Chloroplast Genome Chloroplast Genome EvolutionEvolution

Level 3 Molecular Evolution and Level 3 Molecular Evolution and BioinformaticsBioinformatics

Jim ProvanJim Provan

ReferencesReferences

Douglas SE (1998) “Plastid evolution: origins, Douglas SE (1998) “Plastid evolution: origins, diversity, trends” diversity, trends” Current Opinion in Genetics Current Opinion in Genetics and Development and Development 88: 655-661: 655-661

Sugiura M (1995) “The chloroplast genome” Sugiura M (1995) “The chloroplast genome” Essays in Biochemistry Essays in Biochemistry 3030: 49-57: 49-57

Gray MW (1993) “Origin and evolution of Gray MW (1993) “Origin and evolution of organelle genomes” organelle genomes” Current Opinion in Current Opinion in Genetics and Development Genetics and Development 33: 884-890: 884-890

The chloroplastThe chloroplast

Carries out Carries out photosynthesisphotosynthesisContains own genomeContains own genomeBelieved to be of Believed to be of endosymbiotic originendosymbiotic originPhylogenetically related Phylogenetically related to cyanobacteriato cyanobacteria

Algal lineagesAlgal lineages

RhodophytesRhodophytes ChlorophytesChlorophytes GlaucocystophytesGlaucocystophytes

CryptophytesCryptophytes

HeterokontsHeterokonts

HaptophytesHaptophytes

DinoflagellatesDinoflagellates

ApicomplexansApicomplexans

EuglenoidsEuglenoids

ChlorarachniophytesChlorarachniophytes

PrimaryPrimary(Double (Double membrane)membrane)

SecondarySecondary(Three or more (Three or more membranes)membranes)

Monophyly of primary plastids - Monophyly of primary plastids - chloroplast evidencechloroplast evidence

Phylogeny of SSU Phylogeny of SSU rRNA based on good rRNA based on good sample of both sample of both cyanobacteria and cyanobacteria and plastidsplastids

Also supported by:Also supported by:tuftufAA

atpBatpB

rporpoC1C1

psbpsbAA

OdontellaOdontellaPylaiellaPylaiella

GuillardiaGuillardiaEmilianiaEmiliania

PorphyraPorphyraMarchantiaMarchantia

KlebsormidiumKlebsormidiumChlorellaChlorella

CyanophoraCyanophoraGlaucocystisGlaucocystis

100100

Pseudanabaena PCC 7409Pseudanabaena PCC 7409Pseudanabaena PCC 6903Pseudanabaena PCC 6903PhormidiumPhormidium

Pseudanabaena PCC 7367Pseudanabaena PCC 7367

SSU rRNASSU rRNA

Monophyly of primary plastids - Monophyly of primary plastids - mitochondrial and nuclear mitochondrial and nuclear

evidenceevidence

Tree based on five Tree based on five mitochondrial genes mitochondrial genes shows strong support shows strong support for monophylyfor monophylyNuclear genes:Nuclear genes:

-tubulin - inconclusive-tubulin - inconclusiverRNAs - poorly resolvedrRNAs - poorly resolvedRPB1 - rejectsRPB1 - rejectsTPI / EF-1TPI / EF-1 - weak - weak supportsupportGAPDH / actin - better GAPDH / actin - better supportsupport

CyanidioschyzonCyanidioschyzon

CyanidiumCyanidium

GracilariopsisGracilariopsis

ChondrusChondrus

PorphyraPorphyra

TriticumTriticum

MarchantiaMarchantia

ProtothecaPrototheca

Tetraselmis m.Tetraselmis m.

Tetraselmis s.Tetraselmis s.

98%98%

Secondary plastidsSecondary plastids

Plastid SSU rDNA tree Plastid SSU rDNA tree shows that euglenophytes shows that euglenophytes and chloroarachiophytes and chloroarachiophytes associate with green associate with green algae and that algae and that heterokonts, cryptophytes heterokonts, cryptophytes and haptophytes and haptophytes associate with red algaeassociate with red algaeStudies on nucleomorphs Studies on nucleomorphs also confirm ancestry of also confirm ancestry of cryptophytes and cryptophytes and chloroarachniophyteschloroarachniophytes

Glaucocystis nostochinearumGlaucocystis nostochinearumCyanophora paradoxaCyanophora paradoxaCyanophora paradoxaCyanophora paradoxa

Gloeochaete wittrockianaGloeochaete wittrockianaEuglena gracilisEuglena gracilis

Astasia longaAstasia longaChlorarachnion Chlorarachnion spp.spp.

Chlorarachnion Chlorarachnion spp.spp.Chlorarachnion reptansChlorarachnion reptans

Glycine maxGlycine maxZea maysZea mays

Marchantia polymorphaMarchantia polymorphaClosterium ehrenbergiiClosterium ehrenbergii

Chara Chara spp.spp.Chlorella ellipsoideaChlorella ellipsoidea

Chlorella vulgarisChlorella vulgarisSkeletonema costatumSkeletonema costatum

Pylaiella littoratisPylaiella littoratisHeterosigma akashiwoHeterosigma akashiwoCyanidium caldarumCyanidium caldarum

Galdiera sulphurariaGaldiera sulphurariaGuillardia thetaGuillardia thetaRhodomonas salinaRhodomonas salina

Ochrosphaera neapolitanaOchrosphaera neapolitanaEmiliana huxleyiEmiliana huxleyiPavlova Pavlova cf. cf. salinasalina

Porphyridium aerugineumPorphyridium aerugineumGlaucosphaera vacuolataGlaucosphaera vacuolata

Palmaria palmataPalmaria palmataAntithamnion Antithamnion sp.sp.Chondrus crispusChondrus crispus

The chloroplast genomeThe chloroplast genome

Sequenced chloroplast Sequenced chloroplast genomes range from genomes range from 70kb - 201kb70kb - 201kb

Variation in length Variation in length mainly due to presence mainly due to presence of inverted repeat (IR)of inverted repeat (IR)

Generally 100-250 Generally 100-250 genes:genes:

Gene expressionGene expression

PhotosynthesisPhotosynthesis

MetabolismMetabolism

The inverted repeat (IR)The inverted repeat (IR)

Ranges from 5bk to 76kb in Ranges from 5bk to 76kb in lengthlength

IR contains rRNA genes IR contains rRNA genes plus others:plus others:

None in brown algae (5kb)None in brown algae (5kb)

10 in tobacco (25kb)10 in tobacco (25kb)

40 in geranium (76kb)40 in geranium (76kb)

Present in:Present in:Land plants (exc. legumes)Land plants (exc. legumes)

ChlorophytesChlorophytes

ChromophytesChromophytes

Partial in conifersPartial in conifers

PinusPinus

NicotianaNicotiana

PorphyraPorphyra

Chloroplast genome evolutionChloroplast genome evolution

Rapid and massive Rapid and massive reduction in number of reduction in number of genes:genes:

Transferred to nucleusTransferred to nucleusLostLost

80-90% of plastid 80-90% of plastid proteins are encoded in proteins are encoded in nucleusnucleusGreat overlap in gene Great overlap in gene content suggests that content suggests that last common ancestor of last common ancestor of cpDNA had ~300 genescpDNA had ~300 genes

SynechocystisSynechocystis3573 kbp3573 kbp

~3000 genes~3000 genes

PorphyraPorphyra chloroplast chloroplast201 kbp201 kbp

~250 genes~250 genes

Gene loss in chloroplast Gene loss in chloroplast evolutionevolution

45 genes present in all 45 genes present in all genomesgenomes

Unique losses (68) Unique losses (68) outnumbered by outnumbered by parallel losses (122)parallel losses (122)

Confirms that ancestral Confirms that ancestral plastid genome was plastid genome was already highly reduced already highly reduced from that of from that of cyanobacteriacyanobacteria

Zea Zea (75)(75)

Oryza Oryza (75)(75)

NicotianaNicotiana (76) (76)

Pinus Pinus (69)(69)

Marchantia Marchantia (84)(84)

Euglena Euglena (58)(58)

PorphyraPorphyra (200) (200)

Odontella Odontella (124)(124)

Cyanophora Cyanophora (136)(136)

1 (0)1 (0)

5 (2)5 (2)

12 (0)12 (0)

4 (0)4 (0)

1 (0)1 (0)

7 (5)7 (5)

34 (9)34 (9)

129 (34)129 (34)

20 (1)20 (1)

1 (0)1 (0)

77 (0)77 (0)

99 (3)99 (3)

AncestralAncestralplastidplastid((235)235)

14 (14)14 (14)

Chloroplast gene contentChloroplast gene content

Group 1

Gene expressionPhotosynthesis

Metabolism

Rhodophytes s. l.Glaucocystophytes

Group 1

Gene expressionPhotosynthesis

Metabolism

Rhodophytes s. l.Glaucocystophytes

Group 2

Gene expressionPhotosynthesis

Metabolism

Chlorophytes s. l

Group 2

Gene expressionPhotosynthesis

Metabolism

Chlorophytes s. l

Group 4

Gene expressionPhotosynthesis

Metabolism

Yet to be discovered(cf. Hydrogenosomes in mitochondria)

Group 4

Gene expressionPhotosynthesis

Metabolism

Yet to be discovered(cf. Hydrogenosomes in mitochondria)

Group 3

Gene expressionPhotosynthesis

Metabolism

Non-photosynthtic Chlorophytes(e.g. Epifagus) and apicomplexans

Group 3

Gene expressionPhotosynthesis

Metabolism

Non-photosynthtic Chlorophytes(e.g. Epifagus) and apicomplexans

Chloroplast genes (excluding Chloroplast genes (excluding ycfycf))

TotalTotal

Gene expressionGene expression rRNArRNA tRNAtRNA r-proteinr-protein OtherOther

PhotosynthesisPhotosynthesis RuBisCo/thylakoidRuBisCo/thylakoid ndhndh

Metabolism/misc.Metabolism/misc.

IntronsIntrons

Land PlantsLand Plants AlgaeAlgae

Photosyn.Photosyn. EpifagusEpifagus EuglenaEuglena OthersOthers PorphyraPorphyra

101-107101-107

4430-3230-322-212-215-65-6

29-3029-301111

1-51-5

18-2118-21

4040

441717151522

----

22

66

8282

332727212144

2626--

11

149+149+

113-166113-166

3328-3628-362121-44-44

66-9-9

3131-48-48-/-/1010

77-14-14

-/1/3-/1/3

181181

33353547471818

5353--

2525

--