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Plant desiccation gene found in a nematode

Browne, John,Tunnacliffe, Alan,Burnell, Ann

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Anhyd obiosis Plan desicca ion gene ound in a nema ode When subjec ed o d ough condi ions, some o ganisms en e a s a e o suspended anima ion known as anhyd obiosis1, su i ing o inde ini e pe iods un il ehyd a ion allows hem o esume no mal me abolism. We ha e iden i- ied a gene in he anhyd obio ic nema ode Aphelenchus a enae ha is up egula ed in esponse o desicca ion s ess and whose encoded p o ein sha es sequence simila i y wi h a la e-emb yonic gene ha is induced in many plan s when hey a e dep i ed o wa e . This inding sugges s ha animals and plan s ha unde go anhyd obiosis may use common p o ec i e s a egies agains dehyd a ion, and p o ides a uni ying insigh in o he mechanism o anhyd obiosis. A cha ac e is ic ea u e o anhyd obio ic o ganisms is hei syn hesis o high concen- a ions o non- educing suga s du ing he induc ion o anhyd obiosis1. Fo example, A. a enae accumula es la ge amoun s o ehalose in esponse o dehyd a ion, and his co ela es wi h i s desicca ion ole - ance2. T ehalose p o ec s memb anes and p o eins om desicca ion damage by eplacing s uc u al wa e 1, and con ibu es o he o ma ion o an in acellula o ganic glass3which is hough o s abilize he cell’s con en s. In anhyd obio ic plan s, suc ose has a simila unc ion4. Howe e , se e al lines o e idence indi- ca e ha non- educing suga s alone a e no su icien o con e a s a e o anhyd obiosis, and ha u he adap a ions a e equi ed5,6. A class o p o eins known as LEA ( o ‘la e emb yogenesis abundan ’) p o eins accu- mula e in esponse o wa e de ici in many plan s, and hese a e pa icula ly abundan in anhyd obio ic plan s such as he esu - ec ion plan C a e os igma plan agineum, and in ma u ing seeds and pollen7. We he e o e in es iga ed whe he simila genes a e p esen in A. a enae. We ound ha se e al genes a e up egu- la ed in A. a enae nema odes unde going anhyd obiosis du ing exposu e o 90% ela- i e humidi y o 24 hou s. O pa icula in e es was a s ongly induced ansc ip wi h a leng h o abou 675 bases (Fig. 1a, b), which encodes a p edic ed p o ein o 143 esidues. The sequence o his p o ein indi- ca es ha i is a membe o he g oup-3 subclass o LEA p o eins8; i con ains a leas ou copies o a cha ac e is ic 11-me mo i , and u he echoes o his mo i a e p esen h oughou he sequence (Fig. 1c). The g oup-3 LEA mo i has been p o- posed o o m an amphipa hic a-helix ha di ec s he oligome iza ion o he p o ein9. These p o eins a e ex emely hyd ophilic and a e esis an o dena u a ion by hea — p omp ing sugges ions ha hey help o p e- en damage by wa e s ess, o example by ac ing as hyd a ion bu e , molecula chap- e one, ion sink o memb ane s abilize 1,9. Suc ose glasses a e s abilized in i o by in e ac ion wi h a pu i ied g oup-3 LEA p o ein om Typha la i olia pollen10. Non- educing suga s and LEA p o eins may he e o e ac syne gis ically4,10 o p omo e he o ma ion o a s able ‘bioglass’ in he cy oplasm o anhyd obio ic plan s and in desicca ion- ole an seeds and pollen — he bioglass may ap agile biological mol- ecules in ime and space, and p ese e hem om desicca ion damage. I he newly iden i ied LEA p o ein in A. a enae also s abilizes ehalose glasses in his way du ing desicca ion, he bioglass model o anhyd obiosis can be ex ended o include anhyd obio ic animals. Genomic11 and pa ial p o ein12 sequence in o ma ion indica es ha LEA p o eins may be used by o he nema odes as a de ence agains wa e s ess. The genomes o some mic oo ganisms also con ain sequences ha encode LEA-like p o eins (al hough exp es- sion o hese has no ye been demons a - ed11), including he desicca ion- ole an Deinococcus adiodu ans, which also encodes enzymes o he biosyn hesis o ehalose. A bioglass s a egy o anhyd obiosis could be widely used in biological sys ems and may ha e o igina ed in ancien cell ypes ha we e exposed o wa e s ess. John B owne*, Alan Tunnacli e†, Ann Bu nell* *Depa men o Biology and Ins i u e o Bioenginee ing and Ag oecology, Na ional Uni e si y o I eland Maynoo h, Coun y Kilda e, I eland e-mail: ann.bu [email protected] †Ins i u e o Bio echnology, Uni e si y o Camb idge, Tennis Cou Road, Camb idge CB2 1QT, UK 1. C owe, J. H., Hoeks a, F. A. & C owe, L. M. Annu. Re . Physiol. 54,579–599 (1992). 2. Madin, K. A. C. & C owe, J. H. J. Exp. Zool. 193, 335–346 (1975). 3. C owe, J. H., Ca pen e , J. F. & C owe, L. M. Annu. Re . Physiol. 60,73–103 (1998). 4. Sun, W. Q. & Leopold, A. C. Comp. Biochem. Physiol. 117A, 327–333 (1997). 5. Higa, L. M. & Wome sley, C. Z. J. Exp. Zool. 267,120–129 (1993). 6. Ga cía de Cas o, A. & Tunnacli e, A. FEBS Le . 487, 199–202 (2000). 7. Ing am, J. & Ba els, D. Annu. Re . Plan Physiol. Plan Mol. 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Compe ing inancial in e es s: decla ed none. b ie communica ions 38 NATURE | VOL 416 | 7 MARCH 2002 | www.na u e.com Figu e 1 Desicca ion induces exp ession o a p o ein in he nema ode Aphelenchus a enae ha is homologous wi h ano he emb yonic p o ein p oduced by a plan unde simila ci cums ances. a, Exp ession o he A. a enae la e-emb yonic gene Aa lea1 in esponse o desicca ion s ess, as e ealed by no he n blo ing using an Aa lea1 p obe: lane 1, con ol RNA om esh un ea ed nema odes; lane 2, RNA om nema odes exposed o 90% ela i e humidi y o 24 h. b, Same blo , bu his ime hyb idized wi h an 18S RNA p obe as a loading con ol. c, Local alignmen ( P 42 e 119) o a 121-amino-acid o e lap be ween he p edic ed sequences o Aa lea1 (GenBank accession numbe AF423069) and an emb yonic p o ein om he Eu opean whi e bi ch ( Be ula pendula ; accession numbe S39475). S39475 was he mos closely ela ed LEA-3 sequence o Aa lea1 ha we we e able o de ec in he GenBank da abase. The e a e a leas ou copies o he cha ac e is ic 11-me LEA-3 mo i (highligh ed). © 2002 Macmillan Magazines L d