Food quality, competition, and parasitism influence feeding preference in a neotropical lepidopteran

Journal ArticleWe surveyed Lepidoptera found on 11 species of Inga (Fabaceae:Mimosoideae) co-existing on Barro Colorado Island, Panama, to evaluate factors influencing diet choice. Of the 47 species of caterpillars (747 individuals) recorded, each fed on a distinct set of Inga. In the field, 96% of the individuals were found on young leaves. Growth rates of caterpillars that were fed leaves in the laboratory were 60% higher on young leaves compared to mature leaves

Seed rain along a gradient of degradation in Caribbean dry forest: Effects of dispersal limitation on the trajectory of forest recovery

Questions Tropical dry forests that experience severe disturbances (e.g., fires) often remain degraded for long time periods, during which non-native grasses and trees dominate. One barrier to native tree regeneration in degraded areas may be seed dispersal limitation. To better understand how dispersal limitation influences recovery from degradation, we tested whether the mode and rates of seed dispersal differed in degraded sites dominated either by the exotic tree Leucaena leucocephala or open areas dominated by introduced pasture grasses. We also tested whether L. leucocephala stands facilitate the recruitment of native trees by increasing their seed input compared to open grass areas. Location Guánica Commonwealth Forest, Puerto Rico. Methods Seed rain was measured for one year in traps located within five vegetation types that ranged in degree of forest degradation from open grass to intact native forest. Results In open grass areas, seed rain density was similarly low for L. leucocephala and abiotically dispersed native trees (mean [95% CI] = 50.9 [15.1–171.0] vs. 34.2 [10.3–113.5] seeds m−2 year−1), whereas it was even lower for animal-dispersed native trees (0.14 [0.03–0.67] seeds m−2 year−1). Compared to open grass areas, L. leucocephala-dominated stands, even those with grass understories, had higher seed rain density of animal-dispersed trees (43.0 [12.9–143.6] seeds m−2 year−1), but not abiotically dispersed trees (20.8 [6.3–68.5] seeds m−2 year−1). Conclusions The dominance of L. leucocephala in disturbed Caribbean dry forests does not appear to be mediated by disproportionate seed arrival in open areas compared to native tree seeds. Rather, subsequent factors such as seed and seedling survival likely favor L. leucocephala in highly degraded areas. Since L. leucocephala stands increase the seed rain of animal-dispersed native trees, retaining them in highly disturbed Caribbean dry forests may facilitate the regeneration of native forests

Fire resistance in a Caribbean dry forest: inferences from the allometry of bark thickness

Trees’ resistance to fire-induced mortality increases with bark thickness, which varies widely among species and generally increases with stem diameter. Because dry forests are more fire-prone than wetter forests, bark may be thicker in these forests. However, where disturbances such as hurricanes suppress stem diameter, trees may not obtain fire-resistant bark thickness. In two hurricane-prone Caribbean dry-forest types in Puerto Rico—deciduous forest and scrub forest—we measured bark thickness on 472 stems of 25 species to test whether tree species obtain bark thicknesses that confer fire resistance, whether bark is thicker in the fire-prone scrub forest than in the deciduous forest, and how bark thickness in Caribbean dry forest compares with other tropical ecosystems. Only 5% of stems within a deciduous-forest stand had bark thickness that would provide \u3c 50% probability of top-kill during low-intensity fire. In contrast, thicker-barked trees dominated the scrub forest, suggesting that fires influenced it. Compared with trees of similar diameter in other regions of the tropics, bark in Caribbean dry forest was thinner than in savanna, similar to other seasonally dry forests, and thicker than moist-to-wet forests. Dry-forest species appear to invest more in fire-resistance than species from wetter forests. However, Caribbean dry forests remain highly vulnerable to fire because the trees rarely reach large enough diameters to be fire resistant

Hydraulic architecture explains species moisture dependency but not mortality rates across a tropical rainfall gradient

Intensified droughts are affecting tropical forests across the globe. However, the underlying mechanisms of tree drought response and mortality are poorly understood. Hydraulic traits and especially hydraulic safety margins (HSMs), that is, the extent to which plants buffer themselves from thresholds of water stress, provide insights into species-specific drought vulnerability. We investigated hydraulic traits during an intense drought triggered by the 2015–2016 El Niño on 27 canopy tree species across three tropical forest sites with differing precipitation. We capitalized on the drought event as a time when plant water status might approach or exceed thresholds of water stress. We investigated the degree to which these traits varied across the rainfall gradient, as well as relationships among hydraulic traits and species-specific optimal moisture and mortality rates. There were no differences among sites for any measured trait. There was strong coordination among traits, with a network analysis revealing two major groups of coordinated traits. In one group, there were water potentials, turgor loss point, sapwood capacitance and density, HSMs, and mortality rate. In the second group, there was leaf mass per area, leaf dry matter content, hydraulic architecture (leaf area to sapwood area ratio), and species-specific optimal moisture. These results demonstrated that while species with greater safety from turgor loss had lower mortality rates, hydraulic architecture was the only trait that explained species’ moisture dependency. Species with a greater leaf area to sapwood area ratio were associated with drier sites and reduced their transpirational demand during the dry season via deciduousness

Plant water potential improves prediction of empirical stomatal models

Climate change is expected to lead to increases in drought frequency and severity, with deleterious effects on many ecosystems. Stomatal responses to changing environmental conditions form the backbone of all ecosystem models, but are based on empirical relationships and are not well-tested during drought conditions. Here, we use a dataset of 34 woody plant species spanning global forest biomes to examine the effect of leaf water potential on stomatal conductance and test the predictive accuracy of three major stomatal models and a recently proposed model. We find that current leaf-level empirical models have consistent biases of over-prediction of stomatal conductance during dry conditions, particularly at low soil water potentials. Furthermore, the recently proposed stomatal conductance model yields increases in predictive capability compared to current models, and with particular improvement during drought conditions. Our results reveal that including stomatal sensitivity to declining water potential and consequent impairment of plant water transport will improve predictions during drought conditions and show that many biomes contain a diversity of plant stomatal strategies that range from risky to conservative stomatal regulation during water stress. Such improvements in stomatal simulation are greatly needed to help unravel and predict the response of ecosystems to future climate extremes.Funding for this research was provided by NSF DEB EF-1340270 and the Climate Mitigation Initiative at the Princeton Environmental Institute, Princeton University. SL acknowledges financial support from the China Scholarship Council (CSC). VRD acknowledges funding from Ramón y Cajal fellowship (RYC-2012-10970). BTW was supported by the Next Generation Ecosystem Experiments-Tropics, funded by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research. DJC acknowledges funding from the National Science Centre, Poland (NN309 713340). WRLA was supported in part by NSF DEB 1714972

Factors affecting female space use in ten populations of prairie chickens

Citation: Winder, V. L., Carrlson, K. M., Gregory, A. J., Hagen, C. A., Haukos, D. A., Kesler, D. C., . . . Sandercock, B. K. (2015). Factors affecting female space use in ten populations of prairie chickens. Ecosphere, 6(9), 17. doi:10.1890/es14-00536.1Conservation of wildlife depends on an understanding of the interactions between animal movements and key landscape factors. Habitat requirements of wide-ranging species often vary spatially, but quantitative assessment of variation among replicated studies at multiple sites is rare. We investigated patterns of space use for 10 populations of two closely related species of prairie grouse: Greater Prairie-Chickens (Tympanuchus cupido) and Lesser Prairie-Chickens (T. pallidicinctus). Prairie chickens require large, intact tracts of native grasslands, and are umbrella species for conservation of prairie ecosystems in North America. We used resource utilization functions to investigate space use by female prairie chickens during the 6-month breeding season from March through August in relation to lek sites, habitat conditions, and anthropogenic development. Our analysis included data from 382 radio-marked individuals across a major portion of the extant range. Our project is a unique opportunity to study comparative space use of prairie chickens, and we employed standardized methods that facilitated direct comparisons across an ecological gradient of study sites. Median home range size of females varied similar to 10-fold across 10 sites (3.6-36.7 km(2)), and home ranges tended to be larger at sites with higher annual precipitation. Proximity to lek sites was a strong and consistent predictor of space use for female prairie chickens at all 10 sites. The relative importance of other predictors of space use varied among sites, indicating that generalized habitat management guidelines may not be appropriate for these two species. Prairie chickens actively selected for prairie habitats, even at sites where similar to 90% of the land cover within the study area was prairie. A majority of the females monitored in our study (>95%) had activity centers within 5 km of leks, suggesting that conservation efforts can be effectively concentrated near active lek sites. Our data on female space use suggest that lek surveys of male prairie chickens can indirectly assess habitat suitability for females during the breeding season. Lek monitoring and surveys for new leks provide information on population trends, but can also guide management actions aimed at improving nesting and brood-rearing habitats

Woody plants optimise stomatal behaviour relative to hydraulic risk

Stomatal response to environmental conditions forms the backbone of all ecosystem and carbon cycle models, but is largely based on empirical relationships. Evolutionary theories of stomatal behaviour are critical for guarding against prediction errors of empirical models under future climates. Longstanding theory holds that stomata maximise fitness by acting to maintain constant marginal water use efficiency over a given time horizon, but a recent evolutionary theory proposes that stomata instead maximise carbon gain minus carbon costs/risk of hydraulic damage. Using data from 34 species that span global forest biomes, we find that the recent carbon‐maximisation optimisation theory is widely supported, revealing that the evolution of stomatal regulation has not been primarily driven by attainment of constant marginal water use efficiency. Optimal control of stomata to manage hydraulic risk is likely to have significant consequences for ecosystem fluxes during drought, which is critical given projected intensification of the global hydrological cycle.W.R.L.A. acknowledges funding for this research from NSF 1714972 and from the USDA National Institute of Food and Agriculture, Agricultural and Food Research Initiative Competitive Programme, Ecosystem Services and Agro-Ecosystem Management, grant no. 2017-05521. We thank T. Brodribb and one anonymous reviewer for their insightful reviews, B. Medlyn and Y.S. Lin for sharing data and R. Norby for providing Vcmax data for several species. We appreciate the assistance from Marion Feifel in collecting data of leaf photosynthetic parameters of five European tree species. S.L. acknowledges financial support from the China Scholarship Council (CSC). VRD acknowledges funding from a Ram on y Cajal fellowship (RYC-2012-10970). B.T.W. was supported by the Next Generation Ecosystem Experiments-Tropics, funded by the U.S. Department of Energy, Office of Science, Office of Biological and Environmental Research. DJC acknowledges funding from the National Science Centre, Poland (NN309 713340)

Mapping Brain Response to Pain in Fibromyalgia Patients Using Temporal Analysis of fMRI

Background: Nociceptive stimuli may evoke brain responses longer than the stimulus duration often partially detected by conventional neuroimaging. Fibromyalgia patients typically complain of severe pain from gentle stimuli. We aimed to characterize brain response to painful pressure in fibromyalgia patients by generating activation maps adjusted for the duration of brain responses. Methodology/Principal Findings: Twenty-seven women (mean age: 47.8 years) were assessed with fMRI. The sample included nine fibromyalgia patients and nine healthy subjects who received 4 kg/cm2 of pressure on the thumb. Nine additional control subjects received 6.8 kg/cm2 to match the patients for the severity of perceived pain. Independent Component Analysis characterized the temporal dynamics of the actual brain response to pressure. Statistical parametric maps were estimated using the obtained time courses. Brain response to pressure (18 seconds) consistently exceeded the stimulus application (9 seconds) in somatosensory regions in all groups. fMRI maps following such temporal dynamics showed a complete pain network response (sensory-motor cortices, operculo-insula, cingulate cortex, and basal ganglia) to 4 kg/cm2 of pressure in fibromyalgia patients. In healthy subjects, response to this low intensity pressure involved mainly somatosensory cortices. When matched for perceived pain (6.8 kg/cm2), control subjects showed also comprehensive activation of pain-related regions, but fibromyalgia patients showed significantly larger activation in the anterior insula-basal ganglia complex and the cingulate cortex. Conclusions/Significance: The results suggest that data-driven fMRI assessments may complement conventional neuroimaging for characterizing pain responses and that enhancement of brain activation in fibromyalgia patients may be particularly relevant in emotion-related regions

Endocytic regulation of alkali metal transport proteins in mammals, yeast and plants

The relative concentrations of ions and solutes inside cells are actively maintained by several classes of transport proteins, in many cases against their concentration gradient. These transport processes, which consume a large portion of cellular energy, must be constantly regulated. Many structurally distinct families of channels, carriers, and pumps have been characterized in considerable detail during the past decades and defects in the function of some of these proteins have been linked to a growing list of human diseases. The dynamic regulation of the transport proteins present at the cell surface is vital for both normal cellular function and for the successful adaptation to changing environments. The composition of proteins present at the cell surface is controlled on both the transcriptional and post-translational level. Post-translational regulation involves highly conserved mechanisms of phosphorylation- and ubiquitylation-dependent signal transduction routes used to modify the cohort of receptors and transport proteins present under any given circumstances. In this review, we will summarize what is currently known about one facet of this regulatory process: the endocytic regulation of alkali metal transport proteins. The physiological relevance, major contributors, parallels and missing pieces of the puzzle in mammals, yeast and plants will be discussed.This work was supported by grant BFU2011-30197-C03-03 from the Ministerio de Ciencia e Innovacion (Spain). V.L.-T. is supported by a fellowship from the Universidad Politecnica de Valencia. C. P. is supported by a fellowship from the Consejo Superior de Investigaciones Cientificas (Spain).Mulet Salort, JM.; Llopis Torregrosa, V.; Primo Planta, C.; Marques Romero, MC.; Yenush, L. (2013). Endocytic regulation of alkali metal transport proteins in mammals, yeast and plants. Current Genetics. 59(4):207-230. https://doi.org/10.1007/s00294-013-0401-2S207230594Abe F, Iida H (2003) Pressure-induced differential regulation of the two tryptophan permeases Tat1 and Tat2 by ubiquitin ligase Rsp5 and its binding proteins, Bul1 and Bul2. Mol Cell Biol 23:7566–7584Abriel H, Loffing J, Rebhun JF, Pratt JH, Schild L, Horisberger JD, Rotin D, Staub O (1999) Defective regulation of the epithelial Na+ channel by Nedd4 in Liddle’s syndrome. J Clin Invest 103:667–673. doi: 10.1172/JCI5713Alesutan I, Munoz C, Sopjani M, Dërmaku-Sopjani M, Michael D, Fraser S, Kemp BE, Seebohm G, Föller M, Lang F (2011) Inhibition of Kir2.1 (KCNJ2) by the AMP-activated protein kinase. Biochem Biophys Res Commun 408:505–510. doi: 10.1016/j.bbrc.2011.04.015Alvarez CE (2008) On the origins of arrestin and rhodopsin. BMC Evol Biol 8:222. doi: 10.1186/1471-2148-8-222Amerik AY, Nowak J, Swaminathan S, Hochstrasser M (2000) The Doa4 deubiquitinating enzyme is functionally linked to the vacuolar protein-sorting and endocytic pathways. Mol Biol Cell 11:3365–3380Anderson JA, Huprikar SS, Kochian LV, Lucas WJ, Gaber RF (1992) Functional expression of a probable Arabidopsis thaliana potassium channel in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 89:3736–3740Anderson JA, Nakamura RL, Gaber RF (1994) Heterologous expression of K+ channels in Saccharomyces cerevisiae: strategies for molecular analysis of structure and function. Symp Soc Exp Biol 48:85–97Aniento F, Gu F, Parton RG, Gruenberg J (1996) An endosomal beta COP is involved in the pH-dependent formation of transport vesicles destined for late endosomes. J Cell Biol 133:29–41Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258Arino J, Ramos J, Sychrova H (2010) Alkali metal cation transport and homeostasis in yeasts. Microbiol mol biol rev 74:95–120. doi: 10.1128/mmbr.00042-09Arnason TG, Pisclevich MG, Dash MD, Davies GF, Harkness TA (2005) Novel interaction between Apc5p and Rsp5p in an intracellular signaling pathway in Saccharomyces cerevisiae. Eukaryot Cell 4:134–146. doi: 10.1128/EC.4.1.134-146.2005Arroyo JP, Lagnaz D, Ronzaud C, Vázquez N, Ko BS, Moddes L, Ruffieux-Daidié D, Hausel P, Koesters R, Yang B, Stokes JB, Hoover RS, Gamba G, Staub O (2011) Nedd4-2 modulates renal Na+ –Cl– cotransporter via the aldosterone-SGK1-Nedd4-2 pathway. J Am Soc Nephrol 22:1707–1719. doi: 10.1681/ASN.2011020132Azmi IF, Davies BA, Xiao J, Babst M, Xu Z, Katzmann DJ (2008) ESCRT-III family members stimulate Vps4 ATPase activity directly or via Vta1. Dev Cell 14:50–61. doi: 10.1016/j.devcel.2007.10.021Babst M, Katzmann DJ, Estepa-Sabal EJ, Meerloo T, Emr SD (2002a) Escrt-III: an endosome-associated heterooligomeric protein complex required for mvb sorting. Dev Cell 3:271–282Babst M, Katzmann DJ, Snyder WB, Wendland B, Emr SD (2002b) Endosome-associated complex, ESCRT-II, recruits transport machinery for protein sorting at the multivesicular body. Dev Cell 3:283–289Bache KG, Slagsvold T, Cabezas A, Rosendal KR, Raiborg C, Stenmark H (2004) The growth-regulatory protein HCRP1/hVps37A is a subunit of mammalian ESCRT-I and mediates receptor down-regulation. Mol Biol Cell 15:4337–4346. doi: 10.1091/mbc.E04-03-0250Baietti MF, Zhang Z, Mortier E, Melchior A, Degeest G, Geeraerts A, Ivarsson Y, Depoortere F, Coomans C, Vermeiren E, Zimmermann P, David G (2012) Syndecan-syntenin-ALIX regulates the biogenesis of exosomes. Nat Cell Biol 14:677–685. doi: 10.1038/ncb2502Barajas D, Nagy PD (2010) Ubiquitination of tombusvirus p33 replication protein plays a role in virus replication and binding to the host Vps23p ESCRT protein. Virology 397:358–368. doi: 10.1016/j.virol.2009.11.010Barajas D, Jiang Y, Nagy PD (2009) A unique role for the host ESCRT proteins in replication of Tomato bushy stunt virus. PLoS Pathog 5:e1000705. doi: 10.1371/journal.ppat.1000705Barberon M, Zelazny E, Robert S, Conéjéro G, Curie C, Friml J, Vert G (2011) Monoubiquitin-dependent endocytosis of the iron-regulated transporter 1 (IRT1) transporter controls iron uptake in plants. Proc Natl Acad Sci USA 108:E450–E458. doi: 10.1073/pnas.1100659108Barragán V, Leidi EO, Andrés Z, Rubio L, De Luca A, Fernández JA, Cubero B, Pardo JM (2012) Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. Plant Cell 24:1127–1142. doi: 10.1105/tpc.111.095273Bassil E, Ohto MA, Esumi T, Tajima H, Zhu Z, Cagnac O, Belmonte M, Peleg Z, Yamaguchi T, Blumwald E (2011) The Arabidopsis intracellular Na+/H+ antiporters NHX5 and NHX6 are endosome associated and necessary for plant growth and development. Plant Cell 23:224–239. doi: 10.1105/tpc.110.079426Beaudenon SL, Huacani MR, Wang G, McDonnell DP, Huibregtse JM (1999) Rsp5 ubiquitin-protein ligase mediates DNA damage-induced degradation of the large subunit of RNA polymerase II in Saccharomyces cerevisiae. Mol Cell Biol 19:6972–6979Becuwe M, Vieira N, Lara D, Gomes-Rezende J, Soares-Cunha C, Casal M, Haguenauer-Tsapis R, Vincent O, Paiva S, Léon S (2012) A molecular switch on an arrestin-like protein relays glucose signaling to transporter endocytosis. J Cell Biol 196:247–259. doi: 10.1083/jcb.201109113Belgareh-Touzé N, Léon S, Erpapazoglou Z, Stawiecka-Mirota M, Urban-Grimal D, Haguenauer-Tsapis R (2008) Versatile role of the yeast ubiquitin ligase Rsp5p in intracellular trafficking. Biochem Soc Trans 36:791–796. doi: 10.1042/BST0360791Bhalla V, Oyster NM, Fitch AC, Wijngaarden MA, Neumann D, Schlattner U, Pearce D, Hallows KR (2006) AMP-activated kinase inhibits the epithelial Na+ channel through functional regulation of the ubiquitin ligase Nedd4-2. J Biol Chem 281:26159–26169. doi: 10.1074/jbc.M606045200Blondel MO, Morvan J, Dupre S, Urban-Grimal D, Haguenauer-Tsapis R, Volland C (2004) Direct sorting of the yeast uracil permease to the endosomal system is controlled by uracil binding and Rsp5p-dependent ubiquitylation. Mol Biol Cell 15:883–895. doi: 10.1091/mbc.E03-04-0202Boase NA, Rychkov GY, Townley SL, Dinudom A, Candi E, Voss AK, Tsoutsman T, Semsarian C, Melino G, Koentgen F, Cook DI, Kumar S (2011) Respiratory distress and perinatal lethality in Nedd4-2-deficient mice. Nat Commun 2:287. doi: 10.1038/ncomms1284Boehmer C, Laufer J, Jeyaraj S, Klaus F, Lindner R, Lang F, Palmada M (2008) Modulation of the voltage-gated potassium channel Kv1.5 by the SGK1 protein kinase involves inhibition of channel ubiquitination. Cell Physiol Biochem 22:591–600. doi: 10.1159/000185543Bonifacino JS, Traub LM (2003) Signals for sorting of transmembrane proteins to endosomes and lysosomes. Annu Rev Biochem 72:395–447. doi: 10.1146/annurev.biochem.72.121801.161800Bowers K, Levi BP, Patel FI, Stevens TH (2000) The sodium/proton exchanger Nhx1p is required for endosomal protein trafficking in the yeast Saccharomyces cerevisiae. Mol Biol Cell 11:4277–4294Brett CL, Tukaye DN, Mukherjee S, Rao R (2005) The yeast endosomal Na+K+/H+ exchanger Nhx1 regulates cellular pH to control vesicle trafficking. Mol Biol Cell 16:1396–1405. doi: 10.1091/mbc.E04-11-0999Cao XR, Lill NL, Boase N, Shi PP, Croucher DR, Shan H, Qu J, Sweezer EM, Place T, Kirby PA, Daly RJ, Kumar S, Yang B (2008) Nedd4 controls animal growth by regulating IGF-1 signaling. Sci Signal 1:ra5. doi: 10.1126/scisignal.1160940Carrasquillo R, Tian D, Krishna S, Pollak MR, Greka A, Schlöndorff J (2012) SNF8, a member of the ESCRT-II complex, interacts with TRPC6 and enhances its channel activity. BMC Cell Biol 13:33. doi: 10.1186/1471-2121-13-33Chen L, Hellmann H (2013) Plant E3 Ligases: flexible enzymes in a sessile world1. Mol Plant. doi: 10.1093/mp/sst005Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nürnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448:497–500. doi: 10.1038/nature05999Christie KJ, Martinez JA, Zochodne DW (2012) Disruption of E3 ligase NEDD4 in peripheral neurons interrupts axon outgrowth: linkage to PTEN. Mol Cell Neurosci 50:179–192. doi: 10.1016/j.mcn.2012.04.006Clague MJ, Liu H, Urbé S (2012) Governance of endocytic trafficking and signaling by reversible ubiquitylation. Dev Cell 23:457–467. doi: 10.1016/j.devcel.2012.08.011Clancy JL, Henderson MJ, Russell AJ, Anderson DW, Bova RJ, Campbell IG, Choong DY, Macdonald GA, Mann GJ, Nolan T, Brady G, Olopade OI, Woollatt E, Davies MJ, Segara D, Hacker NF, Henshall SM, Sutherland RL, Watts CK (2003) EDD, the human orthologue of the hyperplastic discs tumour suppressor gene, is amplified and overexpressed in cancer. Oncogene 22:5070–5081. doi: 10.1038/sj.onc.1206775Coonrod EM, Stevens TH (2010) The yeast vps class E mutants: the beginning of the molecular genetic analysis of multivesicular body biogenesis. Mol Biol Cell 21:4057–4060. doi: 10.1091/mbc.E09-07-0603Crespo JL, Daicho K, Ushimaru T, Hall MN (2001) The GATA transcription factors GLN3 and GAT1 link TOR to salt stress in Saccharomyces cerevisiae. J Biol Chem 276:34441–34444. doi: 10.1074/jbc.M103601200Debonneville C, Flores SY, Kamynina E, Plant PJ, Tauxe C, Thomas MA, Münster C, Chraïbi A, Pratt JH, Horisberger JD, Pearce D, Loffing J, Staub O (2001) Phosphorylation of Nedd4-2 by Sgk1 regulates epithelial Na(+) channel cell surface expression. EMBO J 20:7052–7059. doi: 10.1093/emboj/20.24.7052Downes BP, Stupar RM, Gingerich DJ, Vierstra RD (2003) The HECT ubiquitin-protein ligase (UPL) family in Arabidopsis: UPL3 has a specific role in trichome development. Plant J 35:729–742Eisenach C, Chen ZH, Grefen C, Blatt MR (2012) The trafficking protein SYP121 of Arabidopsis connects programmed stomatal closure and K+ channel activity with vegetative growth. Plant J 69:241–251. doi: 10.1111/j.1365-313X.2011.04786.xEkberg J, Schuetz F, Boase NA, Conroy SJ, Manning J, Kumar S, Poronnik P, Adams DJ (2007) Regulation of the voltage-gated K(+) channels KCNQ2/3 and KCNQ3/5 by ubiquitination. Novel role for Nedd4-2. J Biol Chem 282:12135–12142. doi: 10.1074/jbc.M609385200Faresse N, Lagnaz D, Debonneville A, Ismailji A, Maillard M, Fejes-Toth G, Náray-Fejes-Tóth A, Staub O (2012) Inducible kidney-specific Sgk1 knockout mice show a salt-losing phenotype. Am J Physiol Renal Physiol 302:F977–F985. doi: 10.1152/ajprenal.00535.2011Field MC, Gabernet-Castello C, Dacks JB (2007) Reconstructing the evolution of the endocytic system: insights from genomics and molecular cell biology. Adv Exp Med Biol 607:84–96. doi: 10.1007/978-0-387-74021-8_7Fisk HA, Yaffe MP (1999) A role for ubiquitination in mitochondrial inheritance in Saccharomyces cerevisiae. J Cell Biol 145:1199–1208Flinn RJ, Yan Y, Goswami S, Parker PJ, Backer JM (2010) The late endosome is essential for mTORC1 signaling. Mol Biol Cell 21:833–841. doi: 10.1091/mbc.E09-09-0756Fotia AB, Ekberg J, Adams DJ, Cook DI, Poronnik P, Kumar S (2004) Regulation of neuronal voltage-gated sodium channels by the ubiquitin-protein ligases Nedd4 and Nedd4-2. J Biol Chem 279:28930–28935. doi: 10.1074/jbc.M402820200Futter CE, White IJ (2007) Annexins and endocytosis. Traffic 8:951–958. doi: 10.1111/j.1600-0854.2007.00590.xGabriely G, Kama R, Gerst JE (2007) Involvement of specific COPI subunits in protein sorting from the late endosome to the vacuole in yeast. Mol Cell Biol 27:526–540. doi: 10.1128/MCB.00577-06Gajewska B, Shcherbik N, Oficjalska D, Haines DS, Zoladek T (2003) Functional analysis of the human orthologue of the RSP5-encoded ubiquitin protein ligase, hNedd4, in yeast. Curr Genet 43:1–10. doi: 10.1007/s00294-003-0371-xGalan JM, Moreau V, Andre B, Volland C, Haguenauer-Tsapis R (1996) Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J Biol Chem 271:10946–10952Gao T, Liu Z, Wang Y, Cheng H, Yang Q, Guo A, Ren J, Xue Y (2013) UUCD: a family-based database of ubiquitin and ubiquitin-like conjugation. Nucleic Acids Res 41:D445–D451. doi: 10.1093/nar/gks1103Geldner N (2004) The plant endosomal system—its structure and role in signal transduction and plant development. Planta 219:547–560. doi: 10.1007/s00425-004-1302-xGitan RS, Eide DJ (2000) Zinc-regulated ubiquitin conjugation signals endocytosis of the yeast ZRT1 zinc transporter. Biochem J 346:329–336. doi: 10.1042/0264-6021:3460329Gitan RS, Luo H, Rodgers J, Broderius M, Eide D (1998) Zinc-induced inactivation of the yeast ZRT1 zinc transporter occurs through endocytosis and vacuolar degradation. J Biol Chem 273:28617–28624Gómez-Gómez L, Boller T (2000) FLS2: an LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Mol Cell 5:1003–1011Gong X, Chang A (2001) A mutant plasma membrane ATPase, Pma1-10, is defective in stability at the yeast cell surface. Proc Natl Acad Sci USA 98:9104–9109. doi: 10.1073/pnas.161282998Guo J, Wang T, Li X, Shallow H, Yang T, Li W, Xu J, Fridman MD, Yang X, Zhang S (2012) Cell surface expression of human ether-a-go–go-related gene (hERG) channels is regulated by caveolin-3 protein via the ubiquitin ligase Nedd4-2. J Biol Chem 287:33132–33141. doi: 10.1074/jbc.M112.389643Gwizdek C, Hobeika M, Kus B, Ossareh-Nazari B, Dargemont C, Rodriguez MS (2005) The mRNA nuclear export factor Hpr1 is regulated by Rsp5-mediated ubiquitylation. J Biol Chem 280:13401–13405. doi: 10.1074/jbc.C500040200Haas TJ, Sliwinski MK, Martínez DE, Preuss M, Ebine K, Ueda T, Nielsen E, Odorizzi G, Otegui MS (2007) The Arabidopsis AAA ATPase SKD1 is involved in multivesicular endosome function and interacts with its positive regulator LYST-INTERACTING PROTEIN5. Plant Cell 19:1295–1312. doi: 10.1105/tpc.106.049346Harkness TA, Davies GF, Ramaswamy V, Arnason TG (2002) The ubiquitin-dependent targeting pathway in Saccharomyces cerevisiae plays a critical role in multiple chromatin assembly regulatory steps. Genetics 162:615–632Hasenbrink G, Schwarzer S, Kolacna L, Ludwig J, Sychrova H, Lichtenberg-Fraté H (2005) Analysis of the mKir2.1 channel activity in potassium influx defective Saccharomyces cerevisiae strains determined as changes in growth characteristics. FEBS Lett 579:1723–1731. doi: 10.1016/j.febslet.2005.02.025Hatakeyama R, Kamiya M, Takahara T, Maeda T (2010) Endocytosis of the aspartic acid/glutamic acid transporter Dip5 is triggered by substrate-dependent recruitment of the Rsp5 ubiquitin ligase via the arrestin-like protein Aly2. Mol Cell Biol 30:5598–5607. doi: 10.1128/MCB.00464-10Hayashi M, Fukuzawa T, Sorimachi H, Maeda T (2005) Constitutive activation of the pH-responsive Rim101 pathway in yeast mutants defective in late steps of the MVB/ESCRT pathway. Mol Cell Biol 25:9478–9490. doi: 10.1128/mcb.25.21.9478-9490.2005He P, Lee SJ, Lin S, Seidler U, Lang F, Fejes-Toth G, Naray-Fejes-Toth A, Yun CC (2011) Serum- and glucocorticoid-induced kinase 3 in recycling endosomes mediates acute activation of Na+/H+ exchanger NHE3 by glucocorticoids. Mol Biol Cell 22:3812–3825. doi: 10.1091/mbc.E11-04-0328Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc Natl Acad Sci USA 104:12217–12222. doi: 10.1073/pnas.0705306104Hein C, Springael JY, Volland C, Haguenauer-Tsapis R, André B (1995) NPl1, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol Microbiol 18:77–87Henke G, Maier G, Wallisch S, Boehmer C, Lang F (2004) Regulation of the voltage gated K+ channel Kv1.3 by the ubiquitin ligase Nedd4-2 and the serum and glucocorticoid inducible kinase SGK1. J Cell Physiol 199:194–199. doi: 10.1002/jcp.10430Herberth S, Shahriari M, Bruderek M, Hessner F, Müller B, Hülskamp M, Schellmann S (2012) Artificial ubiquitylation is sufficient for sorting of a plasma membrane ATPase to the vacuolar lumen of Arabidopsis cells. Planta 236:63–77. doi: 10.1007/s00425-012-1587-0Hicke L, Dunn R (2003) Regulation of membrane protein transport by ubiquitin and ubiquitin-binding proteins. Annu Rev Cell Dev Biol 19:141–172. doi: 10.1146/annurev.cellbio.19.110701.154617Hicke L, Riezman H (1996) Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell 84:277–287Hicke L, Zanolari B, Riezman H (1998) Cytoplasmic tail phosphorylation of the alpha-factor receptor is required for its ubiquitination and internalization. J Cell Biol 141:349–358Hoppe T, Matuschewski K, Rape M, Schlenker S, Ulrich HD, Jentsch S (2000) Activation of a membrane-bound transcription factor by regulated ubiquitin/proteasome-dependent processing. Cell 102:577–586Hsu C, Morohashi Y, Yoshimura S, Manrique-Hoyos N, Jung S, Lauterbach MA, Bakhti M, Grønborg M, Möbius W, Rhee J, Barr FA, Simons M (2010) Regulation of exosome secretion by Rab35 and its GTPase-activating proteins TBC1D10A-C. J Cell Biol 189:223–232. doi: 10.1083/jcb.200911018Hu G, Caza M, Cadieux B, Chan V, Liu V, Kronstad J (2013) Cryptococcus neoformans requires the ESCRT protein Vps23 for iron acquisition from heme, for capsule formation, and for virulence. Infect Immun 81:292–302. doi: 10.1128/IAI.01037-12Huang F, Kirkpatrick D, Jiang X, Gygi S, Sorkin A (2006) Differential regulation of EGF receptor internalization and degradation by multiubiquitination within the kinase domain. Mol Cell 21:737–748. doi: 10.1016/j.molcel.2006.02.018Huang F, Goh LK, Sorkin A (2007) EGF receptor ubiquitination is not necessary for its internalization. Proc Natl Acad Sci USA 104:16904–16909. doi: 10.1073/pnas.0707416104Huibregtse JM, Scheffner M, Beaudenon S, Howley PM (1995) A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc Natl Acad Sci USA 92:2563–2567Hurst AC, Meckel T, Tayefeh S, Thiel G, Homann U (2004) Trafficking of the plant potassium inward rectifier KAT1 in guard cell protoplasts of Vicia faba. Plant J 37:391–397Husnjak K, Dikic I (2012) Ubiquitin-binding proteins: decoders of ubiquitin-mediated cellular functions. Annu Rev Biochem 81:291–322. doi: 10.1146/annurev-biochem-051810-094654Ibl V, Csaszar E, Schlager N, Neubert S, Spitzer C, Hauser MT (2012) Interactome of the plant-specific ESCRT-III component AtVPS2.2 in Arabidopsis thaliana. J Proteome Res 11:397–411. doi: 10.1021/pr200845nIchimura T, Yamamura H, Sasamoto K, Tominaga Y, Taoka M, Kakiuchi K, Shinkawa T, Takahashi N, Shimada S, Isobe T (2005) 14-3-3 proteins modulate the expression of epithelial Na + channels by phosphorylation-dependent interaction with Nedd4-2 ubiquitin ligase. J Biol Chem 280:13187–13194. doi: 10.1074/jbc.M412884200Jegla TJ, Zmasek CM, Batalov S, Nayak SK (2009) Evolution of the human ion channel set. Comb Chem High Throughput Screen 12:2–23Jenness DD, Li Y, Tipper C, Spatrick P (1997) Elimination of defective alpha-factor pheromone receptors. Mol Cell Biol 17:6236–6245Jespersen T, Membrez M, Nicolas CS, Pitard B, Staub O, Olesen SP, Baró I, Abriel H (2007) The KCNQ1 potassium channel is down-regulated by ubiquitylating enzymes of the Nedd4/Nedd4-like family. Cardiovasc Res 74:64–74. doi: 10.1016/j.cardiores.2007.01.008Jolliffe CN, Harvey KF, Haines BP, Parasivam G, Kumar S (2000) Identification of multiple proteins expressed in murine embryos as binding partners for the WW domains of the ubiquitin-protein ligase Nedd4. Biochem J 351(Pt 3):557–565Kallay LM, Brett CL, Tukaye DN, Wemmer MA, Chyou A, Odorizzi G, Rao R (2011) Endosomal Na+(K+)/H+ exchanger Nhx1/Vps44 functions independently and downstream of multivesicular body formation. J Biol Chem 286:44067–44077. doi: 10.1074/jbc.M111.282319Kamsteeg EJ, Savelkoul PJ, Hendriks G, Konings IB, Nivillac NM, Lagendijk AK, van der Sluijs P, Deen PM (2008) Missorting of the Aquaporin-2 mutant E258K to multivesicular bodies/lysosomes in dominant NDI is associated with its monoubiquitination and increased phosphoryla