Conservation of magnetite biomineralization genes in all domains of life and implications for magnetic sensing

Animals use geomagnetic fields for navigational cues, yet the sensory mechanism underlying magnetic perception remains poorly understood. One idea is that geomagnetic fields are physically transduced by magnetite crystals contained inside specialized receptor cells, but evidence for intracellular, biogenic magnetite in eukaryotes is scant. Certain bacteria produce magnetite crystals inside intracellular compartments, representing the most ancient form of biomineralization known and having evolved prior to emergence of the crown group of eukaryotes, raising the question of whether magnetite biomineralization in eukaryotes and prokaryotes might share a common evolutionary history. Here, we discover that salmonid olfactory epithelium contains magnetite crystals arranged in compact clusters and determine that genes differentially expressed in magnetic olfactory cells, contrasted to nonmagnetic olfactory cells, share ancestry with an ancient prokaryote magnetite biomineralization system, consistent with exaptation for use in eukaryotic magnetoreception. We also show that 11 prokaryote biomineralization genes are universally present among a diverse set of eukaryote taxa and that nine of those genes are present within the Asgard clade of archaea Lokiarchaeota that affiliates with eukaryotes in phylogenomic analysis. Consistent with deep homology, we present an evolutionary genetics hypothesis for magnetite formation among eukaryotes to motivate convergent approaches for examining magnetite-based magnetoreception, molecular origins of matrix-associated biomineralization processes, and eukaryogenesis.

Diversity and Divergence: Evolution of defense chemistry in the tropical tree genus Inga

Plants are widely recognized as chemical factories, with each species producing dozens to hundreds of unique secondary metabolites. These compounds shape the interactions between plants and their natural enemies. Here we explore how plants generate chemical diversity, and what evolutionary processes have led to novel compounds and unique chemical profiles. We comprehensively characterized the chemical profile of one-third of the species of tropical rainforest trees in the genus Inga (~ 100, Fabaceae) and applied phylogenetic comparative methods to understand the mode of chemical defense evolution. We show that: 1) Each Inga species produces exceptionally high levels of phytochemical diversity, despite costs, tradeoffs and biosynthetic constraints. 2) Closely related species have highly divergent defense profiles, with individual compounds, major compound classes and complete profiles showing little to no phylogenetic signal. 3) We show that the evolution of a species' chemical profile shows a signature of divergent adaptation, implying that it is advantageous for a species to have distinct chemistry from close relatives to avoid shared natural enemies. 4) Finally, we hypothesize a model where deep homology of biosynthetic pathways and rapid changes in regulatory mechanisms may better explain the observed large shifts in defense chemicals between closely related taxa.

Pre-metazoan origin of neuropeptide signalling

Neuropeptides are a diverse class of signalling molecules in metazoans. They occur in all animals with a nervous system and also in neuron-less placozoans. However, their origin has remained unclear because no neuropeptide shows deep homology across lineages and none have been found in sponges. Here, we identify two neuropeptide precursors, phoenixin and nesfatin, with broad evolutionary conservation. By database searches, sequence alignments and gene-structure comparisons we show that both precursors are present in bilaterians, cnidarians, ctenophores and sponges. We also found phoenixin and a secreted nesfatin precursor homolog in the choanoflagellate Salpingoeca rosetta. Phoenixin in particular, is highly conserved, including its cleavage sites, suggesting that prohormone processing occurs also in choanoflagellates. In addition, based on phyletic patterns and negative pharmacological assays we question the originally proposed GPR-173 (SREB3) as a phoenixin receptor. Our findings indicate that signalling by secreted neuropeptide homologs has pre-metazoan origins and thus evolved before neurons.

The Shh/Gli3 gene regulatory network precedes the origin of paired fins and reveals the deep homology between distal fins and digits

One of the central problems of vertebrate evolution is understanding the relationship among the distal portions of fins and limbs. Lacking comparable morphological markers of these regions in fish and tetrapods, these relationships have remained uncertain for the past century and a half. Here we show that Gli3 functions in controlling the proliferative expansion of distal progenitors are shared among dorsal and paired fins as well as tetrapod limbs. Mutant knockout gli3 fins in medaka (Oryzias latipes) form multiple radials and rays, in a pattern reminiscent of the polydactyly observed in Gli3-null mutant mice. In limbs, Gli3 controls both anterior–posterior patterning and cell proliferation, two processes that can be genetically uncoupled. In situ hybridization, quantification of proliferation markers, and analysis of regulatory regions reveal that in paired and dorsal fins, gli3 plays a main role in controlling proliferation but not in patterning. Moreover, gli3 down-regulation in shh mutant fins rescues fin loss in a manner similar to how Gli3 deficiency restores digits in the limbs of Shh mutant mouse embryos. We hypothesize that the Gli3/Shh gene pathway preceded the origin of paired appendages and was originally involved in modulating cell proliferation. Accordingly, the distal regions of dorsal fins, paired fins, and limbs retain a deep regulatory and functional homology that predates the origin of paired appendages.

Organization and composition of apicomplexan kinetochores reveals plasticity in chromosome segregation across parasite modes of division

Kinetochores are multiprotein assemblies directing mitotic spindle attachment and chromosome segregation. In apicomplexan parasites, most known kinetochore components and associated regulators are apparently missing, suggesting a minimal structure with limited control over chromosome segregation. In this study, we use interactomics combined with deep homology searches to identify six divergent eukaryotic kinetochore proteins in apicomplexan parasites, in addition to a set of eight apicomplexan components (AKiTs) that bear no detectable sequence similarity to known proteins. The nanoscale organization of the apicomplexan kinetochore includes four subdomains, each displaying different evolutionary rates across the phylum. Functional analyses confirm AKiTs are essential for mitosis and reveal architectures parallel to biorientation at metaphase. Furthermore, we identify a homolog of MAD1 at the apicomplexan kinetochore, suggesting conserved spindle assembly checkpoint signaling. Finally, we show unexpected plasticity in kinetochore composition and segregation throughout the parasite lifecycle, indicating diverse requirements to maintain fidelity of chromosome segregation across apicomplexan modes of division.

Dental replacement in Mesozoic birds: evidence from newly discovered Brazilian enantiornithines

Polyphyodonty—multiple tooth generations—in Mesozoic birds has been confirmed since the nineteenth century. Their dental cycle had been assessed through sparse data from tooth roots revealed through broken jawbones and disattached teeth. However, detailed descriptions of their tooth cycling are lacking, and the specifics of their replacement patterns remain largely unknown. Here we present unprecedented µCT data from three enantiornithine specimens from the Upper Cretaceous of southeastern Brazil. The high resolution µCT data show an alternating dental replacement pattern in the premaxillae, consistent with the widespread pattern amongst extinct and extant reptiles. The dentary also reveals dental replacement at different stages. These results strongly suggest that an alternating pattern was typical of enantiornithine birds. µCT data show that new teeth start lingually within the alveoli, resorb roots of functional teeth and migrate labially into their pulp cavities at an early stage, similar to modern crocodilians. Our results imply that the control mechanism for tooth cycling is conserved during the transition between non-avian reptiles and birds. These first 3D reconstructions of enantiornithine dental replacement demonstrate that 3D data are essential to understand the evolution and deep homology of archosaurian tooth cycling.

DrosophilaMale Accessory Gland Displays Developmental Ground Plan of a Primitive Prostate

Conservation of developmental genetic toolkits of functionally comparable organs from disparate phyla reveals their deep homology, which may help overcome the challenges of their confounding categorization as either homologous or analogous organs. A male accessory sexual organ in mammals, prostate, for instance, is anatomically disparate from its phylogenetically distant counterpart—the male accessory gland (MAG)—in insects likeDrosophila. By examining a select set of toolkit gene expression patterns, here we show thatDrosophilaMAG displays deep homology with the mammalian prostate. Like mammalian prostate, MAG morphogenesis is marked by recruitment of fibroblast growth factor receptor, FGFR, a tubulogenesis toolkit signaling pathway, starting early during its adepithelial genesis. Specialization of the individual domains of the developing MAG tube on the other hand is marked by expression of a posterior Hox gene transcription factor, Abd-B, while Hh-Dpp signaling marks its growth.DrosophilaMAG thus reveals developmental design of unitary bud-derived tube—a ground plan that appears to have been reiteratively co-opted during evolutionary diversification of male accessory sexual organs across distant phylogeny.

The role of CLV signalling in the negative regulation of mycorrhizal colonisation and nitrogen response of tomato

Plants form mutualistic nutrient acquiring symbioses with microbes, including arbuscular mycorrhizal fungi. The formation of these symbioses is costly and plants employ a negative feedback loop termed autoregulation of mycorrhizae (AOM) to limit arbuscular mycorrhizae (AM) formation. We provide evidence for the role of one leucine-rich-repeat receptor like kinase (FAB), a hydroxyproline O-arabinosyltransferase enzyme (FIN) and additional evidence for one receptor like protein (SlCLV2) in the negative regulation of AM formation in tomato. Reciprocal grafting experiments suggest that the FAB gene acts locally in the root, while the SlCLV2 gene may act in both the root and the shoot. External nutrients including phosphate and nitrate can also strongly suppress AM formation. We found that FAB and FIN are required for nitrate suppression of AM but are not required for the powerful suppression of AM colonisation by phosphate. This parallels some of the roles of legume homologs in the autoregulation of the more recently evolved symbioses with nitrogen-fixing bacteria leading to nodulation. This deep homology in the symbiotic role of these genes suggests that in addition to the early signalling events that lead to the establishment of AM and nodulation, the autoregulation pathway might also be considered part of the common symbiotic toolkit that enabled plants to form beneficial symbioses.

The Shh/Gli3 gene regulatory network precedes the origin of paired fins and reveals the deep homology between distal fins and digits

One of the central problems of vertebrate evolution is understanding the relationship among the distal portions of fins and limbs. Lacking comparable morphological markers of these regions in fish and tetrapods, these relationships have remained uncertain for the past century and a half. Here we show that Gli3 functions in controlling the proliferative expansion of distal progenitors are shared among median and paired fins as well as tetrapod limbs. Mutant knockout gli3 fins in medaka (Oryzias latipes) form multiple radials and rays, in a pattern reminiscent of the polydactyly observed in Gli3 null mutant mice. In limbs, Gli3 controls both anterior-posterior patterning and cell proliferation, two processes that can be genetically uncoupled. In situ hybridization, quantification of proliferation markers, and analysis of regulatory regions reveal that in paired and median fins, gli3 plays a main role in controlling proliferation but not in patterning. Moreover, gli3 downregulation in shh mutant fins rescues fin loss in a manner similar to how Gli3-deficiency restores digits in the limbs of Shh mutant mouse embryos. We hypothesize that the Gli3/Shh pathway preceded the origin of paired appendages and was originally involved in modulating cell proliferation. Accordingly, the distal regions of median fins, paired fins, and limbs retain a deep regulatory and functional homology that predates the origin of paired appendages.

The role of CLV signalling in the negative regulation of mycorrhizal colonisation and nitrogen response of tomato

Plants form mutualistic nutrient acquiring symbioses with microbes, including arbuscular mycorrhizal fungi. The formation of these symbioses is costly and plants employ a negative feedback loop termed autoregulation of mycorrhizae (AOM) to limit arbuscular mycorrhizae (AM) formation. We provide evidence for the role of one leucine-rich-repeat receptor like kinase (FAB), a hydroxyproline O-arabinosyltransferase enzyme (FIN) and additional evidence for one receptor like protein (SlCLV2) in the negative regulation of AM formation in tomato. Reciprocal grafting experiments suggest that the FAB gene acts locally in the root, while the SlCLV2 gene may act in both the root and the shoot. External nutrients including phosphate and nitrate can also strongly suppress AM formation. We found that FAB and FIN are required for nitrate suppression of AM but are not required for the powerful suppression of AM colonisation by phosphate. This parallels some of the roles of legume homologs in the autoregulation of the more recently evolved symbioses with nitrogen-fixing bacteria leading to nodulation. This deep homology in the symbiotic role of these genes suggests that in addition to the early signalling events that lead to the establishment of AM and nodulation, the autoregulation pathway might also be considered part of the common symbiotic toolkit that enabled plants to form beneficial symbioses.HighlightWe describe the role of CLV signalling elements in the negative regulation of arbuscular mycorrhizal symbioses of tomato, including influencing nitrate but not phosphate suppression of mycorrhizal colonisation.