All Ways Lead to Rome—Meiotic Stabilization Can Take Many Routes in Nascent Polyploid Plants

Newly formed polyploids often show extensive meiotic defects, resulting in aneuploid gametes, and thus reduced fertility. However, while many neopolyploids are meiotically unstable, polyploid lineages that survive in nature are generally stable and fertile; thus, those lineages that survive are those that are able to overcome these challenges. Several genes that promote polyploid stabilization are now known in plants, allowing speculation on the evolutionary origin of these meiotic adjustments. Here, I discuss results that show that meiotic stability can be achieved through the differentiation of certain alleles of certain genes between ploidies. These alleles, at least sometimes, seem to arise by novel mutation, while standing variation in either ancestral diploids or related polyploids, from which alleles can introgress, may also contribute. Growing evidence also suggests that the coevolution of multiple interacting genes has contributed to polyploid stabilization, and in allopolyploids, the return of duplicated genes to single copies (genome fractionation) may also play a role in meiotic stabilization. There is also some evidence that epigenetic regulation may be important, which can help explain why some polyploid lineages can partly stabilize quite rapidly.

Genome-wide Identification, Evolutionary and Functional Analyses of Kfb Family Members in Potato

Background: Kelch repeat F-box (KFB) proteins play vital roles in the regulation of multitudinous biochemical and physiological processes in plants, including growth and development, stress response and secondary metabolism. Multiple KFBs have been characterized in various plant species, but this family members have not been systematically identified and analyzed in potato. Results: Genome and transcriptome analyses of StKFB gene family were conducted to dissect the structure, evolution and function of the KFBs in Solanum tuberosum L. Totally, 44 StKFB members were identified and were classified into 5 groups according to their structural and phylogenetic features. The chromosomal localization analysis showed that the 44 StKFB genes were located on 12 chromosomes. Among these genes, two pairs of genes (StKFB15/16 and StKFB40/41) were predicted to be tandemly duplicated genes, and one pair of genes (StKFB15/29) was segmentally duplicated genes. The syntenic analysis showed that the KFBs in potato were closely related to the KFBs in tomato and pepper. Expression profiles of StKFBs in 13 different tissues and in potato plants with different treatments uncovered distinct spatial expression patterns of these genes and their potential roles in response to various stresses. Transcriptomic and qRT-PCR analyses of StKFBs deciphered that multiple StKFB genes were differentially expressed in three colored potato tubers. Genes that were highly expressed in yellow fleshed tubers (Jin-16) and were lowly expressed in the red- (Red Rose-2) or purple-fleshed (Xisen-8) tubers, such as StKFB07, StKFB15, StKFB23, StKFB29 and StKFB44, may negatively regulate anthocyanin biosynthesis.Conclusions: This study reports the structure, evolution and expression characteristics of the KFB family in potato. These findings set the stage for further study of functional mechanisms of StKFBs, and also provide candidate genes for potato genetic improvement.

A tandem duplication in Drosophila melanogaster shows enhanced expression beyond the gene copy number

Tandem duplicated genes are common features of genomes, but the phenotypic consequences of their origins are not well understood. It is not known whether a simple doubling of gene expression should be expected, or else some other expression outcome. This study describes an experimental framework using engineered deletions to assess any contribution of locally-acting cis- and globally-acting trans-regulatory factors to expression interactions of particular tandem duplicated genes. Acsx1L (CG6300) and Acsx1R (CG11659) are tandem duplicates of a putative acyl-CoA synthetase gene found in D. melanogaster. Experimental deletions of the duplicated segments were used to investigate whether the presence of one tandem duplicated block influences the expression of its neighbor. Acsx1L, the gene in the left block, shows much higher expression than either its duplicate Acsx1R or the single Acsx1 in D. simulans. Acsx1L expression decreases drastically upon deleting the right-hand duplicated block. Crosses among wildtype and deletion strains show that high tandem expression is primarily due to cis-acting interactions between the duplicated blocks. No effect of these genes on cuticular hydrocarbons was detected. Sequence and phylogenetic analysis suggest that the duplication rose to fixation in D. melanogaster and has been subject to extensive gene conversion. Some strains actually carry three tandem copies, yet strains with three Acsx1s do not have higher expression levels than strains with two. Surveys of tandem duplicate expression have typically not found the expected twofold increase in expression. This study suggests that cis-regulatory interactions between duplicated blocks could be responsible for this trend.

Illegitimate Recombination between Duplicated Genes Generated from Recursive Polyploidizations Accelerated the Divergence of the Genus Arachis

The peanut (Arachis hypogaea L.) is the leading oil and food crop among the legume family. Extensive duplicate gene pairs generated from recursive polyploidizations with high sequence similarity could result from gene conversion, caused by illegitimate DNA recombination. Here, through synteny-based comparisons of two diploid and three tetraploid peanut genomes, we identified the duplicated genes generated from legume common tetraploidy (LCT) and peanut recent allo-tetraploidy (PRT) within genomes. In each peanut genome (or subgenomes), we inferred that 6.8–13.1% of LCT-related and 11.3–16.5% of PRT-related duplicates were affected by gene conversion, in which the LCT-related duplicates were the most affected by partial gene conversion, whereas the PRT-related duplicates were the most affected by whole gene conversion. Notably, we observed the conversion between duplicates as the long-lasting contribution of polyploidizations accelerated the divergence of different Arachis genomes. Moreover, we found that the converted duplicates are unevenly distributed across the chromosomes and are more often near the ends of the chromosomes in each genome. We also confirmed that well-preserved homoeologous chromosome regions may facilitate duplicates’ conversion. In addition, we found that these biological functions contain a higher number of preferentially converted genes, such as catalytic activity-related genes. We identified specific domains that are involved in converted genes, implying that conversions are associated with important traits of peanut growth and development.

New Genes in the Drosophila Y Chromosome: Lessons from D. willistoni

Y chromosomes play important roles in sex determination and male fertility. In several groups (e.g., mammals) there is strong evidence that they evolved through gene loss from a common X-Y ancestor, but in Drosophila the acquisition of new genes plays a major role. This conclusion came mostly from studies in two species. Here we report the identification of the 22 Y-linked genes in D. willistoni. They all fit the previously observed pattern of autosomal or X-linked testis-specific genes that duplicated to the Y. The ratio of gene gains to gene losses is ~25 in D. willistoni, confirming the prominent role of gene gains in the evolution of Drosophila Y chromosomes. We also found four large segmental duplications (ranging from 62 kb to 303 kb) from autosomal regions to the Y, containing ~58 genes. All but four of these duplicated genes became pseudogenes in the Y or disappeared. In the GK20609 gene the Y-linked copy remained functional, whereas its original autosomal copy degenerated, demonstrating how autosomal genes are transferred to the Y chromosome. Since the segmental duplication that carried GK20609 contained six other testis-specific genes, it seems that chance plays a significant role in the acquisition of new genes by the Drosophila Y chromosome.

Muller’s ratchet of the Y chromosome with gene conversion

Muller’s ratchet is a process in which deleterious mutations are fixed irreversibly in the absence of recombination. The degeneration of the Y chromosome, and the gradual loss of its genes, can be explained by Muller’s ratchet. However, most theories consider single-copy genes, and may not be applicable to Y chromosomes, which have a number of duplicated genes in many species, which are probably undergoing concerted evolution by gene conversion. We developed a model of Muller’s ratchet to explore the evolution of the Y chromosome. The model assumes a non-recombining chromosome with both single-copy and duplicated genes. We used analytical and simulation approaches to obtain the rate of gene loss in this model, with special attention to the role of gene conversion. Homogenization by gene conversion makes both duplicated copies either mutated or intact. The former promotes the ratchet, and the latter retards, and we ask which of these counteracting forces dominates under which conditions. We found that the effect of gene conversion is complex, and depends upon the fitness effect of gene duplication. When duplication has no effect on fitness, gene conversion accelerates the ratchet of both single-copy and duplicated genes. If duplication has an additive fitness effect, the ratchet of single-copy genes is accelerated by gene duplication, regardless of the gene conversion rate, whereas gene conversion slows the degeneration of duplicated genes. Our results suggest that the evolution of the Y chromosome involves several parameters, including the fitness effect of gene duplication by increasing dosage and gene conversion rate.

The Role of Ancestral Duplicated Genes in Adaptation to Growth on Lactate, a Non-Fermentable Carbon Source for the Yeast Saccharomyces cerevisiae

The cell central metabolism has been shaped throughout evolutionary times when facing challenges from the availability of resources. In the budding yeast, Saccharomyces cerevisiae, a set of duplicated genes originating from an ancestral whole-genome and several coetaneous small-scale duplication events drive energy transfer through glucose metabolism as the main carbon source either by fermentation or respiration. These duplicates (~a third of the genome) have been dated back to approximately 100 MY, allowing for enough evolutionary time to diverge in both sequence and function. Gene duplication has been proposed as a molecular mechanism of biological innovation, maintaining balance between mutational robustness and evolvability of the system. However, some questions concerning the molecular mechanisms behind duplicated genes transcriptional plasticity and functional divergence remain unresolved. In this work we challenged S. cerevisiae to the use of lactic acid/lactate as the sole carbon source and performed a small adaptive laboratory evolution to this non-fermentative carbon source, determining phenotypic and transcriptomic changes. We observed growth adaptation to acidic stress, by reduction of growth rate and increase in biomass production, while the transcriptomic response was mainly driven by repression of the whole-genome duplicates, those implied in glycolysis and overexpression of ROS response. The contribution of several duplicated pairs to this carbon source switch and acidic stress is also discussed.

Divergent Antiviral Mechanisms of Two Viperin Homeologs in a Recurrent Polyploid Fish

Polyploidy and subsequent diploidization provide genomic opportunities for evolutionary innovations and adaptation. The researches on duplicated gene evolutionary fates in recurrent polyploids have seriously lagged behind that in paleopolyploids with diploidized genomes. Moreover, the antiviral mechanisms of Viperin remain largely unclear in fish. Here, we elaborate the distinct antiviral mechanisms of two viperin homeologs (Cgviperin-A and Cgviperin-B) in auto-allo-hexaploid gibel carp (Carassius gibelio). First, Cgviperin-A and Cgviperin-B showed differential and biased expression patterns in gibel carp adult tissues. Subsequently, using co-immunoprecipitation (Co-IP) screening analysis, both CgViperin-A and CgViperin-B were found to interact with crucian carp (C. auratus) herpesvirus (CaHV) open reading frame 46 right (ORF46R) protein, a negative herpesvirus regulator of host interferon (IFN) production, and to promote the proteasomal degradation of ORF46R via decreasing K63-linked ubiquitination. Additionally, CgViperin-B also mediated ORF46R degradation through autophagosome pathway, which was absent in CgViperin-A. Moreover, we found that the N-terminal α-helix domain was necessary for the localization of CgViperin-A and CgViperin-B at the endoplasmic reticulum (ER), and the C-terminal domain of CgViperin-A and CgViperin-B was indispensable for the interaction with degradation of ORF46R. Therefore, the current findings clarify the divergent antiviral mechanisms of the duplicated viperin homeologs in a recurrent polyploid fish, which will shed light on the evolution of teleost duplicated genes.

Rapid gene evolution in an ancient post-transcriptional and translational regulatory system compensates for meiotic X chromosomal inactivation

SUMMARYIt is conventionally assumed that conserved pathways evolve slowly with little participation of gene evolution. Nevertheless, it has been recently observed that young genes can take over fundamental functions in essential biological processes, for example, development and reproduction. It is unclear how newly duplicated genes are integrated into ancestral networks and reshape the conserved pathways of important functions. Here, we investigated origination and function of two autosomal genes that evolved recently in Drosophila: Poseidon and Zeus, which were created by RNA-based duplications from the X-linked CAF40, a subunit of the conserved CCR4-NOT deadenylase complex involved in post-transcriptional and translational regulation. Knockdown and knockout assays show that the two genes quickly evolved critically important functions in viability and male fertility. Moreover, our transcriptome analysis demonstrates that the three genes have a broad and distinct effect in the expression of hundreds of genes, with almost half of the differentially expressed genes being perturbed exclusively by one paralog, but not the others. Co-immunoprecipitation and tethering assays show that the CAF40 paralog Poseidon maintains the ability to interact with the CCR4-NOT deadenylase complex and might act in post-transcriptional mRNA regulation. The rapid gene evolution in the ancient post-transcriptional and translational regulatory system may be driven by evolution of sex chromosomes to compensate for the meiotic X chromosomal inactivation (MXCI) in Drosophila.