655

Plastid evolution: origins, diversity, trends

Susan E Douglas
The amazing diversity of extant photosynthetic eukaryotes is acclttiring plastids is ongoing ;ts evidenccrl I)! tcrtiar)
largely a result of the presence of formerly free-living cndos) nil,ioscs of chtorophytc. cryptophytc, hctcrokont
photosynthesizing organisms that have been sequestered by and Ilaptoph~tc :tlgac by tiillotl;t~:cllatcs [ 10.1 11.
eukaryotic hosts and established as plastids in a process Sttpcrimposcd on this asscmbl:tgc 3rc those organisms (most-
known as endosymbiosis. The evolutionary history of these ly parasitic) that ha\c apparcnrl) lost the capacity to
endosymbiotic events was traditionally investigated by studying photos! nrhcsi/.c ycr retain \ cstiijal I)N:i-containing ptastids
ultrastructural features and pigment characteristics but in (~tpi”“iiIllcsans, p:tr:tsitic pl;tints, colorless cryptonion;tds
recent years has been approached using molecular sequence 2nd ctt~lcnoicls).
data and gene trees. Two important developments, more
detailed studies of members of the Cyanobacteria (from which lntcrest in the c\,oltttion of pliotos!,nthctic cttkaryotcs \\.;ts
plastids ultimately derive) and the availability of complete first sp;trkcti 1)~ Schimpcr O\‘CI ;I ccntttr) 21~0 through
plastid genome sequences from a wide variety of plant and microscopic in\,csti gations of \3riotts protists [ 131. llis
algal lineages, have allowed a more accurate reconstruction of okr~3tions 2nd those of hlc1-cscl~ko~3k~ [ 1.31 lctl I0 the
plastid evolution. concept th:tt c\tant alfi;tc ;trosc I)? taking tip tlifferentl\
pijimcnted bacterial cndos) nihionrs. At‘ter la) iry dormant

Addresses for sc\,cral ~lccatlcs. this notion \\as rc\ itatizcd b\

Canadian Institute for Advanced Research Program in Evolutionary RI;tr,qtlis’s fornittlation of the cndos)mI~iont hylwthc-
Biology and Natlonal Research Council Institute for Marine sis [l-l]. Iittrasrructural. I~iochcniic3t. 3iid molccttlar
Biosciences, 141 1 Oxford Street, Hallfax, Nova Scotia, Canada B3H
ph? Iogcnctic stttdics ha\ c since been cmpto~cd to ttnra\~ct
321; e-mall: susan.douglas@nrc.ca
the c\~oltttionur~ histor!, of plastids and their hosts.
Current Opinion in Genetics & Development 1998, 8:655-661

t ~ltrastrttcttir~tl srttdics, p;~rticttl:trl~ of rhc mcnibr;tncs sttr-

rottndinfi lhc pl:tstid :tnd rhosc of tlic th\lakoids ha\c
c Current Biology Ltd ISSN 0959-437X been ttscd :ts the basis for c\oltttion;try scl;cnics [ 1.5.101.

Abbreviations ‘I’hosc plxrids sttrrottndcd II)- Ib.0 mcmbrancs

Cab chlorophyll a/b complex (rhodophytc, gl:tttcocystoph> Tc :tnd chloroph!-tc/iiicta-
FCP fucoxanthin chlorophyll a/c complex phyrc) ;trosc b)- prini:tr)- cndos~mbiosis. \\ hcrc;ts those
HLIP high-light-inducible protein
sttrrottndcd 1,~ three (cttglcnophyws 2nd sonic tlinotlagcl-
LHC light-harvesting complex
Pcb prochlorophyte chlorophyll a/b-bIndIng protein latcs) :tnd four mcmbrancs (haptophytcs, hctcrokonts,
crytoph)~tcs. chlorarachniol,h~tcs) ;trosc 1,) secondary
cnclos~nil~iosis 11 7,181. Similarly, the prcscncc of phyco-
Introduction t,iliprotcins and chlorophylls N, !, and J’ ha\c Ixen ttsed 3s
‘l’hc cnxI;t\.cnicnI of a l’hotos!-ntlictic prokar~otc II)- ;I prim- phytogcnctic niarkcrs [ 19.201. \\.ith cmcrgiiij: data thar
iti\ c cttk:tryotc and its con\.crsioti ro ;tti cncrg!-l,rodttcin:: indicate nittttiplc origins of cliffcrcnt pigments ~tnion;: the
org:ancllc (plastid) \\.;Is one of the kcv c\.olttrionarv c\‘cnIs pro~hloroph~rc grottps of cynolxtctcria ~21”,22~ and the
contril~tttin,~ I0 the biodi\~crsit~ of prcscn’-d;ty orfi;tnisnis. prcscncc of more 1h;tn one light-har\csting sbsrcm in ccr-
Although plastid-hcarin:: organisms sho\z~ iticrcdiblc \.arict> Uin cynolxtctcri:t [2.3] and plastitls [L-l]. tio\ve\ cr, it hits
in morphology, pigmentation and lift c)-clc. it no\v seems I~cconic cl-idcnt that pigment composition is not :t rctiahlc
certain that the) c;tn all 1~ traced to ;I single sttcccssful c\ oltttionar) indicator anion:: c\:tnol)~Wri:t Icr alone plas-
cntlos!tnl,iotic c\‘ent I,ct\vccn a c)anol~actcrittni-like tids. ‘I‘hcsc stttdics h:t\ c, noncrhclcss. pro\ idccl tts \Vith ;I
;tnccWtr :tnd ;I cttkar)otic ph:t~olroph (I;igttrc 1) [ 14,.5”]. Ixxtcr indication of the \orts of light-har\.cstinfi complc~-
Sttbsccjttcnt I0 this signific;tnt c~oltttionar~ inno\2tion. Iwo cs that ma! ha\,c Ixcn prcscn’ in the last coninion
m;tior lincacl;cs - rhodopli?rc and chloroph) rc/ ;tnccswr of pl:tstids.
mct:tphytc -:tppc:tr to h:t\c Ltriscrt. In addition. ;I smalt
grottp of algae kno\\,n :I\ glattcoc\.stoph~~cs, lhc plasticIs of :\lthottgh plastid gene scqt~~n~cs ha\c been ttscfttl in
which silill rct;tin die pcp~ido,~lvcaii w;tll of tlic cntiosvmbi- studying the relationships among cttharykc photosynrhet-
otic 3ncc‘scor, coniprisc ;I third linqqc [6**1, I.~ollowin;: the ic lincagcs, it mttst 1x2 rcmenilwcd thut Ihc\. rctlcct the
cstal,lishnicnt of thcsc three grottps of ;~lgac, scconcl:tr> histories of gcncs thcniscl\-cs and do not al~~tj \ accurawl~~
cndosvnil~iotic CI cnts Ixx\\ccn cttkatyotic lxtrIncrs rclxscnt the c\ottttion of lineages. Incongrttcnr rcsttlts
occttrrcd, rcsttlting in the continual acqttisition of phoro- h:t\ c Ixcn olxtincd bccattsc of the otxttrrcncc of lateral
ynthctic capabilit) \)) di\,crse cttkar~otic hosts [i-9]. gcnc transfers [75]. I~ttrtherniorc, mcthodolo~ic~tt prol~lcnis
Some of lhcsc c\cnIs ha\ c stnbiliscd in the formarion of rhc in algorirhms ttscd for ph>-logcnctic anal> scs hit\ c ) ictrlctl
cr\ lxophbws, cl~lor;trachniol,h) ccs. hctcrokonts, h:tpto- contlictin,q results did chc lack of c\wltttionary information
phytcs. cttglcnoids and dinotla~cll2ws bttt the process of contained within single gcncs h;~s pro\.cd I0 lx ;I constraint.
656 Genomes and evolution

Figure 1

Possible scenario for the ongin of extant

ertiaty endosymbioses Parasitism Loss of photosynthp
plastids by primary, secondary and tertiary
endosymbioses. Large coloured ovals
represent plastids and the width of the
surrounding line represents the number of
membranes (thick, two; thin, one; shaded,
Cryptomonads Haptophytes Apicomplexans Chlorarachniophytes peptidoglycan still present). Small coloured
Heterokonts Dinoflagellates Euglenoids circles represent nuclei (and nucleomorphs)
of eukaryotic hosts of different origins.
Pigments that have been documented In
plastids of the different lineages and in the
cyanobacteria (from which the common
ancestor is derived) are shown in italics.
Dotted arrows indicate that dinoflagellate
and apicomplexan plastids could have
arisen from either rhodophyte or
PI3
chlorophyte/metaphyte lineages.

Rhodophytes Chlorophytes Glaucocystophytes

g: @Am Eukaryotic host

Cyanobacterium
Current Opinion in Genetics & Development

‘The recent acquisition of complete plastid genome subject of excellent recent reviews [4,5”,40]. The ultimate
sequences from a number of green [Z--28] and non-green test of monophyly, however, rests with the determination
photosynthetic eukaryotes [29-321, as well as the cyanobac- of congruence of both host (nuclear and mitochondrial)
terium Syne&ocystir PCC6803 [33] allows comparisons of and endosymbiont (plastid) phylogenetic trees. As summa-
gene complement and order as a means of determining rized below, plastid trees provide moderate to good
relationships among plastids that are not affected by anom- support for monophyly, mitochondrial trees support the
alies in nucleotide sequence [34,35”,36’,37’]. In addition, sisterhood of rhodophytes and chlorophytes/metaphytes
phylogenetic analyses based on concatenated plastid gene (no glaucocystophyte data is available yet) and most
homologs from entire genomes offer sufficient evolutionary nuclear trees are as yet inconclusive on this matter.
information to identify distinct lineages [38”] and to more
accurately estimate divergence times [39’]. Although there are few examples where all three plastid-
bearing groups and eubacterial ancestors have been
A single origin of primary plastids? sampled extensively and phylogenetic reconstruction has
‘I’hree groups - rhodophytes, glaucocystophytes and been free of artefacts such as substitutional bias [41,42] or
chlorophytes/metaphytes -contain plastids that are the uneven rates of nucleotide substitutions [43], the majority
result of primary endosymbiosis of a prokaryotic rather of the data from plastid gene trees point to a single origin
than a eukaryotic ancestor. Support for a single origin of from within the cyanobacterial assemblage. Small subunit
these primary plastids is overwhelming and has been the rRNA has been well sampled from plastids and a wide
 Plastid evolution: origins, diversity, trends Douglas 657

spectrum of cyanobacteria and provides strong sup- gent nature of the rhodophyte RPBl sequence may, how-
port [6”,44’] whereas four other plastid genes (t~fA, ~fpB, ever, have obscured the true relationship between these
rpK1 and p&A) all provide moderate support (for details, two groups.
see [S”]). One plastid gene that has been extensively stud-
ied, J-M,, has been the object of gene duplications and In addition to gene trees. several other lines of evidence sup-
numerous lateral transfers between different groups of port the single origin of primary plastids. ‘I’he transit peptides
eubacteria as IveIl as bctwccn cubacteria and plastid ances- of the nuclear-encoded rhodophytc R-phycoerythrin [.5X]and
tors [ZS] and cannot be used to reconstruct the early history cyanellar ferredoxin-NADP+ oxidoreductase [SC)] genes can
of photosynthetic eukaryotes. GroEI, (chapcronin cpn60) both direct cytoptasmically sythesized polypeptides into pea
has also been used as an evolutionary marker [35) but suf- plastids, indicating that the import machineries of these
fers from the problem of paralogy. A rcccnt study has shown groups are homologous. Furthermore, the position of the sin-
that one of the two copies ofgluM present in the putative gle intron in the transit pcptides of nuclear-encoded plastid
cyanobacterial ancestor was retained in the ancestor of GAPDFI is in the same position in rhodophytes and land
rhodophyte and gtaucocystophyte plastids (groEL1) and plants. again indicating homology [.%I. Although there is no
lost from the chlorophyte/metaph);te lineage, whereas the data yet for gtaucoc)stophytes, the photosystem I light har-
other, gmEL2, was transferred to the nucleus (now catted lzsting complex proteins (LHCPs) of red and green algae
CON) in the ancestor of att three primary plastids and dupli- ha\-c been shown to be immunologically related to each other
cated in the chtoroph~te/metaI~hytc lincagc, generating but not to those of cyanobactcria [60], indicating that they
qncc and (plop [#I’]. arose in the common ancestor of these two groups after acclui-
sition of the cyanobacterial endosymbiont. Likewise. the
Although mitochondrial data is missing for glaucoqsto- prescncc of gene clusters - such as ~tpA/rp.s2/q~
phytes, single anal?;ses of Coxl [47] and Cox3 [Ml, and the and p.~l/Bi\~H - in plastids of all three groups that arc absent
combined analysis of four concatenated mitochondrial pro- in qanobacteria, again indicate that these clusters were crcat-
teins (Coxl-3 and Cob) [W’] support the sisterhood of ed in the common ancestor of these groups after
rhodophytes and chtorophytes/metaphytcs. ‘I’hrough the endosymbiosis [2,3]. ‘I’he similarities in gent content of plas-
acquisition of whole mitochondrial genome sequences of tid genomes from the three groups despite their extreme
other protists (and particularly a glaucocystophyte) by such reduction from a cyanobacterial gcnome after endosymbiosis
groups as the Organelle Genome Ylegasequencing arc unlikely to be caused by convergence and thus also favour
Program [SO”] we should gain further insight into the ori- a single primary origin [61].
gin of primary plastids.
Multiple secondary endosymbioses
Of the nine different nuclear genes - 3’ rRNAs, p-tubulin, As shown in Figure 2, at lcast seven groups appear to have
triosephosphate isomerase. elongation factor 1-a. RNA derived their plastids by secondary endosymbiosis (for
polymerase II large subunit, glyceraldehyde-3-phosphate review, see [So*]). Cryptomonads and chlorarachniophytcs
dehydrogenase and actin -that have been used for phylo- still retain a \,estigc of the nucleus of their eukaryotic
genetic reconstruction, the only trees that include endosymbionts as a nucleomorph and the origins of their
glaucocystophytes are those based on SSIT rRNA and actin. endosymbionts are from the rhodophyte and chlorophyte
SSLr rRNA trees consistently place rhodophytes, glauco- lineages, respecti\.ely [53”]. Heterokonts and haptophytes
cystophytes and chlorophytes/metaphytes with the ‘crown’ do not contain nuctcomorphs but their affiliations with
taxa l.511, an d although rhodophytcs and rhodophytes and crypytophytes in plastid gene-derived
chlorophytes/metaphytes rarely form sister groups, a weak trees indicates that their plastids are of rhodophyte origin.
grouping of rhodophytes and gtaucocystophytes is Eugtenophytes contain green-pigmented plastids and cur-
seen [6”,52,53”]. Actin trees, however, support the clus- rent evidence favours the view that this group was derived
tering of rhodophytes and chtorophytes/metaphytes and, in from a close relative of the kinetoplastid lineage that
some cases, rhodophytes, glaucocystophytes and chloro- engulfed a chlorophyte. The host partners of both dinofla-
phytes/metaphytes [6”,51’]. Glyceraldehyde-3-phosphate geltates and apicomplexans are sister groups within the
dehydrogenase (GAPDH) trees weakly support the sister early diverging alveotate group [62] and their plastids may
relationship of rhodophytes and chlorophytes/meta- be of common origin [63] but as dinoflagellates appear to
phytes [55,56]. Results from the other six molecules are have gained plastids numerous times [64] and there are
plagued by such problems as insufficient sampling of taxa, scant data from dinoflagellate plastid genomcs, the relat-
insufficient numbers of phylogenetically informative char- cdness of the endosymbionts remains unknown.
acters, paratogy, gene duplication, high sequence Phylogenetic analysis of tuf; from the 35 kb circle of three
divergence or the use of methods that do not correct for apicomplexans positions them with the chlorophyte/meta-
rapidly evolving sequences (for details, see [S”]). The phyte lineage although with low bootstrap support [6S’].
only study that rejects the sister relationship of On the other hand, the presence of ORFq70 (~~$24) and
rhodophytes and chtorophytes/metaphytes is one based on C/PC: (two genes found in plastids of rhodophytc ancestry)
RNA polymerase II large subunit (RPBl) sequences [57’]. on the 35 kb circle of Apicomptexa [66”] argues for a
Very weak taxonomic sampling and the extremely di\,er- rhodophyte endosymbiont [67].
6513 Genomes and evolution

Figure 2

Chlorarachniophytes
a (NM) (5)*

Chlorobionts

-, 93 Haptophytes (6)’
100
--.._J Chlorarachniophytes (5)’
I Euglyphlna (2)

Heterokont algae (321*

Dinogflagellates (7)’

Cryptomonads (6)‘

Acanthamoeba (31
--T-_:::bCryptomonads (NM)*
------- 1 Red algae (49)

I””
--I Choanoflagellates (2)
Complete genomes
Of rl1c -3000 fi”‘l”S cncodcd on rhc gcnon1c of lllC
c~anol)~ictcriiim ~y1’//~l/r//c~‘.s/i,..~ I’(XXXO3 [.33]. onl! l OO-ZOO
Radlata (1 1) ;irc found on p’lastid gcnonics, indicaring That ;I iii:rs\i\ c
Zygomycetes (9) Ions of gcncs (xxiii-reel foll01\ iii:: cndo\! nil,iosis ;iiicl
csC;ihlishnicnt of rhc pl:isrid. Sonic of thcsc g:cnc\ wci-c
transferrctl lo the n~iclciis, of which tlicrc ;irc 4-l docir-
Basldomycetes (38) mcntcd cwniplcs [3X”] - \I hcrcls rcdund:int gcncs
\vcrc losr oiirright. Ikspitc this cnornioiis loss. rod:i! ‘5
rli\u-sc plastic! gcnonicc ha\ c :irri\,ctl at :in incrcdil>l\
Ascomycetes (8 1) similar gcnc set. ;I phcnonicnon inwrprctcd ;is supporr ot
3 nionophylctic origin of priniur! plasticls (01 1. ‘I’llc
dctailcd tr;icking of ficnc contcnT from nine piiblishcd
plastic1 gcnonics clcgkintlv cicnionstr3ws p:iucrn\ in gcnc
Phylogenetic tree of major eukaryotic groups belonging to the crown loss as \VCll LIS IlO\\ the gcnc di\trihution seen iii c\uiiT
taxa (redrawn from van de Peer and de Wachter [53*-l; see original
oi-ganisnis cotild dcri\c from chc \iliglc cndos~nil~iosis of
paper for methodological details). The groups containing plastids of
secondary origin (chlorarachniophytes, haptophytes, heterokonts,
;I c~~inob~ictcriiim-lihc anccslor I.38”]. (:oni~~Lltation ot
dinoflagellates, apicomplexans and cryptophytes) are mdlcated in rhc ratio of g:cnomc rc;iI-r;liigciiiciits bct\\ccn pairs 01‘
boldface with asterisks. Euglenolds are derived from an early branching plasrid gcnonics al1o\\s an xciir;iTc nicisurc of flit ph\-
group related to kinetoplastids and are not included in the crown. The ;ilthoiigli not of tlic niorc
lofi~ii) ot‘ land plant plasticis,
nucleomorphs (NM) of chlorarachnlophytes (derived from chlorophytes)
disrantly rclatcd plastids [;;b*].
are clearly dlstinguished from those of cryptomonads (derived from
rhodophytes). The number of sequences compnslng each cluster is
shown m parenthesis after the taxon name and the bootstrap values on ‘l’hc analysis of plastici hwnc clristcrs. pi-cicirl:irl\ I:irgc
the Imes. The scale bar indicates evolutjonary distance. ones like the rih)sonial protein opcrons. h;i\,c pro\ ccl Iisc-
furl for tracing pl:isrid relationships [.37’.7?‘.7.3]. ‘I‘lIcsc
Pigments and the nature of the common stiidics all confirm the c~;inoI~;ic~cri;il origin ofpl:istids and
ancestor the divcrjicncc in10 t-hrcc I>riniar) linc;ig;cs disclrsscd
I’lastids cc,ntain a di\.crsity of pigments :lnd light-har\,csting kiho\,c (l:igurc 1). ‘I’hc accluisition of coniplctc pla\rid
coniple~cs (I .!I( k) and tu 0 scenarios can bc cn\ is:igcd for gcnonics, howxcr. has rakcn this type of an:il>sis :I \tcp
such ;I distrib&)n. ‘I’hc common anccsfor ot‘ plastids corU furrhcr. l;or instance. cornprison of the order of plastic1
Ii;ivc contained ;I ntlnil,cr ofdiffcrcnt photopigments and asso- gcncs from tlic rhodopliycc /‘o/p//y/u p///;/)//w// anal rhc
ciatcd lighr-har\cstin :: systems t,ut only one t)pe ~;is rctaincd cr);ptonion;icl (;~~i//u/~h thlcT0 shops iinniistakal~ly that tlic
in each lincagc Acr endos~nil~iosis [G-4]. :iltcrnari\cl>, nc\\ latrcr orifiin:itcd t,!, cndos~nil~iosis of ;I ctikar! 0Tc \ cr>
 Plastid evolution: origins, diversity, trends Douglas 659

Figure 3 Warts and land plants), the branching order reflects the fos-
sil record. This latter result is confirmed by a larger dataset
psbB/rmA of 58 concatenated homologous protein sequences from
five land plants [39’], which additionally provides revised
molecular estimates for the divergence times of the major
land plant groups.

Conclusions
psaB/A
New information gleaned from analyses of complete plastid
(63%)

rpsl4
genomes has built on previous ultrastructural, biochemical
(99%) and molecular studies and has refined our views on plastid
evolution. il’hereas results from a number of studies have
converged on the consensus that plastids arose by a single
primary endosymbiosis of a eubacterium from within the
atplrpol
cyanobacterial radiation, recent rcvelacions of hitherto
(63%) underestimated diversity in this group leaves room for
future modifications of this concept. Continued study of this
psbJLFE (45%) fascinating group of photosynthetic bacteria combined with
ycf4/7 (96%)
in-depth studies of the secrets held by plastid genomes of
both primary and secondary origins \vill further clarify the
details of this landmark e\x)lutionary exnt and provide
Plastid gene clusters conserved between the rhodophyte Porphyra insights into patterns of organelle genomc evolution.
purpurea and the cryptophyte Giullardia theta. Gene clusters that are
colinear between the two plastids are shaded. Regions that are
unshaded contain G. theta genes rearranged in order compared to
Acknowledgements
/? purpurea. Numbers represent the proportion (%) of the F! purpurea
cluster remaining in the G. theta cluster. Arrows indicate the position
and transcriptional orientation of the rRNA cistrons.

References and recommended reading

Papers of particular interest, published within the annual penod of review,
have been highlighted as:
much like the former [32]. As shown in Figure 3, three
very long segments (two of -30 kb and one of 17 kb) of the l of special interest
**of outstanding interest
cryptomonad plastid genome are colinear, albeit reduced
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Interestingly, the junctions of many of the conserlzd syn- 2. Douglas SE: Chloroplast origins and evolution. In The n/lolecu/ar
ten? groups contain tRYAs, indicating that these genes Biology of Cyanobacteria. Edited by Bryant DA. Amsterdam: Kluwer
Academic Publishers; 1994:91-l 18.
ma): provide sites for recombination. Two segments
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plastids. Annu Rev Want Physiol Plant MO/ B/o/ 1995, 46:549-575.
regions of the rRNA genes suggest that the directly repeat-
4. Gray MW, Spencer DF: Organellar evolution. In Evoluf~on of
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transformed into the inverted repeat commonly seen in Collins MA. Cambridge: Cambridge University Press; 1996:109-l 26.
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.. secondary endosymbiosis. In Or/g/ns of Algae and The/r flasbds.
Edited by Bhattacharya D. Vienna, New York: Springer-Verlag;
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gins from both sequence-based phylogenles and other plastld traits such as
concatenated plastid genes for phylogenetic inference, sim- ultrastructure and pigmentation. Processes such as lateral gene transfers,
ilar to the study published on mitochondrial relationships gene duplications, gene loss and gene relocations that have Impacted on
our understanding of plastid evolution are clearly documented.
[49”]. By constructing an alignment of 45 proteins common
to all nine published plastid sequences as well as the 6. Bhattacharya D, Schmidt HA: Division Glaucocystophyta. In Origins
.. of Algae and Their Rasbds. Edited by Bhattacharya D. Vienna,
cyanobacterium ,~~~e~~oc~~.~isPCC6803, and using a variety New York: Springer-Verlag; 1997:139-l 48.
of phylogenetic methods, Alartin and coworkers [38”] have The unravelllng of the evolutionary history of this small entgmatlc group of
algae through sequence analysis of nuclear- and cyanelle-encoded genes IS
obtained a single tree upheld with high bootstrap support clearly presented in this review. The work described supports the position of
that strongly endorses the single origin of plastids from a glaucocystophytes as one of the three lineages of pnmary plastids.

cyanobacterium-like ancestor. Furthermore, three previ- 7. Douglas SE, Murphy CA, Spencer DF, Gray MW: Molecular
evidence that cryptomonad algae are evolutionary chimaeras of
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of an engulfed eukaryotic alga. froc Nat/ Acad Sci USA 1994,
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J Plankton Res 1981, 3:389-401. analysis of the genome of the unicellular cyanobacterium
Synechocystis sp. strain PCC6803. II. Sequence determination of
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