Genome Size Variation: Consequences and Evolution
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Genome Size Variation: Consequences and Evolution Ilia Leitch D N VALUE D N VALUE Genome size variation: consequences and evolution (i) How genome size varies across plants (ii) What are the consequence of this variation (iii) How did such variation evolve Early genome size studies in plants First genome size of a plant: Lilium longiflorum Ogur M et al. 1951. Exp. Cell Res. 2: 73-89. Concept of C-value: D N DNA amount in unreplicated VALUE gametic nucleus Swift H. 1950. Proc. Natl. Acad. Sci. USA 36: 643-654. Plant DNA C-values database www.kew.org/genomesize/homepage.html 5150 species Land plants Algae 4427 angiosperms 91 Chlorophyta 207 gymnosperms 44 Phaeophyta 87 pteridophytes 118 Rhodophyta 176 bryophytes C-values in angiosperms range nearly 2000-fold Genlisea UtriculariaTrillium Fritillaria margaretae rhombifoliumgibba assyriaca 1C = 0.065 pg 1C1C = 0.090 = 111.5 pg pg 1C = 127.4 pg Greilhuber et al. 2006. GreilhuberGrif etet alal.. 2006.1980. Bennett. 1972. Plant Biology PlantTsitologiya Biology Proc. Roy. Soc. Lond. B 8: 770-777 8: 22:770-777 1331-1338 181: 109-135. Range of DNA amounts in land plants Angiosperms (1.4%) 0.065 – 127.4 Gymnosperms (25%) 2.3 – 36.0 Seed plants Seed Monilophytes (0.6%) 0.8 – 72.7 Vascular plants Lycophytes (0.4%) 0.16 – 12.0 Bryophytes (1%) 0.09 – 6.4 1C DNA amount (pg) DNA amount in algae DNA amount in algae Phaeophyta Rhodophyta Chlorophyta 44 species 118 species 153 species Kapraun DF. 2005. Kapraun DF. 2007. Annals of Botany 95: 7-44. Annals of Botany 99: 677-701 Range of DNA amounts in algae 0.065 – 127.4 Angiosperms Gymnosperms 2.3 – 36.0 Monilophytes 0.8 – 72.7 Lycophytes 0.16 – 12.0 Bryophytes 0.09 – 6.4 Phaeophyta (2.9%) 0.1 – 0.9 Rhodophyta (1.8%) 0.017 – 1.4 Chlorophyta (1.3%) 0.013 – 23.4 Ostreococcus tauri (Prasinophyta) Chloroplast & starch grain Mitochondrion Golgi body Nucleus 0.1 μm 1C = 0.013 pg (12.56 Mb) Derelle et al. 2006. Genome analysis of the smallest free-living eukaryote Ostreococcus tauri unveils many unique features. Proc Natl Acad Sci 103: 11647-11652. Genome size variation Fritillaria assyriaca Genlisea margaretae Ostreococcus tauri 1C = 127.4 pg 1C = 0.065 pg 1C = 0.01 pg C-value paradox Thomas CA. 1971. The genetic organization of chromosomes. Annual Review of Genetics 5: 237-256. ‘why the lowly liverwort has 18 times as much DNA as we have, and the slimy, dull salamander known as Amphiuma has 26 times our complement of DNA’. Comings DE. 1972. Advances in Human Genetics 3: 237-431. C-value enigma Gregory TR. 2001. Coincidence, co-evolution, or causation? DNA content, cell size, and the C-value enigma. Biological Reviews 76: 65-101. What types of non-coding DNA sequences predominate in genomes of different sizes? What are the mechanisms involved in generating genome size variation? What are the evolutionary forces driving genome size changes? What are the consequences of genome size variation? How has genome size evolved? Variation of genome size: Consequences at nuclear level ) 3 400 ) 3 m 8 m μ μ 300 6 200 4 100 2 0 Centromere ( volume Chromosome volume ( Chromosome volume 0 5 10 15 20 5 10 15 20 2 1C DNA amount (pg) 1C DNA amount (pg) 0 1 Bennett et al. 1983. Bennett et al. 1981. J. Cell Sci. 63: 173-179. J. Cell Sci. 47: 91-115. ) 35 3 3.5 m m) x μ μ 30 25 3.0 2 20 15 m)x 10 2.5 μ ( 10 5 2.0 Mean total SC length length SC total Mean 0 ( volume nuclear Log Mean total SC length ( 0 10 20 30 40 1.0 1.5 2.0 1C DNA amount (pg) Log DNA per cell (pg) Anderson et al. 1985. Baetcke et al. 1967. Exp. Cell Res. 156: 367-378. Proc. Natl. Acad. Sci. USA 58: 533-540. Variation of genome size: Consequences of timing Mitosis Meiosis 30 300 20 200 10 100 Duration of meiosis (h) Duration of mitosis (h) 0 30 60 90 100 0 15 30 45 DNA amount per cell (pg) 1C1C DNA DNA amount amount (pg) (pg) Van't Hof & Sparrow AH. 1963. Bennett MD. 1977. Proc. Natl. Acad. Sci. USA 49: 897-902. Phil. Trans. Roy. Soc. B 277: 201-277. Variation of genome size: Consequences at cell and tissue level 0.8 160 0.6 ) 3 120 x 10 0.4 3 80 m μ ( 40 0.2 Mass of 100 seeds (g) Pollen volume dehiscenceat 0 0 0 102030 0102030 1C DNA amount (pg) 1C DNA amount (pg) Relationship between pollen Relationship between seed volume and DNA amount weight and DNA amount in in 16 grass species. 12 Allium species. Bennett et al. 1972 Bennett et al. 1972 Consequences of variation in DNA amount Whole plant level a) Life cycle options b) Life strategy options c) Ecology options d) Coping with environmental change Consequences of variation in DNA amount Whole plant level a) Life cycle options Bennett MD. 1972. Nuclear DNA content and minimum generation time in herbaceous plants. Proceedings of the Royal Society of London Series B-Biological Sciences 181: 109-135. Consequences: life cycle options 400 300 Fritillaria meleagris 1C = 70.7 pg Arabidopsis 200 thaliana 1C = 0.16 pg 100 Duration of meiosis (h) meiosis of Duration 0 0 50 100 150 200 250 3C DNA amount (pg) Bennett MD. 1977. Phil. Trans. Roy. Soc. B 277: 201-277. Consequences: life cycle options No species in this triangle Obligate Max. limiting perennials DNA amount for annuals E U L A V - Annuals and C perennials A N D Max. limiting DNA amount for ephemerals Annuals and perennials Ephemerals 7 52 weeks weeks MINIMUM GENERATION TIME Bennett MD. 1972. Proc. Roy. Soc. Lond. B 181: 109-135. Consequences of variation in DNA amount Life cycle options: Conclusions • DNA amount can impose limits on the type of life cycle a species can display • Species with small genomes may be ephemerals, annuals or perennials • Species with large genomes are restricted to being obligate perennials Consequences of variation in DNA amount Whole plant level a) Life cycle options b) Life strategy options c) Ecology options d) Coping with environmental change Consequences of variation in DNA amount Whole plant level b) Life strategy options: Potential to become a weed Bennett, Leitch & Hanson. 1998. DNA amounts in two samples of angiosperm weeds. Annals of Botany 82: 121-134. Consequences: option to be a weed Method DNA amounts for 156 angiosperms recognised as weeds compared with 2685 non-weed species Consequences: option to be a weed Non-weed species Weeds (c. 0.1 – 127.4 pg) (0.16 – 25.1 pg) 25 250 200 Mean 1C 20 Mean 1C 150 7.0 pg 15 2.9 pg 100 10 Max = Max = 50 127.4 pg 5 25.1 pg No. of species No. of species 0 Number of species 0 Number of species 00 10025 20050 30075 100 400 125 500 00 10025 20050 75 300 100 400 125 500 1C1C DNA DNA amount amount (pg) (pg) 1C1C DNADNA amount (pg)(pg) Bennett, Leitch & Hanson. 1998. DNA amounts in two samples of angiosperm weeds. Annals of Botany 82: 121-134. Success of an invasive weed ● Rapid establishment or completion of reproductive development ● Short generation time ● Rapid production of many small seeds Consequences: option to be a weed 12 10 8 6 4 % of all species which are weeds 2 0 0123456 Group (increasing DNA amount) Consequences of variation in DNA amount Whole plant level a) Life cycle options b) Life style options c) Ecology options d) Coping with environmental change Genome size and latitude Pop. Several Picea sitchensis Miksche 1967, 1971 Sp. Tropical vs. temperate grasses Avdulov 1931 Sp. 329 tropical vs. 527 temperate plants Levin and Funderburg 1979 + correlation Sp. 17 Poaceae and 15 Fabaceae crops Bennett 1976 Pop. 24 Berberis in Patagonia Bottini et al. 2000 Sp. 20 Arachis duranensis in Argentina/ Temsch & Greilhuber 2001 Bolivia Pop. Several Festuca arundinacea Ceccarelli et al. 1992 Pop. North American cultivars of Zea mays Rayburn et al. 1985 Sp. 162 British plants Grime and Mowforth 1982 - correlation Sp. 23 Arctic plants Bennett et al. 1982 Pop. 22 N American Zea mays Rayburn et al. 1985 Pop. 11 N American Zea mays Laurie & Bennett 1985 Sp. 18 pines Joyner et al. 2001 Pop. 6 Allium cepa cultivars Bennett et al. 2000 Pop. Several Picea glauca Teoh & Rees 1976 Pop. 10 Dactylis glomerata Creber et al. 1994 no correlation Sp. 11 Tropical vs. Temperate Pines Hall et al. 2000 Sp. 19 Helianthus Sims & Price 1985 Consequences: ecology options 401 species in the state of California Knight & Ackerly. 2002. Variation in nuclear DNA content across environmental gradients: a quantile regression analysis. Ecology Letters 5: 66-76. Consequences: ecology options Species with large genomes excluded from extreme environments Species with small genomes can occupy all DNA amount DNA amount environments Ecological parameter e.g. temperature Knight & Ackerly. 2002. Ecology Letters 5: 66-76. Consequences: ecology options annual annual 25 perennial perennial 20 15 10 5 1C DNA amount (pg) 0 0.8 18 22 26 30 34 38 42 1.0 July maximum temperature (°C) 1.2 1.4 1.6 Knight & Ackerly. 2002. Variation in nuclear DNA content across environmental gradients: a quantile regression analysis. Ecology Letters 5: 66-76. Consequences: ecology options annual 25 perennial 0.05 0.00 20 -0.05 15 -0.10 10 -0.15 -0.20 5 1C DNA amount (pg) Quadratic coefficient -0.25 0 -0.30 0 18 22 26 30 34 38 42 015 2040608010030 45 60 75 90 July maximum temperature (°C) Conditional quantile Knight & Ackerly.