Patterns and Evolution of Nucleotide Landscapes in Seed Plants

288

220

Genomic DNA base composition (GC content) is predicted to significantly affect genome functioning and species ecology. Although several hypotheses have been put forward to address the biological impact of GC content variation in microbial and vertebrate organisms, the biological significance of GC content diversity in plants remains unclear because of a lack of sufficiently robust genomic data. Using flow cytometry, we report genomic GC contents for 239 species representing 70 of 78 monocot families and compare them with genomic characters, a suite of life history traits and climatic niche data using phylogeny-based statistics. GC content of monocots varied between 33.6% and 48.9%, with several groups exceeding the GC content known for any other vascular plant group, highlighting their unusual genome architecture and organization. GC content showed a quadratic relationship with genome size, with the decreases in GC content in larger genomes possibly being a consequence of the higher biochemical costs of GC base synthesis. Dramatic decreases in GC content were observed in species with holocentric chromosomes, whereas increased GC content was documented in species able to grow in seasonally cold and/or dry climates, possibly indicating an advantage of GC-rich DNA during cell freezing and desiccation. We also show that genomic adaptations associated with changing GC content might have played a significant role in the evolution of the Earth's contemporary biota, such as the rise of grass-dominated biomes during the mid-Tertiary. One of the major selective advantages of GC-rich DNA is hypothesized to be facilitating more complex gene regulation.plant genome | genome size evolution | Poaceae | phylogenetic regression | geographical stratification D eep insights into the genomic architecture of model plants are rapidly accumulating, especially because of advances being made in high-throughput next generation and third generation sequencing techniques (1). However, the genomic constitution of the vast majority of nonmodel plants still remains unknown (2), impeding our understanding of the relationship between particular genomic architectures and evolutionary fitness in various environments. One of the important qualitative aspects of genomic architecture is the genomic nucleotide composition, which is usually expressed as the proportion of guanine and cytosine bases in the DNA molecule (GC content). In prokaryotes, the GC content is a well-studied and widely used character in taxonomy (3), and numerous studies have shown both the impact of GC content on microbial ecology and the influence of the environment in shaping the DNA base composition of microbial communities (4-7). The DNA base composition is also frequently discussed in relation to the evolution of the isochore structure in humans and other homeothermic (warm-blooded) vertebrates (i.e., birds and mammals) (8-10). In contrast, considerably less attention has been paid to the biological relevance of genomic GC content variation in plants (11), with genomic GC co...

Section: Resultsmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Ecological and evolutionary significance of genomic GC content diversity in monocots

Šmarda

Bureš

Horová

et al. 2014

288

220

“…According to this model, GC-biased gene conversion results from the GC bias of the mismatch repair machinery, so highly recombinogenic genes, which would form heteroduplexes at a higher frequency, would tend to be more GC rich. Recently, it was shown that grasses, in general, display strongly decreasing GC gradients along transcripts (42), and it was suggested that GC-biased gene conversion would explain them if gene conversion was higher at the 5′ end of grass genes. Except for the sharp reversal at the 3′ end, which may not be a universal feature of bz haplotypes, the 5′ to 3′ bz gene conversion gradient described here would support that suggestion.…”

Section: Discussionmentioning

confidence: 99%

Polarized gene conversion at the bz locus of maize

Dooner

2014

Nucleotide diversity is greater in maize than in most organisms studied to date, so allelic pairs in a hybrid tend to be highly polymorphic. Most recombination events between such pairs of maize polymorphic alleles are crossovers. However, intragenic recombination events not associated with flanking marker exchange, corresponding to noncrossover gene conversions, predominate between alleles derived from the same progenitor. In these dimorphic heterozygotes, the two alleles differ only at the two mutant sites between which recombination is being measured. To investigate whether gene conversion at the bz locus is polarized, two large diallel crossing matrices involving mutant sites spread across the bz gene were performed and more than 2,500 intragenic recombinants were scored. In both diallels, around 90% of recombinants could be accounted for by gene conversion. Furthermore, conversion exhibited a striking polarity, with sites located within 150 bp of the start and stop codons converting more frequently than sites located in the middle of the gene. The implications of these findings are discussed with reference to recent data from genome-wide studies in other plants.meiotic recombination | conversion polarity

“…In light of the association between seedling MNase HS regions and recombination hotspots, we tested whether MNase HS regions are also enriched for tracts of GC-biased gene conversion. Conversion tracts arise when base mismatches at recombination junctions resolve in favor of G+C nucleotides relative to A+T nucleotides (15,16). We assessed the historical influence of GC-biased gene conversion on the maize lineage, using PHASTbias with an alignment of 12 monocots and eudicots (17), although limiting the alignment to only grasses had no significant effect (SI Appendix, Fig.…”

Section: Strong Sustained Gc-biased Gene Conversion Surrounds Mnase Hsmentioning

confidence: 99%

Open chromatin reveals the functional maize genome

Rodgers-Melnick

Vera

Bass

et al. 2016

266

276

Cellular processes mediated through nuclear DNA must contend with chromatin. Chromatin structural assays can efficiently integrate information across diverse regulatory elements, revealing the functional noncoding genome. In this study, we use a differential nuclease sensitivity assay based on micrococcal nuclease (MNase) digestion to discover open chromatin regions in the maize genome. We find that maize MNase-hypersensitive (MNase HS) regions localize around active genes and within recombination hotspots, focusing biased gene conversion at their flanks. Although MNase HS regions map to less than 1% of the genome, they consistently explain a remarkably large amount (∼40%) of heritable phenotypic variance in diverse complex traits. MNase HS regions are therefore on par with coding sequences as annotations that demarcate the functional parts of the maize genome. These results imply that less than 3% of the maize genome (coding and MNase HS regions) may give rise to the overwhelming majority of phenotypic variation, greatly narrowing the scope of the functional genome.A ll cellular processes involving the nuclear DNA, including transcription, recombination, and replication, must contend with local chromatin states. Each of these processes can affect phenotypic variation, either directly or through constraints on natural selection. To date, humans and several model systems with small genomes have had their chromatin landscapes wellcharacterized (1-4). However, with a limited number of wellstudied large, complex genomes, many general principles relating chromatin structure to genome regulation remain unknown. Here, we examine the large genome of maize (Zea mays L.), a model crop species. The importance of maize within international agriculture motivates our central question: Which portions of the genome contribute to quantitative trait variation? Several features of maize biology, such as the capacity for large controlled crosses, rapid decay of linkage disequilibrium (LD), high genetic diversity, and substantial spacing between genes, make it an excellent experimental system for pursuing this question.Fine-scale characterization of the chromatin structural landscape requires an assay that can distinguish accessible (open) from condensed chromatin at the nucleosomal to subnucleosomal scales. In general, chromatin accessibility may be assayed through in situ digestion of the nuclear DNA with a non-sequence-specific nuclease, followed by quantification of the resulting DNA fragments (5). Micrococcal nuclease (MNase) cleaves DNA between nucleosomes, revealing genome-wide nucleosome occupancy (6, 7). However, differential sensitivity to MNase digestion also reveals chromatin accessibility, with genomic regions of open chromatin preferentially recovered under light-digestion relative to heavydigestion conditions (8). In maize, a differential MNase sensitivity assay with microarray quantification [differential nuclease sensitivity (DNS)-chip] demonstrated that MNase hypersensitive (MNase HS) regions are positively assoc...