Evolution of diapause in the African turquoise killifish by remodeling ancient gene regulatory landscape

Suspended animation states such as hibernation or diapause allow organisms to survive extreme environments. But the mechanisms underlying the evolution of these extreme survival states are unknown. The African turquoise killifish has evolved diapause as a form of suspended development to survive the complete drought that occurs every year in its habitat. Here we show that many gene duplicates - paralogs - exhibit specialized expression in diapause versus normal development in the African turquoise killifish. Surprisingly, paralogs with specialized expression in diapause are evolutionarily very ancient, and they are also present even in vertebrates that do not exhibit diapause. Profiling the chromatin accessibility landscape among different fish species reveals an evolutionarily recent increase in chromatin accessibility at these very ancient paralogs, suggesting rewiring of their regulatory landscape. The increase in chromatin accessibility in the African turquoise killifish is linked to the presence of new binding sites for transcription factors (e.g., FOXO, REST, and PPAR), due to both de novo mutations and transposable element insertion. Interestingly, accessible chromatin regions in diapause are enriched for lipid metabolism genes. By performing lipidomics in different fish species, we uncover a specific lipid profile in African turquoise killifish embryos in diapause. Notably, select very long-chain fatty acids are high in diapause, suggesting they may be used for long-term survival in this state. Together, our multi-omic analysis indicates that diapause is driven by regulatory innovation of very ancient gene programs that are critical for survival. Our work also suggests a mechanism for how complex adaptations evolve in nature and offers strategies by which a suspended animation program could be reactivated in other species for long-term preservation.

Gonadotrophin-releasing hormone receptors in GtoPdb v.2021.3

GnRH1 and GnRH2 receptors (provisonal nomenclature [39], also called Type I and Type II GnRH receptor, respectively [85]) have been cloned from numerous species, most of which express two or three types of GnRH receptor [85, 84, 114]. GnRH I (p-Glu-His-Trp-Ser-Tyr-Gly-Leu-Arg-Pro-Gly-NH2) is a hypothalamic decapeptide also known as luteinizing hormone-releasing hormone, gonadoliberin, luliberin, gonadorelin or simply as GnRH. It is a member of a family of similar peptides found in many species [85, 84, 114] including GnRH II (pGlu-His-Trp-Ser-His-Gly-Trp-Tyr-Pro-Gly-NH2 (which is also known as chicken GnRH-II). Receptors for three forms of GnRH exist in some species but only GnRH I and GnRH II and their cognate receptors have been found in mammals [85, 84, 114]. GnRH1 receptors are expressed by pituitary gonadotrophs, where they mediate the effects of GnRH on gonadotropin hormone synthesis and secretion that underpin central control of mammalian reproduction. GnRH analogues are used in assisted reproduction and to treat steroid hormone-dependent conditions [58]. Notably, agonists cause desensitization of GnRH-stimulated gonadotropin secretion and the consequent reduction in circulating sex steroids is exploited to treat hormone-dependent cancers of the breast, ovary and prostate [58]. GnRH1 receptors are selectively activated by GnRH I and all lack the COOH-terminal tails found in other GPCRs. GnRH2 receptors do have COOH-terminal tails and (where tested) are selective for GnRH II over GnRH I. GnRH2 receptors are expressed by some primates but not by humans [88]. Phylogenetic classifications divide GnRH receptors into three [85] or five groups [129] and highlight examples of gene loss through evolution, with humans retaining only one ancient gene. The structure of the GnRH1 receptor in complex with elagolix has been elucidated [132].

Ancient Gene Capture and Recent Gene Loss Shape the Evolution of Orthopoxvirus-Host Interaction Genes

Orthopoxviruses (ORPV) include smallpox (variola) virus, one of the most devastating human pathogens, and vaccinia virus, comprising the vaccine used for smallpox eradication. Among roughly 200 ORPV genes, about half are essential for genome replication and expression as well as virion morphogenesis, whereas the remaining half consists of accessory genes counteracting the host immune response.

Ancient gene duplications, rather than polyploidization, facilitate diversification of petal pigmentation patterns in Clarkia gracilis (Onagraceae)

It has been suggested that gene duplication and polyploidization create opportunities for the evolution of novel characters. However, the connections between the effects of polyploidization and morphological novelties have rarely been examined. In this study, we investigated whether petal pigmentation patterning in an allotetraploid Clarkia gracilis has evolved as a result of polyploidization. C. gracilis is thought to be derived through a recent polyploidization event with two diploid species, C. amoena huntiana and an extinct species that is closely related to C. lassenensis. We reconstructed phylogenetic relationships of the R2R3-MYBs (the regulators of petal pigmentation) from two subspecies of C. gracilis and the two purported progenitors, C. a. huntiana and C. lassenensis. The gene tree reveals that these R2R3-MYB genes have arisen through duplications that occurred before the divergence of the two progenitor species, i.e., before polyploidization. After polyploidization and subsequent gene loss, only one of the two orthologous copies inherited from the progenitors was retained in the polyploid, turning it to diploid inheritance. We examined evolutionary changes in these R2R3-MYBs and in their expression, which reveals that the changes affecting patterning (including expression domain contraction, loss-of-function mutation, cis-regulatory mutation) occurred after polyploidization within the C. gracilis lineages. Our results thus suggest that polyploidization itself is not necessary in producing novel petal color patterns. By contrast, duplications of R2R3-MYB genes in the common ancestor of the two progenitors have apparently facilitated diversification of petal pigmentation patterns.

Evolution of the codling moth pheromone via an ancient gene duplication

BackgroundDefining the origin of genetic novelty is central to our understanding of the evolution of novel traits. Diversification among fatty acid desaturase (FAD) genes has played a fundamental role in the introduction of structural variation in fatty acyl derivatives. Because of its central role in generating diversity in insect semiochemicals, the FAD gene family has become a model to study how gene family expansions can contribute to the evolution of lineage-specific innovations. Here we used the codling moth (Cydia pomonella) as a study system to decipher the proximate mechanism underlying the production of the ∆8∆10 signature structure of olethreutine moths. Biosynthesis of the codling moth sex pheromone, (E8,E10)-dodecadienol (codlemone), involves two consecutive desaturation steps, the first of which is unusual in that it generates anE9 unsaturation. The second step is also atypical: it generates a conjugated diene system from theE9 monoene C12intermediate via 1,4-desaturation.ResultsHere we describe the characterization of the FAD gene acting in codlemone biosynthesis. We identify 27 FAD genes corresponding to the various functional classes identified in insects and Lepidoptera. These genes are distributed across theC. pomonellagenome in tandem arrays or isolated genes, indicating that the FAD repertoire consists of both ancient and recent duplications and expansions. Using transcriptomics, we show large divergence in expression domains: some genes appear ubiquitously expressed across tissue and developmental stages; others appear more restricted in their expression pattern. Functional assays using heterologous expression systems reveal that one gene, Cpo_CPRQ, which is prominently and exclusively expressed in the female pheromone gland, encodes an FAD that possesses bothE9 and ∆8∆10 desaturation activities. Phylogenetically, Cpo_CPRQ clusters within the Lepidoptera-specific ∆10/∆11 clade of FADs, a classic reservoir of unusual desaturase activities in moths.ConclusionsOur integrative approach shows that the evolution of the signature pheromone structure of olethreutine moths relied on a gene belonging to an ancient gene expansion. Members of other expanded FAD subfamilies do not appear to play a role in chemical communication. This advises for caution when postulating the consequences of lineage-specific expansions based on genomics alone.

Extensive non-redundancy in a recently duplicated developmental gene family

BackgroundIt has been proposed that recently duplicated genes are more likely to be redundant with one another compared to ancient paralogues. The evolutionary logic underpinning this idea is simple, as the assumption is that recently derived paralogous genes are more similar in sequence compared to members of ancient gene families. We set out to test this idea by using molecular phylogenetics and exploiting the genetic tractability of the model nematode,Caenorhabditis elegans,in studying the nematode-specific family of Hedgehog-related genes, the Warthogs. Hedgehog is one of a handful of signal transduction pathways that underpins the development of bilaterian animals. While having lost abona fideHedgehog gene, most nematodes have evolved an expanded repertoire of Hedgehog-related genes, ten of which reside within the Warthog family.ResultsWe have characterised their evolutionary origin and their roles inC. elegansand found that these genes have adopted new functions in aspects of post-embryonic development, including left–right asymmetry and cell fate determination, akin to the functions of their vertebrate counterparts. Analysis of various double and triple mutants of the Warthog family reveals that more recently derived paralogues are not redundant with one another, while a pair of divergent Warthogs do display redundancy with respect to their function in cuticle biosynthesis.ConclusionsWe have shown that newer members of taxon-restricted gene families are not always functionally redundant despite their recent inception, whereas much older paralogues can be, which is considered paradoxical according to the current framework in gene evolution.

Phylogenetic and biochemical analysis of calsequestrin structure and association of its variants with cardiac disorders

Calsequestrin is among the most abundant proteins in muscle sarcoplasmic reticulum and displays a high capacity but a low affinity for Ca2+ binding. In mammals, calsequestrin is encoded by two genes, CASQ1 and CASQ2, which are expressed almost exclusively in skeletal and cardiac muscles, respectively. Phylogenetic analysis indicates that calsequestrin is an ancient gene in metazoans, and that the duplication of the ancestral calsequestrin gene took place after the emergence of the lancelet. CASQ2 gene variants associated with catecholaminergic polymorphic ventricular tachycardia (CPVT) in humans are positively correlated with a high degree of evolutionary conservation across all calsequestrin homologues. The mutations are distributed in diverse locations of the calsequestrin protein and impart functional diversity but remarkably manifest in a similar phenotype in humans.