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Green Genes—Comparative Genomics of the Green Branch of Life

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Green Genes—Comparative Genomics of the Green Branch of Life View metadata, citation and similar papers at core.ac.uk brought to you by CORE provided by Elsevier - Publisher Connector Leading Edge Essay Green Genes—Comparative Genomics of the Green Branch of Life John L. Bowman,1,* Sandra K. Floyd,1 and Keiko Sakakibara1 1School of Biological Sciences, Monash University, Clayton Campus, Melbourne, Victoria 3800, Australia *Correspondence: [email protected] DOI 10.1016/j.cell.2007.04.004 As more plant genome sequences become available, researchers are increasingly using comparative genomics to address some of the major questions in plant biology. Such questions include the evolution of photosynthesis and multicellularity, the developmental genetic changes responsible for alterations in body plan, and the origin of important plant innovations such as roots, leaves, and vascular tissue. All plants are descended from a sin- scapes and whose evolution allowed genome. Plastid genome sequences gle eukaryotic ancestor that acquired the subsequent colonization of land are available from all major plant lin- a photosynthetic cyanobacterium as by the metazoans. Plastid genome eages, and perhaps surprisingly, the an endosymbiont (the ancestral plas- sequences are available for species plastid genomes from all lineages are tid). The acquisition of a cyanobacte- in all major lineages of plants, and similar in size and gene content. The rial endosymbiont was a momentous nuclear genome sequences have plastids of the glaucophytes (called event in the evolution of life on Earth been determined for a red alga, two cyanelles) still retain a peptidoglycan leading to a shift of most primary chlorophytes, and three distinct line- cell wall characteristic of the ances- production from prokaryotic cyano- ages of land plants. Here, we high- tral cyanobacterial endosymbiont and bacteria to photosynthetic eukaryo- light some of the major evolutionary yet have genomes similar to those of tes. Although the endosymbiosis of a transitions in the evolution of land other plants. The continuing nuclear cyanobacterium was a singular event plants and some key questions that bombardment of plastid-derived in the history of life, plastids have are beginning to be addressed by DNA is thought to have contributed also been transmitted horizontally comparing genome sequences from significantly to the genome content to other eukaryotic lineages via sec- a diverse range of plant species. of plants, with as much as 18% of ondary endosymbiotic events where the genome of the model flowering unrelated eukaryotes acquired endo- The Algal Origins of the plant (angiosperm) Arabidopsis thal- symbiotic plants. There are five or so Photosynthetic Eukaryotes iana thought to have been derived eukaryotic lineages, one of which is Following the capture of a cyanobac- from the cyanobacterial endosym- plants (Keeling et al., 2005). Within terium by the plant ancestor, the evo- biont (Martin et al., 2002). The con- the plants, three distinct groups have lution of the endosymbiont genome tribution of cyanobacterial genes to been identified (Figure 1): the glau- was characterized by wholesale algal nuclear genomes has not been cophytes (little-known freshwater transfer of genetic material to the host analyzed in detail, but substantial dif- algae), rhodophytes (red algae), and nuclear genome, resulting in a reduc- ferences might have contributed to the green plants (which include green tion in the endosymbiont genome differing genomic trajectories in the algae and land plants). The rhodo- and an enrichment of the host nuclear major plant lineages. phytes are primarily marine algae and include reef-building coralline algae; Table 1. Plant Genomes for Which Sequence Is Available (circa March 2007) they provide a source of agar and Size (Mb) # of Genes form the basis of the billion-dollar Cyanidioschyzon merolae (unicellular red alga) 16.5 5331 nori industry in Japan. The green plants, by far the most diverse of the Ostreococcus tauri (unicellular green alga) 12.56 8166 three groups, comprise two major Chlamydomomas reinhardtii (unicellular green alga) 136 >15,000 clades: the chlorophytes (freshwater Physcomitrella patens (moss) 487 >20,000 and marine algae) and the strepto- phytes (including the paraphyletic Selaginella moellendorfii (lycophyte) 85? ? charophycean freshwater algae and Oryza sativa (rice) 389 41,000 the land plants). It was the land plants Populus trichocarpa (popular tree) 485 45,000 (embryophytes) that colonized and eventually dominated terrestrial land- Arabidopsis thaliana (flowering plant) 140 27,500 Cell 129, April 20, 2007 ©2007 Elsevier Inc. 229 Figure 1. Phylogenetic Relationships among Plants Depicted are relationships among the three lineages of plants: glaucophytes (freshwater algae; blue), rhodophytes (red algae; red), and the green plants (chlorophytes, charophytes, and land plants; green). Estimated dates for some nodes are listed in millions of years be- fore present. The primary endosymbiotic event is estimated to have occurred at least 1.6 bil- lion years ago. A deep split within the green lineage created the chlorophyte clade and the charophyte plus land plant clade. Note that both the charophytes and the bryophytes are grades and are not monophyletic. Major events in the evolution of land plants are de- marcated with arrows. Species for which com- plete nuclear genome sequences are available are listed in color (photographs at right; the three angiosperm species are pictured upper left). Species positioned in large phylogenetic gaps where genome sequences would be informative (black) include the following: the basal lineage of land plants, the liverworts, charophycean algal lineages (Chara, Coleo- chaete) that are sisters to land plants, and the gymnosperms, which are the sister group to flowering plants (angiosperms). Also included is a multicellular chlorophytic green alga. Sec- ondary endosymbiotic events have occurred within both the red algae (e.g., diatoms, pic- tured) and green plants. Pie chart shows the relative species richness of the major clades. The vast majority of species within the Plantae are angiosperms (250,000 species), with other groups having substantially fewer described species (numbers approximated): glaucophytes 13; rhodophytes 5,920; chlorophytes 3,720, charo- phytes 3,400; bryophytes 17,000 (liverworts 7,000, mosses 10,000, hornworts 100); lycophytes 1,225; ferns 12,000; gymnosperms 800. Photos from top: Opuntia basilaris, Ginkgo biloba, Selaginella kraussiana, Physcomitrella patens, Marchantia polymorpha, Chara sp., Coleochaete sp., Chlamydomomas reinhardtii, Hydrodictyon sp., Ostreococcus tauri, Cyanidioschyzon merolae. Photos courtesy of Gayle Dupper, Institute of Forest Genetics, Placerville, CA, USA (poplar), Charles Delwiche, University of Maryland (Chara), James Umen, Salk Institute (Chlamydomonas), Hervé Moreau, Université Pierre et Marie Curie-Paris (Ostreococcus), and Tsuneyoshi Kuroiwa, Rikkyo University (Cyanidioschyzon). There are three plant species for between genes (Derelle et al., 2006). mitochondrial) and for both forward which almost complete genome One remarkable feature of the O. and reverse genetics (reviewed in information for nucleus, chloroplast, tauri genome is its extreme heteroge- Grossman et al., 2007). Additional red and mitochondrion is available: the neity with 2 chromosomes differing and green algal genome sequences, red alga Cyanidioshyzon merolae, the from the other 18 in GC content and such as the sequences of two other marine prasinophycean green alga transposable element distribution, Ostreococcus genomes (US Depart- Ostreococcus tauri, and the chloro- suggesting horizontal acquisition of ment of Energy Joint Genome Insti- phycean green alga Chlamydomonas at least one of its chromosomes. In tute, www.jgi.doe.gov), are required reinhardtii (Table 1). These unicel- contrast, the C. reinhardtii genome to assess whether these character- lular algae are ideal models for cell is larger and contains more genes. A istics are unique or more general for biology because the cells are mono- comparative genomics study using these taxa. plastidic, with C. merolae and O. tauri the Chlamydomonas, Arabidopsis, By producing oxygen as a waste cells also containing only a single and human genomes facilitated the product, the evolution of photosyn- mitochondrion and Golgi body, the identification of genes involved in thetic cyanobacteria 3.5 billion years division of which can be synchro- flagellar development and function in ago dramatically altered the Earth’s nized. C. merolae lives in acidic hot both Chlamydomonas and humans, ecosystem. Following the primary springs but can be grown in culture. including genes involved in human endosymbiotic event that defines Its genome is compact with most disease (angiosperms lack the flag- plants, this eukaryotic lineage evolved genes lacking introns (Matsuzaki et ellated sperm found in many other to become the dominant primary pro- al., 2004). The phytoplankton O. tauri organisms) (Li et al., 2004). C. rein- ducer in both aquatic and terrestrial is a picoeukaryote comprising cells hardtii is a sophisticated model for habitats. Comparisons among algal that are about the size of prokaryotes investigating photosynthesis and fun- genome sequences can provide (about 1 µm in diameter). Its genome damental cell biology with tools avail- information to elucidate characteris- is similarly compact with an aver- able for transformation of all three tics of the ancestral photosynthetic age spacing of only 197 basepairs genomes
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