surviving starvation: changes accompanying starvation tolerance in a bdelloid rotifer

Surviving Starvation: Changes Accompanying StarvationTolerance in a Bdelloid Rotifer

Roberto Marotta,1* Andrea Uggetti,1 Claudia Ricci,2 Francesca Leasi,1 and Giulio Melone1

1Dipartimento di Biologia, Universita degli Studi di Milano, 20133 Milano, Italy2Dipartimento di Protezione dei Sistemi Agroalimentare e Urbano e Valorizzazione delle Biodiversita,Universita degli Studi di Milano, 20133 Milano, Italy

ABSTRACT Bdelloid rotifers survive desiccation andstarvation by halting activity and entering a kind of dor-mancy. To understand the mechanisms of survival in theabsence of food source, we studied the anatomical and ul-trastructural changes occurring in a bdelloid species,Mac-rotrachela quadricornifera Milne 1886, after starvationfor different periods. The starved rotifers present a pro-gressive reduction of body size accompanied with a con-sistent reduction of the volume of the stomach syncytium,where lipid inclusions and digestive vacuoles tend to fadewith prolonged starvation. Similar reduction occurs in thevitellarium gland, in which yolk granules progressivelydecrease in number and size. The changes observed in thesyncytia of the stomach and the vitellarium suggest thatduring starvation M. quadricornifera uses resourcesdiverted from the stomach syncytium first and from thevitellarium syncytium later, resources that are normallyallocated to reproduction. The fine structure of starvedbdelloids is compared with that of anhydrobiotic bdelloids,revealing that survival during either forms of dormancy issustained by different physiological mechanisms. J. Morphol.273:1–7, 2012. � 2011Wiley Periodicals, Inc.

KEY WORDS: rotifers; extreme adaptation; starvation;dormancy; morphology; electron microscopy; CLSM

INTRODUCTION

Bdelloid rotifers, like other freshwater inverte-brates, are capable of surviving conditions incom-patible with life by halting activity, lowering me-tabolism to undetectable levels, and resumingactive life when conditions become suitable again.Such capability of a reversible life suspension is aform of dormancy. Commonly, dormancy in fresh-water habitats is cued by water evaporation and istermed anhydrobiosis (e.g., Crowe et al., 1992).However, anhydrobiosis is not the only form of dor-mancy; indeed, bdelloid species were found to tol-erate prolonged starvation by suspending activityand reproduction until food is available again(Ricci and Perletti, 2006).

During starvation, animals in general and roti-fers in particular can survive longer if they allocateresources to maintenance instead of to reproduction(e.g., Kirk, 1997). When dormant, starved bdelloidssuspend reproduction and can survive periods that

are longer than their regular lifespan. To eitherstressful conditions, starvation or desiccation, bdel-loids appear to react with similar responses: theycontract into a ‘‘tun’’ shape and halt activity andreproduction. When conditions become suitableagain, bdelloids resume activity and, in a couple ofdays, reproduction. Bdelloids that experienced ei-ther starvation or desiccation were found to havean average fecundity as high as that of theunstressed controls (Ricci and Covino, 2005; Ricciand Perletti, 2006). Remarkably, the time spent instarvation or in anhydrobiosis is totally disregardedby the recovered rotifers. Thus, the two dormancyforms seem to evoke similar responses, and reason-ably the adjustments a bdelloid undergoes inresponse to either stresses might be similar.

The morphology of an anhydrobiotic bdelloid hasrecently been investigated by Marotta et al. (2010),showing that the anhydrobiont loses internal waterand compress structures, maintaining tissues andorgan integrity. Here, we document the morphologi-cal and structural changes associated with starva-tion in the bdelloid rotifer Macrotrachela quadricor-nifera using light, electron, and confocal microscopy

Roberto Marotta, Andrea Uggetti, and Claudia Ricci contributedequally to this study.

Roberto Marotta is currently at Istituto Italiano di Tecnologia(IIT), Via Morego 30, 16163 Genova, Italy.

Andrea Uggetti is currently at Istituto Neurologico Carlo Besta,Via Celoria 11, 20133 Milano, Italy.

Francesca Leasi is currently at Imperial College London, SilwoodPark, Buckhurst Road, Ascot, SL5 7PY Berkshire, UK.

Contract grant sponsor: FIRST.

*Correspondence to: Roberto Marotta, Via Morego 30, 20133 Gen-ova, Italy. E-mail: [email protected]

Received 18 December 2010; Revised 4 May 2011;Accepted 19 June 2011

Published online 25 August 2011 inWiley Online Library (wileyonlinelibrary.com)DOI: 10.1002/jmor.11000

JOURNAL OF MORPHOLOGY 273:1–7 (2012)

� 2011 WILEY PERIODICALS, INC.

to understand if similar anatomical adaptationssustain the two forms of dormancy.

MATERIALS AND METHODS

Macrotrachela quadricornifera Milne 1886, originally isolatedfrom mosses around Milan, Italy, is cultivated under laboratoryconditions (Ricci, 1991). From a batch culture, eggs were trans-ferred and hatchlings were cultivated till the age of 8 days.From the cohort, 100 rotifers were isolated and assigned tothree groups: 1) 40 rotifers were starved for 20 days (20-daystarved), 2) 40 rotifers were starved for 35 days (35-daystarved), and 3) 20 rotifers were cultivated and fed regularly(fed controls). Starvation was induced by replacing the usualculture medium with deionized water previously filtered with a0.15-lm mesh filter (Ricci and Perletti, 2006). Although bacteriamay have been present in the water medium, they are unlikelyto have contributed significantly to maintenance or to nutrition,because the rotifer culture medium was water filtered through0.15-lm mesh filter.Of the 40 treated rotifers from Groups 1 and 2, 20 from each

group were processed for morphological studies, and theremaining 20 were re-fed regularly after the end of the starva-tion period serving as controls for recovery after starvation(starvation controls).

Light Microscopy and Transmission ElectronMicroscopy

The rotifers belonging to the three experimental groups (exceptthe starvation controls) were processed at the end of the starva-tion period. These were fixed in 2% glutaraldehyde in 0.025 moll21 cacodylate buffer (pH 7.2–7.4) for 2 h, washed in 0.125 moll21 cacodylate buffer, postfixed with 1% OsO4 in 0.075 mol l21

cacodylate buffer for 2 h, washed in distilled water, stained intoto overnight in 2% aqueous uranyl acetate, dehydrated in agraded ethanol series, and embedded in both SPURR and EPONresin. For light microscopy (LM) investigation, sections were cutwith a Reichert Ultracut E microtome, stained with crystal violet,and observed with a Jenaval light microscope. For transmissionelectron microscopy (TEM), thin sections were cut with a ReichertUltracut E microtome, stained with lead citrate and uranyl ace-tate, and observed with a JEOL 100SX transmission electronmicroscope. The morphology is described on parafrontal sectionsof rotifers from 20- and 35-day starved groups and comparedwith similar sections from the fed controls.

Confocal Laser Scanning Microscopy

Three specimens from each experimental group were fixed at48C overnight in 4% paraformaldehyde in 0.1 mol l21 phos-phate-buffered saline (PBS), pH 7.4. They were then rinsedrepeatedly in 0.1 mol l21 PBS and permeabilized for 2 h in PBT(0.1 mol l21 PBS with 0.2% Triton X-100). Samples were stainedwith 1 lmol l21 DAPI (4,6-diamidino-2-phenylindole; Sigma,Italy), rinsed in 0.1 mol l21 PBS, and mounted in 3% DABCO(Sigma, Italy). Specimens were observed with a confocal laserscanning microscope (CLSM, Leica TCS-SP2). Series of opticalsections were projected as a fluorescence maximum projectionfor reconstruction.

RESULTS

During the first days of starvation, rotifers laid1 or 2 eggs, but they terminated reproduction lateron, ceasing movements and contracting into a tun-shape morphology. Recovery of the bdelloids after20 and 35 days of starvation was 87 and 74%,respectively. At the end of starvation, none of the

starved rotifers contained eggs at any stage ofmaturation, whereas fed controls had eggs at dif-ferent maturation stages.

Light MicroscopyFed controls. When contracted, rotifers have a

characteristic tun shape (about 110 lm in lengthand 98 lm in width, n 5 3), being their head andfoot retracted into the trunk telescopically (Fig.1A–C). Either extremities show epidermal foldsthat in the frontal section appear as small digita-tions (Fig. 1A,B). Digestive glands, trochi, stomachsyncytium, intestine, nervous ganglia, retrocere-bral, and pedal glands are greatly compressed, butmaintain their histological characteristics and rec-ognizability. The largest organs are the pairedvitellaria and the stomach syncytium (Fig. 1B).

20-day starved. General appearance and orga-nization of these rotifers are similar to the fed con-trols, although their size is smaller (about 92 lmin length and 78 lm in width, n 5 3; Fig. 1D–F).The body cavity is still visible, although reduced,and the organs appear compressed and closelypacked together (Fig. 1E).

35-day starved. Body organization and generalanatomy are still recognizable (Fig. 1G–I). Thebody size is even more reduced (about 86 lm inlength and 73 lm in width, n 5 3). The reductionof body size is mostly attributable to the shrinkageof vitellaria and stomach syncytium (Fig. 1H).

Confocal Microscopy

All the observed rotifers possess �650 nuclei,and the major difference between starved and fedrotifers concerns the distance between nuclei thatare closer to each other in the starved specimens(Fig. 1C,F,I). Stained with DAPI, the eight nucleiof the vitellaria of fed and starved rotifers differremarkably. In fed animals they are mostlyeuchromatic, and heterochromatin is localized atthe nucleus periphery: the nuclear central regiondoes not fluoresce, probably in correspondencewith the nucleolar region (Fig. 1C). After DAPIstaining, the vitellaria nuclei of the starved roti-fers show scattered fluorescence, and the nucleolusis no longer recognizable (Fig. 1F,I), whereas theoocyte nuclei, visible in the germarium, are similarin both fed and starved rotifers (Fig. 1C,F,I).

Electron Transmission Microscopy

The major ultrastructural differences betweenstarved and fed rotifers concern stomach syncytiumand vitellarium, all other structures maintainingsimilar fine structure as in the fed controls.

Stomach SyncytiumFed controls. The lumen of the stomach is

narrow and elongated and is bordered by a

2 R. MAROTTA ET AL.

Journal of Morphology

‘‘terminal web’’ (about 0.2-lm thick) beneath theplasma membrane (Fig. 2A,B). The terminal webis pierced by numerous pores, the terminal webpores, small cylindrical diverticula that extendfrom the stomach lumen into the stomach cyto-plasm (Fig. 2A,B). Small particles, possibly foodremains, are visible both in the stomach lumenand in the terminal web pores (Fig. 2B). In thestomach cytoplasm, similar particles are containedinto digestive vesicles (diameter varying between80 nm and 1 lm), produced through phagocytosisof the plasma membrane lining the cytoplasmatic

surface of the terminal web pores (Fig. 2B). Thedigestive vesicles merge and form larger phagoso-mal vesicles, joining to primary lysosomes, recog-nizable as roundish small electron-dense granules(diameter 0.25–0.5 lm). Heterophagic vacuoles (di-ameter 2–5 lm) result after this process (Fig. 2A).Numerous lipid droplets (diameter 0.9–1.1 lm)are also present inside the stomach cytoplasm(Fig. 2A).

20-day starved. In these rotifers, the stomachlumen is narrower and no food particles are recog-nizable inside the terminal web pores (Fig. 2C,D).

Fig. 1. Macrotrachela quadricornifera: LM and CLSM of normally fed contracted (A–C), 20-day starved (D–F), and 35-daystarved (G–I) specimens. A: Whole mount of a normally fed animal at LM; B: sagittal section through a normally fed rotifer (modi-fied after Marotta et al., 2010); C: whole mount of a normally fed animal at CLSM after DAPI staining; D: whole mount of a 20-day starved animal at LM; E: sagittal section through a 20-day starved rotifer; F: whole mount of a 20-day starved animal atCLSM after DAPI staining; G: whole mount of a 35-day starved animal at LM; H: sagittal section through a 35-day starved rotifer;and I: whole mount of a 35-day starved animal at CLSM after DAPI staining. The arrows in the CLSM images point to the vitella-rium; the arrowheads point to the oocytes of the germarium. Scale bars: A–I, 25 lm.

STARVATION TOLERANCE IN A BDELLOID ROTIFER 3


Heterophagic vacuoles lack in the stomach cyto-plasm that instead contains several large lipidcontaining vesicles, probably lipophagosomes (2.3–3.5 lm in diameter; Fig. 2C). Small empty phago-somal vesicles (diameter ranging from 0.1 to 0.2

lm) are still evident in the stomach cytoplasm, to-gether with several large lysosomes (Fig. 2C,D).

35-day starved. In their stomach lumen andterminal web pores, no food particles are present.As in the rotifers starved for 20 days, the phagoso-

Fig. 2. Macrotrachela quadricornifera: TEM of the stomach syncytium of normally fed contracted (A, B), 20-day starved (C, D),and 35-day starved (E, F) specimens. A: General view of the elongated stomach lumen (asterisks) of normally fed rotifer: note thelarge heterophagic vacuoles (arrow), the lipid droplets (arrowheads), and the cytoplasm filled with digestive vesicles; B: details ofthe ciliated stomach lumen showing alimentary particles inside the terminal web pores (arrowheads) and numerous digestivevesicles inside the stomach cytoplasm (arrows); C: general view of the elongated stomach lumen (black asterisk) of a 20-day starvedrotifer: note several electron-dense lysosomes (arrowheads) and a single lipid granule (white asterisk); D: details of the ciliatedstomach lumen: any alimentary particles are visible inside the terminal web pores (arrowheads); E: general view of the stomachsyncytium of a 35-day starved rotifer: note the stomach lumen (asterisk), several large lipid with an inner electron transparentcore (arrowheads), and many mitochondria clumped together with electron-dense inclusions (arrows); and F: higher magnificationthrough three mitochondria with subspherical electron-dense inclusions (arrowhead) close to a partially digested lipid granule (as-terisk). The mitochondrial cristae are clearly visible inside the mitochondria (arrows). Scale bars: A, 1.5 lm; B, 0.5 lm; C, 1 lm; D,0.4 lm; E, 1.5 lm; F, 0.25 lm.

4 R. MAROTTA ET AL.


mal vesicles of the stomach cytoplasm are emptyand small (diameter of about 0.1 lm), and theheterophagic vacuoles are absent (Fig. 2E). The stom-ach syncytium contains several partially digestedlipid vesicles, probably lipophagolysosomes. Theycontain mono/multivesicular inclusions and multila-mellar bodies, and their inner core is partially empty(Fig. 2E,F). The mitochondria of the stomach cyto-plasm have peculiar electron-dense inclusions insidetheir matrix; these inclusions appear subspherical orpolyhedrical in shape, and their size ranges from 50to 85 nm (Fig. 2E,F).

VitellariumFed controls. The cytoplasm of the vitellarium

contains abundant endoplasmic reticulum, ribo-some-like granules (about 25 nm in diameter), andnumerous roundish electron-dense yolk granules(diameter 0.2–0.6 lm; Fig. 3A,B). The eight largenuclei of the vitellarium (about 4.5 lm in diame-ter) are mostly euchromatic and contain a largenucleolus, about 2.5 lm in diameter (Fig. 3A).

20-day starved. The vitellarium has the samegeneral organization as in the fed controls, withmitochondria, endoplasmic reticulum, and ribo-somes (Fig. 3C). The vitellarium cytoplasm con-tains many yolk granules that appear partiallydigested and differ in size. Some of them are com-pletely empty; others maintain a core filled withan electron-dense yolk (Fig. 3C,D).

35-day starved. In these rotifers, the cytoplasmcontains several mitochondria and a well-devel-oped endoplasmic reticulum; no yolk granules arevisible (Fig. 3E). The mitochondria are larger thanin the fed controls, irregular in shape, andarranged in cluster. In some mitochondria, thecristae are only partially discernible; other mito-chondria are completely degraded, maintainingonly their external membrane (Fig. 3F). Multila-mellar bodies are present inside empty vacuoles(Fig. 3G).

DISCUSSION

Two rotifer groups starved for 20 and 35 days,respectively, are considered here. The rotifersrecovered in high percentages if starved for 20days, not differently from previous results (87 vs.about 90%, Ricci and Perletti, 2006). The effect ofstarvation lasting 35 days was not investigatedpreviously: in this study, the recovery was ratherhigh, equal to 74%. Remarkably, 35 days corre-spond to the average life duration of a normallyfed M. quadricornifera. Not surprisingly, mortalityof the starved rotifers increases with starvationduration; nevertheless, 60 days of starvation werefound to be tolerated by about 10% of the rotifers(Ricci and Perletti, 2006). To avoid the risk ofinvestigating the structure of animals incapable of

recovery, we decided to set the long-starvationtreatment to 35 days to be confident that ourobservations concern viable animals, althoughstressed for the long starvation.

The comparison between the fed rotifers, usedas control reference, and the two starved groupsclearly evidences that body size decreases atincreasing starvation time: about 47% of body vol-ume is lost after 20-day starvation, and another10% is lost after 35-day starvation. The fact thatprolonged periods of starvation cause body sizereduction is not surprising (e.g., Bowen et al.,1976); nevertheless, the general anatomy of bothstarved rotifer groups is similar to that of the fedcontrols.

Two organs change size and structure and thusare the major responsible for body volume reduc-tion: stomach syncytium and vitellarium glands.Reasonably, no food particles are visible in thestomach lumen as well as in the terminal webpores of the starved animals; the absence of foodparticles and heterophagic vacuoles in the stomachsyncytium of either starved groups is consistentwith the arrest of any digestive process. Phagoso-mal vesicles and their merging with primary lyso-somes, present in the controls, are no longer visi-ble in any of the starved groups. Moreover, thereduction in the number and size of both lipiddroplets and yolk granules, respectively, in thestomach cytoplasm and in the vitellarium, togetherwith the changes in their fine structure observedduring starvation, clearly suggests that their con-tent is used by rotifers through a process ofautophagy (Scott et al., 2004). However, the lipiddroplets and yolk granule content cannot sustainsurvival endlessly, and rotifer recovery decreaseswith starvation duration (Ricci and Perletti, 2006),probably because energy reserves are exhausted.The observed mitochondria degradation in the 35-day starved rotifers may represent a further strat-egy to survive to starvation, extracting energythrough a process of selective removal of mitochon-dria, known as mitophagy (Tolkovsky, 2009). It isindeed well known that the starvation may inducemitophagy in yeast and mammals (Goldman et al.,2010).

Other animals, e.g., planarian platyhelminthesor tardigrades, are capable to survive starvationperiods by metabolizing lipid reserves (Bowenet al., 1976; Kristensen, 1982; Reuner et al., 2010).Planarian platyhelminthes are capable of autolysisof cells and tissues and perform autophagy to pro-mote their survival (Bowen et al., 1976). Tardi-grades, capable of dormancy, possess storage cellsthat decrease in size after starvation and desicca-tion, suggesting that they do release energy tomaintain metabolism during dormancy (Reuneret al., 2010). Rotifers are incapable of regeneration(they are eutelic) and do not possess ‘‘storagecells.’’ They can mainly divert resources from other



uses, as occurs for the yolk granules of the vitella-rium.

Survival during starvation was suggested to besustained by the reduction of metabolic costs and

of energy investments (Ricci and Perletti, 2006).The major energy expense of rotifers consists inthe synthesis of egg reserves produced by the yolkgland, the vitellarium, because all the oocytes are

Fig. 3. Macrotrachela quadricornifera: TEM of the vitellarium of a normally fed contracted (A, B), 20-day starved (C, D), and35-day starved (E–G) specimens. A: View of the vitellarium of normally fed rotifer: note the characteristic euchromatic nucleus(white asterisk) and the numerous electron-dense lipid droplets inside the cytoplasm (arrowheads); B: high magnification of threeyolk granules of different diameters; C: view of the vitellarium of a 20-day starved rotifer: note the partially digested yolk granulesof different size (asterisks); D: high magnification of three yolk granules of different diameters; E: view of the vitellarium of a35-day starved rotifer: note the three large clustered mitochondria (arrowhead) and the multilamellar body (arrow); F: high magni-fication through a group of mitochondria at different degrees of degradation. In some mitochondria, the cristae are still visible(arrowheads); in others, the cristae are partially (double arrowhead) and completely (arrow) disappeared; and G: vacuole (arrow-head) with inside three multilamellar bodies (asterisk). Scale bars: A, 1.2 lm; B, 0.2 lm; C, 1.2 lm; D, 0.5 lm; E, 1.3 lm; F, 0.9lm; G, 0.9 lm.

6 R. MAROTTA ET AL.


already present at birth and undergo maturationbefore being released as eggs (Pagani et al., 1993).Thus, rotifers can save considerable resources ifthey reduce yolk production and egg laying andkeep maintenance costs at the minimum. This isactually what occurs to bdelloid rotifers that inter-rupt reproduction, arrest movements, and enterdormancy, saving energy expenses in response tostarvation (Ricci and Perletti, 2006). The arrest ofreproduction in favor of survival is also the strat-egy followed by other rotifer species (Kirk, 1997).Nevertheless, despite the apparent null cost of dor-mancy, some basal maintenance seems to beneeded in the starved bdelloids because lipid andprotein reserves present in the stomach and in thevitellaria disappear with increasing time of dor-mancy.

Although starvation produces progressive deple-tion of some structures, desiccation, that in thebdelloids induces anhydrobiosis, produces arrange-ments aimed to a prompt return to full functional-ity. Anhydrobiotic bdelloids seem to pack struc-tures to regain the complete functionality at rehy-dration, but do not seem to use any of theirstructures to sustain survival. Yolk granules per-sist in the vitellarium, and only structures thatare connected to extant metabolism, such as heter-ophagic vacuoles in the stomach syncytium ornucleoli in vitellarium nuclei, are not visible in theanhydrobiotic rotifers, unlike in the starved ones(Marotta et al., 2010). Thus, although apparentlyboth desiccation and starvation induce a similarform of dormancy in bdelloid rotifers (Ricci et al.,1987; Ricci and Perletti, 2006), the mechanismsunderlying this reversible life suspension appearto differ. During starvation, reserves present inspecific organs, namely stomach syncytium andvitellarium glands, are metabolized and disappear,although at a very low rate; during desiccationthese structures are ‘‘prepared’’ to be ready for fullfunctioning at rehydration. It is peculiar that therecovery curves of bdelloid species after desiccationand after starvation are very similar, but thismight be a mere coincidence, because the ultra-

structural changes of the bdelloids after eachstress differ, indicating that starvation and dessi-cation induce different strategies of dormancy.

ACKNOWLEDGMENTS

R. Marotta is grateful to M. Ferraguti who per-mitted time to be spent on this research.

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surviving starvation: changes accompanying starvation tolerance in a bdelloid rotifer

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