Megacycles of atmospheric carbon dioxide concentration correlate with fossil plant genome size

Tectonic processes drive megacycles of atmospheric carbon dioxide (CO(2)) concentration, c(a), that force large fluctuations in global climate. With a period of several hundred million years, these megacycles have been linked to the evolution of vascular plants, but adaptation at the subcellular scale has been difficult to determine because fossils typically do not preserve this information. Here we show, after accounting for evolutionary relatedness using phylogenetic comparative methods, that plant nuclear genome size (measured as the haploid DNA amount) and the size of stomatal guard cells are correlated across a broad taxonomic range of extant species. This phylogenetic regression was used to estimate the mean genome size of fossil plants from the size of fossil stomata. For the last 400 Myr, spanning almost the full evolutionary history of vascular plants, we found a significant correlation between fossil plant genome size and c(a), modelled independently using geochemical data. The correlation is consistent with selection for stomatal size and genome size by c(a) as plants adapted towards optimal leaf gas exchange under a changing CO(2) regime. Our findings point to the possibility that major episodes of change in c(a) throughout Earth history might have selected for changes in genome size, influencing plant diversification.     

Mutational equilibrium model of genome size evolution

The paper describes a mutational equilibrium model of genome size evolution. This model is different from both adaptive and junk DNA models of genome size evolution in that it does not assume that genome size is maintained either by positive or stabilizing selection for the optimum genome size (as in adaptive theories) or by purifying selection against too much junk DNA (as in junk DNA theories). Instead the genome size is suggested to evolve until the loss of DNA through more frequent small deletions is equal to the rate of DNA gain through more frequent long insertions. The empirical basis for this theory is the finding of a strong correlation and of a clear power-function relationship between the rate of mutational DNA loss (per bp) through small deletions and genome size in animals. Genome size scales as a negative 1.3 power function of the deletion rate per nucleotide. Such a relationship is not predicted by either adaptive or junk DNA theories. However, if genome size is maintained at equilibrium by the balance of mutational forces, this empirilical relationship can be readily accommodated. Within this framework, this finding would imply that the rate of DNA gain through large insertions scales up a quarter-power function of genome size. On this view, as genome size grows, the rate of growth through large insertions is increasing as a quarter power function of genome size and the rate of DNA loss through small deletions increases linearly, until eventually, at the stable equilibrium genome size value, rates of growth and loss equal each other. The current data also suggest that the long-term variation is genome size in animals is brought about to a significant extent by changes in the intrinsic rates of DNA loss through small deletions. Both the origin of mutational biases and the adaptive consequences of such a mode of evolution of genome size are discussed.     

An evolutionary correlate of genome size change in plethodontid salamanders

Variation in the amount of nuclear DNA, the C-value, does not correlate with differences in morphological complexity. There are two classes of explanations for this observation, which is known as the ''C-value paradox''. The quantity of DNA may serve a ''nucleotypic'' function that is positively selected. Alternatively, large genomes may consist of junk DNA, which increases until it negatively affects fitness. Attempts to resolve the C-value paradox focus on the link between genome size and fitness. This link is usually sought in life history traits, particularly developmental rates. I examined the relationship among two life history traits, egg size and embryonic developmental time and genome size, in 15 species of plethodontid salamanders. Surprisingly, there is no correlation between egg size and developmental time, a relationship included in models of life history evolution. However, genome size is positively correlated with embryonic developmental time, a result that is robust with respect to many sources of variation in the data. Without information on the targets of natural selection it is not possible with these data to distinguish between nucleotypic and junk DNA explanations for the C-value paradox.     

Genome size evolution: sizing Mammalian genomes

The study of genome size (GS) and its variation is so fascinating to the scientific community because it constitutes the link between the present-day analytical and molecular studies of the genome and the old trunk of the holistic and synthetic view of the genome. The GS of several taxa vary over a broad range and do not correlate with the complexity of the organisms (the C-value paradox). However, the biology of transposable elements has let us reach a satisfactory view of the molecular mechanisms that give rise to GS variation and novelties, providing a less perplexing view of the significance of the GS (C-enigma). The knowledge of the composition and structure of a genome is a pre-requisite for trying to understand the evolution of the main genome signature: its size. The radiation of mammals provides an approximately 180-million-year test case for theories of how GS evolves. It has been found from data-mining GS databases that GS is a useful cyto-taxonomical instrument at the level of orders/superorders, providing genomic signatures characterizing Monotremata, Marsupialia, Afrotheria, Xenarthra, Laurasiatheria, and Euarchontoglires. A hypothetical ancestral mammalian-like GS of 2.9-3.7 pg has been suggested. This value appears compatible with the average values calculated for the high systematic levels of the extant Monotremata (～2.97 pg) and Marsupialia (～4.07 pg), suggesting invasion of mobile DNA elements concurrently with the separation of the older clades of Afrotheria (～5.5 pg) and Xenarthra (～4.5 pg) with larger GS, leaving the Euarchontoglires (～3.4 pg) and Laurasiatheria (～2.8 pg) genomes with fewer transposable elements. However, the paucity of GS data (546 mammalian species sized from 5,488 living species) for species, genera, and families calls for caution. Considering that mammalian species may be vanished even before they are known, GS data are sorely needed to phenotype the effects brought about by their variation and to validate any hypotheses on GS evolution in mammals.     

Karyotype diversity and genome size variation in Neotropical Maxillariinae orchids

• Orchidaceae is a widely distributed plant family with very diverse vegetative and floral morphology, and such variability is also reflected in their karyotypes. However, since only a low proportion of Orchidaceae has been analysed for chromosome data, greater diversity may await to be unveiled. Here we analyse both genome size (GS) and karyotype in two subtribes recently included in the broadened Maxillariinea to detect how much chromosome and GS variation there is in these groups and to evaluate which genome rearrangements are involved in the species evolution.
• To do so, the GS (14 species), the karyotype – based on chromosome number, heterochromatic banding and 5S and 45S rDNA localisation (18 species) – was characterised and analysed along with published data using phylogenetic approaches.
• The GS presented a high phylogenetic correlation and it was related to morphological groups in Bifrenaria (larger plants – higher GS). The two largest GS found among genera were caused by different mechanisms: polyploidy in Bifrenaria tyrianthina and accumulation of repetitive DNA in Scuticaria hadwenii. The chromosome number variability was caused mainly through descending dysploidy, and x=20 was estimated as the base chromosome number.
• Combining GS and karyotype data with molecular phylogeny, our data provide a more complete scenario of the karyotype evolution in Maxillariinae orchids, allowing us to suggest, besides dysploidy, that inversions and transposable elements as two mechanisms involved in the karyotype evolution. Such karyotype modifications could be associated with niche changes that occurred during species evolution.

     

Genome size variation in parrots: longevity and flying ability

Several hypotheses have been proposed to explain genome size variation in birds. However, no general consensus has been reached thus far. In this study, we analysed the inter- and intraspecific variation of genome size in some parrot species, and we tested the hypotheses that (1) weaker fliers have larger genomes, and (2) long-living species have lower DNA content. In general, parrots have a mean genome size (2.93 pg/nucleus) comparable to that of other avian orders. Amazona ochrocephala tresmariae has the highest genome size (4.30 pg/nucleus) among parrots. As expected, weaker flyers have larger genomes than better ones. In contrast to our prediction, we found a positive correlation between genome size and longevity. Finally, the species-group Amazona has a higher DNA content than the two groups Ara and Cacatua . Since oxidative stress is causally related to longevity, we suggest that DNA oxidative damage could have acted to some extent as a constraint on GS variation in parrots and perhaps also in other avian orders.     

Climate and growth form: the consequences for genome size in plants

The adaptive significance of nuclear DNA variation in angiosperms is still widely debated. The discussion mainly revolves round the causative factors influencing genome size and the adaptive consequences to an organism according to its growth form and environmental conditions. Nuclear DNA values are now known for 3874 angiosperm species (including 773 woody species) from over 219 families (out of a total of 500) and 181 species of woody gymnosperms, representing all the families. Therefore, comparisons have been made on not only angiosperms, taken as a whole, but also on the subsets of data based on taxonomic groups, growth forms, and environment. Nuclear DNA amounts in woody angiosperms are restricted to less than 23.54 % of the total range of herbaceous angiosperms; this range is further reduced to 6.8 % when woody and herbaceous species of temperate angiosperms are compared. Similarly, the tropical woody dicots are restricted to less than 50.5 % of the total range of tropical herbaceous dicots, while temperate woody dicots are restricted to less than 10.96 % of the total range of temperate herbaceous dicots. In the family Fabaceae woody species account for less than 14.1 % of herbaceous species. Therefore, in the total angiosperm sample and in subsets of data, woody growth form is characterized by a smaller genome size compared with the herbaceous growth form. Comparisons between angiosperm species growing in tropical and temperate regions show highly significant differences in DNA amount and genome size in the total angiosperm sample. However, when only herbaceous angiosperms were considered, significant differences were obtained in DNA amount, while genome size showed a non-significant difference. An atypical result was obtained in the case of woody angiosperms where mean DNA amount of tropical species was almost 25.04 % higher than that of temperate species, which is because of the inclusion of 85 species of woody monocots in the tropical sample. The difference becomes insignificant when genome size is compared. Comparison of tropical and temperate species among dicots and monocots and herbaceous monocots taken separately showed significant differences both in DNA amount and genome size. In herbaceous dicots, while DNA amount showed significant differences the genome size varies insignificantly. There was a non-significant difference among tropical and temperate woody dicots. In three families, i.e., Poaceae, Asteraceae, and Fabaceae the temperate species have significantly higher DNA amount and genome size than the tropical ones. Woody gymnosperms had significantly more DNA amount and genome size than woody angiosperms, woody eudicots, and woody monocots. Woody monocots also had significantly more DNA amount and genome size than woody eudicots. Lastly, there was no significant difference between deciduous and evergreen hardwoods. The significance of these results in relation to present knowledge on the evolution of genome size is discussed.     

Genome size and extinction risk in vertebrates

The hypothesis of 'selfish DNA' is tested for the case of animals using the relation between genome size and conservation status of a given species. In contrast to plants, where the larger genome was previously shown to increase the likelihood of extinction, the picture is more complicated in animals. At the within-families and within-orders levels, the larger genome increases the risk of extinction only in reptiles and birds (which have the smallest genomes among tetrapods). In fishes and amphibians, the effect is caused by the higher taxonomic levels (above order). In several phylogenetic lineages of anamniotes, there is a correlation between a higher fraction of threatened species and a lower number of extant species in a lineage with the larger genome. In mammals, no effect was observed at any taxonomic level. The obtained data support the concept of hierarchical selection. It is also shown that, in plants and reptiles, the probability of being threatened increases from less than 10% to more than 80% with the increase in genome size, which can help in establishing conservation priorities.     

The dynamic ups and downs of genome size evolution in Brassicaceae

Crucifers (Brassicaceae, Cruciferae) are a large family comprisingsome 338 genera and c. 3,700 species. The family includes importantcrops as well as several model species in various fields ofplant research. This paper reports new genome size (GS) datafor more than 100 cruciferous species in addition to previouslypublished C-values (the DNA amount in the unreplicated gameticnuclei) to give a data set comprising 185 Brassicaceae taxa,including all but 1 of the 25 tribes currently recognized. Evolutionof GS was analyzed within a phylogenetic framework based ongene trees built from five data sets (matK, chs, adh, trnLF,and ITS). Despite the 16.2-fold variation across the family,most Brassicaceae species are characterized by very small genomeswith a mean 1C-value of 0.63 pg. The ancestral genome size (ancGS)for Brassicaceae was reconstructed as ^anc1C = 0.50 pg. Approximately50% of crucifer taxa analyzed showed a decrease in GS comparedwith the ancGS. The remaining species showed an increase inGS although this was generally moderate, with significant increasesin C-value found only in the tribes Anchonieae and Physarieae.Using statistical approaches to analyze GS, evolutionary gainsor losses in GS were seen to have accumulated disproportionatelyfaster within longer branches. However, we also found that GShas not changed substantially through time and most likely evolvespassively (i.e., a tempo that cannot be distinguished betweenneutral evolution and weak forms of selection). The data revealan apparent paradox between the narrow range of small GSs overlong evolutionary time periods despite evidence of dynamic genomicprocesses that have the potential to lead to genome obesity(e.g., transposable element amplification and polyploidy). Toresolve this, it is suggested that mechanisms to suppress amplificationand to eliminate amplified DNA must be active in Brassicaceaealthough their control and mode of operation are still poorlyunderstood.     

Evolution of genome size: a phylogenetic test of the DNA loss hypothesis

It has been recently suggested that the C-value paradox, the lack of an obvious association between organismal complexity and genome size, can result simply from biases in insertion and deletion rates--the DNA loss hypothesis. This hypothesis has been heavily criticized, particularly because its evidence, a negative relationship between genome size and DNA loss rate, is based on a highly selective use of the available data. In this study it is show that even the even the most favorable interpretation of the data favoring the DNA loss hypothesis is largely an artifact of phylogenetic nonindependence, supporting the assertion made by other authors that the mechanisms underlying genome size evolution might be more complex than envisioned by the DNA loss hypothesis.     

Evolutionary dynamics of intron size, genome size, and physiological correlates in archosaurs

It has been proposed that intron and genome sizes in birds are reduced in comparison with mammals because of the metabolic demands of flight. To test this hypothesis, we examined the sizes of 14 introns in a nonflying relative of birds, the American alligator (Alligator mississippiensis), and in 19 flighted and flightless birds in 12 taxonomic orders. Our results indicate that a substantial fraction (66%) of the reduction in intron size as well as in genome size had already occurred in nonflying archosaurs. Using phylogenetically independent contrasts, we found that the proposed inverse correlation of genome size and basal metabolic rate (BMR) is significant among amniotes and archosaurs, whereas intron and genome size variation within birds showed no significant correlation with BMR. We show statistically that the distribution of genome sizes in birds and mammals is underdispersed compared with the Brownian motion model and consistent with strong stabilizing selection; that genome size differences between vertebrate clades are overdispersed and punctuational; and that evolution of BMR and avian intron size is consistent with Brownian motion. These results suggest that the contrast between genome size/BMR and intron size/BMR correlations may be a consequence of different intensities of selection for these traits and that we should not expect changes in intron size to be significantly associated with metabolically costly behaviors such as flight.     

Genome size correlates with reproductive fitness in seed beetles

The ultimate cause of genome size (GS) evolution in eukaryotes remains a major and unresolved puzzle in evolutionary biology. Large-scale comparative studies have failed to find consistent correlations between GS and organismal properties, resulting in the ‘C-value paradox’. Current hypotheses for the evolution of GS are based either on the balance between mutational events and drift or on natural selection acting upon standing genetic variation in GS. It is, however, currently very difficult to evaluate the role of selection because within-species studies that relate variation in life-history traits to variation in GS are very rare. Here, we report phylogenetic comparative analyses of GS evolution in seed beetles at two distinct taxonomic scales, which combines replicated estimation of GS with experimental assays of life-history traits and reproductive fitness. GS showed rapid and bidirectional evolution across species, but did not show correlated evolution with any of several indices of the relative importance of genetic drift. Within a single species, GS varied by 4–5% across populations and showed positive correlated evolution with independent estimates of male and female reproductive fitness. Collectively, the phylogenetic pattern of GS diversification across and within species in conjunction with the pattern of correlated evolution between GS and fitness provide novel support for the tenet that natural selection plays a key role in shaping GS evolution.     

Evolution of genome size: A phylogenetic test of the DNA loss hypothesis

It has been recently suggested that the C-value paradox, the lack of an obvious association between organismal complexity and genome size, can result simply from biases in insertion and deletion rates—the DNA loss hypothesis. This hypothesis has been heavily criticized, particularly because its evidence, a negative relationship between genome size and DNA loss rate, is based on a highly selective use of the available data. In this study it is shown that the even the most favorable interpretation of the data favoring the DNA loss hypothesis is largely an artifact of phylogenetic nonindependence, supporting the assertion made by other authors that the mechanisms underlying genome size evolution might be more complex than envisioned by the DNA loss hypothesis. The text was submitted by the author in English.     

The problem of the eukaryotic genome size

The current state of knowledge concerning the unsolved problem of the huge interspecific eukaryotic genome size variations not correlating with the species phenotypic complexity (C-value enigma also known as C-value paradox) is reviewed. Characteristic features of eukaryotic genome structure and molecular mechanisms that are the basis of genome size changes are examined in connection with the C-value enigma. It is emphasized that endogenous mutagens, including reactive oxygen species, create a constant nuclear environment where any genome evolves. An original quantitative model and general conception are proposed to explain the C-value enigma. In accordance with the theory, the noncoding sequences of the eukaryotic genome provide genes with global and differential protection against chemical mutagens and (in addition to the anti-mutagenesis and DNA repair systems) form a new, third system that protects eukaryotic genetic information. The joint action of these systems controls the spontaneous mutation rate in coding sequences of the eukaryotic genome. It is hypothesized that the genome size is inversely proportional to functional efficiency of the anti-mutagenesis and/or DNA repair systems in a particular biological species. In this connection, a model of eukaryotic genome evolution is proposed.     

Mechanisms of recent genome size variation in flowering plants

BACKGROUND AND AIMS: Plant nuclear genomes vary tremendously in DNA content, mostly due to differences in ancestral ploidy and variation in the degree of transposon amplification. These processes can increase genome size, but little is known about mechanisms of genome shrinkage and the degree to which these can attenuate or reverse genome expansion. This research focuses on characterizing DNA removal from the rice and Arabidopsis genomes, and discusses whether loss of DNA has effectively competed with amplification in these species. METHODS: Retrotransposons were analyzed for sequence variation within several element families in rice and Arabidopsis. Nucleotide sequence changes in the two termini of individual retrotransposons were used to date their time of insertion. KEY RESULTS: An accumulation of small deletions was found in both species, caused by unequal homologous recombination and illegitimate recombination. The relative contribution of unequal homologous recombination compared to illegitimate recombination was higher in rice than in Arabidopsis. However, retrotransposons are rapidly removed in both species, as evidenced by the similar apparent ages of intact elements (most less than 3 million years old) in these two plants and all other investigated plant species. CONCLUSIONS: Differences in the activity of mechanisms for retrotransposon regulation or deletion generation between species could explain current genome size variation without any requirement for natural selection to act on this trait, although the results do not preclude selection as a contributing factor. The simplest model suggests that significant genome size variation is generated by lineage-specific differences in the molecular mechanisms of DNA amplification and removal, creating major variation in nuclear DNA content that can then serve as the substrate for fitness-based selection.     

Coincidence,coevolution, or causation? DNA content,cellsize, and the C‐value enigma

Variation in DNA content has been largely ignored as a factor in evolution, particularly following the advent of sequence-based approaches to genomic analysis. The significant genome size diversity among organisms (more than 200000-fold among eukaryotes) bears no relationship to organismal complexity and both the origins and reasons for the clearly non-random distribution of this variation remain unclear. Several theories have been proposed to explain this 'C-value enigma' (heretofore known as the 'C-value paradox'), each of which can be described as either a mutation pressure' or 'optimal DNA' theory. Mutation pressure theories consider the large portion of non-coding DNA in eukaryotic genomes as either 'junk' or 'selfish' DNA and are important primarily in considerations of the origin of secondary DNA. Optimal DNA theories differ from mutation pressure theories by emphasizing the strong link between DNA content and cell and nuclear volumes. While mutation pressure theories generally explain this association with cell size as coincidental, the nucleoskeletal theory proposes a coevolutionary interaction between nuclear and cell volume, with DNA content adjusted adaptively following shifts in cell size. Each of these approaches to the C-value enigma is problematic for a variety of reasons and the preponderance of the available evidence instead favours the nucleotypic theory which postulates a causal link between bulk DNA amount and cell volume. Under this view, variation in DNA content is under direct selection via its impacts on cellular and organismal parameters. Until now, no satisfactory mechanism has been presented to explain this nucleotypic effect. However, recent advances in the study of cell cycle regulation suggest a possible 'gene nucleus interaction model' which may account for it. The present article provides a detailed review of the debate surrounding the C-value enigma, the various theories proposed to explain it, and the evidence in favour of a causal connection between DNA content and cell size. In addition, a new model of nucleotypic influence is developed, along with suggestions for further empirical investigation. Finally, some evolutionary implications of genome size diversity are considered, and a broadening of the traditional 'biological hierarchy' is recommended.     

Endopolyploidy in seed plants is differently correlated to systematics, organ, life strategy and genome size

Endopolyploidy is a systemic feature in seed plants. A negative correlation between genome size and endopolyploidization has been claimed previously, assuming that a minimum amount of DNA, necessary for certain cell functions, has to be acquired by endopolyploidization of the corresponding cells in plants with small genomes. This assumption was based on the analysis of only a limited set of data from few species. In the present study the endopolyploidization of several organs of 54 seed plant species belonging to two gymnosperm and 14 angiosperm families was investigated. The results revealed a low negative correlation between genome size and endopolyploidization. However, differences between the families, between the different organs of a given species and between the different life‐cycle types with regard to endopolyploidization became obvious. A three‐way analysis of variance with covariate to quantify the impact of the different factors on the extent of endopolyploidization suggested that taxonomic position is the major factor determining the degree of endopolyploidy within a species, while life cycle, genome size and organ type have a minor but also significant effect on endopolyploidization. The comparison of habitats of 16 investigated Central European species implies that endopolyploidization represents a mean to accelerate the growth of plant species in niches, which require and support fast development.     

Evolution of genome size in Brassicaceae

BACKGROUND AND AIMS: Brassicaceae, with nearly 340 genera and more than 3350 species, anchors the low range of angiosperm genome sizes. The relatively narrow range of DNA content (0.16 pg < 1C < 1.95 pg) was maintained in spite of extensive chromosomal change. The aim of this study was to erect a cytological and molecular phylogenetic framework for a selected subset of the Brassicacae, and use this as a template to examine genome size evolution in Brassicaceae. METHODS: DNA contents were determined by flow cytometry and chromosomes were counted for 34 species of the family Brassicaceae and for ten Arabidopsis thaliana ecotypes. The amplified and sequenced ITS region for 23 taxa (plus six other taxa with known ITS sequences) were aligned and used to infer evolutionary relationship by parsimony analysis. KEY RESULTS: DNA content in the species studied ranged over 8-fold (1C = 0.16-1.31 pg), and 4.4-fold (1C = 0.16-0.71 pg) excluding allotetraploid Brassica species. The 1C DNA contents of ten Arabidopsis thaliana ecotypes showed little variation, ranging from 0.16 pg to 0.17 pg. CONCLUSIONS: The tree roots at an ancestral genome size of approximately 1x = 0.2 pg. Arabidopsis thaliana (1C = 0.16 pg; approximately 157 Mbp) has the smallest genome size in Brassicaceae studied here and apparently represents an evolutionary decrease in genome size. Two other branches that represent probable evolutionary decreases in genome size terminate in Lepidium virginicum and Brassica rapa. Branches in the phylogenetic tree that represent probable evolutionary increases in genome size terminate in Arabidopsis halleri, A. lyrata, Arabis hirsuta, Capsella rubella, Caulanthus heterophyllus, Crucihimalaya, Lepidium sativum, Sisymbrium and Thlaspi arvense. Branches within one clade containing Brassica were identified that represent two ancient ploidy events (2x to 4x and 4x to 6x) that were predicted from published comparative mapping studies.     

不同生活型被子植物功能性状与基因组大小的关系

基因组大小在被子植物物种之间存在着巨大的变异, 但目前对不同生活型被子植物功能性状与基因组大小的关系缺乏统一的认识。本研究基于被子植物245科2,226属11,215个物种的基因组大小数据, 探讨了不同生活型物种种子重量、最大植株高度和叶片氮、磷含量4个功能性状与基因组大小之间的关系。结果表明, 被子植物最大植株高度和种子重量与基因组大小间的关系在草本和木本植物中存在显著差异。草本植物最大植株高度与基因组大小的关系不显著, 但种子重量与其呈极显著的正相关关系。木本植物最大植株高度与基因组大小显著负相关, 但种子重量与其关系不显著。木本植物叶片氮含量与基因组大小呈显著正相关, 但其他生活型植物的叶片氮、磷含量与基因组大小均无显著相关性。本研究表明被子植物功能性状与基因组大小的相关性在不同生活型间存在差异, 这为深入研究植物多种功能性状和植物生活型与基因组大小的权衡关系在植物演化和生态适应中的作用提供了重要依据。