CURRENT BIOLOGY

Preferential nitrogen and carbon exchange dynamics in Mucoromycotina "fine root endophyte"-plant symbiosis
Howard NOA, Williams A, Durant E, Pressel S, Daniell TJ and Field KJ
Mucoromycotina "fine root endophyte" (MFRE) fungi are an understudied group of plant symbionts that regularly co-occur with arbuscular mycorrhizal fungi. The functional significance of MFRE in plant nutrition remains underexplored, particularly their role in plant nitrogen (N) assimilation from the variety of sources typically found in soils. Using four N-labeled N sources to track N transfer between MFRE and Plantago lanceolata, applied singly and in tandem, we investigated N source discrimination, preference, and transfer to host plants by MFRE. We traced movement of C from plants to MFRE to determine the impact of N source type on plant carbon (C) allocation to MFRE. We found that MFRE preferentially transferred N derived from glycine and ammonium to plant hosts over that derived from nitrate and urea, regardless of other N sources present. MFRE mycelium supplied with glycine and ammonium contained more plant-derived carbon than those supplied with other N sources. We show that the MFRE directly assimilates and metabolizes organic compounds, retaining C to meet its own metabolic requirements and transferring N to plant hosts. Our findings highlight diversity in the function of endomycorrhizal associations, with potentially profound implications for our understanding of the physiology and ecology of plant-fungal symbioses.
An Ediacaran bilaterian with an ecdysozoan affinity from South Australia
Hughes IV, Evans SD and Droser ML
Molecular clocks and Cambrian-derived metazoans strongly suggest a Neoproterozoic origin of many animal clades. However, fossil bilaterians are rare in the Ediacaran, and no definitive ecdysozoan body fossils are known from the Precambrian. Notably, the base of the Cambrian is characterized by an abundance of trace fossils attributed to priapulid worms, suggesting that major divisions among ecdysozoan groups occurred prior to this time. This is supported by ichnofossils from the latest Ediacaran or early Cambrian left by a plausible nematoid, although definitively attributing this inferred behavior to crown-Nematoida remains contentious in the absence of body fossils. Given the high probability of the evolution of Ecdysozoa in the Proterozoic, the otherwise prolific fossil record of the Ecdysozoa, and the identification of more than 100 distinct Ediacaran genera, it is striking that no Ediacaran body fossils have been confidently assigned to this group. Here, we describe Uncus dzaugisi gen. et. sp. nov. from the Ediacara Member (South Australia), a smooth, vermiform organism with distinct curvature and anterior-posterior differentiation. The depth of relief of Uncus is unique among Ediacara fossils and consistent with a rigid outer cuticle. Ecological relationships and associated trace fossils demonstrate that Uncus was motile. Body morphology and the inferred style of movement are consistent with Nematoida, providing strong evidence for at least an ecdysozoan affinity. This validates the Precambrian origin of Ecdysozoa, reconciling a major gap between predicted patterns of animal evolution and the fossil record..
Ecdysteroid-dependent molting in tardigrades
Yamakawa S and Hejnol A
Although molting is a defining feature of the most species-rich animal taxa-the Ecdysozoa, including arthropods, tardigrades, nematodes, and others-its evolutionary background remains enigmatic. In pancrustaceans, such as insects and decapods, molting is regulated by the ecdysteroid (Ecd) hormone and its downstream cascade (Figure 1A, see also the text). However, whether Ecd-dependent molting predates the emergence of the arthropods and represents an ancestral machinery in ecdysozoans remains unclear. For example, involvement of the Ecd hormone in molting regulation has been suggested only in some parasitic nematodes outside of arthropods, and insect Ecd synthesis and receptor genes are lacking in some ecysozoan lineages (Figure S1A). In this study, we investigated the role of Ecd in the molting process of the tardigrade Hypsibius exemplaris. We show that the endogenous Ecd level periodically increases during the molting cycle of H. exemplaris. The pulse treatment with exogenous Ecd induced molting, whereas an antagonist of the Ecd receptor suppressed the molting. Our spatial and temporal gene expression analysis revealed the putative regulatory organs and Ecd downstream cascades. We demonstrate that tardigrade molting is regulated by the Ecd hormone, supporting the ancestry of Ecd-dependent molting in panarthropods. Furthermore, we were able to identify the putative neural center of molting regulation in tardigrades. This region may be homologous to the neural center in the protocerebrum of pancrustaceans and represent an ancestral state of panarthropods. Together, our results suggest that Ecd-dependent molting evolved in the early-late Ediacaran, 22-76 million years earlier than previously suggested..
Biochemically plausible models of habituation for single-cell learning
Eckert L, Vidal-Saez MS, Zhao Z, Garcia-Ojalvo J, Martinez-Corral R and Gunawardena J
The ability to learn is typically attributed to animals with brains. However, the apparently simplest form of learning, habituation, in which a steadily decreasing response is exhibited to a repeated stimulus, is found not only in animals but also in single-cell organisms and individual mammalian cells. Habituation has been codified from studies in both invertebrate and vertebrate animals as having ten characteristic hallmarks, seven of which involve a single stimulus. Here, we show by mathematical modeling that simple molecular networks, based on plausible biochemistry with common motifs of negative feedback and incoherent feedforward, can robustly exhibit all single-stimulus hallmarks. The models reveal how the hallmarks arise from underlying properties of timescale separation and reversal behavior of memory variables, and they reconcile opposing views of frequency and intensity sensitivity expressed within the neuroscience and cognitive science traditions. Our results suggest that individual cells may exhibit habituation behavior as rich as that which has been codified in multi-cellular animals with central nervous systems and that the relative simplicity of the biomolecular level may enhance our understanding of the mechanisms of learning.
Heat stress: Pollen tubes ROSted by heat stress
Begcy K
Male gametophyte development is highly sensitive to elevated temperatures. A new study identifies potential drivers of reproductive thermoresilience during pollen tube growth by comparing a set of thermotolerant and thermosensitive tomato cultivars.
Impaired pheromone detection and abnormal sexual behavior in female mice deficient for ancV1R
Kondo H, Iwata T, Sato K, Koshiishi R, Suzuki H, Murata K, Spehr M, Touhara K, Nikaido M and Hirota J
Ancient vomeronasal receptor type-1 (ancV1R), a putative vomeronasal receptor, is highly conserved across a wide range of vertebrates and is expressed in the majority of vomeronasal sensory neurons, co-expressing with canonical vomeronasal receptors, V1Rs and V2Rs. The pseudogenization of ancV1R is closely associated with vomeronasal organ (VNO) degeneration, indicating its critical role in pheromone sensing. However, the specific role of ancV1R remains unknown. In this study, to elucidate the function of ancV1R, we conducted phenotypic analyses of ancV1R-deficient female mice. Behavioral analyses showed that ancV1R-deficient females exhibited rejective responses toward male sexual behavior and displayed no preference for male urine. Physiological analyses demonstrate that the loss-of-function mutation of ancV1R reduced VNO response to various pheromone cues, including male urine, the sexual enhancing pheromone exocrine gland-secreting peptide 1 (ESP1), and β-estradiol 3-sulfate. Pre-exposure to ESP1 did not overcome the rejection behavior caused by ancV1R deficiency. Analysis of neural activity in the vomeronasal system revealed increased responses in the medial amygdala and posteromedial cortical amygdala of mutant females upon contact with males but not in response to male urine alone. Additionally, upon male contacts, ancV1R-deficient females exhibited increased neural activity in the lateral septum, a stress-associated brain region, along with elevated stress hormone levels. Such effects were not observed in females exposed solely to male urine. These findings suggest that, in females, ancV1R facilitates VNO responses to pheromone stimuli and plays a crucial role in perceiving males as mating partners. The absence of ancV1R results in failure of male perception, leading to abnormal sexual behaviors and stress responses upon male contact.
Novel off-context experience constrains hippocampal representational drift
Elyasaf G, Rubin A and Ziv Y
The hippocampus forms unique neural representations for distinct experiences, supporting the formation of different memories. Hippocampal representations gradually change over time as animals repeatedly visit the same familiar environment ("representational drift"). Such drift has also been observed in other brain areas, such as the parietal, visual, auditory, and olfactory cortices. While the underlying mechanisms of representational drift remain unclear, a leading hypothesis suggests that it results from ongoing learning processes. According to this hypothesis, because the brain uses the same neural substrates to support multiple distinct representations, learning of novel stimuli or environments leads to changes in the neuronal representation of a familiar one. If this is true, we would expect drift in a given environment to increase following new experiences in other, unrelated environments (i.e., off-context experiences). To test this hypothesis, we longitudinally recorded large populations of hippocampal neurons in mice while they repeatedly visited a familiar linear track over weeks. We introduced off-context experiences by placing mice in a novel environment for 1 h after each visit to the familiar track. Contrary to our expectations, these novel episodes decreased place cells' representational drift. Our findings are consistent with a model in which representations of distinct memories occupy different areas within the neuronal activity space, and the drift of each of them within that space is constrained by the area occupied by the others.
Archaeogenetics: Four letters from Pompeii
Harper K
As archaeogenetics - the study of DNA from (pre-)historical samples - comes of age, it complements and contrasts historical and archaeological records in novel ways. DNA from victims of the eruption of Vesuvius that destroyed Pompeii provides an interesting case study.
Mechanical forces instruct division plane orientation of cambium stem cells during radial growth in Arabidopsis thaliana
Höfler M, Liu X, Greb T and Alim K
Robust regulation of cell division is central to the formation of complex multi-cellular organisms and is a hallmark of stem cell activity. In plants, due to the absence of cell migration, the correct placement of newly produced cell walls during cell division is of eminent importance for generating functional tissues and organs. In particular, during the radial growth of plant shoots and roots, precise regulation and organization of cell divisions in the cambium are essential to produce adjacent xylem and phloem tissues in a strictly bidirectional manner. Although several intercellular signaling cascades have been identified to instruct tissue organization during radial growth, the role of mechanical forces in guiding cambium stem cell activity has been frequently proposed but, so far, not been functionally investigated on the cellular level. Here, we coupled anatomical analyses with a cell-based vertex model to analyze the role of mechanical stress in radial plant growth at the cell and tissue scale. Simulations based on segmented cellular outlines of radially growing Arabidopsis hypocotyls revealed a distinct stress pattern with circumferential stresses in cambium stem cells, which coincided with the orientation of cortical microtubules. Integrating stress patterns as a cue instructing cell division orientation was sufficient for the emergence of typical cambium-derived cell files and agreed with experimental results for stress-related tissue organization in confining mechanical environments. Our work thus underlines the significance of mechanical forces in tissue organization through self-emerging stress patterns during the growth of plant organs.
Plastid translocon recycling in dinoflagellates demonstrates the portability of complex plastids between hosts
Lewis WH, Paris G, Beedessee G, Kořený L, Flores V, Dendooven T, Gallet B, Yee DP, Lam S, Decelle J, Luisi BF and Waller RF
The plastids of photosynthetic organisms on land are predominantly "primary plastids," derived from an ancient endosymbiosis of a cyanobacterium. Conversely, the plastids of marine photosynthetic organisms were mostly gained through subsequent endosymbioses of photosynthetic eukaryotes generating so-called "complex plastids." The plastids of the major eukaryotic lineages-cryptophytes, haptophytes, ochrophytes, dinoflagellates, and apicomplexans-were posited to derive from a single secondary endosymbiosis of a red alga in the "chromalveloate" hypothesis. Subsequent phylogenetic resolution of eukaryotes has shown that separate events of plastid acquisition must have occurred to account for this distribution of plastids. However, the number of such events and the donor organisms for the new plastid endosymbioses are still not resolved. A perceived bottleneck of endosymbiotic plastid gain is the development of protein targeting from the hosts into the new plastids, and this supposition has often driven hypotheses toward minimizing the number of plastid-gain events to explain plastid distribution in eukaryotes. But how plastid-protein-targeting is established for new endosymbionts is often unclear, which makes it difficult to assess the likelihood of plastid transfers between lineages. Here, we show that Kareniaceae dinoflagellates, which possess complex plastids known to be derived from haptophytes, acquired all the necessary protein import machinery from these haptophytes. Furthermore, cryo-electron tomography revealed that no additional membranes were added to the Kareniaceae complex plastid during serial endosymbiosis, suggesting that the haptophyte-derived import processes were sufficient. Our analyses suggest that complex red plastids are preadapted for horizontal transmission, potentially explaining their widespread distribution in algal diversity.
Partially dissociable roles of the orbitofrontal cortex and dorsal hippocampus in context-dependent hierarchical associations
Peterson S, Chavira J, Garcia Arango JA, Seamans D, Cimino ED and Keiflin R
Reward cues are often ambiguous; what is good in one context is not necessarily good in another. To solve this ambiguity, animals form hierarchical associations in which the context gates the retrieval of appropriate cue-evoked memories. These hierarchical associations regulate cue-elicited behavior and influence subsequent learning, promoting the inference of context-dependency. The orbitofrontal cortex (OFC) and dorsal hippocampus (DH) are both proposed to encode a "cognitive map" encompassing hierarchical, context-dependent associations. However, OFC- and DH-specific contributions to the different functional properties of hierarchical associations remain controversial. Using chemogenetic inactivation in rats, we show that the OFC is essential to both properties of hierarchical associations (performance regulation and learning bias). In contrast, DH's role appears limited to the contextual learning bias conferred by hierarchical associations. This work establishes the OFC as a critical orchestrator of hierarchical associations and provides insights into the extended circuits mediating the functional properties of these associations.
Adaptation to visual sparsity enhances responses to isolated stimuli
Gou T, Matulis CA and Clark DA
Sensory systems adapt their response properties to the statistics of their inputs. For instance, visual systems adapt to low-order statistics like mean and variance to encode stimuli efficiently or to facilitate specific downstream computations. However, it remains unclear how other statistical features affect sensory adaptation. Here, we explore how Drosophila's visual motion circuits adapt to stimulus sparsity, a measure of the signal's intermittency not captured by low-order statistics alone. Early visual neurons in both ON and OFF pathways alter their responses dramatically with stimulus sparsity, responding positively to both light and dark sparse stimuli but linearly to dense stimuli. These changes extend to downstream ON and OFF direction-selective neurons, which are activated by sparse stimuli of both polarities but respond with opposite signs to light and dark regions of dense stimuli. Thus, sparse stimuli activate both ON and OFF pathways, recruiting a larger fraction of the circuit and potentially enhancing the salience of isolated stimuli. Overall, our results reveal visual response properties that increase the fraction of the circuit responding to sparse, isolated stimuli.
Plant defense metabolites influence the interaction between an insect herbivore and an entomovirus
Wang JY, Fan NN, Yuan Y, Bass C, Siemann E, Ji XY, Jiang JX and Wan NF
The tri-trophic interaction of plants, insect herbivores, and entomoviruses is an important topic in ecology and pest control. The susceptibility of insect herbivores to entomoviruses (e.g., nucleopolyhedroviruses) is influenced by host plants; however, the role of plant secondary metabolites in determining such susceptibility is poorly understood. Metabolomic analyses of Brassica oleracea, Glycine max, and Ipomoea aquatica plants, which differ in how they affect the susceptibility of Spodoptera exigua to nucleopolyhedroviruses among 14 plants, suggested that the plant secondary metabolites genistein, kaempferol, quercitrin, and coumarin play a role in influencing nucleopolyhedroviruses susceptibility. Subsequently, transcriptomic analysis of caterpillars, treated with nucleopolyhedroviruses alone or with one of these four phenolics, identified four genes (CYP340K4, CXE18, GSTe, and GSTe1) that were significantly downregulated by the phenolics. Functional characterization of these genes suggested that their downregulation significantly increased larval sensitivity to nucleopolyhedroviruses and altered aspects of the immune response. Our findings provide new insight into the role of plant defense metabolites in influencing the interactions between insect herbivores and entomopathogens and identify plant secondary metabolites as potential synergists of viral agents for the control of agricultural pests.
A new and large monofenestratan reveals the evolutionary transition to the pterodactyloid pterosaurs
Hone DWE, Fitch A, Selzer S, Lauer R and Lauer B
For over a century, there was a major gap in our understanding of the evolution of the flying Mesozoic reptiles, the pterosaurs, with a major morphological gap between the early forms and the derived pterodactyloids. Recent discoveries have found a cluster of intermediate forms that have the head and neck of the pterodactyloids but the body of the early grade, yet this still leaves fundamental gaps between these intermediates and both earlier and more derived pterosaurs. Here, we describe a new and large Jurassic pterosaur, Skiphosoura bavarica gen. et sp. nov., preserved in three dimensions, that helps bridge the gap between current intermediate pterosaurs and the pterodactyloids. A new phylogeny shows that there is a general progression of key characteristics of increasing head size, increasing length of neck and wing metacarpal, modification to the fifth toe that supports the rear wing membrane, and gradual reduction in tail length and complexity from earlier pterosaurs into the first pterodactyloids. This also shows a clear evolution of the increasing terrestrial competence of derived pterosaurs. Furthermore, this closes gaps between the intermediates and their ancestors and descendants, and it firmly marks the rhamphorhynchines and ctenochasmatid clades as, respectively, being the closest earliest and latest groups to this succession of transitional forms.
Higher-order cortical and thalamic pathways shape visual processing streams in the mouse cortex
Han X and Bonin V
Mammalian visual functions rely on distributed processing across interconnected cortical and subcortical regions. In higher-order visual areas (HVAs), visual features are processed in specialized streams that integrate feedforward and higher-order inputs from intracortical and thalamocortical pathways. However, the precise circuit organization responsible for HVA specialization remains unclear. We investigated the cellular architecture of primary visual cortex (V1) and higher-order visual pathways in the mouse, focusing on their roles in shaping visual representations. Using in vivo functional imaging and neural circuit tracing, we found that HVAs preferentially receive inputs from both V1 and higher-order pathways tuned to similar spatiotemporal properties, with the strongest selectivity seen in layer 2/3 neurons. These neurons exhibit target-specific tuning and sublaminar specificity in their projections, reflecting cell-type-specific visual information flow. In contrast, HVA layer 5 pathways nonspecifically broadcast visual signals across cortical areas, suggesting a role in distributing HVA outputs. Additionally, thalamocortical pathways from the lateral posterior thalamic nucleus (LP) provide highly specific, nearly non-overlapping visual inputs to HVAs, complementing intracortical inputs and contributing to input functional diversity. Our findings suggest that the convergence of laminar and cell-type-specific pathways V1 and higher-order intracortical and thalamocortical pathways plays a key role in shaping the functional specialization and diversity of HVAs.
Ecology: Re-complexifying impoverished food webs
Schmitz OJ
Traditional conservation holds that non-native species introductions lead to the loss of ecosystem complexity and function. Yet, new research shows that they can restore complexity as well.
A tug-of-war between germ cell motility and intercellular bridges controls germline cyst formation in mice
Levy EW, Leite I, Joyce BW, Shvartsman SY and Posfai E
Gametes in many species develop in cysts-clusters of germ cells formed by incomplete cytokinesis-that remain connected through intercellular bridges (ICBs). These connections enable sharing of cytoplasmic components between germ cells and, in the female germ line, enrich select cells in the cyst to become the oocyte(s). In mice, germline cysts of variable sizes are generated during embryonic development, thought to result from cyst fractures. Studies of fixed samples failed to capture fracture events, and thus, the mechanism remained elusive. Here, we use high-resolution live imaging of germ cells within their native tissue environment to visualize germline cyst dynamics. With this novel approach, we reveal a striking motile phenotype of gonad-resident germ cells and show that this randomly oriented cell-autonomous motile behavior during cyst formation underlies fracture events. Conversely, we show that stabilized ICBs help resist excessive fracturing. Additionally, we find that motility and thus fracture rates gradually decrease during development in a sex-dependent manner, completely ceasing by the end of cyst-forming divisions. These results lead to a model where the opposing activities of developmentally regulated cell motility and stable ICBs give rise to cysts of variable sizes. We corroborate these results by developing a model that uses experimentally measured fracture rates to simulate cyst formation and fracture and show that it can reproduce experimentally measured cyst sizes in both male and female. Understanding how variable cysts form will enable further studies of mammalian oocyte selection and establishment of the ovarian reserve.
Basal ganglia: Uniting circuit logic between matrix and striosome
Kerkhoff WG and Stauffer WR
A new study has identified a novel direct-indirect circuit architecture connecting the striosome compartment of the striatum with midbrain dopamine neurons. This circuit has the potential to integrate limbic and sensorimotor functions and to exert substantial control over biological reinforcement leaning.
Hidden evolutionary constraints dictate the retention of coronavirus accessory genes
Goldstein SA, Feeley TM, Babler KM, Hilbert ZA, Downhour DM, Moshiri N and Elde NC
Coronaviruses exhibit many mechanisms of genetic innovation, including the acquisition of accessory genes that originate by capture of cellular genes or through duplication of existing viral genes. Accessory genes influence viral host range and cellular tropism, but little is known about how selection acts on these variable regions of virus genomes. We used experimental evolution of mouse hepatitis virus (MHV) encoding a cellular AKAP7 phosphodiesterase and an inactive native phosphodiesterase, NS2, to model the evolutionary fate of accessory genes. After courses of serial infection, the gene encoding inactive NS2, ORF2, unexpectedly remained intact, suggesting it is under cryptic constraint uncoupled from the function of NS2. By contrast, AKAP7 was retained under strong selection but rapidly lost under relaxed selection. Experimental evolution also led to altered viral replication in a cell-type-specific manner and changed the relative proportions of subgenomic viral RNA in plaque-purified viral isolates, revealing additional mechanisms of adaptation. Guided by the retention of MHV ORF2 and similar patterns in related betacoronaviruses, we analyzed ORF8 of SARS-CoV-2, which is proposed to have arisen via gene duplication and contains premature stop codons in several globally successful lineages. As with MHV ORF2, the coding-defective SARS-CoV-2 ORF8 gene remained largely intact in these lineages, mirroring patterns observed during MHV experimental evolution, challenging assumptions on the dynamics of gene loss in virus genomes, and extending these findings to viruses currently adapting to humans.
Evolutionary biology: Co-option and the evolution of morphological novelty
Ridgway AM and McGregor AP
The molecular mechanisms underlying evolution of morphological novelties are not well understood, although co-option is often inferred. A new study demonstrates that the partial co-option of the trichome gene regulatory network underlies the evolution of novel projections on Drosophila male genitalia.
Social play fosters cooperation in wild adult chimpanzees
Samuni L, Mielke A, Crockford C and Wittig RM
Adult social play is a universal human trait, promoting the tolerance, bonding, cooperation, and collective action that sustain our large and complex societies. Play serves as a conduit for transmitting positive emotions, thereby stimulating psychological resilience to stressors and facilitating the positive intent and trust essential for cooperation emergence. In contrast, non-human adult social play is considered rare, and its role in cooperation remains unknown. We address this gap by studying the play behavior of 57 adult chimpanzees (Pan troglodytes) in Taï National Park, Côte d'Ivoire, where adult social play and collective action regularly occur. We show that adult female and male chimpanzees play more during times of increased mate competition (with males mainly playing with immatures) and with adult partners they had recent disputes with, highlighting the role of play in regulating social tension that can undermine cooperation. Chimpanzees also preferred playing with adult partners with whom they share strong affiliative bonds, aligning with the idea that play is associated with social familiarity and trust. Finally, adult chimpanzees were more likely to play before collectively defending their territory against outsiders and hunting monkeys. Those who played together were subsequently more likely to collaborate, reinforcing the notion that the positive feedback signaled via play can facilitate cooperation. Our findings demonstrate the sustained significance of adult social play throughout the chimpanzee lifespan, providing valuable insights into the evolution of adult social play and its societal functions, from diffusing tension to supporting social bonds and collective action.