Plant nuclear genome size (GS) varies over three orders of magnitude and is correlated with cell size and growth rate. We explore whether these relationships can be owing to geometrical scaling constraints. These would produce an isometric GS-cell volume relationship, with the GS-cell diameter relationship with the exponent of 1/3. In the GS-cell division relationship, duration of processes limited by membrane transport would scale at the 1/3 exponent, whereas those limited by metabolism would show no relationship. We tested these predictions by estimating scaling exponents from 11 published datasets on differentiated and meristematic cells in diploid herbaceous plants. We found scaling of GS-cell size to almost perfectly match the prediction. The scaling exponent of the relationship between GS and cell cycle duration did not match the prediction. However, this relationship consists of two components: (i) S phase duration, which depends on GS, and has the predicted 1/3 exponent, and (ii) a GS-independent threshold reflecting the duration of the G1 and G2 phases. The matches we found for the relationships between GS and both cell size and S phase duration are signatures of geometrical scaling. We propose that a similar approach can be used to examine GS effects at tissue and whole plant levels.

Department of Botany Faculty of Science Charles University Benátská 2 Praha 2 Czech Republic

Zobrazit více v PubMed

Bennett M. D., Leitch I. J. 2010. Plant DNA C-values database (release 5.0, December 2010). See http://www.kew.org/cvalues/.

Pellicer J., Fay M., Leitch I. J. 2010. The largest eukaryotic genome of them all? Bot. J. Linn. Soc. 164, 10–1510.1111/j.1095-8339.2010.01072.x (doi:10.1111/j.1095-8339.2010.01072.x) DOI

Bennett M. D. 1987. Variation in genomic form in plants and its ecological implications. New Phytol. 106, 177–20010.1111/j.1469-8137.1987.tb04689.x (doi:10.1111/j.1469-8137.1987.tb04689.x) DOI

Thompson K. 1990. Genome size, seed size and germination temperature in herbaceous angiosperms. Evol. Trends Plants 4, 113–116

Knight C., Beaulieu J. 2008. Genome size scaling through phenotype space. Ann. Bot. (Lond.) 101, 759–76610.1093/aob/mcm321 (doi:10.1093/aob/mcm321) PubMed DOI PMC

Francis D., Davies M., Barlow P. 2008. A strong nucleotypic effect on the cell cycle regardless of ploidy level. Ann. Bot. (Lond.) 101, 747–75710.1093/aob/mcn038 (doi:10.1093/aob/mcn038) PubMed DOI PMC

Hof J. V., Bjerknes C. 1981. Similar replicon properties of higher-plant cells with different S periods and genome sizes. Exp. Cell Res. 136, 461–46510.1016/0014-4827(81)90027-6 (doi:10.1016/0014-4827(81)90027-6) PubMed DOI

Bayliss M. W. 1976. Variation of cell cycle duration within suspension cultures of Daucus carota and its consequence for the induction of ploidy changes with colchicine. Protoplasma 88, 279–28510.1007/BF01283252 (doi:10.1007/BF01283252) PubMed DOI

Gong J., Traganos F., Darzynkiewicz Z. 1993. Simultaneous analysis of cell cycle kinetics at two different DNA ploidy levels based on DNA content and cyclin B measurements. Cancer Res. 53, 5096–5099 PubMed

Storchová Z., Breneman A., Cande J., Dunn J., Burbank K., O'Toole E., Pellman D. 2006. Genome-wide genetic analysis of polyploidy in yeast. Nature 443, 541–54710.1038/nature05178 (doi:10.1038/nature05178) PubMed DOI

Knight C., Molinari N., Petrov D. 2005. The large genome constraint hypothesis: evolution, ecology and phenotype. Ann. Bot. (Lond.) 95, 177–19010.1093/aob/rnci011 (doi:10.1093/aob/rnci011) PubMed DOI PMC

Beaulieu J., Leitch I., Patel S., Pendharkar A., Knight C. 2008. Genome size is a strong predictor of cell size and stomatal density in angiosperms. New Phytol. 179, 975–98610.1111/j.1469-8137.2008.02528.x (doi:10.1111/j.1469-8137.2008.02528.x) PubMed DOI

Knight C. A., Clancy R. B., Götzenberger L., Dann L., Beaulieu J. M. 2010. On the relationship between pollen size and genome size. J. Bot. 2010, 7.10.1155/2010/612017 (doi:10.1155/2010/612017) DOI

Gruner A., Hoverter N., Smith T., Knight C. A. 2010. Genome size is a strong predictor of root meristem growth rate. J. Bot. 2010, 4. (doi:10.1155/2010/390414) DOI

Leishman M. 1999. How well do plant traits correlate with establishment ability? Evidence from a study of 16 calcareous grassland species. New Phytol. 141, 487–49610.1046/j.1469-8137.1999.00354.x (doi:10.1046/j.1469-8137.1999.00354.x) DOI

Hessen D., Jeyasingh P., Neiman M., Weider L. 2010. Genome streamlining and the elemental costs of growth. Trends Ecol. Evol. 25, 75–8010.1016/j.tree.2009.08.004 (doi:10.1016/j.tree.2009.08.004) PubMed DOI

Maranon T., Grubb P. J. 1993. Physiological basis and ecological significance of the seed size and relative growth rate relationship in Mediterranean annuals. Funct. Ecol. 7, 591–59910.2307/2390136 (doi:10.2307/2390136) DOI

Knight C., Ackerly D. 2002. Variation in nuclear DNA content across environmental gradients: a quantile regression analysis. Ecol. Lett. 5, 66–7610.1046/j.1461-0248.2002.00283.x (doi:10.1046/j.1461-0248.2002.00283.x) DOI

Morgan H., Westoby M. 2005. The relationship between nuclear DNA content and leaf strategy in seed plants. Ann. Bot. (Lond.) 96, 1321–133010.1093/aob/mci284 (doi:10.1093/aob/mci284) PubMed DOI PMC

Suda J., Kyncl T., Freiova R. 2003. Nuclear DNA amounts in Macaronesian angiosperms. Ann. Bot. (Lond.) 92, 153–16410.1093/aob/mcg104 (doi:10.1093/aob/mcg104) PubMed DOI PMC

Leitch I. J., Bennett M. D. 2007. Genome size and its uses: the impact of flow cytometry. In Flow cytometry with plant cells (eds Dolezel J., Greilhuber J., Suda J.), pp. 153–176 Weinheim, Germany: Wiley-VCH

Peters R. H. 1986. The ecological implications of body size. Cambridge, UK: Cambridge University Press

Connor E., McCoy E. 1979. Statistics and biology of the species-area relationship. Am. Nat. 113, 791–83310.1086/283438 (doi:10.1086/283438) DOI

Martinez N. 1992. Constant connectance in community food webs. Am. Nat. 139, 1208–121810.1086/285382 (doi:10.1086/285382) DOI

Reich P., Oleksyn J., Wright I., Niklas K., Hedin L., Elser J. 2010. Evidence of a general 2/3-power law of scaling leaf nitrogen to phosphorus among major plant groups and biomes. Proc. R. Soc. B 277, 877–88310.1098/rspb.2009.1818 (doi:10.1098/rspb.2009.1818) PubMed DOI PMC

Tilman D. 1999. The ecological consequences of changes in biodiversity: a search for general principles. Ecology 80, 1455–1474

Niklas K. 1994. The scaling of plant and animal body-mass, length and diameter. Evolution 48, 44–5410.2307/2410002 (doi:10.2307/2410002) PubMed DOI

West G., Brown J., Enquist B. 1997. A general model for the origin of allometric scaling laws in biology. Science 276, 122–12610.1126/science.276.5309.122 (doi:10.1126/science.276.5309.122) PubMed DOI

Moses M., Brown J. 2003. Allometry of human fertility and energy use. Ecol. Lett. 6, 295–30010.1046/j.1461-0248.2003.00446.x (doi:10.1046/j.1461-0248.2003.00446.x) DOI

Savage V., Gillooly J., Woodruff W., West G., Allen A., Enquist B., Brown J. 2004. The predominance of quarter-power scaling in biology. Funct. Ecol. 18, 257–28210.1111/j.0269-8463.2004.00856.x (doi:10.1111/j.0269-8463.2004.00856.x) DOI

Reich P., Tjoelker M., Machado J., Oleksyn J. 2006. Universal scaling of respiratory metabolism, size and nitrogen in plants. Nature 439, 457–46110.1038/nature04282 (doi:10.1038/nature04282) PubMed DOI

Brown J., West G. 2001. Scaling in biology. Oxford, UK: Oxford University Press

Price C., Enquist B. 2007. Scaling mass and morphology in leaves: an extension of the WBE model. Ecology 88, 1132–114110.1890/06-1158 (doi:10.1890/06-1158) PubMed DOI

Enquist B., Kerkhoff A., Stark S., Swenson N., McCarthy M., Price C. 2007. A general integrative model for scaling plant growth, carbon flux and functional trait spectra. Nature 449, 218–22210.1038/nature06061 (doi:10.1038/nature06061) PubMed DOI

Milla R., Reich P. 2007. The scaling of leaf area and mass: the cost of light interception increases with leaf size. Proc. R. Soc. B 274, 2109–211410.1098/rspb.2007.0417 (doi:10.1098/rspb.2007.0417) PubMed DOI PMC

Niklas K., Cobb E., Niinemets U., Reich P., Sellin A., Shipley B., Wright I. 2007. ‘Diminishing returns’ in the scaling of functional leaf traits across and within species groups. Proc. Natl Acad. Sci. USA 104, 8891–889610.1073/pnas.0701135104 (doi:10.1073/pnas.0701135104) PubMed DOI PMC

West G., Enquist B., Brown J. 2009. A general quantitative theory of forest structure and dynamics. Proc. Natl Acad. Sci. USA 106, 7040–704510.1073/pnas.0812294106 (doi:10.1073/pnas.0812294106) PubMed DOI PMC

Mori S., et al. 2010. Mixed-power scaling of whole-plant respiration from seedlings to giant trees. Proc. Natl Acad. Sci. USA 107, 1447–145110.1073/pnas.0902554107 (doi:10.1073/pnas.0902554107) PubMed DOI PMC

Baetcke K., Sparrow A., Nauman C., Schwemme S. S. 1967. Relationship of DNA content to nuclear and chromosome volumes and to radiosensitivity (LD50). Proc. Natl Acad. Sci. USA 58, 533–54010.1073/pnas.58.2.533 (doi:10.1073/pnas.58.2.533) PubMed DOI PMC

Gregory T. 2001. Coincidence, coevolution, or causation? DNA content, cell size, and the C-value enigma. Biol. Rev. 76, 65–10110.1017/S1464793100005595 (doi:10.1017/S1464793100005595) PubMed DOI

Price H., Sparrow A., Nauman A. 1973. Correlations between nuclear volume, cell volume and DNA content in meristematic cells of herbaceous angiosperms. Experientia 29, 1028–102910.1007/BF01930444 (doi:10.1007/BF01930444) DOI

Cavalier-Smith T. 1978. Nuclear volume control by nucleoskeletal DNA, selection for cell volume and cell growth rate, and the solution of the DNA C-value paradox. J. Cell Sci. 34, 247. PubMed

Smith R. 2009. Use and misuse of the reduced major axis for line-fitting. Am. J. Phys. Anthropol. 140, 476–48610.1002/ajpa.21090 (doi:10.1002/ajpa.21090) PubMed DOI

Hodgson J., et al. 2010. Stomatal vs. genome size in angiosperms: the somatic tail wagging the genomic dog? Ann. Bot. (Lond.) 105, 573–58410.1093/aob/mcq011 (doi:10.1093/aob/mcq011) PubMed DOI PMC

Jolicoeur P. 1975. Linear regressions in fishery research: come comments. J. Fish. Res. Board Can. 32, 1491–149410.1139/f75-171 (doi:10.1139/f75-171) DOI

Legendre P., Legendre L. 1998. Numerical ecology. Amsterdam, The Netherlands: Elsevier Science

Beemster G., Vusser K., De Tavernier E., De Bock K., De Inze D. 2002. Variation in growth rate between Arabidopsis ecotypes is correlated with cell division and A-type cyclin-dependent kinase activity. Plant Physiol. 129, 854–86410.1104/pp.002923 (doi:10.1104/pp.002923) PubMed DOI PMC

Melaragno J. E., Mehrotra B., Coleman A. W. 1993. Relationship between endopolyploidy and cell size in epidermal tissue of Arabidopsis. Plant Cell 5, 1661–166810.1105/tpc.5.11.1661 (doi:10.1105/tpc.5.11.1661) PubMed DOI PMC

Jovtchev G., Schubert V., Meister A., Barow M., Schubert I. 2006. Nuclear DNA content and nuclear and cell volume are positively correlated in angiosperms. Genome Res. 114, 77–8210.1159/000091932 (doi:10.1159/000091932) PubMed DOI

Gray J., Kolesik P., Hoj P., Coombe B. 1999. Confocal measurement of the three-dimensional size and shape of plant parenchyma cells in a developing fruit tissue. Plant J. 19, 229–23610.1046/j.1365-313X.1999.00512.x (doi:10.1046/j.1365-313X.1999.00512.x) PubMed DOI

Cavalier-Smith T. 2005. Economy, speed and size matter: evolutionary forces driving nuclear genome miniaturization and expansion. Ann. Bot. (Lond.) 95, 147–17510.1093/aob/mci010 (doi:10.1093/aob/mci010) PubMed DOI PMC

Kozlowski J., Konarzewski M., Gawelczyk A. 2003. Cell size as a link between noncoding DNA and metabolic rate scaling. Proc. Natl Acad. Sci. USA 100, 14 080–14 08510.1073/pnas.2334605100 (doi:10.1073/pnas.2334605100) PubMed DOI PMC

DeLong J., Okie J., Moses M., Sibly R., Brown J. 2010. Shifts in metabolic scaling, production and efficiency across major evolutionary transitions of life. Proc. Natl Acad. Sci. USA 107, 12 941–12 94510.1073/pnas.1007783107 (doi:10.1073/pnas.1007783107) PubMed DOI PMC

Méchali M. 2010. Eukaryotic DNA replication origins: many choices for appropriate answers. Nat. Rev. Mol. Cell. Biol. 11, 728–73810.1038/nrm2976 (doi:10.1038/nrm2976) PubMed DOI

Bennett M. D. 1972. Nuclear DNA content and minimum generation time in herbaceous plants. Proc. R. Soc. Lond. B 181, 109–13510.1098/rspb.1972.0042 (doi:10.1098/rspb.1972.0042) PubMed DOI

Kuroki Y., Tanaka R. 1973. Duration of mitotic cell cycle in root tip cells of male Rumex acetosa. Jpn. J. Genet. 48, 19–2610.1266/jjg.48.19 (doi:10.1266/jjg.48.19) DOI

Powell M., Davies M., Francis D. 1986. The influence of zinc on the cell cycle in the root meristem of a zinc-tolerant and zoinc-nontolerant cultivar of Festuca rubra L. New Phytol. 102, 419–42810.1111/j.1469-8137.1986.tb00819.x (doi:10.1111/j.1469-8137.1986.tb00819.x) PubMed DOI

King P. 1980. Plant tissue culture and the cell cycle. Adv. Biomed. Eng. 18, 1–38

Barlow P. 1973. Mitotic cycles in root meristems. In The cell cycle in development and differentiation (eds Balls M., Billet F. S.), pp. 133–165 Cambridge, UK: British Society for Developmental Biology Symposium

R Development Core Team 2010. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing; See http://www.R-project.org/.

Ebert T., Russell M. 1994. Allometry and model II nonlinear regression. J. Theor. Biol. 168, 367–37210.1006/jtbi.1994.1116 (doi:10.1006/jtbi.1994.1116) DOI

Francis D., Barlow P. 1988. Temperature and the cell cycle. In Plants and temperature (eds Long S. P., Woodward F. I.), pp. 181–201 Cambridge, U: Company of Biologists PubMed

Ivanov V., Dubrovsky J. 1997. Estimation of the cell-cycle duration in the root apical meristem: a model of linkage between cell-cycle duration, rate of cell production, and rate of root growth. Int. J. Plant Sci. 158, 757–76310.1086/297487 (doi:10.1086/297487) DOI

Garnier E. 1991. Resource capture, biomass allocation and growth in herbaceous plants. Trends Ecol. Evol. 6, 126–13110.1016/0169-5347(91)90091-B (doi:10.1016/0169-5347(91)90091-B) PubMed DOI

Vinogradov A. 1995. Nucleotypic effect in homeotherms: body-mass-corrected basal metabolic rate of mammals is related to genome size. Evolution 49, 1249–125910.2307/2410449 (doi:10.2307/2410449) PubMed DOI

Starostova Z., Kratochvil L., Frynta D. 2005. Dwarf and giant geckos from the cellular perspective: the bigger the animal, the bigger its erythrocytes? Funct. Ecol. 19, 744–74910.1111/j.1365-2435.2005.01020.x (doi:10.1111/j.1365-2435.2005.01020.x) DOI

Vinogradov A., Anatskaya O., Kudryavtsev B. 2001. Relationship of hepatocyte ploidy levels with body size and growth rate in mammals. Genome 44, 350–36010.1139/g01-015 (doi:10.1139/g01-015) PubMed DOI

Gregory T. 2005. The evolution of the genome. San Diego, CA: Elsevier

Nagl W. 1974. Mitotic cycle time in perennial and annual plants with various amounts of DNA and heterochromatin. Dev. Biol. 39, 342–346 PubMed

The smallest angiosperm genomes may be the price for effective traps of bladderworts

New estimates and synthesis of chromosome numbers, ploidy levels and genome size variation in Allium sect. Codonoprasum: advancing our understanding of the unresolved diversification and evolution of this section

Genome size is strongly linked to carbohydrate storage and weakly linked to root sprouting ability in herbs

Stoichiometry versus ecology: the relationships between genome size and guanine-cytosine content, and tissue nitrogen and phosphorus in grassland herbs

Shoot apical meristem and plant body organization: a cross-species comparative study

Genome size as a key to evolutionary complex aquatic plants: polyploidy and hybridization in Callitriche (Plantaginaceae)

Continuous morphological variation correlated with genome size indicates frequent introgressive hybridization among Diphasiastrum species (Lycopodiaceae) in Central Europe

Ecological effects of cell-level processes: genome size, functional traits and regional abundance of herbaceous plant species