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Wendel, J. F.

Publications and source records attributed to Wendel, J. F..

At least 19 recordsLinked to original sources

Four genome assemblies of new wild Gossypium hirsutum accessions from the Yucatan Peninsula, the center of domestication

Gossypium hirsutum is a leading source of natural cotton fiber, accounting for most of the market share. While domestication and improvement have led to significant gains in fiber quantity and quality, the narrow germplasm base of modern cultivars creates vulnerabilities, including to emerging pests. Wild populations provide a reservoir for genetic diversity that may be valuable in identifying and transferring resistance or stress-adaptation alleles to modern breeding lines. Here we report four new genome assemblies of G. hirsutum representing distinct populations from its center of diversity in Yucatan, Mexico. These chromosome-level assemblies are highly contiguous and structurally similar to existing G. hirsutum genomes; however, comparative analyses highlight their distinctiveness, suggesting they form a valuable reservoir of untapped diversity. Preliminary analyses of nucleotide-binding leucine-rich repeat (NLR) immune receptor genes underscore this variation, suggesting presence-absence variation may exist among populations. These findings demonstrate the potential of these new genomic resources for discovery of novel disease resistance alleles and, generally, for expanding the narrow germplasm base of the modern cotton cultivars.

genomics↗

Population Genomics Informs Conservation Strategies for Critically Endangered Kokia Species in Hawaii

Island endemic species are particularly vulnerable to extinction due to their limited geographic ranges and small population sizes. Kokia is a genus found exclusively in the Hawaiian Islands, whose species were once major components of local forests but have experienced significant population reductions due to habitat destruction and the consequences of invasive species. Although conservation of Kokia species has been an ongoing topic for over a century, records regarding historical efforts are sparse. Recently generated genomes for each of the three extant species provide the foundation for understanding genetic diversity and population structure for future conservation work. Whole genome resequencing of K. cookei (n = 23 samples), K. drynarioides (n = 92), and K. kauaiensis (n = 45) suggests that K. drynarioides has the lowest overall diversity, reflecting propagation from a limited part of the remaining gene pool, whereas K. kauaiensis exhibits the most diversity. Diversity in the primarily graft-propagated K. cookei is higher than expected, and slightly higher than in the free-living K. drynarioides. Notably, our analyses identified a source of novel variation in K. cookei in a cultivated plant historically labeled K. drynarioides. Population structure analyses reveal a single population for K. cookei, but three groups for each of the other two species. Importantly, our analyses identify clusters of related individuals, reflected in genetic distance and clustering metrics, which provide valuable information for increasing diversity in managed populations and in ex situ conservation collections. These results provide a genomic framework for ongoing efforts in restoring and maintaining diversity in these critically endangered Hawaiian species.

genomics↗

Sewing the future of cotton: a multi-omics study combining nanomechanics, transcriptomics, and phenotypic traits

Cellulose microfibrils that are essential for mechanical strength and overall quality of cotton fibers. This study quantifies and compares the nanoscale structural and mechanical properties of cellulose microfibrils such as microfibril dimensions, crossover count and angles, roughness, and Youngs modulus for two popular cotton species: Gossypium hirsutum (Gh) and Gossypium barbadense (Gb) fibers across four growth stages (8, 12, 18, and 22 days post-anthesis) using atomic force microscopy (AFM). Our results revealed for the first time that Gb fibers exhibit a better alignment, finer dimensions, and higher stiffness compared to Gh fibers at nanoscale, resulting in smoother fiber surfaces, and improved quality at macroscale. We are also the first to develop machine-learning models to predict macroscale phenotypic traits specifically boll length and cellulose content using nanoscale features alone and in combination with multi-omics modalities, substantially enhancing the predictive accuracy and highlighting opportunities for robust cross-species modeling of cotton fiber traits.

biophysics↗

Comparative multi-omics profiling of Gossypium hirsutum and Gossypium barbadense fibers at high temporal resolution reveals key differences in polysaccharide composition and associated glycosyltransferases

Among the two allopolyploid cultivated species of cotton, Gossypium barbadense is known for its superior quality fiber compared to G. hirsutum. Length and strength are key determinants of the fiber quality. Although the mature fibers are dried cell walls consisting mainly cellulose, the dynamic remodeling of pectin, xyloglucan, and xylan polysaccharides during fiber growth significantly impact the final fiber quality. Comprehensive knowledge about polysaccharides and their biosynthesis during fiber development of the cultivated species is important for improving fiber quality. In this study, comparative large-scale glycome, transcriptome and proteome profiling were conducted daily on fibers of both cotton species covering critical stages of fiber development spanning primary cell wall synthesis and the transition to secondary wall synthesis. Interspecific comparisons revealed that a delayed accumulation of cellulose content, as well as the occurrence of lower levels and differential compositions of non-fucosylated/fucosylated xyloglucans, homogalacturonans, and highly branched Rhamnogalacturonan-I polysaccharides might be contributing to longer fiber phenotypes of G. barbadense relative to G. hirsutum. Our study also suggests, differential temporal compositions of heteroxylans might contribute to variation in cellulose microfibril arrangement and strength of fiber exists between the two species of cotton. Comparative transcriptomic analysis identified differentially expressed polysaccharide-synthesizing glycosyltransferases that might underlie fiber quality differences between the two species. Transcripts encoding many cell wall localized expansins were more abundant in G. barbadense than in G. hirsutum. Overall, these findings extend our knowledge regarding the molecular factors that contribute to fiber quality and provide insights for targeted cotton fiber improvement. SIGNIFICANCE STATEMENTComparative multi-omics profiling of two major commercial cotton species, Gossypium hirsutum and Gossypium barbadense revealed substantial differences in polysaccharide structures and expressed polysaccharide-synthesizing glycosyltransferases, that potentially contribute to differences in fiber length and strength. The molecular details elucidated in the present study contribute to the goal of improving fiber quality and its commercial value.

plant biology↗

Proteomics-based models of gene expression and cellular control of cotton fiber development

The shapes and material properties of cotton seed coat trichoblasts are the basis of a multibillion-dollar natural fiber industry. As such, these highly specialized cells are low-hanging fruit for intentional trait engineering. However, broad successes will require more mechanistic knowledge about their systems-level cellular controls. This time-series study integrates daily measurements of purified fiber transcriptomes and proteomes with multiscale fiber phenotyping datasets that span the same developmental interval. Abundance profiles of the subcellular proteomes are the foundation of the analyses. This resource article provides direct information concerning which homoeologs operate and informative depictions of how compartmentalized cellular systems change during developmental transitions. Prediction accuracy was partially validated by analysis of the protein expression group 11, which contained multiple known secondary cell wall cellulose synthases and dozens of unknown proteins and an averaged profile that was strongly correlated with a sharp state transition in cellulose microfibril alignment and increased cellulose content. The dataset as a whole can serve as a hypothesis-generating machine to guide future experiments that relate to cell shape and growth rate control, reversible tissue formation, and cell wall remodeling. Integration of mRNA and protein abundance revealed widespread evidence for post-transcriptional control. In addition, there were hundreds of transcriptionally controlled genes with differing timepoints of transition. This latter gene set can be used to more reliably analyze transcriptional control networks and to generate collections of gene expression drivers for cotton fiber research. The protein and transcript data are organized into user-friendly tables and a web interface that can be searched using any plant ortholog of interest based on developmental time, abundance, annotations, or phenotypic association.

plant biology↗

Developmental variability in cotton fiber cell wall properties linked to important agronomic traits

The economic value of cotton is based on its long, thin, strong, and twisted trichoblasts that emerge from the ovule epidermis. The mature dried fiber cell reflects the outcome of a rapid tapering of the nascent trichoblast, weeks of polarized diffuse growth, followed by a transition to persistent secondary cell wall synthesis. Highly conserved and dynamic microtubule and cellulose microfibril-based anisotropic growth control modules are central to all of these phases. In this paper, we developed novel quantitative phenotyping and computational modeling pipelines to analyze fiber growth behaviors at a daily resolution. We uncovered unexpected variability in growth rate, cell wall properties, and cell geometry across a critical window of fiber development. Finite element computational modeling of fiber growth was used to analyze the instability of cell diameter control and predict how spatial gradients of fiber and matrix material properties can interact to dictate the patterns of shape change. As an initial step toward gaining insight into the molecular orchestration of cellulose biosynthesis, expression profiles of a broad set of relevant genes were quantified across the same developmental timeline and correlated with fiber phenotypes. This analysis identified specific candidate genes that may serve as targets for fiber quality improvement.

plant biology↗

Dynamics of duplicated gene regulatory networks governing cotton fiber development following polyploidy

Cotton fiber development entails complex genome-wide gene regulatory networks (GRN) that remain mostly unexplored. Here we present integrative analyses of fiber GRNs using public RNA-seq datasets, integrated with multi-omics genomic, transcriptomic, and cistromic data. We detail the fiber co-expression dynamics and regulatory connections, validating findings with external datasets and transcription factor (TF) binding site data. We elucidate previously uncharacterized TFs that regulate genes involved in fiber-related functions and cellulose synthesis, and identify the regulatory role of two homoeologous G2-like transcription factors on fiber length. Analysis of duplicated gene expression and network relationships in allopolyploid cotton, which has two co-resident genomes (A, D), revealed novel aspects of asymmetric subgenomic developmental contributions. Whereas D-based homoeolog pairs drive higher overall gene expression from the D subgenome, TFs from the A subgenome play a preferential regulatory role in the fiber gene regulatory network. Following allopolyploid formation, it appears that the trans-regulatory roles of TFs diversified more rapidly between homoeologs than did the cis-regulatory elements of their target genes. Our approach underscores the utility of network analysis for detection of master regulators and provides fresh perspectives on fiber development and polyploid functional genomics, through the lens of co-expression and GRN dynamics.

bioinformatics↗

A high-resolution model of gene expression during Gossypium hirsutum (cotton) fiber development

Cotton fiber development relies on complex and intricate biological processes to transform newly differentiated fiber initials into the mature, extravagantly elongated cellulosic cells that are the foundation of this economically important cash crop. Here we extend previous research into cotton fiber development by employing controlled conditions to minimize variability and utilizing time-series sampling and analyses to capture daily transcriptomic changes from early elongation through the early stages of secondary wall synthesis (6 to 24 days post anthesis; DPA). A majority of genes are expressed in fiber, largely partitioned into two major coexpression modules that represent genes whose expression generally increases or decreases during development. Differential gene expression reveals a massive transcriptomic shift between 16 and 17 DPA, corresponding to the onset of the transition phase that leads to secondary wall synthesis. Subtle gene expression changes are captured by the daily sampling, which are discussed in the context of fiber development. Coexpression and gene regulatory networks are constructed and associated with phenotypic aspects of fiber development, including turgor and cellulose production. Key genes are considered in the broader context of plant secondary wall synthesis, noting their known and putative roles in cotton fiber development. The analyses presented here highlight the importance of fine-scale temporal sampling on understanding developmental processes and offer insight into genes and regulatory networks that may be important in conferring the unique fiber phenotype.

cell biology↗

Daily glycome and transcriptome profiling reveals polysaccharide structures and glycosyltransferases critical for cotton fiber growth

Cotton fiber length and strength are key determinants of its quality. Dynamic changes in the pectin, xyloglucan, xylan, and cellulose polysaccharide epitopes content during fiber growth contribute to complex remodeling of fiber cell wall (CW) and quality. Detailed knowledge about polysaccharide compositional and structural alteration in the fiber during fiber elongation and strengthening is vastly limited. Here, large-scale glycome profiling coupled with fiber phenotype and transcriptome profiling was conducted on fiber collected daily covering the most critical fiber developmental window. High temporal resolution profiling allowed us to identify specific polysaccharide epitopes associated with distinct fiber phenotypes that might contribute to fiber quality. This study revealed the critical role of highly branched RG-I pectin epitopes such as, {beta}-1,4-linked-galactans, {beta}-1,6-linked-galactans, and arabinogalactans, in addition to earlier reported homogalacturonans and xyloglucans in the formation of cotton-fiber-middle-lamella and contributing to fiber plasticity and elongation. We also propose the essential role of heteroxylans (Xyl-MeGlcA and Xyl-3Ar), as a guiding factor for secondary CW cellulose-microfibril arrangement, thus contributing to fiber strength. Correlation analysis of glycome and transcriptome data identified several key putative glycosyltransferases involved in synthesizing the critical polysaccharide epitopes. Novel details discovered here provide a foundation to identify molecular factors that dictate important fiber traits.

plant biology↗

Genomic diversity and evolution in the Hawaiian Islands endemic Kokia (Malvaceae)

Island species are highly vulnerable due to habitat destruction and their often small population sizes with reduced genetic diversity. The Hawaiian Islands constitute the most isolated archipelago on the planet, harboring many endemic species. Kokia is an endangered flowering plant genus endemic to these islands, encompassing three extant and one extinct species. Recent studies provided evidence of unexpected genetic diversity within Kokia. Here, we provide high quality genome assemblies for all three extant Kokia species, including an improved genome for K. drynarioides. All three Kokia genomes contain 12 chromosomes exhibiting high synteny within and between Kokia and the sister taxon Gossypioides kirkii. Gene content analysis revealed a net loss of genes in K. cookei compared to other species, whereas the gene complement in K. drynarioides remains stable and that of K. kauaiensis displays a net gain. A dated phylogeny estimates the divergence time from the last common ancestor for the three Kokia species at [~]1.2 million years ago (mya), with the sister taxa [K. cookei + K. drynarioides] diverging [~]0.8 mya. Kokia appears to have followed a stepping-stone pattern of colonization and diversification of the Hawaiian Archipelago, likely starting on low or now submerged older islands. The genetic resources provided may benefit conservation efforts of this endangered endemic genus.

genomics↗

The Gossypium herbaceum L. Wagad genome as a resource for understanding cotton domestication

Gossypium herbaceum is a species of cotton native to Africa and Asia that is one of the two domesticated diploids. Together with its sister-species G. arboreum, these A-genome taxa represent models of the extinct A-genome donor of modern polyploid cotton, which provide about 95% of cotton grown worldwide. As part of a larger effort to characterize variation and improve resources among diverse diploid and polyploid cotton genomes, we sequenced and assembled the genome of G. herbaceum cultivar (cv) Wagad, representing the first domesticated accession for this species. This chromosome-level genome was generated using a combination of PacBio long-read technology, HiC, and Bionano optical mapping and compared to existing genome sequences in cotton. We compare the genome of this cultivar to the existing genome of wild G. herbaceum subspecies africanum to elucidate changes in the G. herbaceum genome concomitant with domestication, and extend these analyses to gene expression using available RNA-seq. Our results demonstrate the utility of the G. herbaceum cv Wagad genome in understanding domestication in the diploid species, which could inform modern breeding programs.

genomics↗

Organellar transcripts dominate the cellular mRNA pool across plants of varying ploidy levels

Mitochondrial and plastid functions depend on coordinated expression of proteins encoded by genomic compartments that have radical differences in copy number of organellar and nuclear genomes. In polyploids, doubling of the nuclear genome may add challenges to maintaining balanced expression of proteins involved in cytonuclear interactions. Here, we use ribo-depleted RNA-seq to analyze transcript abundance for nuclear and organellar genomes in leaf tissue from four different polyploid angiosperms and their close diploid relatives. We find that, even though plastid genomes contain <1% of the number of genes in the nuclear genome, they generate the majority (69.9-82.3%) of mRNA transcripts in the cell. Mitochondrial genes are responsible for a much smaller percentage (1.3-3.7%) of the leaf mRNA pool but still produce much higher transcript abundances per gene compared to nuclear genome. Nuclear genes encoding proteins that functionally interact with mitochondrial or plastid gene products exhibit mRNA expression levels that are consistently more than ten-fold lower than their organellar counterparts, indicating an extreme cytonuclear imbalance at the RNA level despite the predominance of equimolar interactions at the protein level. Nevertheless, interacting nuclear and organellar genes show strongly correlated transcript abundances across functional categories, suggesting that the observed mRNA stoichiometric imbalance does not preclude coordination of cytonuclear expression. Finally, we show that nuclear genome doubling does not alter the cytonuclear expression ratios observed in diploid relatives in consistent or systematic ways, indicating that successful polyploid plants are able to compensate for cytonuclear perturbations associated with nuclear genome doubling.

plant biology↗

Variation in cytonuclear expression accommodation among allopolyploid plants

Cytonuclear coevolution is a common feature among plants, which coordinates gene expression and protein products between the nucleus and organelles. Consequently, lineage-specific differences may result in incompatibilities between the nucleus and cytoplasm in hybrid taxa. Allopolyploidy is also a common phenomenon in plant evolution. The hybrid nature of allopolyploids may result in cytonuclear incompatibilities, but the massive nuclear redundancy created during polyploidy affords additional avenues for resolving cytonuclear conflict (i.e., cytonuclear accommodation). Here we evaluate expression changes in organelle-targeted nuclear genes for six allopolyploid lineages that represent four genera (i.e., Arabidopsis, Arachis, Chenopodium, and Gossypium) and encompass a range in polyploid ages. Because incompatibilities between the nucleus and cytoplasm could potentially result in biases toward the maternal homoeolog and/or maternal expression level, we evaluate patterns of homoeolog usage, expression bias, and expression level dominance in cytonuclear genes relative to the background of non-cytonuclear expression changes and to the diploid parents. Although we find subsets of cytonuclear genes in most lineages that match our expectations of maternal preference, these observations are not consistent among either allopolyploids or categories of organelle-targeted genes. Our results indicate that cytonuclear expression accommodation may be a subtle and/or variable phenomenon that does not capture the full range of mechanisms by which allopolyploid plants resolve nuclear-cytoplasmic incompatibilities.

evolutionary biology↗

Dual domestication, diversity, and differential introgression in Old World cotton diploids

Domestication in the cotton genus is remarkable in that it has occurred independently four different times at two different ploidy levels. Relatively little is known about genome evolution and domestication in the cultivated diploid species Gossypium herbaceum and G. arboreum, because of the absence of wild representatives for the latter species, their ancient domestication, and their joint history of human-mediated dispersal and interspecific gene flow. Using in-depth resequencing of a broad sampling from both species, we confirm their independent domestication, as opposed to a progenitor-derivative relationship, showing that diversity (mean {pi} = 2.3x10-3) within species is similar, and that divergence between species is modest (weighted FST=0.4430). Individual accessions were homozygous for ancestral SNPs at over half of variable sites, while fixed, derived sites were at modest frequencies. Notably, two chromosomes with a paucity of fixed, derived sites (i.e., chromosomes 7 and 10) were also strongly implicated in introgression analyses. Collectively, these data demonstrate variable permeability to introgression among chromosomes, which we propose is due to divergent selection under domestication and/or the phenomenon of F2 breakdown in interspecific crosses. Our analyses provide insight into the evolutionary forces influencing diversity and divergence in the diploid cultivated species, and establish a foundation for understanding the contribution of introgression and/or strong parallel selection to the extensive morphological similarities shared between species. Significance statementThe cotton genus (Gossypium) contains four different species that were independently domesticated at least 4,000 years ago. Relatively little is understood about diversity and evolution in the two diploid African-Asian sister-species G. herbaceum and G. arboreum, despite their historical importance in the region and contemporary cultivation, largely in the Indian subcontinent. Here we address questions regarding the relationship between the two species, their contemporary levels of diversity, and their patterns of interspecific gene flow accompanying their several millennia history of human-mediated dispersal and contact. We validate independent domestication of the two species and document the genomic distribution of interspecific genetic exchange.

evolutionary biology↗

Deleterious Mutations Accumulate Faster in Allopolyploid than Diploid Cotton (Gossypium) and Unequally Between Subgenomes

Whole genome duplication (polyploidization) is among the most dramatic mutational processes in nature, so understanding how natural selection differs in polyploids relative to diploids is an important goal. Population genetics theory predicts that recessive deleterious mutations accumulate faster in allopolyploids than diploids due to the masking effect of redundant gene copies, but this prediction is hitherto unconfirmed. Here, we use the cotton genus (Gossypium), which contains seven allopolyploids derived from a single polyploidization event 1-2 million years ago, to investigate deleterious mutation accumulation. We use two methods of identifying deleterious mutations at the nucleotide and amino acid level, along with whole-genome resequencing of 43 individuals spanning six allopolyploid species and their two diploid progenitors, to demonstrate that deleterious mutations accumulate faster in allopolyploids than in their diploid progenitors. We find that, unlike what would be expected under models of demographic changes alone, strongly deleterious mutations show the biggest difference between ploidy levels, and this effect diminishes for moderately and mildly deleterious mutations. We further show that the proportion of nonsynonymous mutations that are deleterious differs between the two co-resident subgenomes in the allopolyploids, suggesting that homoeologous masking acts unequally between subgenomes. Our results provide a genome-wide perspective on classic notions of the significance of gene duplication that likely are broadly applicable to allopolyploids, with implications for our understanding of the evolutionary fate of deleterious mutations. Finally, we note that some measures of selection (e.g. dN/dS,{pi} N/{pi}S) may be biased when species of different ploidy levels are compared.

evolutionary biology↗

Global patterns of subgenome evolution in organelle-targeted genes of sixallotetraploid angiosperms

Whole-genome duplications (WGDs), in which the number of nuclear genome copies is elevated as a result of autopolyploidy or allopolyploidy, are a prominent process of diversification in eukaryotes. The genetic and evolutionary forces that WGD imposes upon cytoplasmic genomes are not well understood, despite the central role that cytonuclear interactions play in eukaryotic function and fitness. Cellular respiration and photosynthesis depend upon successful interaction between the 3000+ nuclear-encoded proteins destined for the mitochondria or plastids and the gene products of cytoplasmic genomes in multi-subunit complexes such as OXPHOS, organellar ribosomes, Photosystems I and II, and Rubisco. Allopolyploids are thus faced with the critical task of coordinating interactions between nuclear and cytoplasmic genes that were inherited from different species. Because cytoplasmic genomes share a more recent history of common descent with the maternal nuclear subgenome than the paternal subgenome, evolutionary "mismatches" between the paternal subgenome and the cytoplasmic genomes in allopolyploids might lead to accelerated rates of evolution in the paternal homoeologs of allopolyploids, either through relaxed purifying selection or strong directional selection to rectify these mismatches. We tested this hypothesis in maternal vs. paternal copies of organelle-targeted genes in six allotetraploids: Brachypodium hybridum, Chenopodium quinoa, Coffea arabica, Gossypium hirsutum, Nicotiana tabacum, and Triticum dicoccoides. We report evidence that allopolyploid subgenomes exhibit unequal rates of protein-sequence evolution, but we did not observe global effects of cytonuclear incompatibilities on paternal homoeologs of organelle-targeted genes. Analyses of gene content revealed mixed evidence for whether organelle-targeted genes re-diploidize more rapidly than non-organelle-targeted genes. Together, these global analyses provide insights into the complex evolutionary dynamics of allopolyploids, showing that allopolyploid subgenomes have separate evolutionary trajectories despite sharing the same nucleus, generation time, and ecological context. AUTHOR SUMMARY Whole genome duplication, in which the size and content of the nuclear genome is instantly doubled, represents one of the most profound forms of mutational change. The consequences of duplication events are equally monumental, especially considering that almost all eukaryotes have undergone whole genome duplications during their evolutionary history. While myriad genetic, cellular, organismal, and ecological effects of whole genome duplications have been extensively documented, relatively little attention has been paid to the diminutive but essential "other" genomes present inside the cell, those of chloroplasts and mitochondria. In this study, we compared the evolutionary patterns of >340,000 genes from 23 species to test whether whole genome duplications are associated with genetic mismatches between the nuclear, mitochondrial, and chloroplast genomes. We discovered tremendous differences between duplicated copies of nuclear genomes; however, mitochondria-nuclear and chloroplast-nuclear mismatches do not appear to be common following whole genome duplications. Together these genomic data represent the most extensive analysis yet performed on how polyploids maintain the delicate and finely tuned balance between the nuclear, mitochondrial, and chloroplast genomes.

evolutionary biology↗

The Gossypium anomalum genome as a resource for cotton improvement and evolutionary analysis of hybrid incompatibility

Cotton is an important crop that has been the beneficiary of multiple genome sequencing efforts, including diverse representatives of wild species for germplasm development. Gossypium anomalum is a wild African diploid species that harbors stress-resistance and fiber-related traits with potential application to modern breeding efforts. In addition, this species is a natural source of cytoplasmic male sterility and a resource for understanding hybrid lethality in the genus. Here we report a high-quality de novo genome assembly for G. anomalum and characterize this genome relative to existing genome sequences in cotton. In addition, we use the synthetic allopolyploids 2(A2D1) and 2(A2D3) to discover regions in the G. anomalum genome potentially involved in hybrid lethality, a possibility enabled by introgression of regions homologous to the D3 (G. davidsonii) lethality loci into the synthetic 2(A2D3) allopolyploid.

genomics↗

Nuclear-cytoplasmic balance: whole genome duplications induce elevated organellar genome copy number

The plant genome is partitioned across three distinct subcellular compartments: the nucleus, mitochondria, and plastids. Successful coordination of gene expression among these organellar genomes and the nuclear genome is critical for plant function and fitness. Whole genome duplication events (WGDs) in the nucleus have played a major role in the diversification of land plants and are expected to perturb the relative copy number (stoichiometry) of nuclear, mitochondrial, and plastid genomes. Thus, elucidating the mechanisms whereby plant cells respond to the cytonuclear stoichiometric imbalance that follow WGDs represents an important yet underexplored question in understanding the evolutionary consequences of genome doubling. We used droplet digital PCR (ddPCR) to investigate the relationship between nuclear and organellar genome copy numbers in allopolyploids and their diploid progenitors in both wheat and Arabidopsis. Polyploids exhibit elevated organellar genome copy numbers per cell, largely preserving the cytonuclear stoichiometry observed in diploids despite the change in nuclear genome copy number. To investigate the timescale over which cytonuclear stoichiometry may respond to WGD, we also estimated organellar genome copy number in Arabidopsis synthetic autopolyploids and in a haploid-induced diploid line. We observed corresponding changes in organellar genome copy number in these laboratory-generated lines, indicating that at least some of the cellular response to cytonuclear stoichiometric imbalance is immediate following WGD. We conclude that increases in organellar genome copy numbers represent a common response to polyploidization, suggesting that maintenance of cytonuclear stoichiometry is an important component in establishing polyploid lineages. Significance StatementWhole genome duplications (WGD) have the potential to alter the stoichiometric balance between nuclear and organellar genomes. We used two separate diploid-polyploid complexes to show that plant cells with WGD exhibit elevated mitochondrial and plastid genome copy numbers, both immediately in lab-generated lines and in natural polyploids.

evolutionary biology↗