scholarly journals A neuroendocrine pathway modulating osmotic stress in Drosophila

2019 ◽  
Author(s):  
Meet Zandawala ◽  
Thomas Nguyen ◽  
Marta Balanyà Segura ◽  
Helena A. D. Johard ◽  
Mirjam Amcoff ◽  
...  

AbstractEnvironmental factors challenge the physiological homeostasis in animals, thereby evoking stress responses. Various mechanisms have evolved to counter stress at the organism level, including regulation by neuropeptides. Although much progress has been made on the mechanisms and neuropeptides influencing nutritional stress, relatively little is known about the factors and pathways regulating osmotic and ionic stresses. Here, we uncover the neuropeptide Corazonin (Crz) as a neuroendocrine factor that modulates the release of an osmoregulatory peptide, CAPA, to regulate tolerance to osmotic and ionic stress. Both knockdown of Crz and acute injections of Crz peptide impact desiccation tolerance and recovery from chill-coma. Comprehensive mapping of the Crz receptor (CrzR) expression identified three pairs of Capa-expressing neurons (Va neurons) in the ventral nerve cord that mediate these effects of Crz. We further show that Crz is released during dry starvation (desiccation) and acts to restore homeostasis by inhibiting CAPA release via inhibition of cAMP production in Va neurons. Finally, knockdown of CrzR in Va neurons also affects CAPA release, and consequently influences desiccation tolerance and chill-coma recovery, considered proxies for diuretic state. Thus, Crz modulates Va neurons to maintain osmotic and ionic homeostasis, which in turn influences stress tolerance. Taken together with our previous work showing that systemic Crz signaling acts to restore nutrients levels by promoting food search and feeding, we propose that Crz signaling also ensures osmotic homeostasis by inhibiting the anti-diuretic CAPA peptides. Thus, Crz ameliorates stress-associated physiology through systemic modulation of both peptidergic neurosecretory cells and the fat body in Drosophila.Author summaryInsects are among the largest groups of animals and have adapted to inhabit almost all environments on Earth. Their success in surviving extreme conditions stems largely from their ability to withstand environmental stress, such as desiccation and cold. However, the neural mechanisms that are responsible for coordinating responses to counter these stresses are largely unknown. To address this, we delineate a neuroendocrine axis utilizing the neuropeptides Corazonin (Crz) and CAPA, that coordinate responses to metabolic and osmotic stress. We show that Crz modulates the release of an anti-diuretic peptide, CAPA from a set of neurosecretory cells. CAPA in turn influences osmotic and ionic balance via actions on the Malpighian tubules (the insect analogs of the kidney) and the intestine. Taken together with earlier work, our data suggest that Crz acts to restore metabolic homeostasis at starvation and as a cosenquence of energy mobilization and ensuing metabolic water production, fluid balance needs to be adjusted and therefore CAPA release is inhibited. Hence, this work provides a mechanistic understanding of the neuroendocrine mitigation of metabolic and osmotic stress by two peptide systems.

PLoS Genetics ◽  
2021 ◽  
Vol 17 (3) ◽  
pp. e1009425
Author(s):  
Meet Zandawala ◽  
Thomas Nguyen ◽  
Marta Balanyà Segura ◽  
Helena A. D. Johard ◽  
Mirjam Amcoff ◽  
...  

Environmental factors challenge the physiological homeostasis in animals, thereby evoking stress responses. Various mechanisms have evolved to counter stress at the organism level, including regulation by neuropeptides. In recent years, much progress has been made on the mechanisms and neuropeptides that regulate responses to metabolic/nutritional stress, as well as those involved in countering osmotic and ionic stresses. Here, we identified a peptidergic pathway that links these types of regulatory functions. We uncover the neuropeptide Corazonin (Crz), previously implicated in responses to metabolic stress, as a neuroendocrine factor that inhibits the release of a diuretic hormone, CAPA, and thereby modulates the tolerance to osmotic and ionic stress. Both knockdown of Crz and acute injections of Crz peptide impact desiccation tolerance and recovery from chill-coma. Mapping of the Crz receptor (CrzR) expression identified three pairs of Capa-expressing neurons (Va neurons) in the ventral nerve cord that mediate these effects of Crz. We show that Crz acts to restore water/ion homeostasis by inhibiting release of CAPA neuropeptides via inhibition of cAMP production in Va neurons. Knockdown of CrzR in Va neurons affects CAPA signaling, and consequently increases tolerance for desiccation, ionic stress and starvation, but delays chill-coma recovery. Optogenetic activation of Va neurons stimulates excretion and simultaneous activation of Crz and CAPA-expressing neurons reduces this response, supporting the inhibitory action of Crz. Thus, Crz inhibits Va neurons to maintain osmotic and ionic homeostasis, which in turn affects stress tolerance. Earlier work demonstrated that systemic Crz signaling restores nutrient levels by promoting food search and feeding. Here we additionally propose that Crz signaling also ensures osmotic homeostasis by inhibiting release of CAPA neuropeptides and suppressing diuresis. Thus, Crz ameliorates stress-associated physiology through systemic modulation of both peptidergic neurosecretory cells and the fat body in Drosophila.


2017 ◽  
Author(s):  
Meet Zandawala ◽  
Richard Marley ◽  
Shireen A. Davies ◽  
Dick R. Nässel

AbstractMultiple neuropeptides are known to regulate water and ion balance in Drosophila melanogaster. Several of these peptides also have other functions in physiology and behavior. Examples are corticotropin-releasing factor-like diuretic hormone (diuretic hormone 44; DH44) and leucokinin (LK), both of which induce fluid secretion by Malpighian tubules (MTs), but also regulate stress responses, feeding, circadian activity and other behaviors. Here, we investigated the functional relations between the LK and DH44 signaling systems. DH44 and LK peptides are only colocalized in a set of abdominal neurosecretory cells (ABLKs). Targeted knockdown of each of these peptides in ABLKs leads to increased resistance to desiccation, starvation and ionic stress. Food ingestion is diminished by knockdown of DH44, but not LK, and water retention is increased by LK knockdown only. Thus, the two colocalized peptides display similar systemic actions, but differ with respect to regulation of feeding and body water retention. We also demonstrated that DH44 and LK have additive effects on fluid secretion by MTs. It is likely that the colocalized peptides are coreleased from ABLKs into the circulation and act on the tubules where they target different cell types and signaling systems to regulate diuresis and stress tolerance. Additional targets seem to be specific for each of the two peptides and subserve regulation of feeding and water retention. Our data suggest that the ABLKs and hormonal actions are sufficient for many of the known DH44 and LK functions, and that the remaining neurons in the CNS play other functional roles.


Agronomy ◽  
2021 ◽  
Vol 11 (3) ◽  
pp. 435
Author(s):  
Agnieszka Ludwiczak ◽  
Monika Osiak ◽  
Stefany Cárdenas-Pérez ◽  
Sandra Lubińska-Mielińska ◽  
Agnieszka Piernik

Salinization is a key soil degradation process. An estimated 20% of total cultivated lands and 33% of irrigated agricultural lands worldwide are affected by high salinity. Much research has investigated the influence of salt (mainly NaCl) on plants, but very little is known about how this is related to natural salinity and osmotic stress. Therefore, our study was conducted to determine the osmotic and ionic salt stress responses of selected C3 and C4 cultivated plants. We focused on the early growth stages as those critical for plant development. We applied natural brine to simulate natural salinity and to compare its effect to NaCl solution. We assessed traits related to germination ability, seedlings and plantlet morphology, growth indexes, and biomass and water accumulation. Our results demonstrate that the effects of salinity on growth are strongest among plantlets. Salinity most affected water absorption in C3 plants (28% of total traits variation), but plant length in C4 plants (17–27%). Compensatory effect of ions from brine were suggested by the higher model plants’ growth success of ca 5–7% under brine compared to the NaCl condition. However, trait differences indicated that osmotic stress was the main stress factor affecting the studied plants.


Rice Science ◽  
2017 ◽  
Vol 24 (5) ◽  
pp. 253-263 ◽  
Author(s):  
Simon Swapna ◽  
Korukkanvilakath Samban Shylaraj

2016 ◽  
Vol 67 (21) ◽  
pp. 5961-5973 ◽  
Author(s):  
Mathilde Royer ◽  
David Cohen ◽  
Nathalie Aubry ◽  
Vera Vendramin ◽  
Simone Scalabrin ◽  
...  

Development ◽  
1992 ◽  
Vol 116 (4) ◽  
pp. 1203-1220 ◽  
Author(s):  
A.Y. Hartenstein ◽  
A. Rugendorff ◽  
U. Tepass ◽  
V. Hartenstein

The complex embryonic phenotype of the six neurogenic mutations Notch, mastermind, big brain, Delta, Enhancer of split and neuralized was analyzed by using different antibodies and PlacZ markers, which allowed us to label most of the known embryonic tissues. Our results demonstrate that all of the neurogenic mutants show abnormalities in many different organs derived from all three germ layers. Defects caused by the neurogenic mutations in ectodermally derived tissues fell into two categories. First, all cell types that delaminate from the ectoderm (neuroblasts, sensory neurons, peripheral glia cells and oenocytes) are increased in number. Secondly, ectodermal tissues that in the wild type form epithelial structures lose their epithelial phenotype and dissociate (optic lobe, stomatogastric nervous system) or show significant differentiative abnormalities (trachea, Malpighian tubules and salivary gland). Abnormalities in tissues derived from the mesoderm were observed in all six neurogenic mutations. Most importantly, somatic myoblasts do not fuse and/or form an aberrant muscle pattern. Cardioblasts (which form the embryonic heart) are increased in number and show differentiative abnormalities; other mesodermal cell types (fat body, pericardial cells) are significantly decreased. The development of the endoderm (midgut rudiments) is disrupted in most of the neurogenic mutations (Notch, Delta, Enhancer of split and neuralized) during at least two stages. Defects occur as early as during gastrulation when the invaginating midgut rudiments prematurely lose their epithelial characteristics. Later, the transition of the midgut rudiments to form the midgut epithelium does not occur. In addition, the number of adult midgut precursor cells that segregate from the midgut rudiments is strongly increased. We propose that, at least in the ectodermally and endodermally derived tissues, neurogenic gene function is primarily involved in interactions among cells that need to acquire or to maintain an epithelial phenotype.


1957 ◽  
Vol 34 (2) ◽  
pp. 276-289
Author(s):  
B. A. KILBY ◽  
ELISABETH NEVILLE

1. Homogenates of fat-body of Schistocerca gregaria Forsk. were shown to catalyse transamination reactions between α-ketoglutarate and numerous α-amino acids. The aspartate/glutamate and alanine/glutamate transaminases were the most active. They were present in both the ‘soluble’ and the mitochondrial fractions of fat-body cells and also in Malpighian tubules and mid-gut wall. The other transaminases in the fat-body were confined to the mitochondrial fraction. 2. Fat-body, Malpighian tubule and mid-gut wall homogenates were able to convert glutamic acid into glutamine, a compound which could also act as an amino-group donor in some transamination reactions. 3. A glutamate-cytochrome c reductase system which involved diphosphopyridine nucleotide was present in fat-body. 4. Fat-body contained an active arginase, but urease could not be detected. A D-amino-acid oxidase was present, together with a less active L-amino-acid oxidase. 5. In general, it appears that amino-acid metabolism in the locust resembles that in higher animals.


Plants ◽  
2020 ◽  
Vol 9 (3) ◽  
pp. 304 ◽  
Author(s):  
Alexander Hofmann ◽  
Sophia Müller ◽  
Thomas Drechsler ◽  
Mareike Berleth ◽  
Katharina Caesar ◽  
...  

Plants employ a number of phosphorylation cascades in response to a wide range of environmental stimuli. Previous studies in Arabidopsis and yeast indicate that histidine kinase AHK1 is a positive regulator of drought and osmotic stress responses. Based on these studies AHK1 was proposed a plant osmosensor, although the molecular basis of plant osmosensing still remains unknown. To understand the molecular role and signaling mechanism of AHK1 in osmotic stress, we have expressed and purified full-length AHK1 from Arabidopsis in a bacterial host to allow for studies on the isolated transmembrane receptor. Purification of the recombinant protein solubilized from the host membranes was achieved in a single step by metal-affinity chromatography. Analysis of the purified AHK1 by SDS-polyacrylamide gel electrophoresis (SDS-PAGE) and immunoblotting show a single band indicating that the preparation is highly pure and devoid of contaminants or degradation products. In addition, gel filtration experiments indicate that the preparation is homogenous and monodisperse. Finally, CD-spectroscopy, phosphorylation activity, dimerization studies, and protein–protein interaction with plant phosphorylation targeting AHP2 demonstrate that the purified protein is functionally folded and acts as phospho-His or phospho-Asp phosphatase. Hence, the expression and purification of recombinant AHK1 reported here provide a basis for further detailed functional and structural studies of the receptor, which might help to understand plant osmosensing and osmosignaling on the molecular level.


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