VALUE D N VALUE D N Ilia Leitch and Martin Lysak 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 Genome size variation: consequences and evolution Sometimes terminology matters… • Holoploid genome – the whole chromosome set with chromosome number n (irrespective of polyploidy, aneuploidy etc.) • Monoploid genome – one chromosome set of an organism and its DNA having the chromosome base number x • Genome size – covering term for the amount of DNA in both holoploid and monoploid genomes Annals of Botany 95: 255-260, 2005. • C-value – DNA content of a holoploid genome with chromosome number n • 1C-value – DNA content of one non-replicated holoploid genome with chromosome number n (= the half of a holoploid non-reduced genome with the chromosome number 2n); cf. 2C-value, 4C-value,… • Cx-value – DNA content of a monoploid genome with chromosome base number x ------------------------------------------------------------------------------------------------------ • Diploids: 1C-value = 1Cx-value • Polyploids: example 2C-value of allohexaploid wheat (Triticum aestivum; 2n=6x=42) is 34.6  1C-value: 17.3 pg; 1Cx-value: 5.8 pg (34.6 : 6) ------------------------------------------------------------------------------------------------------ Remember ! 1 pg = 980 Mbp Sometimes terminology matters… 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. DNA amount in unreplicated gametic nucleus Concept of C-value: Swift H. 1950. Proc. Natl. Acad. Sci. USA 36: 643-654. VALUE D N VALUE D N ’C’ means Constant www.kew.org/genomesize/homepage.html Land plants 4427 angiosperms 207 gymnosperms 87 pteridophytes 176 bryophytes Algae 91 Chlorophyta 44 Phaeophyta 118 Rhodophyta 5150 species Plant DNA C-values database C-values in angiosperms range nearly 2000-fold Utricularia gibba 1C = 0.090 pg Genlisea margaretae 1C = 0.065 pg Trillium rhombifolium 1C = 111.5 pg Fritillaria assyriaca 1C = 127.4 pg Greilhuber et al. 2006. Plant Biology 8: 770-777 Bennett. 1972. Proc. Roy. Soc. Lond. B 181: 109-135. Greilhuber et al. 2006. Plant Biology 8: 770-777 Grif et al. 1980. Tsitologiya 22: 1331-1338 The smallest and largest plant genome dicots, Lentibulariaceae monocots, Melanthiaceae Range of DNA amounts in land plants Lycophytes (0.4%) Monilophytes (0.6%) Angiosperms (1.4%) Gymnosperms (25%) 2.3 – 36.0 0.8 – 72.7 0.16 – 12.0 0.09 – 6.4 0.065 – 127.4 Seedplants Vascularplants 1C DNA amount (pg) Bryophytes (1%) DNA amount variation in angiosperms Mode = 0.6 pg 0 50 100 150 200 250 0 100 200 300 400 500 1C DNA amount (pg) Numberofspecies Max. 127.4 pg 0 25 50 75 100 125 Mode 0.6 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 Bennett et al. 1983. J. Cell Sci. 63: 173-179. Anderson et al. 1985. Exp. Cell Res. 156: 367-378. Baetcke et al. 1967. Proc. Natl. Acad. Sci. USA 58: 533-540. Bennett et al. 1981. J. Cell Sci. 47: 91-115. 0 5 10 15 20 1C DNA amount (pg) 0 10 20 30 40 1C DNA amount (pg) 1.0 1.5 2.0 Log DNA per cell (pg) 5 10 15 20 1C DNA amount (pg) Lognuclearvolume(μm3) 2.0 2.5 3.0 3.5 Centromerevolume(μm3) 2 4 6 8 Chromosomevolume(μm3) 400 300 200 100 0 MeantotalSClength(μm)x102 0 5 10 15 20 25 30 350 5 10 15 20 1C DNA amount (pg) 0 10 20 30 40 1C DNA amount (pg) 1.0 1.5 2.0 Log DNA per cell (pg) 5 10 15 20 1C DNA amount (pg) Lognuclearvolume(μm3) 2.0 2.5 3.0 3.5 Centromerevolume(μm3) 2 4 6 8 Chromosomevolume(μm3) 400 300 200 100 0 MeantotalSClength(μm)x102 0 5 10 15 20 25 30 35 0 5 10 15 20 1C DNA amount (pg) 0 10 20 30 40 1C DNA amount (pg) 1.0 1.5 2.0 Log DNA per cell (pg) 5 10 15 20 1C DNA amount (pg) Lognuclearvolume(μm3) 2.0 2.5 3.0 3.5 Centromerevolume(μm3) 2 4 6 8 Chromosomevolume(μm3) 400 300 200 100 0 MeantotalSClength(μm)x102 0 5 10 15 20 25 30 350 5 10 15 20 1C DNA amount (pg) 0 10 20 30 40 1C DNA amount (pg) 1.0 1.5 2.0 Log DNA per cell (pg) 5 10 15 20 1C DNA amount (pg) Lognuclearvolume(μm3) 2.0 2.5 3.0 3.5 Centromerevolume(μm3) 2 4 6 8Chromosomevolume(μm3) 400 300 200 100 0 MeantotalSClength(μm)x102 0 5 10 15 20 25 30 35 MeantotalSClength (μm)x102 Variation of genome size: Consequences of timing Bennett MD. 1977. Phil. Trans. Roy. Soc. B 277: 201-277. 1C DNA amount (pg) Durationofmeiosis(h) 0 15 30 45 100 200 300 Meiosis Van't Hof & Sparrow AH. 1963. Proc. Natl. Acad. Sci. USA 49: 897-902. Durationofmitosis(h) DNA amount per cell (pg) 0 30 60 90 100 20 30 Mitosis 10 1C DNA amount (pg) Variation of genome size: Consequences at cell and tissue level 0 40 80 120 160 0 10 20 30 1C DNA amount (pg) Pollenvolumeatdehiscence (μm3 x103 ) 0 0.2 0.4 0.6 0.8 0 10 20 30 1C DNA amount (pg) Massof100seeds(g)Relationship between pollen volume and DNA amount in 16 grass species. Bennett et al. 1972 Relationship between seed weight and DNA amount in 12 Allium species. Bennett et al. 1972 Consequences of variation in DNA amount a) Life cycle options b) Life strategy options c) Ecology options d) Coping with environmental change Whole plant level Consequences of variation in DNA amount 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. Whole plant level Consequences: life cycle options 0 100 200 300 400 0 50 100 150 200 250 3C DNA amount (pg) Durationofmeiosis(h) Fritillaria meleagris 1C = 70.7 pg Arabidopsis thaliana 1C = 0.16 pg Bennett MD. 1977. Phil. Trans. Roy. Soc. B 277: 201-277. 7 weeks 52 weeks MINIMUM GENERATION TIME Max. limiting DNA amount for annuals Max. limiting DNA amount for ephemerals Obligate perennials No species in this triangle Ephemerals Annuals and perennials Annuals and perennials Consequences: life cycle options 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 a) Life cycle options b) Life strategy options c) Ecology options d) Coping with environmental change Whole plant level Consequences of variation in DNA amount 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. Whole plant level 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 0 50 100 150 200 250 0 100 200 300 400 500 1C DNA amount (pg) Numberofspecies 0 5 10 15 20 25 0 100 200 300 400 500 1C DNA amount (pg) Numberofspecies Non-weed species Weeds Bennett, Leitch & Hanson. 1998. DNA amounts in two samples of angiosperm weeds. Annals of Botany 82: 121-134. Mean 1C 7.0 pg Mean 1C 2.9 pg 0 25 50 75 100 125 0 25 50 75 100 125 Max = 127.4 pg Max = 25.1 pg (c. 0.1 – 127.4 pg) (0.16 – 25.1 pg) 1C DNA amount (pg)1C DNA amount (pg) No.ofspecies No.ofspecies Success of an invasive weed ● Rapid establishment or completion of reproductive development ● Short generation time ● Rapid production of many small seeds Consequences of variation in DNA amount a) Life cycle options b) Life style options c) Ecology options d) Coping with environmental change Whole plant level 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 Sp. 17 Poaceae and 15 Fabaceae crops Bennett 1976 Pop. 24 Berberis in Patagonia Bottini et al. 2000 Sp. 20 Arachis duranensis in Argentina/ Bolivia Temsch & Greilhuber 2001 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 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 Sp. 11 Tropical vs. Temperate Pines Hall et al. 2000 Sp. 19 Helianthus Sims & Price 1985 Genome size and latitude + correlation - correlation no correlation 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 Ecological parameter e.g. temperature DNAamount Species with large genomes excluded from extreme environments Species with small genomes can occupy all environments Knight & Ackerly. 2002. Ecology Letters 5: 66-76. Consequences: ecology options Summary • The relationship between genome size and environmental factors is not uniform but appears to be stronger for species with large genomes • Species with large genomes are excluded from extreme environments Consequences of variation in DNA amount a) Life cycle options b) Life style options c) Ecology options d) Coping with environmental change Threat of extinction Whole plant level Consequences: Genome size and threat of extinction Is genome size important? Vinogradov AE. 2003. Selfish DNA is maladaptive: evidence from the plant Red List. Trends in Genetics 19: 609-614. Habitat loss Pollution Invasive species Consequences: Genome size and threat of extinction 3036 species Data and analysis Global concern = 305 Local concern = 1329 No concern = 1402 Vinogradov AE. 2003. Selfish DNA is maladaptive: evidence from the plant Red List. Trends in Genetics 19: 609-614. Plant DNA C-values database Consequences: Genome size and threat of extinction Results 0.7 0.9 1.1 1.3 1.5 1.7 No concern Local concern Global concern Conservation status Log1CDNAamount(pg) Conservation status Loggenomesize(pg) No concern Local concern Global concern 7.4 pg 12.5 pg 42.5 pg Vinogradov AE. 2003. Trends in Genetics 19: 609-614. Consequences: Genome size and threat of extinction Conclusions Species with large genomes are at greater risk of extinction than those with small genomes. - Independent of life cycle type (at least partially) - Independent of polyploidy Consequences: Genome size and threat of extinction Threat of extinction of species with large genomes Restricted trait variation (e.g. only large seeds) Reduced rates of diversification (?) Restricted ecological distribution Slow growing obligate perennial More sensitive to pollution DNA amount variation and consequences Summary Huge variation in DNA amount in plants Consequences of this variation visible at: Cellular level Tissue level Whole organism level Possession of large genomes appear to impose constraints which operate at: Functional level Ecological level Evolutionary level