Chloroplast genome evolution
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Chloroplast Genome Evolution. Level 3 Molecular Evolution and Bioinformatics Jim Provan. References. Douglas SE (1998) “Plastid evolution: origins, diversity, trends” Current Opinion in Genetics and Development 8 : 655-661

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Chloroplast Genome Evolution

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Chloroplast genome evolution

Chloroplast Genome Evolution

Level 3 Molecular Evolution and Bioinformatics

Jim Provan


References

References

Douglas SE (1998) “Plastid evolution: origins, diversity, trends” Current Opinion in Genetics and Development 8: 655-661

Sugiura M (1995) “The chloroplast genome” Essays in Biochemistry 30: 49-57

Gray MW (1993) “Origin and evolution of organelle genomes” Current Opinion in Genetics and Development 3: 884-890


The chloroplast

The chloroplast

  • Carries out photosynthesis

  • Contains own genome

  • Believed to be of endosymbiotic origin

  • Phylogenetically related to cyanobacteria


Algal lineages

Rhodophytes

Chlorophytes

Glaucocystophytes

Algal lineages

Primary

(Double membrane)

Secondary

(Three or more membranes)

Cryptophytes

Heterokonts

Haptophytes

Dinoflagellates

Apicomplexans

Euglenoids

Chlorarachniophytes


Monophyly of primary plastids chloroplast evidence

Odontella

Pylaiella

Guillardia

Emiliania

Porphyra

Marchantia

Klebsormidium

100

Chlorella

Cyanophora

Glaucocystis

Pseudanabaena PCC 7409

Pseudanabaena PCC 6903

Phormidium

Pseudanabaena PCC 7367

SSU rRNA

Monophyly of primary plastids - chloroplast evidence

  • Phylogeny of SSU rRNA based on good sample of both cyanobacteria and plastids

  • Also supported by:

    • tufA

    • atpB

    • rpoC1

    • psbA


Monophyly of primary plastids mitochondrial and nuclear evidence

Cyanidioschyzon

Cyanidium

Gracilariopsis

Chondrus

98%

Porphyra

Triticum

Marchantia

Prototheca

Tetraselmis m.

Tetraselmis s.

Monophyly of primary plastids - mitochondrial and nuclear evidence

  • Tree based on five mitochondrial genes shows strong support for monophyly

  • Nuclear genes:

    • -tubulin - inconclusive

    • rRNAs - poorly resolved

    • RPB1 - rejects

    • TPI / EF-1 - weak support

    • GAPDH / actin - better support


Secondary plastids

Glaucocystis nostochinearum

Cyanophora paradoxa

Cyanophora paradoxa

Gloeochaete wittrockiana

Euglena gracilis

Astasia longa

Chlorarachnion spp.

Chlorarachnion reptans

Chlorarachnion spp.

Glycine max

Zea mays

Marchantia polymorpha

Closterium ehrenbergii

Chara spp.

Chlorella ellipsoidea

Chlorella vulgaris

Skeletonema costatum

Pylaiella littoratis

Heterosigma akashiwo

Cyanidium caldarum

Galdiera sulphuraria

Guillardia theta

Rhodomonas salina

Ochrosphaera neapolitana

Emiliana huxleyi

Pavlova cf. salina

Porphyridium aerugineum

Glaucosphaera vacuolata

Palmaria palmata

Antithamnion sp.

Chondrus crispus

Secondary plastids

  • Plastid SSU rDNA tree shows that euglenophytes and chloroarachiophytes associate with green algae and that heterokonts, cryptophytes and haptophytes associate with red algae

  • Studies on nucleomorphs also confirm ancestry of cryptophytes and chloroarachniophytes


The chloroplast genome

The chloroplast genome

  • Sequenced chloroplast genomes range from 70kb - 201kb

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

  • Generally 100-250 genes:

    • Gene expression

    • Photosynthesis

    • Metabolism


The inverted repeat ir

Pinus

Nicotiana

Porphyra

The inverted repeat (IR)

  • Ranges from 5bk to 76kb in length

  • IR contains rRNA genes plus others:

    • None in brown algae (5kb)

    • 10 in tobacco (25kb)

    • 40 in geranium (76kb)

  • Present in:

    • Land plants (exc. legumes)

    • Chlorophytes

    • Chromophytes

    • Partial in conifers


Chloroplast genome evolution1

Synechocystis

3573 kbp

~3000 genes

Porphyra chloroplast

201 kbp

~250 genes

Chloroplast genome evolution

  • Rapid and massive reduction in number of genes:

    • Transferred to nucleus

    • Lost

  • 80-90% of plastid proteins are encoded in nucleus

  • Great overlap in gene content suggests that last common ancestor of cpDNA had ~300 genes


Gene loss in chloroplast evolution

Zea (75)

1 (0)

Oryza (75)

5 (2)

4 (0)

Nicotiana (76)

12 (0)

7 (5)

Pinus (69)

1 (0)

129 (34)

Marchantia (84)

34 (9)

Euglena (58)

14 (14)

1 (0)

Porphyra (200)

Ancestral

plastid

(235)

20 (1)

77 (0)

Odontella (124)

99 (3)

Cyanophora (136)

Gene loss in chloroplast evolution

  • 45 genes present in all genomes

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

  • Confirms that ancestral plastid genome was already highly reduced from that of cyanobacteria


Chloroplast gene content

Chloroplast gene content

Group 1

Gene expression

Photosynthesis

Metabolism

Rhodophytes s. l.

Glaucocystophytes

Group 2

Gene expression

Photosynthesis

Metabolism

Chlorophytes s. l

Group 3

Gene expression

Photosynthesis

Metabolism

Non-photosynthtic Chlorophytes

(e.g. Epifagus) and apicomplexans

Group 4

Gene expression

Photosynthesis

Metabolism

Yet to be discovered

(cf. Hydrogenosomes in mitochondria)


Chloroplast genes excluding ycf

Land Plants

Algae

Photosyn.

Epifagus

Euglena

Others

Porphyra

Chloroplast genes (excluding ycf)

Total

101-107

40

82

113-166

181

Gene expression

rRNA

tRNA

r-protein

Other

4

30-32

2-21

5-6

4

17

15

2

3

27

21

4

3

28-36

21-44

6-9

3

35

47

18

Photosynthesis

RuBisCo/thylakoid

ndh

29-30

11

-

-

26

-

31-48

-/10

53

-

1-5

2

1

7-14

25

Metabolism/misc.

18-21

6

149+

-/1/3

-

Introns


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