Pub Date : 2024-11-05DOI: 10.1016/j.cub.2024.10.022
Michael L Smith, Peter R Marting, Claire S Bailey, Bajaree Chuttong, Erica R Maul, Roberto Molinari, P Prathibha, Ethan B Rowe, Maritza R Spott, Benjamin Koger
Symmetry is pervasive across the tree of life,1,2,3,4,5 and organisms (including humans) build symmetrical structures for reproduction, locomotion, or aesthetics.6,7,8,9 Symmetry, however, does not necessarily span across levels of biological organization (e.g., symmetrical body plans often have asymmetric organs).10 If and how symmetry exists in structures built by social insect collectives, where there is no blueprint or central organizer, remains an open question.11 Here, we show that honey bees actively organize nest contents symmetrically on either side of their double-sided comb; 79% ± 7% of cell contents match their backside counterpart, creating a mirror image inside the nest. Experimentally restricting colonies to opposite sides of comb, we find that independent colonies will symmetrically mimic each other's nest organization. We then examine the mechanism by which independent colonies can indirectly coordinate nest symmetry, showing that 100% of colonies (n = 6) perfectly co-localize their brood nest with a randomly positioned heat source, indicating that heat drives nest site initiation and early brood production. Nest symmetry also has adaptive benefits: two-sided nests grow more quickly, rear more brood, and have a more stable thermal environment than one-sided nests do. Finally, examining the evolutionary origins, we show that symmetry persists in three-dimensional (3D) nests of Apis mellifera and across multiple Apis species, coinciding with the onset of double-sided combs, which made it possible to symmetrically stockpile nest contents. This work shows that, similar to molecular mechanisms that create symmetry in multicellular organisms, there are behavioral processes that create functional symmetry in the collective organization of animal architecture.
{"title":"Form, function, and evolutionary origins of architectural symmetry in honey bee nests.","authors":"Michael L Smith, Peter R Marting, Claire S Bailey, Bajaree Chuttong, Erica R Maul, Roberto Molinari, P Prathibha, Ethan B Rowe, Maritza R Spott, Benjamin Koger","doi":"10.1016/j.cub.2024.10.022","DOIUrl":"https://doi.org/10.1016/j.cub.2024.10.022","url":null,"abstract":"<p><p>Symmetry is pervasive across the tree of life,<sup>1</sup><sup>,</sup><sup>2</sup><sup>,</sup><sup>3</sup><sup>,</sup><sup>4</sup><sup>,</sup><sup>5</sup> and organisms (including humans) build symmetrical structures for reproduction, locomotion, or aesthetics.<sup>6</sup><sup>,</sup><sup>7</sup><sup>,</sup><sup>8</sup><sup>,</sup><sup>9</sup> Symmetry, however, does not necessarily span across levels of biological organization (e.g., symmetrical body plans often have asymmetric organs).<sup>10</sup> If and how symmetry exists in structures built by social insect collectives, where there is no blueprint or central organizer, remains an open question.<sup>11</sup> Here, we show that honey bees actively organize nest contents symmetrically on either side of their double-sided comb; 79% ± 7% of cell contents match their backside counterpart, creating a mirror image inside the nest. Experimentally restricting colonies to opposite sides of comb, we find that independent colonies will symmetrically mimic each other's nest organization. We then examine the mechanism by which independent colonies can indirectly coordinate nest symmetry, showing that 100% of colonies (n = 6) perfectly co-localize their brood nest with a randomly positioned heat source, indicating that heat drives nest site initiation and early brood production. Nest symmetry also has adaptive benefits: two-sided nests grow more quickly, rear more brood, and have a more stable thermal environment than one-sided nests do. Finally, examining the evolutionary origins, we show that symmetry persists in three-dimensional (3D) nests of Apis mellifera and across multiple Apis species, coinciding with the onset of double-sided combs, which made it possible to symmetrically stockpile nest contents. This work shows that, similar to molecular mechanisms that create symmetry in multicellular organisms, there are behavioral processes that create functional symmetry in the collective organization of animal architecture.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":" ","pages":""},"PeriodicalIF":8.1,"publicationDate":"2024-11-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142603659","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-04Epub Date: 2024-10-09DOI: 10.1016/j.cub.2024.09.030
Nicole E Peltier, Akiyuki Anzai, Rubén Moreno-Bote, Gregory C DeAngelis
For the brain to compute object motion in the world during self-motion, it must discount the global patterns of image motion (optic flow) caused by self-motion. Optic flow parsing is a proposed visual mechanism for computing object motion in the world, and studies in both humans and monkeys have demonstrated perceptual biases consistent with the operation of a flow-parsing mechanism. However, the neural basis of flow parsing remains unknown. We demonstrate, at both the individual unit and population levels, that neural activity in macaque middle temporal (MT) area is biased by peripheral optic flow in a manner that can at least partially account for perceptual biases induced by flow parsing. These effects cannot be explained by conventional surround suppression mechanisms or choice-related activity and have substantial neural latency. Together, our findings establish the first neural basis for the computation of scene-relative object motion based on flow parsing.
{"title":"A neural mechanism for optic flow parsing in macaque visual cortex.","authors":"Nicole E Peltier, Akiyuki Anzai, Rubén Moreno-Bote, Gregory C DeAngelis","doi":"10.1016/j.cub.2024.09.030","DOIUrl":"10.1016/j.cub.2024.09.030","url":null,"abstract":"<p><p>For the brain to compute object motion in the world during self-motion, it must discount the global patterns of image motion (optic flow) caused by self-motion. Optic flow parsing is a proposed visual mechanism for computing object motion in the world, and studies in both humans and monkeys have demonstrated perceptual biases consistent with the operation of a flow-parsing mechanism. However, the neural basis of flow parsing remains unknown. We demonstrate, at both the individual unit and population levels, that neural activity in macaque middle temporal (MT) area is biased by peripheral optic flow in a manner that can at least partially account for perceptual biases induced by flow parsing. These effects cannot be explained by conventional surround suppression mechanisms or choice-related activity and have substantial neural latency. Together, our findings establish the first neural basis for the computation of scene-relative object motion based on flow parsing.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":" ","pages":"4983-4997.e9"},"PeriodicalIF":8.1,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11537840/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142399716","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-04DOI: 10.1016/j.cub.2024.10.019
Daniel M Hooper, Callum S McDiarmid, Matthew J Powers, Nicholas M Justyn, Marek Kučka, Nathan S Hart, Geoffrey E Hill, Peter Andolfatto, Yingguang Frank Chan, Simon C Griffith
Carotenoid pigments produce the yellow and red colors of birds and other vertebrates. Despite their importance in social signaling and sexual selection, our understanding of how carotenoid ornamentation evolves in nature remains limited. Here, we examine the long-tailed finch Poephila acuticauda, an Australian songbird with a yellow-billed western subspecies acuticauda and a red-billed eastern subspecies hecki, which hybridize where their ranges overlap. We found that yellow bills can be explained by the loss of C(4)-oxidation, thus preventing yellow dietary carotenoids from being converted to red. Combining linked-read genomic sequencing and reflectance spectrophotometry measurements of bill color collected from wild-sampled finches and laboratory crosses, we identify four loci that together explain 53% of variance in this trait. The two loci of largest effect contain the genes CYP2J19, an essential enzyme for producing red carotenoids, and TTC39B, an enhancer of carotenoid metabolism. A paucity of protein-coding changes and an enrichment of associated upstream variants suggest that the loss of C(4)-oxidation results from cis-regulatory evolution. Evolutionary genealogy reconstruction indicates that the red-billed phenotype is ancestral and that yellow alleles at CYP2J19 and TTC39B first arose and fixed in acuticauda approximately 100 kya. Yellow alleles subsequently introgressed into hecki less than 5 kya. Across all color loci, acuticauda-derived variants show evidence of selective sweeps, implying that yellow bill coloration has been favored by natural selection. Our study illustrates how evolutionary transitions between yellow and red coloration can be achieved by successive selective events acting on regulatory changes at a few interacting genes.
{"title":"Spread of yellow-bill-color alleles favored by selection in the long-tailed finch hybrid system.","authors":"Daniel M Hooper, Callum S McDiarmid, Matthew J Powers, Nicholas M Justyn, Marek Kučka, Nathan S Hart, Geoffrey E Hill, Peter Andolfatto, Yingguang Frank Chan, Simon C Griffith","doi":"10.1016/j.cub.2024.10.019","DOIUrl":"10.1016/j.cub.2024.10.019","url":null,"abstract":"<p><p>Carotenoid pigments produce the yellow and red colors of birds and other vertebrates. Despite their importance in social signaling and sexual selection, our understanding of how carotenoid ornamentation evolves in nature remains limited. Here, we examine the long-tailed finch Poephila acuticauda, an Australian songbird with a yellow-billed western subspecies acuticauda and a red-billed eastern subspecies hecki, which hybridize where their ranges overlap. We found that yellow bills can be explained by the loss of C(4)-oxidation, thus preventing yellow dietary carotenoids from being converted to red. Combining linked-read genomic sequencing and reflectance spectrophotometry measurements of bill color collected from wild-sampled finches and laboratory crosses, we identify four loci that together explain 53% of variance in this trait. The two loci of largest effect contain the genes CYP2J19, an essential enzyme for producing red carotenoids, and TTC39B, an enhancer of carotenoid metabolism. A paucity of protein-coding changes and an enrichment of associated upstream variants suggest that the loss of C(4)-oxidation results from cis-regulatory evolution. Evolutionary genealogy reconstruction indicates that the red-billed phenotype is ancestral and that yellow alleles at CYP2J19 and TTC39B first arose and fixed in acuticauda approximately 100 kya. Yellow alleles subsequently introgressed into hecki less than 5 kya. Across all color loci, acuticauda-derived variants show evidence of selective sweeps, implying that yellow bill coloration has been favored by natural selection. Our study illustrates how evolutionary transitions between yellow and red coloration can be achieved by successive selective events acting on regulatory changes at a few interacting genes.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":" ","pages":""},"PeriodicalIF":8.1,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142582203","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Formin is an important player in promoting apical actin polymerization in pollen tubes, but the mechanism regulating its activity remains unknown. We here identify REN1, a Rho GTPase-activating protein, as a negative regulator of formins in Arabidopsis pollen tubes. Specifically, we found that depletion of REN1 promotes apical actin polymerization and increases the amount of filamentous actin in pollen tubes. Interestingly, the effect of REN1 loss of function phenocopies the effect of formin gain of function, as it causes the formation of supernumerary membrane-derived actin bundles, which leads to tube swelling and membrane deformation. Importantly, inhibition of formins suppresses the phenotypic defects in ren1 mutant pollen tubes. We further demonstrate that REN1 physically interacts with the Arabidopsis formin protein AtFH5, predominantly with the C terminus, and inhibits the ability of AtFH5 to nucleate and assemble actin in vitro. Depletion of AtFH5 partially suppresses the phenotype in ren1 mutant pollen tubes, demonstrating that REN1 regulates apical actin polymerization at least partially through inhibiting AtFH5. We thus uncover a novel mechanism regulating formins and actin polymerization in plants.
{"title":"A RhoGAP controls apical actin polymerization by inhibiting formin in Arabidopsis pollen tubes.","authors":"Yanan Xu, Jiangfeng Shen, Huaqiang Ruan, Xiaolu Qu, Yingchao Li, Yingjie Wang, Peiyu Li, Ran Yi, Haiyun Ren, Yi Zhang, Shanjin Huang","doi":"10.1016/j.cub.2024.09.053","DOIUrl":"10.1016/j.cub.2024.09.053","url":null,"abstract":"<p><p>Formin is an important player in promoting apical actin polymerization in pollen tubes, but the mechanism regulating its activity remains unknown. We here identify REN1, a Rho GTPase-activating protein, as a negative regulator of formins in Arabidopsis pollen tubes. Specifically, we found that depletion of REN1 promotes apical actin polymerization and increases the amount of filamentous actin in pollen tubes. Interestingly, the effect of REN1 loss of function phenocopies the effect of formin gain of function, as it causes the formation of supernumerary membrane-derived actin bundles, which leads to tube swelling and membrane deformation. Importantly, inhibition of formins suppresses the phenotypic defects in ren1 mutant pollen tubes. We further demonstrate that REN1 physically interacts with the Arabidopsis formin protein AtFH5, predominantly with the C terminus, and inhibits the ability of AtFH5 to nucleate and assemble actin in vitro. Depletion of AtFH5 partially suppresses the phenotype in ren1 mutant pollen tubes, demonstrating that REN1 regulates apical actin polymerization at least partially through inhibiting AtFH5. We thus uncover a novel mechanism regulating formins and actin polymerization in plants.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":" ","pages":"5040-5053.e6"},"PeriodicalIF":8.1,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142460458","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-04Epub Date: 2024-10-11DOI: 10.1016/j.cub.2024.09.034
Carlos M Rodriguez-Reza, Aya Sato-Carlton, Peter M Carlton
Sensing and control of size are critical for cellular function and survival. A striking example of size sensing occurs during meiosis in the nematode Caenorhabditis elegans. C. elegans chromosomes compare the lengths of the two chromosome "arms" demarcated by the position of their single off-center crossover, and they differentially modify these arms to ensure that sister chromatid cohesion is lost specifically on the shorter arm in the first meiotic division, while the longer arm maintains cohesion until the second division. While many of the downstream steps leading to cohesion loss have been characterized, the length-sensing process itself remains poorly understood. Here, we have used cytological visualization of short and long chromosome arms, combined with quantitative microscopy, live imaging, and simulations, to investigate the principles underlying length-sensitive chromosome partitioning. By quantitatively analyzing short-arm designation patterns on fusion chromosomes carrying multiple crossovers, we develop a model in which a short-arm-determining factor originates at crossover designation sites, diffuses within the synaptonemal complex, and accumulates within crossover-bounded chromosome segments. We demonstrate experimental support for a critical assumption of this model: that crossovers act as boundaries to diffusion within the synaptonemal complex. Further, we develop a discrete simulation based on our results that recapitulates a wide variety of observed partitioning outcomes in both wild-type and previously reported mutants. Our results suggest that the concentration of a diffusible factor is used as a proxy for chromosome length, enabling the correct designation of short and long arms and proper segregation of chromosomes.
{"title":"Length-sensitive partitioning of Caenorhabditis elegans meiotic chromosomes responds to proximity and number of crossover sites.","authors":"Carlos M Rodriguez-Reza, Aya Sato-Carlton, Peter M Carlton","doi":"10.1016/j.cub.2024.09.034","DOIUrl":"10.1016/j.cub.2024.09.034","url":null,"abstract":"<p><p>Sensing and control of size are critical for cellular function and survival. A striking example of size sensing occurs during meiosis in the nematode Caenorhabditis elegans. C. elegans chromosomes compare the lengths of the two chromosome \"arms\" demarcated by the position of their single off-center crossover, and they differentially modify these arms to ensure that sister chromatid cohesion is lost specifically on the shorter arm in the first meiotic division, while the longer arm maintains cohesion until the second division. While many of the downstream steps leading to cohesion loss have been characterized, the length-sensing process itself remains poorly understood. Here, we have used cytological visualization of short and long chromosome arms, combined with quantitative microscopy, live imaging, and simulations, to investigate the principles underlying length-sensitive chromosome partitioning. By quantitatively analyzing short-arm designation patterns on fusion chromosomes carrying multiple crossovers, we develop a model in which a short-arm-determining factor originates at crossover designation sites, diffuses within the synaptonemal complex, and accumulates within crossover-bounded chromosome segments. We demonstrate experimental support for a critical assumption of this model: that crossovers act as boundaries to diffusion within the synaptonemal complex. Further, we develop a discrete simulation based on our results that recapitulates a wide variety of observed partitioning outcomes in both wild-type and previously reported mutants. Our results suggest that the concentration of a diffusible factor is used as a proxy for chromosome length, enabling the correct designation of short and long arms and proper segregation of chromosomes.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":" ","pages":"4998-5016.e6"},"PeriodicalIF":8.1,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142460482","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-04DOI: 10.1016/j.cub.2024.09.078
Eve V Kakudji, Samantha C Lewis
Eve Kakudji and Samantha Lewis discuss the structure and function of mitochondrial nucleoids - large nucleoprotein complexes containing mitochondrial DNA and the regulatory factors necessary for its packaging, replication, transcription, and repair.
Eve Kakudji 和 Samantha Lewis 讨论了线粒体核苷酸的结构和功能--大型核蛋白复合物包含线粒体 DNA 及其包装、复制、转录和修复所需的调控因子。
{"title":"Mitochondrial nucleoids.","authors":"Eve V Kakudji, Samantha C Lewis","doi":"10.1016/j.cub.2024.09.078","DOIUrl":"https://doi.org/10.1016/j.cub.2024.09.078","url":null,"abstract":"<p><p>Eve Kakudji and Samantha Lewis discuss the structure and function of mitochondrial nucleoids - large nucleoprotein complexes containing mitochondrial DNA and the regulatory factors necessary for its packaging, replication, transcription, and repair.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":"34 21","pages":"R1067-R1068"},"PeriodicalIF":8.1,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142582233","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-04Epub Date: 2024-10-02DOI: 10.1016/j.cub.2024.09.012
David Alais, David Burr, Thomas A Carlson
Food is fundamental to survival, and our brains are highly attuned to rapidly process food stimuli. Neural signals show that foods can be discriminated as edible or inedible as early as 85 ms after stimulus onset,1 distinguished as processed or unprocessed beginning at 130 ms,2 and as high or low density from 165 ms.3 Recent evidence revealed specialized processing of food stimuli in the ventral visual pathway,4,5,6 an area that underlies perception of faces and other important objects. For many visual objects, perception can be biased toward recent perceptual history (known as serial dependence7,8). We examined serial dependence for food in two large samples (n > 300) who rated sequences of food images for either "appeal" or "calories." Ratings for calories were highly correlated between participants and were similar for males and females. Appeal ratings varied considerably between participants, consistent with the idiosyncratic nature of food preferences, and tended to be higher for males than females. High-calorie ratings were associated with high appeal, especially in males. Importantly, response biases showed clear positive serial dependences: higher stimulus values in the previous trials led to positive biases, and vice versa. The effects were similar for males and females and for calories and appeal ratings and were remarkably consistent across participants. These findings square with recently found food selectively in the visual temporal cortex, reveal a new mechanism influencing food decision-making, and suggest a new sensory-level component that could complement cognitive strategies in diet intervention.
{"title":"Positive serial dependence in ratings of food images for appeal and calories.","authors":"David Alais, David Burr, Thomas A Carlson","doi":"10.1016/j.cub.2024.09.012","DOIUrl":"10.1016/j.cub.2024.09.012","url":null,"abstract":"<p><p>Food is fundamental to survival, and our brains are highly attuned to rapidly process food stimuli. Neural signals show that foods can be discriminated as edible or inedible as early as 85 ms after stimulus onset,<sup>1</sup> distinguished as processed or unprocessed beginning at 130 ms,<sup>2</sup> and as high or low density from 165 ms.<sup>3</sup> Recent evidence revealed specialized processing of food stimuli in the ventral visual pathway,<sup>4</sup><sup>,</sup><sup>5</sup><sup>,</sup><sup>6</sup> an area that underlies perception of faces and other important objects. For many visual objects, perception can be biased toward recent perceptual history (known as serial dependence<sup>7</sup><sup>,</sup><sup>8</sup>). We examined serial dependence for food in two large samples (n > 300) who rated sequences of food images for either \"appeal\" or \"calories.\" Ratings for calories were highly correlated between participants and were similar for males and females. Appeal ratings varied considerably between participants, consistent with the idiosyncratic nature of food preferences, and tended to be higher for males than females. High-calorie ratings were associated with high appeal, especially in males. Importantly, response biases showed clear positive serial dependences: higher stimulus values in the previous trials led to positive biases, and vice versa. The effects were similar for males and females and for calories and appeal ratings and were remarkably consistent across participants. These findings square with recently found food selectively in the visual temporal cortex, reveal a new mechanism influencing food decision-making, and suggest a new sensory-level component that could complement cognitive strategies in diet intervention.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":" ","pages":"5090-5096.e1"},"PeriodicalIF":8.1,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11537180/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142371307","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-04Epub Date: 2024-10-08DOI: 10.1016/j.cub.2024.09.020
Adil R Wani, Budhaditya Chowdhury, Jenny Luong, Gonzalo Morales Chaya, Krishna Patel, Jesse Isaacman-Beck, Matthew S Kayser, Mubarak Hussain Syed
Complex behaviors arise from neural circuits that assemble from diverse cell types. Sleep is a conserved behavior essential for survival, yet little is known about how the nervous system generates neuron types of a sleep-wake circuit. Here, we focus on the specification of Drosophila 23E10-labeled dorsal fan-shaped body (dFB) long-field tangential input neurons that project to the dorsal layers of the fan-shaped body neuropil in the central complex. We use lineage analysis and genetic birth dating to identify two bilateral type II neural stem cells (NSCs) that generate 23E10 dFB neurons. We show that adult 23E10 dFB neurons express ecdysone-induced protein 93 (E93) and that loss of ecdysone signaling or E93 in type II NSCs results in their misspecification. Finally, we show that E93 knockdown in type II NSCs impairs adult sleep behavior. Our results provide insight into how extrinsic hormonal signaling acts on NSCs to generate the neuronal diversity required for adult sleep behavior. These findings suggest that some adult sleep disorders might derive from defects in stem cell-specific temporal neurodevelopmental programs.
复杂的行为产生于由不同类型细胞组成的神经回路。睡眠是一种对生存至关重要的保守行为,但人们对神经系统如何产生睡眠-觉醒回路的神经元类型知之甚少。在这里,我们重点研究了果蝇23E10标记的背侧扇形体(dFB)长场切向输入神经元的规格,这些神经元投射到中央复合体中扇形体神经鞘的背层。我们利用品系分析和遗传测年法鉴定了两种生成 23E10 dFB 神经元的双侧 II 型神经干细胞(NSCs)。我们发现,成年 23E10 dFB 神经元表达蜕皮激素诱导蛋白 93(E93),而 II 型神经干细胞中蜕皮激素信号或 E93 的缺失会导致它们的规格错误。最后,我们发现在 II 型 NSCs 中敲除 E93 会损害成人的睡眠行为。我们的研究结果让我们深入了解了外在激素信号如何作用于 NSCs,从而产生成人睡眠行为所需的神经元多样性。这些发现表明,一些成人睡眠障碍可能源于干细胞特异性时间神经发育程序的缺陷。
{"title":"Stem cell-specific ecdysone signaling regulates the development of dorsal fan-shaped body neurons and sleep homeostasis.","authors":"Adil R Wani, Budhaditya Chowdhury, Jenny Luong, Gonzalo Morales Chaya, Krishna Patel, Jesse Isaacman-Beck, Matthew S Kayser, Mubarak Hussain Syed","doi":"10.1016/j.cub.2024.09.020","DOIUrl":"10.1016/j.cub.2024.09.020","url":null,"abstract":"<p><p>Complex behaviors arise from neural circuits that assemble from diverse cell types. Sleep is a conserved behavior essential for survival, yet little is known about how the nervous system generates neuron types of a sleep-wake circuit. Here, we focus on the specification of Drosophila 23E10-labeled dorsal fan-shaped body (dFB) long-field tangential input neurons that project to the dorsal layers of the fan-shaped body neuropil in the central complex. We use lineage analysis and genetic birth dating to identify two bilateral type II neural stem cells (NSCs) that generate 23E10 dFB neurons. We show that adult 23E10 dFB neurons express ecdysone-induced protein 93 (E93) and that loss of ecdysone signaling or E93 in type II NSCs results in their misspecification. Finally, we show that E93 knockdown in type II NSCs impairs adult sleep behavior. Our results provide insight into how extrinsic hormonal signaling acts on NSCs to generate the neuronal diversity required for adult sleep behavior. These findings suggest that some adult sleep disorders might derive from defects in stem cell-specific temporal neurodevelopmental programs.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":" ","pages":"4951-4967.e5"},"PeriodicalIF":8.1,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11537841/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142388865","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-04Epub Date: 2024-10-07DOI: 10.1016/j.cub.2024.09.019
Adrien Anckaert, Stéphane Declerck, Laure-Anne Poussart, Stéphanie Lambert, Catherine Helmus, Farah Boubsi, Sébastien Steels, Anthony Argüelles-Arias, Maryline Calonne-Salmon, Marc Ongena
Arbuscular mycorrhizal (AM) fungi (e.g., Rhizophagus species) recruit specific bacterial species in their hyphosphere. However, the chemical interplay and the mutual benefit of this intricate partnership have not been investigated yet, especially as it involves bacteria known as strong producers of antifungal compounds such as Bacillus velezensis. Here, we show that the soil-dwelling B. velezensis migrates along the hyphal network of the AM fungus R. irregularis, forming biofilms and inducing cytoplasmic flow in the AM fungus that contributes to host plant root colonization by the bacterium. During hyphosphere colonization, R. irregularis modulates the biosynthesis of specialized metabolites in B. velezensis to ensure stable coexistence and as a mechanism to ward off mycoparasitic fungi and bacteria. These mutual benefits are extended into a tripartite context via the provision of enhanced protection to the host plant through the induction of systemic resistance.
丛枝菌根(AM)真菌(如根瘤菌属)在其下膜中吸收特定的细菌物种。然而,这种错综复杂的合作关系中的化学相互作用和互惠互利尚未得到研究,尤其是涉及到已知具有很强的抗真菌化合物产生能力的细菌,如 Velezensis 杆菌。在这里,我们发现,生活在土壤中的 B. velezensis 会沿着互作真菌 R. irregularis 的菌丝网络迁移,形成生物膜并诱导互作真菌的细胞质流动,从而促进细菌在寄主植物根部的定殖。在下球定殖过程中,R. irregularis 会调节 B. velezensis 中特殊代谢物的生物合成,以确保稳定共存,并作为一种抵御寄生真菌和细菌的机制。通过诱导宿主植物产生系统抗性,为宿主植物提供更强的保护,从而将这些互利关系扩展到三方关系中。
{"title":"The biology and chemistry of a mutualism between a soil bacterium and a mycorrhizal fungus.","authors":"Adrien Anckaert, Stéphane Declerck, Laure-Anne Poussart, Stéphanie Lambert, Catherine Helmus, Farah Boubsi, Sébastien Steels, Anthony Argüelles-Arias, Maryline Calonne-Salmon, Marc Ongena","doi":"10.1016/j.cub.2024.09.019","DOIUrl":"10.1016/j.cub.2024.09.019","url":null,"abstract":"<p><p>Arbuscular mycorrhizal (AM) fungi (e.g., Rhizophagus species) recruit specific bacterial species in their hyphosphere. However, the chemical interplay and the mutual benefit of this intricate partnership have not been investigated yet, especially as it involves bacteria known as strong producers of antifungal compounds such as Bacillus velezensis. Here, we show that the soil-dwelling B. velezensis migrates along the hyphal network of the AM fungus R. irregularis, forming biofilms and inducing cytoplasmic flow in the AM fungus that contributes to host plant root colonization by the bacterium. During hyphosphere colonization, R. irregularis modulates the biosynthesis of specialized metabolites in B. velezensis to ensure stable coexistence and as a mechanism to ward off mycoparasitic fungi and bacteria. These mutual benefits are extended into a tripartite context via the provision of enhanced protection to the host plant through the induction of systemic resistance.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":" ","pages":"4934-4950.e8"},"PeriodicalIF":8.1,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142388866","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Pub Date : 2024-11-04Epub Date: 2024-10-04DOI: 10.1016/j.cub.2024.09.015
Nathan W Cooper, Scott W Yanco, Clark S Rushing, T Scott Sillett, Peter P Marra
Identifying the processes that limit populations is a foundational objective of ecology and an urgent need for conservation. For migratory animals, researchers must study individuals throughout their annual cycles to determine how environmental conditions limit demographic rates within each period of the annual cycle and also between periods through carry-over effects and seasonal interactions.1,2,3,4,5,6 Our poor understanding of the rates and causes of avian migration mortality7 hinders the identification of limiting factors and the reversal of widespread avian population declines.8,9 Here, we implement new methods to estimate apparent survival (hereafter survival) during migration directly from automated telemetry data10 in Kirtland's Warblers (Setophaga kirtlandii) and indirectly from mark-recapture data in Black-throated Blue Warblers (S. caerulescens). Previous experimental and observational studies of our focal species and other migratory songbirds have shown strong effects of Caribbean precipitation and habitat quality on food availability,11,12,13,14 body condition,12,13,14,15,16,17,18,19 migration timing,11,12,15,16,20,21,22,23 natal dispersal,24,25 range dynamics,26 reproductive success,20,22,27 and annual survival.18,19,20,23,28,29,30,31 Building on this research, we test the hypotheses that environmental conditions during the non-breeding period affect subsequent survival during spring migration and breeding. We found that reduced precipitation and environmental productivity in the non-breeding period strongly influenced survival in both species, primarily by reducing survival during spring migration. Our results indicate that climate-driven environmental conditions can carry over to affect survival in subsequent periods and thus likely play an important role in year-round population dynamics. These lethal carry-over effects may be widespread and are likely magnified by intensifying climate change.
{"title":"Non-breeding conditions induce carry-over effects on survival of migratory birds.","authors":"Nathan W Cooper, Scott W Yanco, Clark S Rushing, T Scott Sillett, Peter P Marra","doi":"10.1016/j.cub.2024.09.015","DOIUrl":"10.1016/j.cub.2024.09.015","url":null,"abstract":"<p><p>Identifying the processes that limit populations is a foundational objective of ecology and an urgent need for conservation. For migratory animals, researchers must study individuals throughout their annual cycles to determine how environmental conditions limit demographic rates within each period of the annual cycle and also between periods through carry-over effects and seasonal interactions.<sup>1</sup><sup>,</sup><sup>2</sup><sup>,</sup><sup>3</sup><sup>,</sup><sup>4</sup><sup>,</sup><sup>5</sup><sup>,</sup><sup>6</sup> Our poor understanding of the rates and causes of avian migration mortality<sup>7</sup> hinders the identification of limiting factors and the reversal of widespread avian population declines.<sup>8</sup><sup>,</sup><sup>9</sup> Here, we implement new methods to estimate apparent survival (hereafter survival) during migration directly from automated telemetry data<sup>10</sup> in Kirtland's Warblers (Setophaga kirtlandii) and indirectly from mark-recapture data in Black-throated Blue Warblers (S. caerulescens). Previous experimental and observational studies of our focal species and other migratory songbirds have shown strong effects of Caribbean precipitation and habitat quality on food availability,<sup>11</sup><sup>,</sup><sup>12</sup><sup>,</sup><sup>13</sup><sup>,</sup><sup>14</sup> body condition,<sup>12</sup><sup>,</sup><sup>13</sup><sup>,</sup><sup>14</sup><sup>,</sup><sup>15</sup><sup>,</sup><sup>16</sup><sup>,</sup><sup>17</sup><sup>,</sup><sup>18</sup><sup>,</sup><sup>19</sup> migration timing,<sup>11</sup><sup>,</sup><sup>12</sup><sup>,</sup><sup>15</sup><sup>,</sup><sup>16</sup><sup>,</sup><sup>20</sup><sup>,</sup><sup>21</sup><sup>,</sup><sup>22</sup><sup>,</sup><sup>23</sup> natal dispersal,<sup>24</sup><sup>,</sup><sup>25</sup> range dynamics,<sup>26</sup> reproductive success,<sup>20</sup><sup>,</sup><sup>22</sup><sup>,</sup><sup>27</sup> and annual survival.<sup>18</sup><sup>,</sup><sup>19</sup><sup>,</sup><sup>20</sup><sup>,</sup><sup>23</sup><sup>,</sup><sup>28</sup><sup>,</sup><sup>29</sup><sup>,</sup><sup>30</sup><sup>,</sup><sup>31</sup> Building on this research, we test the hypotheses that environmental conditions during the non-breeding period affect subsequent survival during spring migration and breeding. We found that reduced precipitation and environmental productivity in the non-breeding period strongly influenced survival in both species, primarily by reducing survival during spring migration. Our results indicate that climate-driven environmental conditions can carry over to affect survival in subsequent periods and thus likely play an important role in year-round population dynamics. These lethal carry-over effects may be widespread and are likely magnified by intensifying climate change.</p>","PeriodicalId":11359,"journal":{"name":"Current Biology","volume":" ","pages":"5097-5103.e3"},"PeriodicalIF":8.1,"publicationDate":"2024-11-04","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142379239","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":1,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}