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The fate of 35S rRNA genes in the allotetraploid grass Brachypodium hybridum.

ABSTRACT: Nucleolar dominance (ND) consists of the reversible silencing of 35S/45S rDNA loci inherited from one of the ancestors of an allopolyploid. The molecular mechanisms by which one ancestral rDNA set is selected for silencing remain unclear. We applied a combination of molecular (Southern blot hybridization and reverse-transcription cleaved amplified polymorphic sequence analysis), genomic (analysis of variants) and cytogenetic (fluorescence in situ hybridization) approaches to study the structure, expression and epigenetic landscape of 35S rDNA in an allotetraploid grass that exhibits ND, Brachypodium hybridum (genome composition DDSS), and its putative progenitors, Brachypodium distachyon (DD) and Brachypodium stacei (SS). In progenitor genomes, B. stacei showed a higher intragenomic heterogeneity of rDNA compared with B. distachyon. In all studied accessions of B. hybridum, there was a reduction in the copy number of S homoeologues, which was accompanied by their inactive transcriptional status. The involvement of DNA methylation in CG and CHG contexts in the silencing of the S-genome rDNA loci was revealed. In the B. hybridum allotetraploid, ND is stabilized towards the D-genome units, irrespective of the polyphyletic origin of the species, and does not seem to be influenced by homoeologous 35S rDNA ratios and developmental stage.

SUBMITTER: Borowska-Zuchowska N

PROVIDER: S-EPMC7497271 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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The fate of 35S rRNA genes in the allotetraploid grass Brachypodium hybridum.

Borowska-Zuchowska Natalia N Kovarik Ales A Robaszkiewicz Ewa E Tuna Metin M Tuna Gulsemin Savas GS Gordon Sean S Vogel John P JP Hasterok Robert R

The Plant journal : for cell and molecular biology 20200703 5

Nucleolar dominance (ND) consists of the reversible silencing of 35S/45S rDNA loci inherited from one of the ancestors of an allopolyploid. The molecular mechanisms by which one ancestral rDNA set is selected for silencing remain unclear. We applied a combination of molecular (Southern blot hybridization and reverse-transcription cleaved amplified polymorphic sequence analysis), genomic (analysis of variants) and cytogenetic (fluorescence in situ hybridization) approaches to study the structure, ...[more]

PMID: 32506573

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Project description:Background:Allopolyploid plants often show wider environmental tolerances than their ancestors; this is expected to be due to the merger of multiple distinct genomes with a fixed heterozygosity. The complex homoeologous gene expression could have been evolutionarily advantageous for the adaptation of allopolyploid plants. Despite multiple previous studies reporting homoeolog-specific gene expression in allopolyploid species, there are no clear examples of homoeolog-specific function in acclimation to a long-term stress condition. Results:We found that the allopolyploid grass Brachypodium hybridum and its ancestor Brachypodium stacei show long-term heat stress tolerance, unlike its other ancestor, Brachypodium distachyon. To understand the physiological traits of B. hybridum, we compared the transcriptome of the 3 Brachypodium species grown under normal and heat stress conditions. We found that the expression patterns of approximately 26% and approximately 38% of the homoeolog groups in B. hybridum changed toward nonadditive expression and nonancestral expression, respectively, under normal condition. Moreover, we found that B. distachyon showed similar expression patterns between normal and heat stress conditions, whereas B. hybridum and B. stacei significantly altered their transcriptome in response to heat after 3 days of stress exposure, and homoeologs that were inherited from B. stacei may have contributed to the transcriptional stress response to heat in B. hybridum. After 15 days of heat exposure, B. hybridum and B. stacei maintained transcriptional states similar to those under normal conditions. These results suggest that an earlier response to heat that was specific to homoeologs originating from B. stacei contributed to cellular homeostasis under long-term heat stress in B. hybridum. Conclusions:Our results provide insights into different regulatory events of the homoeo-transcriptome that are associated with stress acclimation in allopolyploid plants.

Project description:Background and aimsIt is accepted that contemporary allopolyploid species have originated recurrently, but very few cases have been documented using multiple natural formations of the same species. To extend our knowledge, we have investigated the multiple origins, genetic variation and structure of the allotetraploid grass Brachypodium hybridum with respect to its progenitor diploid species B. distachyon (D genome) and B. stacei (S genome). For this, our primary focus is the Iberian Peninsula, an evolutionary hotspot for the genus Brachypodium.MethodsWe analysed 342 B. hybridum individuals from 36 populations using ten nuclear SSR loci and two plastid loci. The B. hybridum genetic profiles were compared with those previously reported for B. stacei and B. distachyon. In addition, phylogenetic analysis of the plastid data was performed for a reduced subset of individuals.Key resultsThe nuclear simple sequence repeat (SSR) genetic analysis detected medium to high genetic diversity, with a strong south-to-north genetic structure cline, and a high selfing rate in B. hybridum. Comparative genetic analysis showed a close relatedness of current B. hybridum D allelic profiles with those of B. distachyon, but a lack of similarity with those of B. stacei, suggesting another B. stacei source for the B. hybridum S alleles. Plastid analysis detected three different bidirectional allopolyploidization events: two involved distinct B. distachyon-like ancestors and one involved a B. stacei-like ancestor. The south-eastern Iberian Peninsula B. hybridum populations were more genetically diverse and could have originated from at least two hybridization events whereas north-eastern/north-western Iberian Peninsula B. hybridum populations were less diverse and may have derived from at least one hybridization event.ConclusionsThe genetic and evolutionary evidence supports the plausible in situ origin of the south-eastern and northern Iberian Peninsula B. hybridum allopolyploids from their respective local B. distachyon and unknown B. stacei ancestors. The untapped multiple origins and genetic variation detected in these B. hybridum populations opens the way to future evolutionary analysis of allopolyploid formation and genomic dominance and expression in the B. hybridum-B. distachyon-B. stacei grass model complex.

Project description:Climate change endangers food security and our ability to feed the ever-increasing human population. Weeds are the most important biotic stress, reducing crop-plant productivity worldwide. Chemical control, the main approach for weed management, can be strongly affected by temperature. Previously, we have shown that temperature-dependent non-target site (NTS) resistance of Brachypodium hybridum is due to enhanced detoxification of acetyl-CoA carboxylase inhibitors. Here, we explored the transcriptional basis of this phenomenon. Plants were characterized for the transcriptional response to herbicide application, high-temperature and their combination, in an attempt to uncover the genetic basis of temperature-dependent pinoxaden resistance. Even though most of the variance among treatments was due to pinoxaden application (61%), plants were able to survive pinoxaden application only when grown under high-temperatures. Biological pathways and expression patterns of members of specific gene families, previously shown to be involved in NTS metabolic resistance to different herbicides, were examined. Cytochrome P450, glucosyl transferase and glutathione-S-transferase genes were found to be up-regulated in response to pinoxaden application under both control and high-temperature conditions. However, biological pathways related to oxidation and glucose conjugation were found to be significantly enriched only under the combination of pinoxaden application and high-temperature. Analysis of reactive oxygen species (ROS) was conducted at several time points after treatment using a probe detecting H2O2/peroxides. Comparison of ROS accumulation among treatments revealed a significant reduction in ROS quantities 24 h after pinoxaden application only under high-temperature conditions. These results may indicate significant activity of enzymatic ROS scavengers that can be correlated with the activation of herbicide-resistance mechanisms. This study shows that up-regulation of genes related to metabolic resistance is not sufficient to explain temperature-dependent pinoxaden resistance. We suggest that elevated activity of enzymatic processes at high-temperature may induce rapid and efficient pinoxaden metabolism leading to temperature-dependent herbicide resistance.

Project description:Background and aimsThe Brachypodium genus represents a useful model system to study grass genome organization. Palaeogenomic analyses (e.g. Murat F, Armero A, Pont C, Klopp C, Salse J. 2017. Reconstructing the genome of the most recent common ancestor of flowering plants. Nature Genetics49: 490-496) have identified polyploidization and dysploidy as the prime mechanisms driving the diversity of plant karyotypes and nested chromosome fusions (NCFs) crucial for shaping grass chromosomes. This study compares the karyotype structure and evolution in B. distachyon (genome Bd), B. stacei (genome Bs) and in their putative allotetraploid B. hybridum (genomes BdBs).MethodsBrachypodium chromosomes were measured and identified using multicolour fluorescence in situ hybridization (mcFISH). For higher resolution, comparative chromosome barcoding was developed using sets of low-repeat, physically mapped B. distachyon-derived bacterial artificial chromosome (BAC) clones.Key resultsAll species had rather small chromosomes, and essentially all in the Bs genome were morphometrically indistinguishable. Seven BACs combined with two rDNA-based probes provided unambiguous and reproducible chromosome discrimination. Comparative chromosome barcoding revealed NCFs that contributed to the reduction in the x = 12 chromosome number that has been suggested for the intermediate ancestral grass karyotype. Chromosome Bd3 derives from two NCFs of three ancestral chromosomes (Os2, Os8, Os10). Chromosome Bs6 shows an ancient Os8/Os10 NCF, whilst Bs4 represents Os2 only. Chromosome Bd4 originated from a descending dysploidy that involves two NCFs of Os12, Os9 and Os11. The specific distribution of BACs along Bs9 and Bs5, in both B. stacei and B. hybridum, suggests a Bs genome-specific Robertsonian rearrangement.ConclusionsmcFISH-based karyotyping identifies all chromosomes in Brachypodium annuals. Comparative chromosome barcoding reveals rearrangements responsible for the diverse organization of Bd and Bs genomes and provides new data regarding karyotype evolution since the split of the two diploids. The fact that no chromosome rearrangements were observed in B. hybridum compared with the karyotypes of its phylogenetic ancestors suggests prolonged genome stasis after the formation of the allotetraploid.

Project description:Herbicide-resistance mutations may impose a fitness penalty in herbicide-free environments. Moreover, the fitness penalty associated with herbicide resistance is not a stable parameter and can be influenced by ecological factors. Here, we used two Brachypodium hybridum accessions collected from the same planted forest, sensitive (S) and target-site resistance (TSR) to photosystem II (PSII) inhibitors, to study the effect of agro-ecological parameters on fitness penalty. Both accessions were collected in the same habitat, thus, we can assume that the genetic variance between them is relatively low. This allow us to focus on the effect of PSII TSR on plant fitness. S plants grains were significantly larger than those of the TSR plants and this was associated with a higher rate of germination. Under low radiation, the TSR plants showed a significant fitness penalty relative to S plants. S plants exhibiting dominance when both types of plants were grown together in a low-light environment. In contrast to previous documented studies, under high-light environment our TSR accession didn't show any significant difference in fitness compared to the S accession. Nitrogen deficiency had significant effect on the R compared to the S accession and was demonstrated in significant yield reduction. TSR plants also expressed a high fitness penalty, relative to the S plants, when grown in competition with wheat plants. Two evolutionary scenarios can be suggested to explain the coexistence of both TSR and S plants in the same habitat. The application of PSII inhibitors may have created selective pressure toward TSR dominancy; termination of herbicide application gave an ecological advantage to S plants, creating changes in the composition of the seed bank. Alternatively, the high radiation intensities found in the Mediterranean-like climate may reduce the fitness penalty associated with TSR. Our results may suggest that by integrating non-herbicidal approaches into weed-management programs, we can reduce the agricultural costs associated with herbicide resistance.

Dataset Information

The fate of 35S rRNA genes in the allotetraploid grass Brachypodium hybridum.

Publications

The fate of 35S rRNA genes in the allotetraploid grass Brachypodium hybridum.

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