气候变化领域集成服务门户(CCPortal): A unique Malpighian tubule architecture in Tribolium castaneum informs the evolutionary origins of systemic osmoregulation in beetles

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DOI	10.1073/pnas.2023314118
	A unique Malpighian tubule architecture in Tribolium castaneum informs the evolutionary origins of systemic osmoregulation in beetles
	Koyama T.; Naseem M.T.; Kolosov D.; Vo C.T.; Mahon D.; Jakobsen A.S.S.; Jensen R.L.; Denholm B.; O'Donnell M.; Halberg K.V.
发表日期	2021
ISSN	00278424
卷号	118 期号:14
英文摘要	Maintaining internal salt and water balance in response to fluctuating external conditions is essential for animal survival. This is particularly true for insects as their high surface-to-volume ratio makes them highly susceptible to osmotic stress. However, the cellular and hormonal mechanisms that mediate the systemic control of osmotic homeostasis in beetles (Coleoptera), the largest group of insects, remain largely unidentified. Here, we demonstrate that eight neurons in the brain of the red flour beetle Tribolium castaneum respond to internal changes in osmolality by releasing diuretic hormone (DH) 37 and DH47-homologs of vertebrate corticotropin-releasing factor (CRF) hormones-to control systemic water balance. Knockdown of the gene encoding the two hormones (Urinate, Urn8) reduces Malpighian tubule secretion and restricts organismal fluid loss, whereas injection of DH37 or DH47 reverses these phenotypes. We further identify a CRF-like receptor, Urinate receptor (Urn8R), which is exclusively expressed in a functionally unique secondary cell in the beetle tubules, as underlying this response. Activation of Urn8R increases K+ secretion, creating a lumen-positive transepithelial potential that drives fluid secretion. Together, these data show that beetle Malpighian tubules operate by a fundamentally different mechanism than those of other insects. Finally, we adopt a fluorescent labeling strategy to identify the evolutionary origin of this unusual tubule architecture, revealing that it evolved in the last common ancestor of the higher beetle families. Our work thus uncovers an important homeostatic program that is key to maintaining osmotic control in beetles, which evolved parallel to the radiation of the "advanced" beetle lineages. © 2021 National Academy of Sciences. All rights reserved.
英文关键词	Diuretic hormone; Malpighian tubule; Osmoregulation; Secondary cell; Tribolium castaneum
语种	英语
scopus关键词	corticotropin releasing factor; corticotropin releasing factor receptor; fluorescent dye; G protein coupled receptor; potassium; protein Urinate receptor; unclassified drug; vasopressin; adult; animal husbandry; Article; brain nerve cell; cellular distribution; controlled study; dehydration; desiccation; electrophysiology; enzyme linked immunosorbent assay; evolution; ex vivo study; female; fluid balance; gene expression; gene knockdown; gene silencing; genetic code; hemolymph; homeostasis; ion current; male; Malpighian tubule; molecular cloning; nonhuman; organ culture; osmolality; osmoregulation; osmosis; phenotype; polymerase chain reaction; priority journal; protein expression; protein function; protein secretion; RNA extraction; RNA sequencing; secretion (process); sequence homology; signal transduction; Tribolium castaneum
来源期刊	Proceedings of the National Academy of Sciences of the United States of America
文献类型	期刊论文
条目标识符	http://gcip.llas.ac.cn/handle/2XKMVOVA/180005
作者单位	Department of Biology, Section for Cell and Neurobiology, University of Copenhagen, Copenhagen, DK-2100, Denmark; Department of Biology, McMaster University, Hamilton, ON L8S 4K1, Canada; Department of Biological Sciences, California State University San Marcos, San Marcos, CA 92069, United States; Centre for Discovery Brain Sciences, University of Edinburgh, Edinburgh, EH8 9AG, United Kingdom
推荐引用方式 GB/T 7714	Koyama T.,Naseem M.T.,Kolosov D.,et al. A unique Malpighian tubule architecture in Tribolium castaneum informs the evolutionary origins of systemic osmoregulation in beetles[J],2021,118(14).
APA	Koyama T..,Naseem M.T..,Kolosov D..,Vo C.T..,Mahon D..,...&Halberg K.V..(2021).A unique Malpighian tubule architecture in Tribolium castaneum informs the evolutionary origins of systemic osmoregulation in beetles.Proceedings of the National Academy of Sciences of the United States of America,118(14).
MLA	Koyama T.,et al."A unique Malpighian tubule architecture in Tribolium castaneum informs the evolutionary origins of systemic osmoregulation in beetles".Proceedings of the National Academy of Sciences of the United States of America 118.14(2021).