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 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

Carries out photosynthesis Contains own genome Believed to be of endosymbiotic origin Phylogenetically related to cyanobacteria

Algal lineages
Primary

(Double membrane)

Rhodophytes

Chlorophytes

Glaucocystophytes

Secondary

Cryptophytes Heterokonts Haptophytes

Dinoflagellates Apicomplexans

Euglenoids Chlorarachniophytes

(Three or more membranes)

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

Emiliania Porphyra Marchantia

100

Guillardia

Odontella Pylaiella

Cyanophora Glaucocystis Pseudanabaena PCC 7409 Pseudanabaena PCC 6903 Phormidium Pseudanabaena PCC 7367

Klebsormidium Chlorella

SSU rRNA

Monophyly of primary plastids mitochondrial and nuclear evidence

Cyanidioschyzon
Cyanidium Gracilariopsis Chondrus
98%

Porphyra Triticum Marchantia Prototheca Tetraselmis m. Tetraselmis s.

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

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

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

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:
Porphyra

Land plants (exc. legumes) Chlorophytes Chromophytes Partial in conifers

Chloroplast genome evolution

Rapid and massive reduction in number of genes:
Transferred to nucleus Lost

Synechocystis
3573 kbp ~3000 genes

Porphyra chloroplast
201 kbp ~250 genes

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

1 (0) 5 (2) 4 (0) 7 (5) 129 (34) 1 (0) 34 (9) 1 (0) 20 (1) 99 (3) 77 (0) 12 (0)

Zea (75)

Oryza (75)
Nicotiana (76) Pinus (69)

Marchantia (84) Euglena (58)

14 (14)

Ancestral plastid (235)

Porphyra (200) Odontella (124)

Cyanophora (136)

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

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
Photosyn.

Algae

Epifagus
40

Euglena
82

Others 113-166

Porphyra
181

Total
Gene expression rRNA tRNA r-protein Other Photosynthesis RuBisCo/thylakoid

101-107

4 30-32 2-21 5-6

29-30 11 1-5 18-21

4 17 15 2
2 6

3 27 21 4
26 1 149+

3 28-36 21-44 6-9

31-48 -/10 7-14 -/1/3

3 35 47 18
53 25 -

ndh

Metabolism/misc. Introns