Margaret R. Woodhouse

Following Tetraploidy in Maize, a Short Deletion Mechanism Removed Genes Preferentially from One of the Two Homeologs

Following genome duplication and selfish DNA expansion, maize used a heretofore unknown mechanism to shed redundant genes and functionless DNA with bias toward one of the parental genomes.

The pineapple genome and the evolution of CAM photosynthesis

Pineapple (Ananas comosus (L.) Merr.) is the most economically valuable crop possessing crassulacean acid metabolism (CAM), a photosynthetic carbon assimilation pathway with high water-use efficiency, and the second most important tropical fruit. We sequenced the genomes of pineapple varieties F153 and MD2 and a wild pineapple relative, Ananas bracteatus accession CB5. The pineapple genome has one fewer ancient whole-genome duplication event than sequenced grass genomes and a conserved karyotype with seven chromosomes from before the ρ duplication event. The pineapple lineage has transitioned from C3 photosynthesis to CAM, with CAM-related genes exhibiting a diel expression pattern in photosynthetic tissues. CAM pathway genes were enriched with cis-regulatory elements associated with the regulation of circadian clock genes, providing the first cis-regulatory link between CAM and circadian clock regulation. Pineapple CAM photosynthesis evolved by the reconfiguration of pathways in C3 plants, through the regulatory neofunctionalization of preexisting genes and not through the acquisition of neofunctionalized genes via whole-genome or tandem gene duplication.

Altered Patterns of Fractionation and Exon Deletions in Brassica Rapa Support a Two-Step Model of Paleohexaploidy

The genome sequence of the paleohexaploid Brassica rapa shows that fractionation is biased among the three subgenomes and that the least fractionated subgenome has approximately twice as many orthologs as its close (and relatively unduplicated) relative Arabidopsis than had either of the other two subgenomes. One evolutionary scenario is that the two subgenomes with heavy gene losses (I and II) were in the same nucleus for a longer period of time than the third subgenome (III) with the fewest gene losses. This “two-step” hypothesis is essentially the same as that proposed previously for the eudicot paleohexaploidy; however, the more recent nature of the B. rapa paleohexaploidy makes this model more testable. We found that subgenome II suffered recent small deletions within exons more frequently than subgenome I, as would be expected if the genes in subgenome I had already been near maximally fractionated before subgenome III was introduced. We observed that some sequences, before these deletions, were flanked by short direct repeats, a unique signature of intrachromosomal illegitimate recombination. We also found, through simulations, that short—single or two-gene—deletions appear to dominate the fractionation patterns in B. rapa. We conclude that the observed patterns of the triplicated regions in the Brassica genome are best explained by a two-step fractionation model. The triplication and subsequent mode of fractionation could influence the potential to generate morphological diversity—a hallmark of the Brassica genus.

Fractionation mutagenesis and similar consequences of mechanisms removing dispensable or less-expressed DNA in plants.

Unlike in mammals, plants rapidly delete functionless, nonrepetitive DNA from their genomes. Following paleopolyploidies, duplicate genes are deleted by intrachromosomal recombination. This may explain how flowering plants have survived multiple whole genome duplications. Genes are disproportionately lost from one parental subgenome, the subgenome that is less expressed in the polyploid. The origin of this unbalanced expression between genomes remains unknown. The consequences of the tradeoffs between transposon repression and gene expression represent one potential explanation of genome dominance. If so, the same mechanisms may act in heterosis: genome dominance is like inbreeding depression. Regulatory DNA deletion following polyploidy combined with abundant RNA-seq expression datasets are being used to generate testable hypothesizes regarding the function of specific cis-regulatory sequences.

Origin, inheritance, and gene regulatory consequences of genome dominance in polyploids.

Significance Ancient plant polyploids contain dissimilar subgenomes. Subgenomes that have lost fewer genes are subgenomes that tend to express their genes to higher mRNA levels: “genome dominance.” Genome dominance is heritable through multiple rounds of polyploidy and over tens of millions of years. Twenty-four–nucleotide RNA coverage of noncoding, transposon DNA upstream of genes marks the recessive subgenomes of Brassica rapa and Arabidopsis with only a small effect of gene expression. We hypothesize that the “diploid” parent of a tetraploidy with the lowest transposon load was to become the dominant subgenome. The balance of transposon position effects on genes is important for the regulation of quantity (and perhaps to solve the heterosis and C-value paradoxes). Whole-genome duplications happen repeatedly in a typical flowering plant lineage. Following most ancient tetraploidies, the two subgenomes are distinguishable because one subgenome, the dominant subgenome, tends to have more genes than the other subgenome. Additionally, among retained pairs, the gene on the dominant subgenome tends to be expressed more than its recessive homeolog. Using comparative genomics, we show that genome dominance is heritable. The dominant subgenome of one postpolyploidy event remains dominant through a subsequent polyploidy event. We show that transposon-derived 24-nt RNAs target and cover the upstream region of retained genes preferentially when located on the recessive subgenome, and with little regard for a gene’s level of expression. We hypothesize that small RNA (smRNA)-mediated silencing of transposons near genes causes position-effect down-regulation. Unlike 24-nt smRNA coverage, transposon coverage tracks gene expression, so not all transposons behave identically. We propose that successful ancient tetraploids begin as wide crosses between two lines, each evolved for different tradeoffs between transposon silencing and negative position effects on gene expression. We hypothesize that following a chaotic wide-cross/new tetraploid period, genes acquire their new expression balances based on differences in transposon coverage in the parents. We envision patches of silenceable transposon as quantitative cis-regulators of baseline transcription rate. Attractive solutions to heterosis and the C-value paradox are mentioned.

The mop1 (mediator of paramutation1) Mutant Progressively Reactivates One of the Two Genes Encoded by the MuDR Transposon in Maize

Transposons make up a sizable portion of most genomes, and most organisms have evolved mechanisms to silence them. In maize, silencing of the Mutator family of transposons is associated with methylation of the terminal inverted repeats (TIRs) surrounding the autonomous element and loss of mudrA expression (the transposase) as well as mudrB (a gene involved in insertional activity). We have previously reported that a mutation that suppresses paramutation in maize, mop1, also hypomethylates Mu1 elements and restores somatic activity to silenced MuDR elements. Here, we describe the progressive reactivation of silenced mudrA after several generations in a mop1 background. In mop1 mutants, the TIRA becomes hypomethylated immediately, but mudrA expression and significant somatic reactivation is not observed until silenced MuDR has been exposed to mop1 for several generations. In subsequent generations, individuals that are heterozygous or wild type for the Mop1 allele continue to exhibit hypomethylation at Mu1 and mudrA TIRs as well as somatic activity and high levels of mudrA expression. Thus, mudrA silencing can be progressively and heritably reversed. Conversely, mudrB expression is never restored, its TIR remains methylated, and new insertions of Mu elements are not observed. These data suggest that mudrA and mudrB silencing may be maintained via distinct mechanisms.

Different Gene Families in Arabidopsis thaliana Transposed in Different Epochs and at Different Frequencies throughout the Rosids

This work examines the chromosomal positional history of all genes in Arabidopsis thaliana through evolutionary time in the rosid superorder, finding that mobile gene families are under different selection pressure than syntenic gene families. Certain types of gene families, such as those encoding most families of transcription factors, maintain their chromosomal syntenic positions throughout angiosperm evolutionary time. Other nonsyntenic gene families are prone to deletion, tandem duplication, and transposition. Here, we describe the chromosomal positional history of all genes in Arabidopsis thaliana throughout the rosid superorder. We introduce a public database where researchers can look up the positional history of their favorite A. thaliana gene or gene family. Finally, we show that specific gene families transposed at specific points in evolutionary time, particularly after whole-genome duplication events in the Brassicales, and suggest that genes in mobile gene families are under different selection pressure than syntenic genes.

Transposed genes in Arabidopsis are often associated with flanking repeats.

Much of the eukaryotic genome is known to be mobile, largely due to the movement of transposons and other parasitic elements. Recent work in plants and Drosophila suggests that mobility is also a feature of many nontransposon genes and gene families. Indeed, analysis of the Arabidopsis genome suggested that as many as half of all genes had moved to unlinked positions since Arabidopsis diverged from papaya roughly 72 million years ago, and that these mobile genes tend to fall into distinct gene families. However, the mechanism by which single gene transposition occurred was not deduced. By comparing two closely related species, Arabidopsis thaliana and Arabidopsis lyrata, we sought to determine the nature of gene transposition in Arabidopsis. We found that certain categories of genes are much more likely to have transposed than others, and that many of these transposed genes are flanked by direct repeat sequence that was homologous to sequence within the orthologous target site in A. lyrata and which was predominantly genic in identity. We suggest that intrachromosomal recombination between tandemly duplicated sequences, and subsequent insertion of the circular product, is the predominant mechanism of gene transposition.