Protein-coding genes in B chromosomes of the grasshopper Eyprepocnemis plorans

Navarro-Domínguez, Beatriz; Ruiz‐Ruano, Francisco J.; Cabrero, J.; Corral, José M. Miguel del; López-León, María Dolores; Sharbel, Timothy F.; Camacho, Juan Pedro M.

doi:10.1038/srep45200

Cited by 57 publications

(64 citation statements)

References 70 publications

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“…Bioinformatic procedures to search for B chromosome genes were similar to those described in Navarro-Domínguez et al (18) and are graphically summarized in Fig. S5.…”

Section: Methodsmentioning

confidence: 99%

“…Primer pairs anchoring in the same exon were designed with Primer3 (53) preferentially on regions with low sequence variation and high read mapping coverage (Table S9). Quantitative PCR was carried out as described in Navarro-Dominguez et al (18).…”

Section: Methodsmentioning

confidence: 99%

“…Likewise, Valente et al (17) found that a B chromosome in fish contained thousands of gene-like sequences, most of them being fragmented but a few remaining largely intact, with at least three of them being transcriptionally active. Likewise, Navarro-Domínguez et al (18) found evidence for the presence of ten protein-coding genes in the B chromosome of the grasshopper Eyprepocnemis plorans , five of which were active in B-carrying individuals, including three which were apparently pseudogenic. Taken together, these results indicate that B chromosomes are not as inert as previously thought, since they contain protein-coding genes which are actively transcribed even in the case of being pseudogenic.…”

Section: Introductionmentioning

confidence: 99%

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Evolutionary success of a parasitic B chromosome rests on gene content

Ruiz‐Ruano

Navarro-Domínguez

López-León

et al. 2019

Preprint

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26 Supernumerary (B) chromosomes are dispensable genomic elements found in most 27 kinds of eukaryotic genomes. Many show drive mechanisms that give them an 28 advantage in transmission, but how they achieve it remains a mystery. The recent 29 finding of protein-coding genes in B chromosomes has opened the possibility that 30 their evolutionary success is based on their genetic content. Using a protocol based on 31 mapping genomic DNA Illumina reads from B-carrying and B-lacking individuals on 32 the coding sequences of de novo transcriptomes from the same individuals, we 33 identified 25 protein-coding genes in the B chromosome of the migratory locust, 15 of 34 which showed a full coding region. Remarkably, one of these genes (apc1) codes for 35 the large subunit of the Anaphase Promoting Complex or Cyclosome (APC/C), an E3 36 ubiquitin ligase involved in the metaphase-anaphase transition. Sequence comparison 37 of A and B chromosome gene paralogs showed that the latter show B-specific 38 nucleotide changes, neither of which putatively impairs protein function. These 39 nucleotide signatures allowed identifying B-derived transcripts in B-carrying 40 transcriptomes, and demonstrated that they show about similar frequency as 41 A-derived ones. Since B-carrying individuals show higher amounts of apc1 42 transcripts than B-lacking ones, the putatively higher amount of APC1 protein might 43 induce a faster metaphase-anaphase transition in spite of orientation of the two B 44 chromosome chromatids towards the same pole during metaphase, thus facilitating B 45 chromosome non-disjunction. Therefore, apc1 is the first protein-coding gene 46 uncovered in a B chromosome that might be responsible for B chromosome drive. 47 48 Significance Statement 49 The genome of the migratory locust harbors a parasitic chromosome that arose about 50 2 million years ago. It is widespread in natural populations from Asia, Africa, 51 Australia and Europe, i.e. all continents where this species lives. The secret for such 52 an extraordinary evolutionary success is unveiled in this report, as B chromosomes in 53 this species contain active protein-coding genes whose transcripts might interfere with 54 gene expression in the host genome (the A chromosomes), thus facilitating B 55 chromosome mitotic and meiotic drive to provide the transmission advantage which 56 grants its success. One of the B-chromosomal genes (apc1) codes for the large subunit 57 of the Anaphase Promoting Complex or Cyclosome (APC/C) whose expression might 58 provide a mechanistic explanation for B chromosome drive. 59 60 61After 112 years since they were uncovered (1), B chromosomes continue being an 62 enigmatic part of eukaryote genomes. They were first considered as merely 63 genetically inert passengers of eukaryote genomes (2), a view supported by others (3) 64 but criticized by those who argued that B chromosomes are beneficial (4) or parasitic 65 (5) elements. In fact, as in most cases of selfish genetic elements, phenotypic effects 66 of B chromosomes are usually...

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“…Bioinformatic procedures to search for B chromosome genes were similar to those described in Navarro-Domínguez et al (18) and are graphically summarized in Fig. S5.…”

Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Evolutionary success of a parasitic B chromosome rests on gene content

Ruiz‐Ruano

Navarro-Domínguez

López-León

et al. 2019

Preprint

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“…Sequencing of DNA amplified from Bs flow sorted from rye revealed thousands of gene signatures with homology to rye A chromosomes (Martis et al, 2012). A recent study by Navarro‐Domínguez et al (2017) demonstrated that Bs are transcriptionally active and they could interfere with gene expression and regulation in A chromosomes. Therefore, flow sorting of Bs could help to trace their origin and understand their function in crested wheatgrass.…”

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confidence: 99%

Dissecting the Complex Genome of Crested Wheatgrass by Chromosome Flow Sorting

et al. 2019

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Core Ideas Flow sorting enabled to dissect the genome of crested wheatgrass into chromosomes. This is a powerful approach to access the complex genome of a wheat wild relative. Chromosome genomics will support alien introgression breeding of the crop. Wheatgrass (Agropyron sp.) is a potential source of beneficial traits for wheat improvement. Among them, crested wheatgrass [A. cristatum (L.) Gaertn.] comprises a complex of diploid, tetraploid, and hexaploid forms with the basic genome P, with some accessions carrying supernumerary B chromosomes (Bs). In this work, we applied flow cytometry to dissect the complex genome of crested wheatgrass into individual chromosomes to facilitate its analysis. Flow karyotypes obtained after the analysis of 4ʹ,6‐diamidino‐2‐phenylindole (DAPI)‐stained mitotic chromosomes of diploid and tetraploid accessions consisted of three peaks, each corresponding to a group of two or three chromosomes. To improve the resolution, bivariate flow karyotyping after fluorescent labeling of chromosomes with fluorescein isothiocyanate (FITC)‐conjugated probe (GAA)7 microsatellite was applied and allowed discrimination and sorting of P genome chromosomes from wheat–crested wheatgrass addition lines. Chromosomes 1P–6P and seven telomeric chromosomes could be sorted at purities ranging from 81.7 to 98.2% in disomics and from 44.8 to 87.3% in telosomics. Chromosome 7P was sorted at purities reaching 50.0 and 39.5% in diploid and tetraploid crested wheatgrass, respectively. In addition to the whole complement chromosomes (A), Bs could be easily discriminated and sorted from a diploid accession at 95.4% purity. The sorted chromosomes will streamline genome analysis of crested wheatgrass, facilitating gene cloning and development of molecular tools to support alien introgression into wheat.

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“…http://dx.doi.org/10.1101/386995 doi: bioRxiv preprint first posted online plorans, revealed the presence of 10 protein-coding genes carried on the B chromosome (Navarro-63 Domínguez et al 2017). These studies demonstrate that the diversity and complexity of supernumerary 64 B chromosomes has been underestimated, and a better understanding of their origin and composition is 65 necessary.…”

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confidence: 99%