Dosage compensation evolution in plants: theories, controversies and mechanisms

Abstract

In a minority of flowering plants, separate sexes are genetically determined by sex chromosomes. The Y chromosome has a non-recombining region that degenerates, causing a reduced expression of Y genes. In some species, the lower Y expression is accompanied by dosage compensation (DC), a mechanism that re-equalizes male and female expression and/or brings XY male expression back to its ancestral level. Here, we review work on DC in plants, which started as early as the late 1960s with cytological approaches. The use of transcriptomics fired a controversy as to whether DC existed in plants. Further work revealed that various plants exhibit partial DC, including a few species with young and homomorphic sex chromosomes. We are starting to understand the mechanisms responsible for DC in some plants, but in most species, we lack the data to differentiate between global and gene-by-gene DC. Also, it is unknown why some species evolve many dosage compensated genes while others do not. Finally, the forces that drive DC evolution remain mysterious, both in plants and animals. We review the multiple evolutionary theories that have been proposed to explain DC patterns in eukaryotes with XY or ZW sex chromosomes. This article is part of the theme issue ‘Sex determination and sex chromosome evolution in land plants’.

A pan-grass transcriptome reveals patterns of cellular divergence in crops

“…In keeping with genome balance models, we observed that co-expressed WGD homeologues showed expression patterns indicative of dosage compensation 36,37 , whereas this pattern was weaker or non-existent in other duplicate classes (Fig. 3a and Extended Data Fig.…”

Can mechanistic constraints on recombination reestablishment explain the long-term maintenance of degenerate sex chromosomes?

“…A better integration of the different mechanisms of regulatory variation may also be useful, such as mechanisms based on imprinting [72] or based on reallocation of transcription factors to X-linked genes [11]. While the widespread occurrence of DC [72,73] indicates that it is needed at least for some genes, it would be interesting to introduce heterogeneity among genes in selection on dosage, and varying the genetic architecture of DC (local vs global). Several cases of interest should be investigated further, notably cases involving non-random mating [18,29,74] or UV and mating-type chromosomes.…”

“…In particular, the conditions allowing the long-term maintenance of recombination suppression under the SA theory should be investigated further [following 37,38] and combined with models of regulatory evolution. Better integration of the different mechanisms of regulatory variation may also be useful, such as mechanisms based on imprinting [80] or based on the reallocation of transcription factors to X-linked genes [11]. While the widespread occurrence of DC [80,81] indicates that it is needed at least for some genes, it would be interesting to introduce heterogeneity among genes in selection on dosage, and varying the genetic architecture of DC (local vs global).…”

Evolution of sex‐determination in dioecious plants: From active Y to X/A balance?

“…It is interesting that SlWUS1 is not dosage compensated (i.e., not upregulated in males) [ 28 ] despite the location in the oldest stratum 1 [ 33 ] where we may expect dosage compensation to be prevalent, particularly given the recent models predicting that dosage compensation is responsible for evolution of X‐Y recombination repression. [ 34,35 ] This likely reflects the dosage sensitivity of SlWUS1 that should not be altered by evolving dosage compensation system. Taken together, the S. latifolia X chromosome is apparently involved in sex determination with X/Y dosage balance mechanism, that likely operates via the WUS / CLV feedback loop.…”