue). For simplicity, only one of the two alleles in each parental locus was shown. The arrows on each locus indicate transcription (open head, P1, and filled head, P2, all solid lines), low levels of transcription (dashed lines) and no transcription (no arrows). Thick arrows indicate novel gene activation.

Figure 3

Two models for the gene expression changes observed in the allopolyploids. A: The transcriptional regulation model suggests interactive roles of sequence evolution, transcriptional regulation and chromatin modification in modulating the expression of orthologous genes in the allopolyploids. Transcriptional regulators (X, P1 and X′, P2) are compatible with the orthologous loci leading to the expression of both in allotetraploids (A1). Only one regulator (X or X′) is present or compatible with one of the loci leading to the expression of a single locus (A2 or A3). Absence of upstream regulators or incompatibility between the two loci result in silencing of both loci (A4). B:The RNA-mediated pathway model indicates differential accumulation of small RNAs that may act as negative regulators for target genes. Production of small RNAs (siRNA and miRNA) from orthologous genes is associated with downregulation of both genes (“cross out” symbols) in allotetraploids (A5). Production of small RNAs from one species results in silencing of one locus (A6 or 7). Absence of small RNAs promotes transcript accumulation of both orthologous loci (A8). Blue and red colors represent protein regulators (ovals), loci (boxes), small RNAs (short waved lines) and RNA transcripts (long waved lines) from parent 1 (P1) and parent 2 (P2), respectively. The blue and red arrows indicate possible cis (solid lines) or trans (dashed lines) interactions, whereas the arrows on each locus indicate transcription (open head, P1 and filled head, P2, all solid lines) and low levels of transcription (dashed lines). The “+” and “−” indicates accumulation and downregulation of transcripts, respectively, in allotetraploids. Thick arrows indicate upregulation.

Figure 4

A wheel of the models for polyploidy-dependent genomic rearrangements and gene regulation. Eight types of observed changes (bold-type fonts) and their underlying mechanisms (italicized fonts) were arranged circularly around an allotetraploid cell (center). The changes may be mediated by genetic (DNA sequence-dependent, top and red), epigenetic (DNA sequence-independent, bottom and green) mechanisms or both (middle and light blue). The distinctions among some of the classified changes and underlying mechanisms may not be very clear. For example, changes in DNA methylation may activate transposable elements that may in turn induce transposition or chromosomal breakages and exchanges. Similarly, non-additive gene regulation may include subfunctionalization and silencing of homoeologous genes. The dashed ring represents circular interactions among some, if not all, classified changes and predicted models. Additional research is needed in order to provide experimental data for these models. Note that a polyploid organism may experience some but not all changes listed in the diagram. For instance, genomic sequence rearrangements were predominately detected in Brassica and wheat allopolyploids but not in Arabidopsis and cotton allopolyploids. The thickness of arrows may correspond to an arbitrarily level of the changes that have been documented in the polyploids.