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1. Seasonal heterochrony of reproductive development and gene expression in a polymorphic salamander

   https://doi.org/10.1002/dvdy.744  

   Herrboldt, Madison A; Wright, Claire_N C; Bonett, Ronald M (April 2025, Developmental Dynamics)

   Abstract BackgroundLife cycle evolution includes ecological transitions and shifts in the timing of somatic and reproductive development (heterochrony). However, heterochronic changes can be tissue‐specific, ultimately leading to the differential diversification of traits. Salamanders exhibit alternative life cycle polymorphisms involving either an aquatic to terrestrial metamorphosis (biphasic) or retention of aquatic larval traits into adulthood (paedomorphic). In this study, we used gene expression and histology to evaluate how life cycle evolution impacts temporal reproductive patterns in males of a polymorphic salamander. ResultsWe found that heterochrony shifts the distribution of androgen signaling in the integument, which is correlated with significant differences in seasonal reproductive gland development and pheromone gene expression. In the testes, androgen receptor (ar) expression does not significantly vary between morphs or across seasons. We found significant differences in the onset of spermatogenesis, but by peak breeding season the testes were the same with respect to both histology and gene expression. ConclusionThis study provides an example of how seasonal heterochronic shifts in tissue‐specificargene expression can disparately impact seasonal development and expression patterns across tissues, providing a potential mechanism for differential diversification of reproductive traits. 

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2. Transcription factor binding specificities of the oomycete Phytophthora infestans reflect conserved and divergent evolutionary patterns and predict function

   https://doi.org/10.1186/s12864-024-10630-6  

   Vo, Nguyen_N T; Yang, Ally; Leesutthiphonchai, Wiphawee; Liu, Yulong; Hughes, Timothy R; Judelson, Howard S (December 2024, BMC Genomics)

   Abstract BackgroundIdentifying the DNA-binding specificities of transcription factors (TF) is central to understanding gene networks that regulate growth and development. Such knowledge is lacking in oomycetes, a microbial eukaryotic lineage within the stramenopile group. Oomycetes include many important plant and animal pathogens such as the potato and tomato blight agentPhytophthora infestans, which is a tractable model for studying life-stage differentiation within the group. ResultsMining of the P. infestans genome identified 197 genes encoding proteins belonging to 22 TF families. Their chromosomal distribution was consistent with family expansions through unequal crossing-over, which were likely ancient since each family had similar sizes in most oomycetes. Most TFs exhibited dynamic changes in RNA levels through the P. infestanslife cycle. The DNA-binding preferences of 123 proteins were assayed using protein-binding oligonucleotide microarrays, which succeeded with 73 proteins from 14 families. Binding sites predicted for representatives of the families were validated by electrophoretic mobility shift or chromatin immunoprecipitation assays. Consistent with the substantial evolutionary distance of oomycetes from traditional model organisms, only a subset of the DNA-binding preferences resembled those of human or plant orthologs. Phylogenetic analyses of the TF families withinP. infestansoften discriminated clades with canonical and novel DNA targets. Paralogs with similar binding preferences frequently had distinct patterns of expression suggestive of functional divergence. TFs were predicted to either drive life stage-specific expression or serve as general activators based on the representation of their binding sites within total or developmentally-regulated promoters. This projection was confirmed for one TF using synthetic and mutated promoters fused to reporter genesin vivo. ConclusionsWe established a large dataset of binding specificities forP. infestansTFs, representing the first in the stramenopile group. This resource provides a basis for understanding transcriptional regulation by linking TFs with their targets, which should help delineate the molecular components of processes such as sporulation and host infection. Our work also yielded insight into TF evolution during the eukaryotic radiation, revealing both functional conservation as well as diversification across kingdoms. 

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3. Photomorphogenesis of Myxococcus macrosporus: new insights for light-regulation of cell development

   https://doi.org/10.1007/s43630-024-00635-1  

   Graniczkowska, Kinga B; Bizhga, Dorina; Noda, Moraima; Leon, Viridiana; Saraf, Niharika; Feliz, Denisse; Sharma, Gaurav; Nugent, Angela C; Singer, Mitchell; Stojković, Emina A (October 2024, Photochemical & Photobiological Sciences)

   Abstract Myxobacteria are non-photosynthetic bacteria distinguished among prokaryotes by a multicellular stage in their life cycle known as fruiting bodies that are formed in response to nutrient deprivation and stimulated by light. Here, we report an entrained, rhythmic pattern ofMyxococcus macrosporusfruiting bodies, forming consistently spaced concentric rings when grown in the dark. Light exposure disrupts this rhythmic phenotype, resulting in a sporadic arrangement and reduced fruiting-body count.M. macrosporusgenome encodes a red-light photoreceptor, a bacteriophytochrome (BphP), previously shown to affect the fruiting-body formation in the related myxobacteriumStigmatella aurantiaca. Similarly, the formation ofM. macrosporusfruiting bodies is also impacted by the exposure to BphP—specific wavelengths of light. RNA-Seq analysis ofM. macrosporusrevealed constitutive expression of thebphPgene. Phytochromes, as light-regulated enzymes, control many aspects of plant development including photomorphogenesis. They are intrinsically correlated to circadian clock proteins, impacting the overall light-mediated entrainment of the circadian clock. However, this functional relationship remains unexplored in non-photosynthetic prokaryotes. Genomic analysis unveiled the presence of multiple homologs of cyanobacterial core oscillatory gene,kaiC, in various myxobacteria, includingM. macrosporus,S. aurantiaca and M. xanthus. RNA-Seq analysis verified the expression of allkaiChomologs inM. macrosporusand the closely relatedM. xanthus, which lacksbphPgenes. Overall, this study unravels the rhythmic growth pattern duringM. macrosporusdevelopment, governed by environmental factors such as light and nutrients. In addition, myxobacteria may have a time-measuring mechanism resembling the cyanobacterial circadian clock that links the photoreceptor (BphP) function to the observed rhythmic behavior. Graphical abstract 

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4. Diversification of cnidarian mechanosensory neurons across life cycle phases: evidence from Hydrozoa

   Nakanishi, Nagayasu; Takahash, Mako; Kumano, Gaku (May 2025, Integrative and Comparative Biology)

   Over the course of more than half a billion years of independent evolution, cnidarians (e.g. sea anemones, corals and jellyfishes) have evolved diverse, multicellular, mechanosensory structures ranging from tentacles of hydroids to gravity-sensors of moon jellyfish. The ectodermal epithelium of mechanosensory structures houses the mechanosensory neuron – known as the concentric hair cell – characterized by an apical mechanosensory apparatus consisting of a single cilium surrounded by one or multiple rings of microvilli/stereovilli. While distinct concentric hair cell types are known to occur within life-cycle-stage-specific structures such as the sea anemone tentacles, it is unclear whether diverse concentric hair cell types exist across life cycle phases of any cnidarian. Here we report evidence from the hydrozoan Cladonema pacificum that concentric hair cells of sedentary polyps are distinct from those of free-swimming medusae. By carrying out touch assays, we demonstrate that polyps and medusae exhibit distinct mechanosensory behaviors. Moreover, we find that concentric hair cells in the ectodermal epithelium of touch-sensitive regions in polyps differ from those in medusae in the morphology of apical sensory apparatuses. Furthermore, polyp-type concentric hair cells are not retained in the ectoderm of medusa buds, and medusa-type concentric hair cells begin to form de novo during medusa formation. Taken together, these findings suggest that distinct mechanosensitive behaviors of polyps and medusae are mediated by morphologically different sets of mechanosensory neurons that develop via life-cycle-stage-specific mechanisms. We propose that cell type diversification of mechanosensory neurons occurred not only within a given life cycle phase but across life cycle phases in cnidarian evolution. 

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5. Integrative analyses on the ciliates Colpoda illuminate the life history evolution of soil microorganisms

   https://doi.org/10.1128/msystems.01379-23  

   Li, Haichao; Wu, Kun; Feng, Yuan; Gao, Chao; Wang, Yaohai; Zhang, Yuanyuan; Pan, Jiao; Shen, Xiaopeng; Zufall, Rebecca A; Zhang, Yu; et al (June 2024, mSystems)

   Blanchard, Jeffrey Lawrence (Ed.)

   ABSTRACT Microorganisms play a central role in sustaining soil ecosystems and agriculture, and these functions are usually associated with their complex life history. Yet, the regulation and evolution of life history have remained enigmatic and poorly understood, especially in protozoa, the third most abundant group of organisms in the soil. Here, we explore the life history of a cosmopolitan species—Colpoda steinii. Our analysis has yielded a high-quality macronuclear genome forC. steinii, with size of 155 Mbp and 37,123 protein-coding genes, as well as mean intron length of ~93 bp, longer than most other studied ciliates. Notably, we identify two possible whole-genome duplication events inC. steinii, which may account for its genome being about twice the size ofC. inflata’s, another co-existing species. We further resolve the gene expression profiles in diverse life stages ofC. steinii, which are also corroborated inC. inflata. During the resting cyst stage, genes associated with cell death and vacuole formation are upregulated, and translation-related genes are downregulated. While the translation-related genes are upregulated during the excystment of resting cysts. Reproductive cysts exhibit a significant reduction in cell adhesion. We also demonstrate that most genes expressed in specific life stages are under strong purifying selection. This study offers a deeper understanding of the life history evolution that underpins the extraordinary success and ecological functions of microorganisms in soil ecosystems.IMPORTANCEColpodaspecies, as a prominent group among the most widely distributed and abundant soil microorganisms, play a crucial role in sustaining soil ecosystems and promoting plant growth. This investigation reveals their exceptional macronuclear genomic features, including significantly large genome size, long introns, and numerous gene duplications. The gene expression profiles and the specific biological functions associated with the transitions between various life stages are also elucidated. The vast majority of genes linked to life stage transitions are subject to strong purifying selection, as inferred from multiple natural strains newly isolated and deeply sequenced. This substantiates the enduring and conservative nature ofColpoda’s life history, which has persisted throughout the extensive evolutionary history of these highly successful protozoa in soil. These findings shed light on the evolutionary dynamics of microbial eukaryotes in the ever-fluctuating soil environments. This integrative research represents a significant advancement in understanding the life histories of these understudied single-celled eukaryotes. 

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