Transposon-mediated telomere destabilization: a driver of genome evolution in the blast fungus

Abstract The fungus Magnaporthe oryzae causes devastating diseases of crops, including rice and wheat, and in various grasses. Strains from ryegrasses have highly unstable chromosome ends that undergo frequent rearrangements, and this has been associated with the presence of retrotransposons (Magnaporthe oryzae Telomeric Retrotransposons—MoTeRs) inserted in the telomeres. The objective of the present study was to determine the mechanisms by which MoTeRs promote telomere instability. Targeted cloning, mapping, and sequencing of parental and novel telomeric restriction fragments (TRFs), along with MinION sequencing of genomic DNA allowed us to document the precise molecular alterations underlying 109 newly-formed TRFs. These included truncations of subterminal rDNA sequences; acquisition of MoTeR insertions by ‘plain’ telomeres; insertion of the MAGGY retrotransposons into MoTeR arrays; MoTeR-independent expansion and contraction of subtelomeric tandem repeats; and a variety of rearrangements initiated through breaks in interstitial telomere tracts that are generated during MoTeR integration. Overall, we estimate that alterations occurred in approximately sixty percent of chromosomes (one in three telomeres) analyzed. Most importantly, we describe an entirely new mechanism by which transposons can promote genomic alterations at exceptionally high frequencies, and in a manner that can promote genome evolution while minimizing collateral damage to overall chromosome architecture and function.

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Transposon-mediated telomere destabilization: a driver of genome evolution in the blast fungus

10.1101/845669 ◽

2019 ◽

Author(s):

Mostafa Rahnama ◽

Olga Novikova ◽

John Starnes ◽

Li Chen ◽

Shouan Zhang ◽

...

Keyword(s):

Magnaporthe Oryzae ◽

Tandem Repeats ◽

In Planta ◽

Single Spore ◽

Telomere Repeat ◽

Restriction Fragments ◽

Molecular Alterations ◽

Filamentous Ascomycete ◽

Rdna Sequences ◽

Chromosome Alterations

ABSTRACTMagnaporthe oryzae is a filamentous ascomycete fungus that causes devastating diseases of crops that include rice and wheat, and a variety of turf, forage and wild grasses. Strains from ryegrasses possess highly stable chromosome ends that undergo frequent rearrangements during vegetative growth in culture and in planta. Instability is associated with the presence of two related retrotransposons (Magnaporthe oryzaeTelomeric Retrotransposons - MoTeRs) inserted within the telomere repeat tracts. The objective of the present study was to determine the mechanisms by which MoTeRs promote telomere instability. Targeted cloning, restriction mapping, and sequencing of both parental and novel telomeric restriction fragments, along with MinION sequencing of DNA from three single-spore cultures, allowed us to document the molecular alterations for 109 newly-formed telomeres. Rearrangement events included truncations of subterminal rDNA sequences; acquisition of MoTeR insertions by “plain” telomeres; insertion of the MAGGY retrotransposons into MoTeR arrays; expansion and contraction of subtelomeric tandem repeats; MoTeR truncations; duplication and terminalization of internal sequences; and breakage at long, interstitial telomeres generated during MoTeR insertion. Together, our data show that when MoTeRs invade the telomeres, they can dramatically perturb the integrity of chromosome ends, leading to the generation of unprotected DNA termini whose repair has the potential to generate chromosome alterations that extend well into the genome interior.

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Evolution and function of tandem repeats in the major surface protein 1a of the ehrlichial pathogenAnaplasma marginale

Animal Health Research Reviews ◽

10.1079/ahrr200132 ◽

2001 ◽

Vol 2 (2) ◽

pp. 163-174 ◽

Cited By ~ 53

Author(s):

José de la Fuente ◽

Jose C. Garcia-Garcia ◽

Edmour F. Blouin ◽

Sergio D. Rodríguez ◽

Migel A. García ◽

...

Keyword(s):

Tandem Repeats ◽

Control Strategies ◽

Surface Protein ◽

Single Copy ◽

Major Surface Protein ◽

Host Parasite Interactions ◽

Major Surface ◽

And Function ◽

Host Parasite ◽

Bovine Erythrocytes

AbstractThe major surface protein (MSP) 1a of the ehrlichial cattle pathogenAnaplasma marginale, encoded by the single-copy genemsp1α, has been shown to have a neutralization-sensitive epitope and to be an adhesin for bovine erythrocytes and tick cells.msp1αhas been found to be a stable genetic marker for the identification of geographic isolates ofA. marginalethroughout development in acutely and persistently infected cattle and in ticks. The molecular weight of MSP1a varies among geographic isolates ofA. marginalebecause of a varying number of tandemly repeated peptides of 28–29 amino acids. Variation in the sequence of the tandem repeats occurs within and among isolates, and may have resulted from evolutionary pressures exerted by ligand–receptor and host–parasite interactions. These repeated sequences include markers for tick transmissibility that may be important in the identification of ehrlichial pathogens because they may influence control strategies and the design of subunit vaccines.

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Genome Evolution and Function of Resistance Genes

Rice Blast: Interaction with Rice and Control ◽

10.1007/978-0-306-48582-4_9 ◽

2004 ◽

pp. 71-77

Author(s):

Ko Hirano ◽

Shinji Kawasaki

Keyword(s):

Genome Evolution ◽

Resistance Genes ◽

And Function

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Quantitative polymorphism of tandem repeats as a method of epigenetic regulation of the of human cells response to oxidative stress

Nauchno-prakticheskii zhurnal «Medicinskaia genetika» ◽

10.25557/2073-7998.2020.12.68-70 ◽

2020 ◽

pp. 68-70

Author(s):

Н.Н. Вейко ◽

Е.С. Ершова ◽

М.С. Конькова ◽

Е.М. Малиновская ◽

С.В. Костюк

Keyword(s):

Adaptive Response ◽

Spatial Organization ◽

Tandem Repeats ◽

Spatial Configuration ◽

Human Cells ◽

Central Regions ◽

Schizophrenic Patients ◽

Response To Stress ◽

Cell Genome ◽

And Function

Пространственная организация хроматина важна для нормального функционирования клетки. На архитектуру ядра влияют размеры отдельных фрагментов генома, которые коррелируют с числом копий этих фрагментов. Перемещение локусов 1q12 от поверхности ядра в центральные области является ключевой стадией адаптивного ответа клетки на стресс. Мы предположили, что размер локусов 1q12, который коррелирует с содержанием повтора f-SatIII, может влиять на перемещение этих участков хроматина в ядре. Методом FISH на выделенных лимфоцитах показали, что в контроле локусы 1q12 расположены вблизи поверхности ядра, в ядрах лимфоцитов больных шизофренией (БШ) и облученных контрольных клеток локусы 1q12 расположены в центральных районах ядра. Длительное культивирование облученных лимфоцитов сопровождалось гибелью клеток, и снижением содержания f-SatIII в ДНК. Очевидно, что погибали клетки с большим размером 1q12 (много f-SatIII), обогащая популяцию клетками с низким содержанием f-SatIII. В клетках БШ и в облученных клетках мы обнаружили повышение уровня РНК SATIII. Размеры гетерохроматина 1q12 в клетках человека могут влиять на процессы пролиферации и ответа клетки на стресс. Количественный полиморфизм тандемных повторов генома - один из эпигенетических механизмов регуляции ответа клеток на окислительный стресс. The spatial organization of chromatin is important for the normal functioning of the cell. Genome repeat cluster sizes can affect the chromatin spatial configuration and function. The 1q12 heterochromatin loci movement from the periphery to the center of the nucleus is the cells’ universal response to various types of stress. We hypothesized that a large 1q12 domain could affect chromatin movement, thereby inhibiting adaptive response (AR). Using the FISH method, we shown that in the control, 1q12 loci are located near the surface of the nucleus; in the lymphocyte nuclei of schizophrenic patients and irradiated control cells, 1q12 loci are located in the central regions of the nucleus. During prolonged cultivation, the irradiated cells with a large Large f-SatIII amount die and the population is enriched with the cells with low f-SatIII content. In intact SZ patients’ lymphocytes and in irradiated cells we found an increase in SATIII RNA levels. The size of heterochromatin 1q12 loci in human cells can affect to the proliferation and cells’ adaptive response to stress. Quantitative polymorphism of tandem genome repeats is one of the epigenetic mechanisms of genome expression’s regulation.

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tRNA Genes Affect Chromosome Structure and Function via Local Effects

Molecular and Cellular Biology ◽

10.1128/mcb.00432-18 ◽

2019 ◽

Vol 39 (8) ◽

Cited By ~ 5

Author(s):

Omar Hamdani ◽

Namrita Dhillon ◽

Tsung-Han S. Hsieh ◽

Takahiro Fujita ◽

Josefina Ocampo ◽

...

Keyword(s):

Long Range ◽

Binding Sites ◽

Genomic Organization ◽

Chromosome Structure ◽

Trna Genes ◽

Local Effects ◽

Chromosome Architecture ◽

Architectural Proteins ◽

And Function ◽

Chromosome Tethering

ABSTRACT The genome is packaged and organized in an ordered, nonrandom manner, and specific chromatin segments contact nuclear substructures to mediate this organization. tRNA genes (tDNAs) are binding sites for transcription factors and architectural proteins and are thought to play an important role in the organization of the genome. In this study, we investigate the roles of tDNAs in genomic organization and chromosome function by editing a chromosome so that it lacked any tDNAs. Surprisingly our analyses of this tDNA-less chromosome show that loss of tDNAs does not grossly affect chromatin architecture or chromosome tethering and mobility. However, loss of tDNAs affects local nucleosome positioning and the binding of SMC proteins at these loci. The absence of tDNAs also leads to changes in centromere clustering and a reduction in the frequency of long-range HML-HMR heterochromatin clustering with concomitant effects on gene silencing. We propose that the tDNAs primarily affect local chromatin structure, which results in effects on long-range chromosome architecture.

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Histone H1 is essential for mitotic chromosome architecture and segregation in Xenopus laevis egg extracts

The Journal of Cell Biology ◽

10.1083/jcb.200503031 ◽

2005 ◽

Vol 169 (6) ◽

pp. 859-869 ◽

Cited By ~ 79

Author(s):

Thomas J. Maresca ◽

Benjamin S. Freedman ◽

Rebecca Heald

Keyword(s):

Xenopus Laevis ◽

Metaphase Plate ◽

Histone H1 ◽

Linker Histone ◽

Chromosome Architecture ◽

Linker Histone H1 ◽

Egg Extracts ◽

Chromatin Proteins ◽

And Function

During cell division, condensation and resolution of chromosome arms and the assembly of a functional kinetochore at the centromere of each sister chromatid are essential steps for accurate segregation of the genome by the mitotic spindle, yet the contribution of individual chromatin proteins to these processes is poorly understood. We have investigated the role of embryonic linker histone H1 during mitosis in Xenopus laevis egg extracts. Immunodepletion of histone H1 caused the assembly of aberrant elongated chromosomes that extended off the metaphase plate and outside the perimeter of the spindle. Although functional kinetochores assembled, aligned, and exhibited poleward movement, long and tangled chromosome arms could not be segregated in anaphase. Histone H1 depletion did not significantly affect the recruitment of known structural or functional chromosomal components such as condensins or chromokinesins, suggesting that the loss of H1 affects chromosome architecture directly. Thus, our results indicate that linker histone H1 plays an important role in the structure and function of vertebrate chromosomes in mitosis.

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Structure and Function of Glycosylated Tandem Repeats from Candida albicans Als Adhesins

Eukaryotic Cell ◽

10.1128/ec.00235-09 ◽

2009 ◽

Vol 9 (3) ◽

pp. 405-414 ◽

Cited By ~ 38

Author(s):

Aaron T. Frank ◽

Caleen B. Ramsook ◽

Henry N. Otoo ◽

Cho Tan ◽

Gregory Soybelman ◽

...

Keyword(s):

Candida Albicans ◽

Tandem Repeats ◽

Cell Aggregation ◽

Structure And Function ◽

Hydrophobic Surfaces ◽

Content Type ◽

Domain Structures ◽

Aggregation Activity ◽

Fungal Adhesins ◽

And Function

ABSTRACT Tandem repeat (TR) regions are common in yeast adhesins, but their structures are unknown, and their activities are poorly understood. TR regions in Candida albicans Als proteins are conserved glycosylated 36-residue sequences with cell-cell aggregation activity (J. M. Rauceo, R. De Armond, H. Otoo, P. C. Kahn, S. A. Klotz, N. K. Gaur, and P. N. Lipke, Eukaryot. Cell 5:1664–1673, 2006). Ab initio modeling with either Rosetta or LINUS generated consistent structures of three-stranded antiparallel β-sheet domains, whereas randomly shuffled sequences with the same composition generated various structures with consistently higher energies. O- and N-glycosylation patterns showed that each TR domain had exposed hydrophobic surfaces surrounded by glycosylation sites. These structures are consistent with domain dimensions and stability measurements by atomic force microscopy (D. Alsteen, V. Dupres, S. A. Klotz, N. K. Gaur, P. N. Lipke, and Y. F. Dufrene, ACS Nano 3:1677–1682, 2009) and with circular dichroism determination of secondary structure and thermal stability. Functional assays showed that the hydrophobic surfaces of TR domains supported binding to polystyrene surfaces and other TR domains, leading to nonsaturable homophilic binding. The domain structures are like “classic” subunit interaction surfaces and can explain previously observed patterns of promiscuous interactions between TR domains in any Als proteins or between TR domains and surfaces of other proteins. Together, the modeling techniques and the supporting data lead to an approach that relates structure and function in many kinds of repeat domains in fungal adhesins.

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RNA from a simple-tandem repeat is required for sperm maturation and male fertility in Drosophila melanogaster

eLife ◽

10.7554/elife.48940 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 7

Author(s):

Wilbur Kyle Mills ◽

Yuh Chwen G Lee ◽

Antje M Kochendoerfer ◽

Elaine M Dunleavy ◽

Gary H Karpen

Keyword(s):

Drosophila Melanogaster ◽

Male Fertility ◽

Tandem Repeats ◽

Sperm Maturation ◽

Simple Tandem Repeat ◽

Satellite Rnas ◽

Repeated Dnas ◽

And Function ◽

Rna Depletion ◽

Eukaryotic Genomes

Tandemly-repeated DNAs, or satellites, are enriched in heterochromatic regions of eukaryotic genomes and contribute to nuclear structure and function. Some satellites are transcribed, but we lack direct evidence that specific satellite RNAs are required for normal organismal functions. Here, we show satellite RNAs derived from AAGAG tandem repeats are transcribed in many cells throughout Drosophila melanogaster development, enriched in neurons and testes, often localized within heterochromatic regions, and important for viability. Strikingly, we find AAGAG transcripts are necessary for male fertility, and that AAGAG RNA depletion results in defective histone-protamine exchange, sperm maturation and chromatin organization. Since these events happen late in spermatogenesis when the transcripts are not detected, we speculate that AAGAG RNA in primary spermatocytes ‘primes’ post-meiosis steps for sperm maturation. In addition to demonstrating essential functions for AAGAG RNAs, comparisons between closely related Drosophila species suggest that satellites and their transcription evolve quickly to generate new functions.

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