Desiccation enhances rapid cold hardening in the flesh fly Sarcophaga bullata: evidence for cross tolerance between rapid physiological responses

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1 J Comp Physiol B (217) 187:79 86 DOI 1.17/s ORIGINAL PAPER Desition enhnes rpid old hrdening in the flesh fly Srophg ullt: evidene for ross tolerne etween rpid physiologil responses Shu Xi Yi 1 J. D. Gntz 1 Rihrd E. Lee Jr. 1 Reeived: 27 My 216 / Revised: 29 July 216 / Aepted: 22 August 216 / Pulished online: 27 August 216 Springer-Verlg Berlin Heidelerg 216 Astrt Mny insets use rpid old-hrdening (RCH), physiologil response to su-lethl exposure to stressors, suh s hilling nd desition, to enhne their old tolerne within minutes. Reently, drought-indued RCH, triggered y rief, mild desition, ws desried in lrve of the freeze-tolernt gll fly (Eurost solidginis). However, its prevlene nd eologil signifine in other insets is not known. Consequently, we used freezeintolernt model, the flesh fly, Srophg ullt, to investigte the effets nd mehnisms of drought-indued RCH. In ddition, we investigted how drought- nd oldindued RCH intert y exposing flies to oth desition nd hilling. Desition for 3 h inresed lrvl puprition fter old shok from 28 to 4 % the first exmple of drought-indued RCH in oth freeze-intolernt inset nd in non-overwintering life stge. We lso found tht desition nd hilling together enhned the old hrdiness of lrve nd dults more thn either did seprtely, suggesting tht drought nd old trigger distint physiologil mehnisms tht intert to fford greter old tolerne. These results suggest tht drought-indued RCH is highly onserved response used y insets with diverse life history strtegies. Furthermore, the protetive intertion etween drought- nd old-indued RCH suggests tht, in nture, insets use multiple ues nd physiologil mehnisms to fine-tune their response to hnging mient onditions. Communited y H. V. Crey. * Shu Xi Yi yis@mimioh.edu 1 Deprtment of Biology, Mimi University, 7 Est High Street, Oxford, OH 4556, USA Keywords Rpid old-hrdening Drought-indued rpid old-hrdening Srophg ullt Desition Cold tolerne Cross tolerne Introdution Desition nd old re losely linked to environmentl stressors tht eliit similr physiologil responses (Holmstrup et l. 22; Rinehrt et l. 27). Beuse of their similrity, physiologil djustments mde to desition stress often onfer inresed old tolerne in oth freezetolernt nd freeze-intolernt rthropods (Byley et l. 21; Hywrd et l. 27; Sinlir et l. 213). Most limtory responses our sesonlly over weeks or months, nd s result, reserh on ross tolerne often fouses on reltively slow, sesonl limtiztion (Lee nd Denlinger 1991). Yet, mny insets nd other etotherms n lso instntneously enhne their old tolerne in response to rief hilling or desition in proesses known s old- nd drought-indued rpid old-hrdening (RCH) (Lee et l. 1987; Levis et l. 212). Despite the generlity of RCH in insets, little is known out the potentil for ross tolerne resulting from rief exposure to desition nd hilling. In nture, desiting onditions nd low tempertures often our onomitntly. Protrted exposure to oth stressors ours during temperte nd polr winters, whih re hrterized y old or freezing onditions nd the limited vilility of liquid wter (Dnks 2). However, even rief temperture exursions, whih our nturlly s wether front psses, n strongly influene humidity. For exmple, old fronts re low-pressure ir msses tht generlly lower reltive humidity s well s tempertures (Miles 1962; Moeller et l. 1993). Furthermore, due to their

2 8 J Comp Physiol B (217) 187:79 86 smll size, insets ody tempertures losely trk mient tempertures (Sinlir et l. 213). It is likely, then, tht temperte nd polr insets simultneously experiene rpid hilling nd desition s onsequene of voltile wether nd diurnl thermoperiods. In insets, old exposure frequently triggers the umultion of vrious types of osmolytes, whih serve s ryoprotetnts (Lee nd Denlinger 1991). Cryoprotetnts re often low moleulr mss polyols nd sugrs tht mitigte the effets of hilling or freezing (Lee nd Denlinger 21). Mny of these ompounds lso serve s osmoprotetnts nd re umulted during desition (Holmstrup et l. 21). This osmolyti response is tivted during RCH s well; old-indued RCH triggers modest umultion of ryoprotetnts, suh s glyerol, soritol, nd/or gluose, ffeting 1 2 mosm kg 1 inrese in hemolymph osmollity (Lee nd Denlinger 21). Similrly, drought-indued RCH uses ~4 mosm kg 1 inrese in the hemolymph osmollity of Eurost solidginis lrve, though the speifi solutes driving this response were not identified (Levis et l. 212; Gntz nd Lee 215). It is widely epted tht insets physiologil responses to old nd desition re often similr nd tht prolonged exposure to one of these stressors onfers enhned tolerne to the other (Sinlir et l. 213). Though this ross tolerne is primrily known from slow limtory responses, ute exposure to su-lethl desition lso indues physiologil responses tht trigger osmolyte umultion nd enhned old tolerne (Sinlir nd Chown 23; Benoit et l. 29; Levis et l. 212), suggesting tht ross tolerne etween stressors ours even during rief exposure to desition nd hilling. Furthermore, the interply etween temperture nd humidity suggests tht rief, unpreditle ooling, s ours when wether front psses, is prone to onomitntly produe desiting onditions. Despite this, no study hs ddressed the potentil for ross tolerne etween these RCH triggers. Thus, to more fully understnd the reltionship etween the rpid responses to rief desition nd hilling, we investigted the following questions using lrve nd dults of the flesh fly, Srophg ullt: does ute desition indue RCH in this freeze-intolernt fly? Do the responses to hilling nd desition intert to inrese the rte of orgnisml reovery from old shok? Do they lso enhne old tolerne t the tissue-level? And wht effet do these hve on the osmolyti response? Mterils nd methods Inset ulture nd tretments The flesh fly, S. ullt Prker (Dipter: Srophgide), ws rered following the methods desried y Lee nd Denlinger (1985). Lrve nd dults were used to ssess the effets of rief desition on old tolerne, hill om reovery, nd the RCH response. In lrve (n = 3), orgnisml survivl ws evluted y whether they suessfully puprited 72 nd 96 h fter tretment. The sme lrve were used for oth time points; tht is, the 96 h mesurement inluded lrve tht puprited fter 72 h s well. Nerly, ll the lrve tht filed to puprite fter 96 h died without pupriting. In dults (n = 3), ssessment ws mde using the rte of reovery from hill om, determined y return of oordinted movement 2, 3, 4, 6, nd 12 min fter tretment. Coordinted movement ws defined s nturl movements s during wlking or flying. Four-dy-old lrve nd 6-dy-old dults were treted s follows: ontrol (untreted t 25 C), old shoked (CS) (diret trnsfer to 9 C nd held for 2 h), RCH (pretreted t C for 2 h followed y old shok), D + CS (lrve nd dults were desited for 3 nd 4.5 h, respetively, t ~4 % reltive humidity over Drierite t 22 C, followed y old shok), nd D + RCH (desition s desried in D + CS followed y RCH tretment, then old shok). Lrvl nd dult desition times were determined y the time it took to hieve loss of 2 3 % of their fresh mss. We used 2 3 % of fresh mss s trget, euse, in E. solidginis, similr mount of wter loss ws suffiient to trigger drought-indued RCH (Gntz nd Lee 215). Assessment of ellulr viility We ssessed ellulr-level dmge used y old shok with vitl dye ssy using LIVE/DEAD sperm viility kit (Moleulr Proes, Eugene, OR, USA) s dpted y Yi nd Lee (23). Briefly, isolted lrvl ft ody nd dult midgut tissues were hrvested from rndomly seleted, living insets immeditely following the termintion of the tretment. Tissues were inuted in two fluoresent vitl dyes in two-step proess. SYBR-14, memrnepenetrting green dye, stins nulei DNA from ll ells, while propidium iodide, red dye, is exluded y intt memrnes nd only stins the DNA in ells whose memrnes re ompromised y old shok. After the dyes were pplied, fluoresene mirosopy ws used to determine the rtio of undmged to dmged ells. For eh tissue, every ell in four or more disrete fields of view during mirosopy (minimum of 5 ells) ws sored s dmged or undmged. Men ± SE were determined y the verge rtio of undmged ells from 3 to 4 lrve per tretment. Osmollity nd polyol mesurement Hemolymph osmollity ws mesured for ontrol nd desited lrve (n = 1 mesurements) y drwing 2 µl of hemolymph into glss miropillry pipette.

3 J Comp Physiol B (217) 187:79 86 Hemolymph ws pooled from 2 to 3 lrve, nd the osmollity ws mesured using Model 332 Osmometer (Advned Instrument In., Norwood, MA, USA). We only mesured hemolymph osmollity in lrve, euse we were unle to hrvest dequte mounts of hemolymph from dult flies. Cryoprotetive sugrs nd polyols (glyerol, soritol, nd gluose) were mesured in the whole-ody extrts of lrve, s desried y Gntz nd Lee (215). Eh lrv ws homogenized in 1.5-ml Eppendorf tue with.6 N perhlori id (PCA) nd inuted on ie for 5 min. The superntnt ws retined fter entrifugtion for 2 min t 16, g. To neutrlize the PCA extrt, n equivlent mount of 1. M potssium ironte ws dded to the superntnt nd inuted on ie with vented lid for 15 min. Following rief entrifugtion, the superntnt ws liquoted for use in ryoprotetnt ssys. Glyerol ontent ws determined following the method y Holmstrup et l. (1999). Briefly, 2 µl liquot of whole-ody extrt ws dded to 8 µl of reonstituted Free Glyerol Regent (Sigm-Aldrih, St. Louis, MO, USA). Asorne ws red t 54 nm on Jenwy Model 675 UV/Vis spetrophotometer following 15-min inution t 37 C. Vlues re reported s miromoles of glyerol per grm of fresh mss. Soritol ontent ws mesured using olorimetri ssy dpted from Bergmeyer et l. (1974). A retion mixture of 333 µl of neutrlized whole-ody extrt, 666 µl of.1 M sodium pyrophosphte, nd 33 µl of 3 mm NAD ws prepred, nd the initil sorne ws red t 34 nm. Soritol dehydrogense (16.6 µl, 5 mg protein/ ml, Sigm-Aldrih, St. Louis, MO, USA) ws dded to the retion mixture nd inuted for 1 h t room temperture. The finl sorne ws reorded t 34 nm. Soritol ontent ws determined y the differene in sorne from the initil reding to the finl reding. Dt re expressed s miromoles of soritol per grm of fresh mss. Gluose onentrtions were mesured y liquotting whole-ody extrt into 1 μl portions. Gluose ontent ws then determined using olorimetri gluose ssy kit (Sigm-Aldrih, St. Louis, MO, USA). Sttistil nlysis Cold survivl rtes t oth orgnisml nd tissue-levels, hemolymph osmollity, nd polyol ontents were evluted using unpired t tests (SigmPlot 12.5) to determine differenes etween tretment groups, with the signifine level set to P <.5 (n = 3). Response vriles with perentge rtes were rsine-squre root trnsformed to stilize the vrine efore omprison. Onewy ANOVA (SigmPlot 12.5) with post ho Bonferroni orretion ws lso performed to determine whether 81 desition tretment hd signifint effet on the RCH response for orgnisml nd ellulr survivl. All dt re expressed s men ± SE. Results Desition enhned orgnisml old tolerne in RCH treted flies Lrve tht were desited efore eing exposed to disriminting old temperture (old shok) puprited t higher rte thn non-desited, old-shoked lrve, 27.4 ± ± 7.1 % fter 72 h; however, this effet ws not evident fter 96 h (Fig. 1; P >.5). Pretretment with desition nd hilling (D + RCH) further improved the rte of puprition, whih lso exeeded tht of lrve tht were hilled nd old shoked (RCH tretment), 46.1 ± ± 3.9 % nd 63.5 ± ± 2.4 %, fter 72 nd 96 h, respetively (Fig. 1; P <.5). D + RCH tretment in dult flies elerted the rte of reovery from hill om reltive to RCH lone, s 66.7 ± 8.8 % of desited flies were ple of movement within 2 min of reovery ompred to only 2. ± 5.8 % of their non-desited prtners (Fig. 2; P <.5). Similrly, fter 3 min of reovery, 83.3 ± 8.8 % of desited Puprition (%) h 96 h d Tretments Fig. 1 Desition signifintly inresed puprition rtes (%) in the rpid old-hrdening (RCH)-treted lrve. Control lrve were untreted. D-ontrol tretments were only desited without susequent old tretment, while old-shok (CS) tretments reeived the disriminting old exposure lone nd RCH tretments reeived rief hilling. D + CS nd D + RCH represent desition tretment efore CS nd RCH, respetively. Puprition ws oserved 72 nd 96 h fter ompletion of tretment. Groups not shring letters were signifintly different (P <.5, n = 3)

4 82 J Comp Physiol B (217) 187:79 86 % Reovery Time fter tretment (min) D+RCH RCH A Rpid oldhrdening Cold-shok Control Fig. 2 Comprison of the reovery rtes (%) of dults etween RCH tretment lone (RCH, open irles) nd desition plus RCH tretment (D + RCH, losed irles). The ddition of desition to RCH tretments elerted reovery from old shok. Flies ple of oordinted movement were sored s reovered. Dt points not shring letters were signifintly different (P <.5, n = 3) B 1 Non-desited Desited flies ould move ompred to 3. ± 5.8 % of non-desited flies (Fig. 2; P <.5). Slight desition enhned the old-indued RCH response, suggesting tht rief, mild desition triggers physiologil response tht is distint from tht of hilling. Interestingly, the protetive effets of desition lone were only evident in lrve 72 h fter tretment (Fig. 1; P <.5). In ontrst, desition lone did not hve signifint effet on the rte of reovery ompred to untreted ontrols t ny time point etween 2 nd 12 min (dt not shown). % Cell viility d Desition enhned ellulr old tolerne Brief desition enhned ellulr old tolerne of oth lrvl ft ody nd dult midgut ells in old-shoked flies (Figs. 3, 4). Compred to their non-desited ounterprts, desition inresed ell survivl y 24.9 % (CS ± 6.1 % vs. D + CS 48.8 ± 6. %) in the lrvl ft ody (Fig. 3; P <.3) nd y 45. % (CS 13.4 ± 5.8 % vs. D + CS 58.5 ± 8. %) in the dult midgut (Fig. 4, P <.3). In ddition, ellulr viility ssys using lrvl (Fig. 3) nd dult (Fig. 4) ft ody nd midgut tissues orroorted the orgnisml ssessments, s D + RCH tretments enhned old tolerne more thn RCH lone. In lrvl ft ody, only 23.9 ± 6.1 % of ells remined vile following old shok. Cold-indued RCH tretment inresed the rtio of vile ells to 82.1 ± 2.3 % (Fig. 3; P <.1), while 3 h of desition preeding old-indued RCH Fig. 3 Effet of desition on ell viility of lrvl ft ody. Vitl dyes imges of lrvl ft ody tissue. Green ells were sored s live, while red ells were sored s ded. Desition tretment signifintly improved ellulr survivl in oth the D + CS nd D + RCH groups. Non-desited ontrol photo ws tken t 4 mgnifition; ll other photos were tken t 1 mgnifition. Perent of vile ells ounted from vitl dye-stined lrvl ft ody. Control lrve were untreted. Desition tretments were only desited without susequent old tretment, while old-shok (CS) tretments reeived the disriminting old exposure lone. RCH tretments reeived rief hilling. D + CS nd D + RCH represent desition tretment efore CS nd RCH, respetively. Groups not shring letters were signifintly different (P <.5) (olor figure online) tretment further inresed the perentge of vile ells to 95.5 ± 1.5 % (Fig. 3; P <.1). In dult midgut tissues, 4.5-h desition tretment inresed the perentge of vile ells in RCH-treted dults to 96.7 ±.6 % ompred to 77.5 ± 1.8 % fter RCH tretment lone (Fig. 4; P <.1).

5 J Comp Physiol B (217) 187: A Rpid oldhrdening Cold-shok Control Hemolymph osmollity (mosm/kg) Control, Desited 2.5 h Desited 6 h % Cell viility B Non-desited Desited Desition elevted hemolymph osmollity in lrve Fig. 4 Effet of desition on ell viility of dult midguts. Vitl dyes imges of dult midgut tissue. Green ells were sored s live, while red ells were sored s ded. Desition tretment signifintly improved ellulr survivl in oth the D + CS nd D + RCH groups. Non-desited ontrol nd desited rpid old-hrdening photos were tken t 4 mgnifition; ll other photos were tken t 1 mgnifition. Perent of vile ells ounted from dult midgut. Control lrve were untreted. Desition tretments were only desited without susequent old tretment, while oldshok (CS) tretments reeived the disriminting old exposure lone. RCH tretments reeived rief hilling. D + CS nd D + RCH represent desition tretment efore CS nd RCH, respetively. Groups not shring letters were signifintly different (P <.5) (olor figure online) To etter understnd the physiologil mehnisms y whih desition enhnes the RCH response, we mesured hnges in lrvl hemolymph osmollity following desition tretments (Fig. 5). Brief desition used signifint inreses in hemolymph osmollity in timedependent mnner: ± 5.5 mosm kg 1 in untreted ontrols, 48. ± 5.5 mosm kg 1 fter 2.5-h desition, nd 437. ± 8.2 mosm kg 1 fter 6-h desition Fig. 5 Chnges of osmollity in lrvl hemolymph efore nd fter desition. Lrve were strved for 14 h for ll groups prior to desition tretment. Groups not shring letters were signifintly different (P <.5) (P <.5). Though we did not diretly mesure wter loss during these experiments, we n lulte the expeted effet of wter loss on hemolymph osmollity using dehydrtion rtes estlished during drought-indued RCH experiments nd expeted orgnisml wter ontents. Wter ontent of S. ullt lrve is ~71 % (Yi, unpulished dt), nd wter loss rtes were lose to 1 % fresh mss per hour over Drierite. Dehydrtion tretments of 2.5 nd 6 h would e expeted to use 13 nd 32 mosm kg 1 inreses hemolymph osmollity, respetively. Thus, dehydrtion ounts for out hlf of the oserved inreses in hemolymph solute onentrtion. Glyerol, soritol, nd gluose levels did not explin hnges in hemolymph osmollity Glyerol nd soritol levels remined unhnged ross ll tretment groups, though there were slight, ut signifintly inreses in gluose onentrtions following old-indued RCH, desition, desition nd old shok (D + CS), nd desition with old-indued RCH (D + RCH) (Tle 1). Disussion Drought-indued RCH is novel response tht hs only een reported in three freeze-tolernt insets (Sinlir nd Chown 23; Benoit et l. 29; Levis et l. 212). In this study, we investigted whether drought-indued RCH lso ours in non-overwintering stges (lrvl nd dult) of the freeze-intolernt flesh fly, S. ullt. In lrve, pretretment with 3 h of desition signifintly enhned

6 84 J Comp Physiol B (217) 187:79 86 Tle 1 Cryoprotetnt levels in the ody extrts of lrve (men ± SEM, µmol/g FM) Glyerol Soritol Gluose Non-desition Control 3.23 ± ± ±.44 Cold shok (CS) 3.73 ± ± ±.53, RCH 2.85 ± ± ±.34 Desition pretretment Desited only 3.84 ± ± ±.35 Cold shok (D + CS) 3.41 ± ± ±.57 RCH (D + RCH) 3.52 ± ± ±.23 Dt with different letters in the sme olumn indite signifint differene (P <.5) etween tretment groups CS old shok, D + CS desition prior to old-shok tretment, D + RCH desition prior to RCH tretment, RCH rpid old-hrdening the puprition rte 72 h fter old shok, though this effet ws not evident fter 96 h. In dults, 4.5 h desition hd no signifint effet on the rte of reovery from hill om. However, using ellulr-level mesurements of old tolerne, we found evidene of drought-indued RCH in oth the lrvl nd dult life stges. The disrepny etween orgnisml nd ellulr-level ssessments of old hrdiness my e due to the sutle nture of RCH responses; tht is, orgnisml-level ssessments my e too orse to detet the effets of RCH. Despite these limittions, our results re the first exmple of drought-indued RCH in freeze-intolernt inset. Though we found only modest effets of droughtindued RCH in this study, old-indued RCH ws strongly enhned y desition pretretment. This result does not indite tht there is synergy etween drought- nd oldindued RCH; indeed, this study ws not designed to determine if these re synergisti, dditive, or even ntgonisti effets. Yet, desition nd hilling together enhne old tolerne more thn either does seprtely, suggesting tht drought- nd old-indued RCH use different mehnisms tht intert to enhne old tolerne. Differenes in ryoprotetnt umultion during rief hilling nd desition further suggest tht these triggers eliit distint responses. Mny insets, inluding S. ullt, umulte glyerol nd/or soritol during rief hilling (Yoder et l. 26; Lee nd Denlinger 21). In ontrst, rief desition does not use n umultion of glyerol, soritol, trehlose, or gluose in E. solidginis lrve (Levis et l. 212; Gntz nd Lee 215), nd in this study, there were no hnges in glyerol or soritol levels in S. ullt lrve. Thus, future reserh should fous on determining whih ellulr pthwys re tivted y ute desition. Sine the first steps of old-indued RCH inlude lium flux used y hnges in plsm memrne permeility followed y downstrem phosphoryltion of p38 mitogentivted protein kinse (p38 MAPK), oth lium flux nd the reltive undne of phosphorylted p38mapk seem like good strting points for mehnisti studies of drought-indued RCH (Fujiwr nd Denlinger 27; Teets et l. 28, 213). Though little is known out the underpinning mehnisms of drought-indued RCH, the umultion of ryoprotetnts ppers to e importnt. In E. solidginis lrve, rief desition uses ~3 mosm kg 1 inrese in hemolymph osmollity eyond wht is explined y wter loss during dehydrtion, suggesting n umultion of ryoprotetive solutes (Levis et l. 212; Gntz nd Lee 215). Similrly, we found tht desiting S. ullt lrve for 2.5 nd 6 h resulted in ~27 nd ~55 mosm kg 1 inreses in hemolymph osmollity, respetively. Wter loss during desition only explins ~1 nd ~23 mosm kg 1 of the inreses in hemolymph osmollity, suggesting modest umultion of osmolytes during ute dehydrtion to ount for the remining inrese in osmoti pressure. The slight inrese in hemolymph osmollity during desition is onsistent with the mgnitude of the ryoprotetnt response during old-indued RCH, whih usully eliits 1 2 mosm kg 1 inrese in hemolymph osmollity (Overgrd et l. 27). To investigte the use of the inrese in osmoti pressure during desition, we mesured the onentrtions of three ommon ryoprotetive sugrs nd polyols: glyerol, soritol, nd gluose. While our nlyses unovered some signifint inreses in gluose onentrtion, none of these were sustntil enough to signifintly lter hemolymph osmollity or likely to ount for inresed old tolerne. However, ution should e used when interpreting these results, euse we lulted ryoprotetnt onentrtions using fresh mss rther thn dry mss, nd the slight derese in fresh mss (~2 %) resulting from wter loss in desition tretments my influene our results. In ddition, it is possile tht only mesuring ryoprotetnt levels from whole-ody extrts msk the effets of redistriution of these sugrs from one tissue or ody omprtment to nother nd tht iologilly meningful hnges in the distriution of ryoprotetnts were not deteted. Nonetheless, these results suggest tht the ryoprotetnt response to rief desition is driven y the umultion of solutes other thn glyerol, soritol, or gluose. Reently, free mino ids hve gined reognition s prominent prt of the old-hrdening response in some insets (Koštál et l. 211, 212; Yi nd Lee 216). Furthermore, Gntz nd Lee (215) speulted tht inresed hemolymph osmollity during droughtindued RCH ws result of inresed utophgi proteolysis yielding inresed onentrtions of free mino ids. Not only would this lierte mino ids, it would tively derese ville ody wter, s proteolysis is hydrolyti

7 J Comp Physiol B (217) 187:79 86 proess (Blommrt et l. 1997). Reduing ody wter ontent through proteolysis ould hve dptive signifine, sine redution of solvent would inrese the solute onentrtion, whih would hve the sme effet s synthesizing new solutes. Furthermore, utophgy ould oneivly e prt of the RCH response, euse it n quikly nd drmtilly inrese its tivity (Blommrt et l. 1997). In Drosophil melnogster ft ody, 3 h inution in protein defiient medi triggered strvtion-indued utophgy, using signifint inrese in the numer of utophgosomes (Sott et l. 24), nd in perfused rt livers, utophgi proteolysis n degrde up to 5 % of ytosoli protein per hour (Mortimore et l. 1989). Together, these results suggest tht the utophgi response is rpid enough nd suffiiently roust to signifintly ontriute to drought-indued RCH. At the eologil level, the RCH response llows insets to fine-tune their physiologil stte to mth mient onditions. Indeed, RCH is mnifested in vriety of wys tht improve survivl nd reprodutive suess, inluding inresing survivl of su-zero tempertures, enhning freeze-tolerne, deresing the temperture required to indue hill om, suppressing wter loss during desition, s well s preserving flight, mting, ourtship ehvior, lerning, feundity, nd longevity (see review y Lee nd Denlinger 21). Importntly, RCH is indued y eologilly relevnt rtes of hilling (Shreve et l. 24), though drought-indued RCH hs not yet een investigted under field onditions. Furthermore, it is possile tht RCH is more roust response thn is urrently known euse of the omined effets of multiple RCH responses triggered y nturl onditions. It is likely tht insets ommonly fe simultneous exposure to multiple stressors, sine nturl onditions rrely present only one hllenge t time (Holmstrup et l. 21). For exmple, old fronts often use rupt dereses in reltive humidity s well s temperture (Moeller et l. 1993), suggesting tht rief desition nd hilling re likely to e experiened onomitntly. The intertion etween drought- nd old-indued RCH, whih resulted in mrked derese in reovery time nd mortlity rte in this study, ould llow insets to remin tive during the spring nd utumn sesons, espeilly in temperte regions, when the wether is prtiulrly unstle. With this in mind, future reserh should fous on whether drought-indued RCH is triggered in nture nd on the effets of simultneous exposure to multiple RCH triggers under field onditions. In ddition, it would e interesting to investigte the intertions etween rpid physiologil responses triggered y ues other thn hilling nd dehydrtion. RCH n e triggered y high temperture nd noxi, while other stressors, suh s overhydrtion, exposure to ultrviolet light, nd oxidtive stress lso indue rpid physiologil responses (Coulson nd Ble 1991; Rinehrt et l. 2; Lopez-Mrtinez 85 et l. 28, 29). Chrterizing the extent of ross tolerne etween distint rpid physiologil responses, espeilly fousing on eologilly relevnt omintions of ues, my led to greter ppreition of the signifine of rpid limtory responses in insets. Mny stressors re losely linked nd might e expeted to frequently our onomitntly, suh s high temperture nd UV irrdition, noxi nd freezing, hypoxi nd overhydrtion, nd UV irrdition nd oxidtive stress (Storey nd Storey 1988; Hok nd Stnley 21; Thieden et l. 26; Meng et l. 29). Thus, multiple rpid responses my e tivted simultneously under nturl onditions. Perhps, the eologil importne of rpid physiologil dpttion hs een underestimted y not ounting for the intertion etween these responses? In onlusion, we present the first evidene of (1) droughtindued RCH in non-overwintering stge of freeze-intolernt inset nd (2) intertions etween old- nd droughtindued RCH to further enhne stress tolerne. Insets use old-indued RCH to fine-tune their physiologil stte in ny life stge, during ny seson (Lee nd Denlinger 21). In ontrst, drought-indued RCH hs only een investigted in the overwintering lrve of freeze-tolernt moth, Pringleophg mrioni, nd freeze-tolernt fly, E. solidginis (Sinlir nd Chown 23; Levis et l. 212). Our finding tht drought-indued RCH used y S. ullt dults suggests tht this response my e s pervsive, s oldindued RCH is mong inset tx. In ddition, the intertion etween drought- nd old-indued RCH indites tht desition nd hilling trigger distint physiologil mehnisms, though these mehnisms re poorly understood. These results rise numerous questions out the intertion etween distint RCH responses in nture. How similr re the mehnisms triggered y desition nd old? Whih rpid limtory responses intert to further enhne stress tolerne? And how importnt is the interply etween these rpid responses to the suess of insets? Aknowledgments This reserh ws supported y grnts from NSF (#IOB nd PLR ). Compline with ethil stndrds Conflit of interest The uthors delre tht they hve no onflits of interest. Referenes Byley M, Petersen SO, Knigge T, Köhler HR, Holmstrup M (21) Drought limtion onfers old tolerne in the soil ollemoln Folsomi ndid. J Inset Physiol 47(1): Benoit JB, Lopez-Mrtinez G, Elnitsky MA, Lee RE, Denlinger DL (29) Dehydrtion-indued ross tolerne of Belgi ntrti lrve to old nd het is filitted y trehlose umultion. Comp Biohem Physiol A 152(4):

8 86 J Comp Physiol B (217) 187:79 86 Bergmeyer HU, Gruer W, Gutmn I (1974) D-Soritol. In: Bergmeyer HU (ed) Methods of enzymti nlysis. Ademi Press, New York, pp Blommrt EFC, Luiken JJFP, Meijer AJ (1997) Autophgi proteolysis: ontrol nd speifiity. Histohem J 29(5): Coulson SJ, Ble JS (1991) Anoxi indues rpid old hrdening in the housefly Mus domesti (Dipter: Muside). J Inset Physiol 37(7): Dnks HV (2) Dehydrtion in dormnt insets. J Inset Physiol 46(6): Fujiwr Y, Denlinger DL (27) p38 MAPK is likely omponent of the signl trnsdution pthwy triggering rpid old hrdening in the flesh fly Srophg rssiplpis. J Exp Biol 21(18): Gntz JD, Lee RE (215) The limits of drought-indued rpid oldhrdening: extremely rief, mild desition triggers enhned freeze-tolerne in Eurost solidginis lrve. J Inset Physiol 73:3 36 Hywrd SA, Rinehrt JP, Sndro LH, Lee RE, Denlinger DL (27) Slow dehydrtion promotes desition nd freeze tolerne in the Antrti midge Belgi ntrti. J Exp Biol 21(5): Hok WW, Stnley DW (21) Insets in hypoxi. J Inset Physiol 47(6): Holmstrup M, Costnzo JP, Lee RE (1999) Cryoprotetive nd osmoti responses to old limtion nd freezing in freezetolernt nd freeze-intolernt erthworms. J Comp Physiol B 169(3): Holmstrup M, Byley M, Rmløv H (22) Superool or dehydrte? An experimentl nlysis of overwintering strtegies in smll permele rti invertertes. Pro Ntl Ad Si USA 99(8): Holmstrup M, Byley M, Pedersen SA, Zhrissen KE (21) Intertions etween old, desition nd environmentl toxins. In: Denlinger DL, Lee RE (eds) Low temperture iology of insets. Cmridge University Press, New York, pp Koštál V, Zhrdnıčková H, Šimek P (211) Hyperprolinemi lrve of the drosophilid fly, Chymomyz ostt, survive ryopreservtion in liquid nitrogen. Pro Ntl Ad Si 18(32): Koštál V, Šimek P, Zhrdnıčková H, Cimlová J, Štětin T (212) Conversion of the hill suseptile fruit fly lrv (Drosophil melnogster) to freeze tolernt orgnism. Pro Ntl Ad Si USA 19(9): Lee RE, Denlinger DL (1985) Cold tolerne in dipusing nd nondipusing stges of the flesh fly, Srophg rssiplpis. Physiol Entomol 1(3): Lee RE, Denlinger DL (eds) (1991) Insets t low temperture. Chpmn & Hll, New York Lee RE, Denlinger DL (eds) (21) Rpid old-hrdening: eologil signifine nd underpinning mehnisms. Low temperture iology of insets. Cmridge University Press, New York, pp Lee RE, Chen CP, Denlinger DL (1987) A rpid old-hrdening proess in insets. Siene 238(4832): Levis N, Yi S-X, Lee RE (212) Mild desition rpidly inreses freeze tolerne of the goldenrod gll fly, Eurost solidginis: evidene for drought-indued rpid old-hrdening. J Exp Biol 215(21): Lopez-Mrtinez G, Elnitsky MA, Benoit JB, Lee RE, Denlinger DL (28) High resistne to oxidtive dmge in the Antrti midge Belgi ntrti, nd developmentlly linked expression of genes enoding superoxide dismutse, tlse nd het shok proteins. Inset Biohem Mol Biol 38(8): Lopez-Mrtinez G, Benoit JB, Rinehrt JP, Elnitsky MA, Lee RE, Denlinger DL (29) Dehydrtion, rehydrtion, nd overhydrtion lter ptterns of gene expression in the Antrti midge, Belgi ntrti. J Comp Physiol B 179(4): Meng JY, Zhng CY, Zhu F, Wng XP, Lei CL (29) Ultrviolet light-indued oxidtive stress: effets on ntioxidnt response of Helioverp rmiger dults. J Inset Physiol 55(6): Miles MK (1962) Wind, temperture nd humidity distriution t some old fronts over SE. Englnd. Q J R Meteorol So 88(377):286 3 Moeller CC, Huh OK, Roerts HH, Gumley LE, Menzel WP (1993) Response of Louisin ostl environments to old front pssge. J Costl Res 9(2): Mortimore GE, Reet Pösö A, Lrdeux BR (1989) Mehnism nd regultion of protein degrdtion in liver. Dietes/Metol Rev 5(1):49 7 Overgrd J, Mlmendl A, Sørensen JG, Bundy JG, Loeshke V, Nielsen NC, Holmstrup M (27) Metolomi profiling of rpid old hrdening nd old shok in Drosophil melnogster. J Inset Physiol 53(12): Rinehrt JP, Youm GD, Denlinger DL (2) Thermotolerne nd rpid old hrdening meliorte the negtive effets of rief exposures to high or low tempertures on feundity in the flesh fly, Srophg rssiplpis. Physiol Entomol 25(4): Rinehrt JP, Li A, Youm GD, Roih RM, Hywrd SA, Denlinger DL (27) Up-regultion of het shok proteins is essentil for old survivl during inset dipuse. Pro Ntl Ad Si USA 14(27): Sott RC, Shuldiner O, Neufeld TP (24) Role nd regultion of strvtion-indued utophgy in the Drosophil ft ody. Dev Cell 7(2): Shreve SM, Kelty JD, Lee RE (24) Preservtion of reprodutive ehviors during modest ooling: rpid old-hrdening finetunes orgnisml response. J Exp Biol 27(11): Sinlir BJ, Chown SL (23) Rpid responses to high temperture nd desition ut not to low temperture in the freeze tolernt su-antrti terpillr Pringleophg mrioni (Lepidopter, Tineide). J Inset Physiol 49(1):45 52 Sinlir BJ, Ferguson LV, Slehipour-shirzi G, MMilln HA (213) Cross-tolerne nd ross-tlk in the old: relting low tempertures to desition nd immune stress in insets. Integr Comp Biol 53(4): Storey KB, Storey JM (1988) Freeze tolerne in nimls. Physiol Rev 68(1):27 84 Teets NM, Elnitsky MA, Benoit JB, Lopez-Mrtinez G, Denlinger DL, Lee RE (28) Rpid old-hrdening in lrve of the Antrti midge Belgi ntrti: ellulr old-sensing nd role for lium. Am J Physiol-Regul Integr Comp Physiol 294(6):R1938 R1946 Teets NM, Yi S-X, Lee RE, Denlinger DL (213) Clium signling medites old sensing in inset tissues. Pro Ntl Ad Si USA 11(22): Thieden E, Philipsen PA, Wulf HC (26) Ultrviolet rdition exposure pttern in winter ompred with summer sed on time-stmped personl dosimeter redings. Br J Dermtol 154(1): Yi S-X, Lee RE (23) Deteting freeze injury nd sesonl oldhrdening of ells nd tissues in the gll fly lrve, Eurost solidginis (Dipter: Tephritide) using fluoresent vitl dyes. J Inset Physiol 49(11): Yi S-X, Lee RE (216) Cold-hrdening during long-term limtion in freeze-tolernt woolly er terpillr, Pyrrhrti isell. J Exp Biol 219(1):17 25 Yoder JA, Benoit JB, Denlinger DL, Rivers DB (26) Stress-indued umultion of glyerol in the flesh fly, Srophg ullt: evidene inditing nti-desint nd ryoprotetnt funtions of this polyol nd role for the rin in oordinting the response. J Inset Physiol 52(2):22 214

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