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Review

What is the role and nature of programmed cell death in phytoplankton ecology?

, &
Pages 1-14 | Received 26 Aug 2005, Accepted 02 Dec 2005, Published online: 20 Feb 2007

References

  • Adamec , F , Kaftan , D and Nedbal , L . 2005 . Stress-induced filament fragmentation of Calothrix elenkinii (Cyanobacteria) is facilitated by death of high-fluorescence cells . J. Phycol. , 41 : 835 – 839 .
  • Agustí , S . 2004 . Viability and niche segregation of Prochlorococcus and Synechococcus cells across the Central Atlantic Ocean . Aquat. Microb. Ecol. , 36 : 53 – 59 .
  • Agustí , S , Satta , MP , Mura , MP and Benavent , E . 1998 . Dissolved esterase activity as a tracer of phytoplankton lysis: evidence of high phytoplankton lysis rates in the northwestern Mediterranean . Limnol. Oceanogr. , 43 : 1836 – 1849 .
  • Aldsworth , TG , Sharman , RL and Dodd , CER . 1999 . Bacterial suicide through stress . Cell. Mol. Life Sci. , 56 : 378 – 383 .
  • Ameisen , JC . 2002 . On the origin, evolution, and nature of programmed cell death: a timeline of four billion years . Cell Death Diff. , 9 : 367 – 393 .
  • Aravind , L , Dixit , VM and Koonin , EV . 2001 . Apoptotic molecular machinery: vastly increased complexity in vertebrates revealed by genome comparisons . Science , 291 : 1279 – 1284 .
  • Armbrust , JC , Berges , JA , Bowler , C , Green , BR , Martinez , D and Putnam , NH . 2004 . The genome of the diatom Thalassiosira pseudonana: ecology, evolution and metabolism . Science , 306 : 79 – 86 .
  • Arnoult , D , Tatischeff , I , Estaquier , J , Girard , M , Sureau , F , Tissier , JP , Grodet , A , Dellinger , M , Traincard , F , Kahn , A , Ameisen , J and Petit , PX . 2001 . On the evolutionary conservation of the cell death pathway: Mitochondrial release of an apoptosis-inducing factor during Dictyostelium discoideum cell death . Mol. Biol. Cell , 12 : 3016 – 3030 .
  • Baulcombe , D . 2002 . Viral supression of systemic silencing . Trends in Microbiol. , 10 : 306 – 308 .
  • Behrendt , H and Nixdorf , B . 1993 . The carbon balance of phytoplankton production and loss processes based on in situ measurements in a shallow lake . Int. Rev. Gesamt. Hydrobiol. , 78 : 439 – 458 .
  • Berges , JA and Falkowski , PG . 1998 . Physiological stress and cell death in marine phytoplankton: Induction of proteases in response to nitrogen or light limitation . Limnol. Oceanogr. , 43 : 129 – 135 .
  • Berman , T , Kaplan , B , Chava , S , Viner , Y , Sherr , BF and Sherr , EB . 2001 . Metabolically active bacteria in Lake Kinneret . Aquat. Microb. Ecol. , 23 : 213 – 224 .
  • Berman-Frank , I , Bidle , KD , Haramaty , L and Falkowski , PG . 2004 . The demise of the cyanobacterium, Trichodesmium spp., via an autocatalyzed cell death pathway . Limnol. Oceanogr. , 49 : 997 – 1005 .
  • Bidle , KD and Falkowski , PG . 2004 . Cell death in planktonic, photosynthetic microorganisms . Nature Rev. Microbiol. , 2 : 643 – 655 .
  • Bidle , KD , Haramaty , L and Falkowski , PG . Roads to ruin: the development and relationship of programmed cell death and viral infection in phytoplankton. ASLO conference presentation . June 2005 , Santiago, Spain.
  • Brussaard , CPD . 2004 . Viral control of phytoplankton populations – a review . J. Eukaryotic Microbiol. , 51 : 125 – 138 .
  • Brussaard , CPD and Riegman , R . 1998 . Influence of bacteria on phytoplankton cell mortality with phosphorus or nitrogen as the algal-growth-limiting nutrient . Aquat. Microbial Ecol. , 14 : 271 – 280 .
  • Brussaard , CPD , Riegman , R , Noordeloos , AAM , Cadee , GC , Witte , H , Kop , AJ , Nieuwland , G , van Duyl , FC and Bak , RPM . 1995 . Effects of grazing, sedimentation and phytoplankton cell lysis on the structure of a coastal pelagic food web . Mar. Ecol. Prog. Ser. , 123 : 259 – 271 .
  • Brussaard , CPD , Noordeloos , AAM and Riegman , R . 1997 . Autolysis kinetics of the marine diatom Ditylum brightwellii (Bacillariophyceae) under nitrogen and phosphorus limitation and starvation . J. Phycol , 33 : 980 – 997 .
  • Brussaard , CPD , Marie , D , Thyrhaug , R and Bratbak , G . 2001 . Flow cytometric analysis of phytoplankton viability following viral infection . Aquat. Microbial Ecol. , 26 : 157 – 166 .
  • Canter , HM . 1979 . Fungal and protozoan parasites and their importance in the ecology of the phytoplankton . Rep. Freshwat. Biol. Ass. , 47 : 43 – 50 .
  • Casotti , R , Mazza , S , Brunet , C , Vantrepotte , V , Ianora , A and Miralto , A . 2005 . Growth inhibition and toxicity of the diatom aldehyde 2-trans, 4-trans-decadienal on Thalassiosira weissfloggi (Bacillariophyceae) . J. Phycol. , 41 : 7 – 20 .
  • Cohen , GM . 1997 . Caspases: the executioners of apoptosis . Biochem. J. , 326 : 1 – 16 .
  • Cole , JJ . 1982 . Interactions between bacteria and algae in aquatic ecosystems . Annu. Rev. Ecol. Syst. , 13 : 291 – 314 .
  • Costas , E , Aguilera , A , Gonzalez-Gil , S and Lopez-Rodas , V . 1993 . Contact inhibition: also a control for cell proliferation in unicellular algae? . Biol. Bull. , 184 : 1 – 5 .
  • Coveney , MF , Cronberg , G , Enell , M , Larsson , K and Olofsson , L . 1977 . Phytoplankton, zooplankton and bacteria – standing crop and production relationships in a eutrophic lake . Oikos , 29 : 5 – 21 .
  • Crumpton , WG and Wetzel , RG . 1982 . Effects of differential growth and mortality in the seasonal succession of phytoplankton populations in Lawrence Lake, Michigan . Ecology , 63 : 1729 – 1739 .
  • Dunn , SR , Bythell , JC , Le Tissier , MDA , Burnett , WJ and Thomason , JC . 2002 . Programmed cell death and cell necrosis activity during hyperthermic stress-induced bleaching of the sea anemone Aiptasia sp . J. Exp. Mar. Biol. Ecol. , 272 : 29 – 53 .
  • Eloff , JN , Steinitz , Y and Shilo , M . 1976 . Photooxidation of cyanobacteria in natural conditions . Appl. Environ. Microbiol. , 31 : 119 – 126 .
  • Estep , KW and MacIntyre , F . 1989 . Taxonomy, life-cycle, distribution and dasmotrophy of Chrysochromulina – a theory accounting for scales, haptonema, muciferous bodies and toxicity . Mar. Ecol. Prog. Ser. , 57 : 11 – 21 .
  • Fasham , MJR , Ducklow , HW and McKelvie , DS . 1990 . A nitrogen-based model of plankton dynamics in the oceanic mixed layer . J. Mar. Res. , 48 : 591 – 639 .
  • Franklin , DJ and Berges , JA . 2004 . Mortality in cultures of the dinoflagellate Amphidinium carterae during culture senescence and darkness . Proc. R. Soc. Lond. B , 271 : 2099 – 2107 .
  • Frohlich , KU and Madeo , F . 2000 . Apoptosis in yeast – a monocellular organism exhibits altruistic behaviour . FEBS Letters , 473 : 6 – 9 .
  • Fogg , GE and Thake , B . 1987 . Algal Cultures and Phytoplankton Physiology , Wisconsin : University of Wisconsin Press .
  • Forsberg , BR . 1985 . The fate of planktonic primary production . Limnol. Oceanogr. , 30 : 807 – 819 .
  • Freudenthal , HD . 1962 . Symbiodinium gen. nov. and Symbiodinium microadriaticum sp. nov., a zooxanthella: Taxonomy, life cycle, and morphology . J. Protozool. , 9 : 45 – 52 .
  • Gallagher , JC . 1980 . Population genetics of Skeletonema costatum (Bacillariophyceae) in Narragansett Bay . J. Phycol. , 16 : 464 – 474 .
  • Geider , RJ , Delucia , EH , Falkowski , PG , Finzi , AC , Grime , JP , Grace , J , Kana , TM , La Roche , J , Long , SP , Osborne , BA , Platt , T , Prentice , IC , Raven , JA , Schlesinger , WH , Smetacek , V , Stuart , V , Sathyendranath , S , Thomas , RB , Vogelmann , TC , Williams , P and Woodward , FI . 2001 . Primary productivity of planet earth: biological determinants and physical constraints in terrestrial and aquatic habitats . Global Change Biology , 7 : 849 – 882 .
  • Gomez , MP , Harris , JB and Walne , PL . 1974 . Studies of Euglena gracilis in aging cultures. I. Light microscopy and cytochemistry . Br. Phycol. J. , 9 : 163 – 174 .
  • Goodnight , CJ and Stevens , L . 1997 . Experimental studies of group selection: what do they tell us about group selection in nature? . Am. Nat. , 150 : S59 – S79 .
  • Graslkraupp , B , Ruttkaynedecky , B , Koudelka , H , Bukowska , K , Bursch , W and Schultehermann , R . 1995 . In-situ detection of fragmented DNA (TUNEL assay) fails to discriminate among apoptosis, necrosis, and autolytic cell death – a cautionary note . Hepatology , 21 : 1465 – 1468 .
  • Hagen , G and Kochert , G . 1980 . Protein synthesis in a new system for the study of senescence . Exp. Cell Res. , 127 : 451 – 457 .
  • Heiskanen , AS . 1993 . Mass encystment and sinking of dinoflagellates during a spring bloom . Mar. Biol. , 116 : 161 – 167 .
  • Heiskanen , A and Kononen , K . 1994 . Sedimentation of vernal and late summer phytoplankton communities in the coastal Baltic sea . Arch. Hydrobiol. , 131 : 175 – 198 .
  • Holfeld , H . 1998 . Fungal infections of the phytoplankton: seasonality, minimal host density, and specificity in a mesotrophic lake . New Phytol. , 138 : 507 – 517 .
  • Horn , H and Horn , W . 2000 . Sedimentation: the main loss factor in waters dominated by diatoms. Results of long-term investigations . Int. Rev. Hydrobiol. , 85 : 191 – 208 .
  • Imai , I , Ishida , Y and Hata , Y . 1993 . Killing of marine phytoplankton by a gliding bacterium Cytophaga sp., isolated from the coastal Sea of Japan . Mar. Biol. , 116 : 527 – 532 .
  • Jabs , T , Dietrich , RA and Dangl , JL . 1996 . Initiation of runaway cell death in an Arabidopsis mutant by extracellular superoxide . Science , 273 : 1853 – 1856 .
  • Jassby , AD and Goldman , CR . 1974 . Loss rates from a lake phytoplankton community . Limnol. Oceanogr. , 19 : 618 – 627 .
  • Jerome , KR , Vallan , C and Jaggi , R . 2000 . The TUNEL assay in the diagnosis of graft-versus-host disease: caveats for interpretation . Pathology , 32 : 186 – 190 .
  • Jewson , DH , Rippey , BH and Gilmore , WK . 1981 . Loss rates from sedimentation, parasitism, and grazing during the growth, nutrient limitation, and dormancy of a diatom crop . Limnol. Oceanogr. , 26 : 1045 – 1056 .
  • Joint , I , Tait , K , Callow , ME , Callow , JA , Milton , D , Williams , P and Camara , M . 2002 . Cell-to cell communication across the prokaryote-eukaryote boundary . Science , 298 : 1207
  • Jones , AM . 2001 . Programmed cell death in development and defense . Plant Physiol. , 125 : 94 – 97 .
  • Kalff , J and Knoechel , R . 1978 . Phytoplankton and their dynamics in oligotrophic and eutrophic lakes . Annu. Rev. Ecol. Syst. , 9 : 475 – 495 .
  • Kanduc , D , Mittelman , A , Serpico , R , Sinigaglia , E , Sinha , AA , Natale , C , Santacroce , R , Di Corcia , MG , Lucchese , A , Dini , L , Pani , P , Santacroce , S , Simone , S , Bucci , R and Farber , E . 2002 . Cell death: apoptosis versus necrosis (review) . Int. J. Oncol. , 21 : 165 – 170 .
  • Kerr , JFR , Wyllie , AH and Currie , AR . 1972 . Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics . Br. J. Cancer , 26 : 239 – 257 .
  • Kirchman , DL . 1999 . Phytoplankton death in the sea . Nature , 398 : 293 – 294 .
  • Kirk , DL . 1998 . Volvox. Molecular-genetic Origins of Multicellularity and Cellular Differentiation , Cambridge : Cambridge University Press .
  • Kuhn , S . 1998 . Infection of Coscinodiscus spp. by the parasitoid nanoflagellate Pirsonia diadema: II. Selective infection behaviour for host species and individual host cells . J. Plankton Res. , 20 : 443 – 454 .
  • Labat-Moleur , F , Guillermet , C , Lorimier , P , Robert , C , Lantuejoul , S , Brambilla , E and Negoescu , A . 1998 . TUNEL apoptotic detection in tissue sections: critical evaluation and improvement . Histochem. Cytochem. , 46 : 327 – 334 .
  • Lam , E , Kato , N and Lawton , M . 2001 . Programmed cell death, mitochondria and the plant hypersensitive response . Nature , 411 : 848 – 853 .
  • Laun , P , Pichova , A , Madeo , F , Fuchs , J , Ellinger , A , Kohlwein , S , Dawes , I , Frohlich , KU and Breitenbach , M . 2001 . Aged mother cells of Saccharomyces cerevisiae show markers of oxidative stress and apoptosis . Mol. Microbiol. , 39 : 1166 – 1173 .
  • Lederman , L . 2004 . Apoptosis: one way to die . BioTechniques , 37 : 520 – 521 .
  • Lee , D and Rhee , G . 1999 . Circadian rhythm in growth and death of Anabaena flos-aquae (Cyanobacteria) . J. Phycol. , 35 : 694 – 699 .
  • Lee , N , Bertholet , S , Debrabant , A , Muller , J , Duncan , R and Nakhasi , HL . 2002 . Programmed cell death in the unicellular protozoan parasite Leishmania . Cell Death Diff. , 9 : 53 – 64 .
  • Lehman , JT and Sandgren , CD . 1985 . Species-specific rates of growth and grazing loss among freshwater algae . Limnol. Oceanogr. , 30 : 34 – 46 .
  • Leopold , AC . 1961 . Senescence in plant development . Science , 134 : 1727 – 1732 .
  • Lewis , K . 2000 . Programmed cell death in bacteria . Microbiol. Mol. Biol. Ann. Rev. , 64 : 503 – 514 .
  • Lindahl , O . 1983 . On the development of a Gyrodinium aureolum occurrence on the Swedish west coast in 1982 . Mar. Biol. , 77 : 143 – 150 .
  • Lowe , CD , Day , A , Kemp , SJ and Montagnes , DJS . 2005 . There are high levels of functional and genetic diversity in Oxyrrhis marina . J. Eukaryot. Microbiol. , 52 : 250 – 257 .
  • Madeo , F , Frohlich , E and Frohlich , K . 1997 . A yeast mutant showing diagnostic markers of early and late apoptosis . J. Cell Biol. , 139 : 729 – 734 .
  • Madeo , F , Frohlich , E , Ligr , M , Grey , M , Sigrist , SJ , Wolf , DH and Frohlich , KU . 1999 . Oxygen stress: A regulator of apoptosis in yeast . J. Cell Biol. , 145 : 757 – 767 .
  • Malmusi , M and Ackerman , AB . 1999 . “ A critical review of apoptosis in historical perspective ” . Philadelphia : Ardor scribendi .
  • Martin , SJ , Reutelingsperger , CPM , McGahon , AJ , Rader , JA , Van Schie , RCAA , LaFace , DM and Green , DR . 1995 . Early redistribution of plasma membrane phosphatidylserine is a general feature of apoptosis regardless of the initiating stimulus: inhibition by overexpression of Bcl-2 ande Abl . J. Exp. Med. , 182 : 1545 – 1556 .
  • Mason , CA , Hamer , G and Bryers , JD . 1986 . The death and lysis of microorganisms in environmental processes . FEMS Microbiol. Rev. , 39 : 373 – 401 .
  • Medlin , LK , Lange , M and Nothig , EM . 2000 . Genetic diversity in the marine phytoplankton: a review and a consideration of Antarctic phytoplankton . Antarctic Sci. , 12 : 325 – 333 .
  • Nedelcu , AM , Marcu , O and Michod , RE . 2004 . Sex as a response to oxidative stress: a twofold increase in cellular reactive oxygen species activates sex genes . Proc. R. Soc. Lond. B. , 271 : 1591 – 1596 .
  • Ning , SB , Guo , HL , Wang , L and Song , YC . 2002 . Salt stress induces programmed cell death in prokaryotic organism Anabaena . J. Appl. Microbiol. , 93 : 15 – 28 .
  • Noji , T , Passow , U and Smetacek , V . 1986 . Interaction between pelagial and benthal during autumn in Kiel Bight. I. Development and sedimentation of phytoplankton blooms . Ophelia , 26 : 333 – 349 .
  • Oleskin , AV , Botvinko , IV and Tsavkelova , EA . 2000 . Colonial organisation and intracellular communication in microorganisms . Mikrobiologiya , 69 : 249 – 265 .
  • Olie , RA , Durrieu , F , Cornillon , S , Loughran , G , Gross , J , Earnshaw , WC and Golstein , P . 1998 . Apparent caspase independence of programmed cell death in Dictyostelium . Curr. Biol. , 8 : 955 – 958 .
  • Patel , T , Arora , A and Gores , GJ . 1995 . A fluorometric assay for quantitating DNA strand breaks during apoptosis . Anal. Biochem. , 229 : 229 – 235 .
  • Pollingher , U . 1988 . “ Freshwater armored dinoflagellates: growth, reproduction strategies and population dynamics ” . In Growth and reproductive strategies of freshwater phytoplankton , Edited by: Sandgren , CD . Cambridge : Cambridge University Press .
  • Pommerville , JC and Kochert , GD . 1981 . Changes in somatic cell structure during senescence of Volvox carteri . Eur. J. Cell Biol. , 24 : 236 – 243 .
  • Prezelin , BB . 1982 . Effects of light intensity on aging of the dinoflagellate Gonyaulax polyedra . Mar. Biol. , 69 : 129 – 135 .
  • Raff , MC . 1992 . Social controls on cell survival and cell death . Nature , 356 : 397 – 400 .
  • Ratel , D , Boisseau , S , Nasser , V , Berger , F and Wion , D . 2001 . Programmed cell death or cell death programme? That is the question . J. Theor. Biol. , 208 : 385 – 386 .
  • Reddy , PM , Yumnam , DD and Imchen , TY . 1987 . Regulation of differentiation of multiple heterocysts in a blue-green alga, Anabaena variabilis . Arch. Hydrobiol. , 73 : 559 – 574 .
  • Reguera , B and Gonzalez-Gil , S . 2001 . Small cell and intermediate cell formation in species of Dinophysis (Dinophyceae, Dinophysiales) . J. Phycol. , 37 : 318 – 333 .
  • Reynolds , CS . 1984 . The Ecology of Freshwater Phytoplankton , Cambridge : Cambridge University Press .
  • Rynearson , TA and Armbrust , EV . 2005 . Maintenance of clonal diversity during a spring bloom of the centric diatom Ditylum brightwellii . Mol. Ecol. , 14 : 1631 – 1640 .
  • Sakamoto , T , Delgaizo , VB and Bryant , DA . 1998 . Growth on urea can trigger death and peroxidation of the cyanobacterium Synechococcus sp. strain PCC 7002 . Appl. Environ. Microbiol. , 64 : 2361 – 2366 .
  • Sanderson , BL and Frost , TM . 1996 . Regulation of dinoflagellate populations: Relative importance of grazing, resource limitation and recruitment from sediments . Can. J. Fish. Aquat. Sci. , 53 : 1409 – 1417 .
  • Scavia , D and Fahnenstiel , GL . 1987 . Dynamics of Lake Michigan phytoplankton: mechanisms controlling epilimnetic communities . J. Great Lakes Res. , 13 : 103 – 120 .
  • Segovia , M , Haramaty , L , Berges , JA and Falkowski , PG . 2003 . Cell death in the unicellular chlorophyte Dunaliella tertiolecta. A hypothesis on the evolution of apoptosis in higher plants and metazoans . Plant Physiol. , 132 : 1 – 7 .
  • Sheldrake , R . 1974 . The ageing, growth and death of cells . Nature , 250 : 381 – 385 .
  • Shrager , J , Chang , CW , Hauser , E , Harris , R , Tamse , R , Davies , J , Zhang , Z and Grossman , AR . 2003 . Chlamydomonas reinhardtii genome project: sequence analysis, assembly and annotation . Plant Physiol. , 131 : 401 – 408 .
  • Silva , ES and Faust , MA . 1995 . Small cells in the life history of dinoflagellates (Dinophyceae): a review . Phycologia , 34 : 396 – 408 .
  • Sloan Wilson , D . 1997 . Introduction: multilevel selection theory comes of age . Am. Nat. , 150 : S1 – S4 .
  • Sperandio , S , De Belle , I and Bredesen , DE . 2000 . An alternative, nonapoptotic form of programmed cell death . Proc. Natl. Acad. Sci. USA , 97 : 14376 – 14381 .
  • Steele , JH . 1974 . The Structure of Marine Ecosystems , Harvard : Harvard University Press .
  • Suginaka , K , Yamamoto , K , Ashida , H , Sawa , Y and Shibata , H . 1999 . Effect of intracellular glutathione on heat-induced cell death in the cyanobacterium, Synechocystis PCC 6803 . Biosci. Biotechnol. Biochem. , 63 : 1112 – 1115 .
  • Suttle , CA . 2005 . Viruses in the sea . Nature , 437 : 356 – 361 .
  • Tatischeff , I , Petit , PX , Grodet , A , Tissier , J , Duband-Groulet , I and Ameisen , J . 2001 . Inhibition of multicellular development switches cell death of Dictyostelium discoideum towards mammalian-like unicellular apoptosis . Eur. J. Cell Biol. , 80 : 428 – 441 .
  • Thornton , DCO . 2002 . Individuals, clones or groups? Phytoplankton behaviour and units of selection . Ethol. Ecol. Evol. , 14 : 165 – 173 .
  • Tilzer , MM . 1984 . Estimation of phytoplankton loss rates from daily photosynthetic rates and observed biomass changes in Lake Constance . J. Plankton Res. , 6 : 309 – 324 .
  • Toth , GB , Norén , F , Selander , E and Pavia , H . 2004 . Marine dinoflagellates show induced life-history shifts to escape parasite infection in response to water-borne signals . Proc. R. Soc. Lond. B , 271 : 733 – 738 .
  • Uchida , T , Yamaguchi , M , Matsuyama , Y and Honjo , T . 1995 . The red-tide dinoflagellate Heterocapsa sp. kills Gyrodinium instriatum by cell contact . Mar. Ecol. Prog. Ser. , 118 : 301 – 303 .
  • Uren , AG , O'Rourke , KO , Aravind , L , Pisabarro , MT , Seshagiri , S , Koonin , EV and Dixit , MV . 2000 . Identification of paracaspases and metacaspases: two ancient families of caspase-like proteins, one of which plays a key role in MALT lymphoma . Mol. Cell , 6 : 961 – 967 .
  • Usup , G and Azanza , RV . 1988 . “ Physiology and bloom dynamics of the tropical dinoflagellate Pyrodinium bahamense ” . In Physiological Ecology of Harmful Algal Blooms , Edited by: Anderson , DM , Cembella , AD and Hallegraeff , GM . 81 – 94 . Heidelberg : Springer Verlag .
  • Vardi , A , Berman-Frank , I , Rozenberg , T , Hadas , O , Kaplan , A and Levine , A . 1999 . Programmed cell death of the dinoflagellate Peridinium gatunense is mediated by CO2 limitation and oxidative stress . Curr. Biol. , 9 : 1061 – 1064 .
  • Vardi , A , Schatz , D , Beeri , K , Motro , U , Sukenik , A , Levine , A and Kaplan , A . 2002 . Dinoflagellate-cyanobacterium communication may determine the composition of phytoplankton assemblage in a mesotrophic lake . Curr. Biol. , 12 : 1767 – 1772 .
  • Vaux , DL and Korsmeyer , SJ . 1999 . Cell death in development . Cell , 96 : 245 – 254 .
  • Veldhuis , MJW , Kraay , GW and Timmermans , KR . 2001 . Cell death in phytoplankton: correlation between changes in membrane permeability, photosynthetic activity, pigmentation and growth . Eur. J. Phycol. , 36 : 167 – 177 .
  • Vonshak , A , Torzillo , G , Accolla , P and Tomaselli , L . 1996 . Light and oxygen stress in Spirulina platensis (cyanobacteria) grown outdoors in tubular reactors . Physiol. Plant. , 97 : 175 – 179 .
  • Walsh , JJ . 1983 . Death in the sea: Enigmatic phytoplankton losses . Prog. Oceanogr. , 12 : 1 – 86 .
  • Webb , JS , Thompson , LS , James , S , Charlton , T , Tolker-Nielsen , T , Koch , B , Givskov , M and Kjelleberg , S . 2003 . Cell death in Pseudomonas aeruginosa biofilm development . J. Bacteriol. , 185 : 4585 – 4592 .
  • Yoshida , Y . 1962 . Nuclear control of chloroplast activity in Elodea leaf cells . Protoplasma , 54 : 476 – 492 .
  • Zangger , H , Mottram , JC and Fasel , N . 2002 . Cell death in Leishmania induced by stress and differentiation: programmed cell death or necrosis? . Cell Death Diff. , 9 : 1126 – 1139 .

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