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Root-knot nematodes (genus Meloidogyne) exhibit a diversity of reproductive modes ranging from obligatory sexual to fully asexual reproduction. Intriguingly, the most widespread and devastating species to global agriculture are those that reproduce asexually, without meiosis. To disentangle this surprising parasitic success despite the absence of sex and genetic exchanges, we have sequenced and assembled the genomes of three obligatory ameiotic and asexual Meloidogyne. We have compared them to those of relatives able to perform meiosis and sexual reproduction. We show that the genomes of ameiotic asexual Meloidogyne are large, polyploid and made of duplicated regions with a high within-species average nucleotide divergence of ~8%. Phylogenomic analysis of the genes present in these duplicated regions suggests that they originated from multiple hybridization events and are thus homoeologs. We found that up to 22% of homoeologous gene pairs were under positive selection and these genes covered a wide spectrum of predicted functional categories. To biologically assess functional divergence, we compared expression patterns of homoeologous gene pairs across developmental life stages using an RNAseq approach in the most economically important asexually-reproducing nematode. We showed that >60% of homoeologous gene pairs display diverged expression patterns. These results suggest a substantial functional impact of the genome structure. Contrasting with high within-species nuclear genome divergence, mitochondrial genome divergence between the three ameiotic asexuals was very low, signifying that these putative hybrids share a recent common maternal ancestor. Transposable elements (TE) cover a ~1.7 times higher proportion of the genomes of the ameiotic asexual Meloidogyne compared to the sexual relative and might also participate in their plasticity. The intriguing parasitic success of asexually-reproducing Meloidogyne species could be partly explained by their TE-rich composite genomes, resulting from allopolyploidization events, and promoting plasticity and functional divergence between gene copies in the absence of sex and meiosis.

An analysis of pancreatic ductal adenocarcinoma genomes indicates that many of these tumours undergo polyploidization and chromothripsis, leading to rapid acquisition of genetic changes required for tumour progression.

Investigators have long searched for a polyploidy paradigm—rules or principles that might be common following polyploidization (whole-genome duplication, WGD). Here we attempt to integrate what is known across the more thoroughly investigated polyploid systems on topics ranging from genetics to ecology. We found that while certain rules may govern gene retention and loss, systems vary in the prevalence of gene silencing vs. homeolog loss, chromosomal change, the presence of a dominant genome (in allopolyploids), and the relative importance of hybridization vs. genome doubling per se. In some lineages, aspects of polyploidization are repeated across multiple origins, but in other species multiple origins behave more stochastically in terms of genetic and phenotypic change. Our investigation also reveals that the path to synthesis is hindered by numerous gaps in our knowledge of even the best-known systems. Particularly concerning is the absence of linkage between genotype and phenotype. Moreover, most recent studies have focused on the genetic and genomic attributes of polyploidy, but rarely is there an ecological or physiological context. To promote a path to a polyploidy paradigm (or paradigms), we propose a major community goal over the next 10-20 yr to fill the gaps in our knowledge of well-studied polyploids. Before a meaningful synthesis is possible, more complete data sets are needed for comparison—systems that include comparable genetic, genomic, chromosomal, proteomic, as well as morphological, physiological, and ecological data. Also needed are more natural evolutionary model systems, as most of what we know about polyploidy continues to come from a few crop and genetic models, systems that often lack the ecological context inherent in natural systems and necessary for understanding the drivers of biodiversity.

Sugarcane, the world’s most harvested crop by tonnage, has shaped global history, trade and geopolitics, and is currently responsible for 80% of sugar production worldwide 1 . While traditional sugarcane breeding methods have effectively generated cultivars adapted to new environments and pathogens, sugar yield improvements have recently plateaued 2 . The cessation of yield gains may be due to limited genetic diversity within breeding populations, long breeding cycles and the complexity of its genome, the latter preventing breeders from taking advantage of the recent explosion of whole-genome sequencing that has benefited many other crops. Thus, modern sugarcane hybrids are the last remaining major crop without a reference-quality genome. Here we take a major step towards advancing sugarcane biotechnology by generating a polyploid reference genome for R570, a typical modern cultivar derived from interspecific hybridization between the domesticated species ( Saccharum officinarum ) and the wild species ( Saccharum spontaneum ). In contrast to the existing single haplotype (‘monoploid’) representation of R570, our 8.7 billion base assembly contains a complete representation of unique DNA sequences across the approximately 12 chromosome copies in this polyploid genome. Using this highly contiguous genome assembly, we filled a previously unsized gap within an R570 physical genetic map to describe the likely causal genes underlying the single-copy Bru1 brown rust resistance locus. This polyploid genome assembly with fine-grain descriptions of genome architecture and molecular targets for biotechnology will help accelerate molecular and transgenic breeding and adaptation of sugarcane to future environmental conditions. We build a polyploid reference genome for hybrid sugarcane cultivar R570, improving on its current ‘mosaic monoploid’ representation, enabling fine-grain description of genome architecture and the exploration of candidate genes underlying the Bru1 brown rust resistance locus.

Background Polyploidy or whole-genome duplication is now recognized as being present in almost all lineages of higher plants, with multiple rounds of polyploidy occurring in most extant species. The ancient evolutionary events have been identified through genome sequence analysis, while recent hybridization events are found in about half of the world’s crops and wild species. Building from this new paradigm for understanding plant evolution, the papers in this Special Issue address questions about polyploidy in ecology, adaptation, reproduction and speciation of wild and cultivated plants from diverse ecosystems. Other papers, including this review, consider genomic aspects of polyploidy. Approaches Discovery of the evolutionary consequences of new, evolutionarily recent and ancient polyploidy requires a range of approaches. Large-scale studies of both single species and whole ecosystems, with hundreds to tens of thousands of individuals, sometimes involving ‘garden’ or transplant experiments, are important for studying adaptation. Molecular studies of genomes are needed to measure diversity in genotypes, showing ancestors, the nature and number of polyploidy and backcross events that have occurred, and allowing analysis of gene expression and transposable element activation. Speciation events and the impact of reticulate evolution require comprehensive phylogenetic analyses and can be assisted by resynthesis of hybrids. In this Special Issue, we include studies ranging in scope from experimental and genomic, through ecological to more theoretical. Conclusions The success of polyploidy, displacing the diploid ancestors of almost all plants, is well illustrated by the huge angiosperm diversity that is assumed to originate from recurrent polyploidization events. Strikingly, polyploidization often occurred prior to or simultaneously with major evolutionary transitions and adaptive radiation of species, supporting the concept that polyploidy plays a predominant role in bursts of adaptive speciation. Polyploidy results in immediate genetic redundancy and represents, with the emergence of new gene functions, an important source of novelty. Along with recombination, gene mutation, transposon activity and chromosomal rearrangement, polyploidy and whole-genome duplication act as drivers of evolution and divergence in plant behaviour and gene function, enabling diversification, speciation and hence plant evolution.

Artificial polyploidy that brings about increase in cell size confers changes in histo-morphology leading to altered phenotype, causing changes in physiological attributes and enhanced concentration of secondary metabolites. The altered phenotype is generally a manifestation of tissue hardiness reflected as robust plant type. Based on a case study undertaken on an industrially important grass, Cymbopogon khasianus (2 n = 60) valued for its citral rich essential oil, here we report that the artificial polyploidy not only brings about enhancement in concentration of essential oil but also facilitates lodging tolerance. The latter is contributed by ploidy mediated changes that occur to the cells and tissues in various plant organs by way of increased wall thickening, tissue enhancement and epidermal depositions that enable robust features. An exhaustive illustrated account covering various micro-/macro-morphological, skeletal and histochemical features constituting growth and development vis-a-vis ploidy mediated changes is presented highlighting the novelties realized on account of induced polyploidy.

The growing wealth of knowledge on whole-plant genome sequences is highlighting the key role of transposable elements (TEs) in plant evolution, as a driver of drastic changes in genome size and as a source of an important number of new coding and regulatory sequences. Together with polyploidization events, TEs should thus be considered the major players in evolution of plants. This review outlines the major mechanisms by which TEs impact plant genome evolution and how polyploidy events can affect these impacts, and vice versa. These include direct effects on genes, by providing them with new coding or regulatory sequences, an effect on the epigenetic status of the chromatin close to genes, and more subtle effects by imposing diverse evolutionary constraints to different chromosomal regions. These effects are particularly relevant after polyploidization events. Polyploidization often induces bursts of transposition probably due to a relaxation in their epigenetic control, and, in the short term, this can increase the rate of gene mutations and changes in gene regulation due to the insertion of TEs next to or into genes. Over longer times, TE bursts may induce global changes in genome structure due to inter-element recombination including losses of large genome regions and chromosomal rearrangements that reduce the genome size and the chromosome number as part of a process called diploidization. TEs play an essential role in genome and gene evolution, in particular after polyploidization events. Polyploidization can induce TE activity that may explain part of the new phenotypes observed. TEs may also play a role in the diploidization that follows polyploidization events. However, the extent to which TEs contribute to diploidization and fractionation bias remains unclear. Investigating the multiple factors controlling TE dynamics and the nature of ancient and recent polyploid genomes may shed light on these processes.

[This corrects the article DOI: 10.1371/journal.pone.0192869.].