SUMOylation is required for normal development of linear elements and wild-type meiotic recombination in Schizosaccharomyces pombe

Špı́rek, Mário; Estreicher, Anna; Csaszar, Edina; Wells, Jennifer L.; McFarlane, Ramsay J.; Watts, Felicity Z.; Loidl, Josef

doi:10.1007/s00412-009-0241-5

Cited by 32 publications

(41 citation statements)

References 46 publications

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“…However, structures resembling the axial elements of SCs, the so-called linear elements, appear in S. pombe. Structural components of linear elements include Rec10p (a distant homolog of S. cerevisiae Red1p), Hop1p, Rec25p, Rec4p, Rec27p, and Pmt3p (S. pombe's SUMO protein) (1159). Detailed structural components of SCs (including the central elements and recombination nodules) in N. crassa were observed previously by using a nuclear spreading protocol with electron microscopy (1160, 1161); however, the components of N. crassa SCs are still unknown.…”

Section: Sexual Developmentmentioning

confidence: 92%

The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species

Schmoll

Dattenböck

Carreras-Villaseñor

et al. 2016

Microbiol Mol Biol Rev

163

195

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SUMMARYThe genusTrichodermacontains fungi with high relevance for humans, with applications in enzyme production for plant cell wall degradation and use in biocontrol. Here, we provide a broad, comprehensive overview of the genomic content of these species for “hot topic” research aspects, including CAZymes, transport, transcription factors, and development, along with a detailed analysis and annotation of less-studied topics, such as signal transduction, genome integrity, chromatin, photobiology, or lipid, sulfur, and nitrogen metabolism inT. reesei,T. atroviride, andT. virens, and we open up new perspectives to those topics discussed previously. In total, we covered more than 2,000 of the predicted 9,000 to 11,000 genes of eachTrichodermaspecies discussed, which is >20% of the respective gene content. Additionally, we considered available transcriptome data for the annotated genes. Highlights of our analyses include overall carbohydrate cleavage preferences due to the different genomic contents and regulation of the respective genes. We found light regulation of many sulfur metabolic genes. Additionally, a new Golgi 1,2-mannosidase likely involved inN-linked glycosylation was detected, as were indications for the ability ofTrichodermaspp. to generate hybrid galactose-containingN-linked glycans. The genomic inventory of effector proteins revealed numerous compounds unique toTrichoderma, and these warrant further investigation. We found interesting expansions in theTrichodermagenus in several signaling pathways, such as G-protein-coupled receptors, RAS GTPases, and casein kinases. A particularly interesting feature absolutely unique toT. atrovirideis the duplication of the alternative sulfur amino acid synthesis pathway.

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Section: Sexual Developmentmentioning

confidence: 92%

The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species

Schmoll

Dattenböck

Carreras-Villaseñor

et al. 2016

Microbiol Mol Biol Rev

163

195

View full text Add to dashboard Cite

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“…Several lines of evidence indicate that protein modification by the ubiquitin-related protein SUMO plays a role in meiosis (28)(29)(30)(31)(32)(33)(34). In particular, the SC itself seems to contain SUMO because the SC can be stained with SUMOspecific antibodies along its entire axis (28).…”

Section: -1-1-red1 Interaction Is Essential For Meiotic Checkpoint Smentioning

confidence: 99%

Synaptonemal complex formation and meiotic checkpoint signaling are linked to the lateral element protein Red1

Eichinger

Jentsch

2010

Proc. Natl. Acad. Sci. U.S.A.

100

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Meiosis generates four haploid daughters from a diploid parental cell. Central steps of meiosis are the pairing and recombination of homologous chromosomes followed by their segregation in two rounds of cell division. Meiotic recombination is monitored by a specialized DNA damage checkpoint pathway and is guided by a unique chromosomal structure called synaptonemal complex (SC), but how these events are coordinated is unclear. Here, we identify the SC protein Red1 as a crucial regulator of early meiosis. Red1 interacts with two subunits of the 9-1-1 checkpoint complex via two distinct 9-1-1 subunit-specific motifs. Association of 9-1-1 with Red1 is essential not only for meiotic checkpoint activation but for SC formation. Moreover, Red1 becomes SUMO-modified, which fosters interaction of Red1 with the central SC element Zip1, thereby securing timely SC formation. Thus, Red1, in addition to its structural role in the SC, is a crucial coordinator of meiosis by coupling checkpoint signaling to SC formation.checkpoint | meiosis | SUMO T he central activity of meiosis is the equal distribution of the genetic material of a diploid cell into four daughter cells. A key step of meiosis occurs in pachytene, in which the homologous chromosomes (i.e., the parental chromosomes, each containing two sister chromatids) align (synapsis). This alignment facilitates the exchange of parental information by homologous recombination and is crucial for chromosome segregation during the first meiotic division.The juxtaposition of the homologs in pachytene involves a unique chromosome structure known as the synaptonemal complex (SC), which assembles along the entire length of the bundled chromosomes (1, 2). The SC-induced arrangement of chromosomes appears to favor genetic exchange between homologs rather than sister chromatids. SC formation starts along each pair of homologous sister chromatids with the assembly of 50-nm-thick fibers, termed axial elements, which later become the so-called "lateral elements" of the SC. The axial elementcoated parental homologs finally associate via components of the central element, which zip the axial elements together, forming the SC. In Saccharomyces cerevisiae, the proteins Hop1 and Red1 are structural components of the lateral element, whereas the coiled-coil protein Zip1, which homo (oligo)-dimerizes during SC formation, forms the "steps" of the ladder-like central region. SC "zipping" is thought to take place by serial Zip1-Red1 interactions along the entire SC axis (1, 2).Early meiosis is under the control of the meiotic recombination checkpoint (called the meiotic checkpoint here; it is also known as the pachytene checkpoint), which prevents meiotic progression in the presence of unrepaired recombination intermediates. A key element of the meiotic surveillance pathway is the ring-shaped, heterotrimeric 9-1-1 complex (the proteins Rad9, Hus1, and Rad1 in mammals; the proteins Ddc1, Mec3, and Rad17 in S. cerevisiae), which is structurally related to the homotrimeric DNA-encircling DNA polymerase...

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“…For example, confluent sumoylation of chromosomal axes is observed during meiosis in S. pombe, where SCs do not form as no central element components are deposited [27]. Instead, sumoylation of the chromosomal axes is a prerequisite for normal levels of meiotic recombination [28]. Therefore, although the confluent SUMO staining of SCs suggests a role for sumoylation in SC formation, this staining pattern is not necessarily important for synapsis, but could represent a (yeast-specific) chromosomal patterning event important for the DNA damage response and repair of meiotic double-strand breaks.…”

Section: Sumo-dependent Recombination In Yeast: Sumo Localizes To Aximentioning

confidence: 97%

SUMO meets meiosis: An encounter at the synaptonemal complex

Watts

Hoffmann

2011

BioEssays

Self Cite

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Recent discoveries have identified the small ubiquitin-like modifier (SUMO) as the potential 'missing link' that could explain how the synaptonemal complex (SC) is formed during meiosis. The SC is important for a variety of chromosome interactions during meiosis and appears ladder-like. It is formed when 'axes' of the two homologous chromosomes become connected by the deposition of transverse filaments, forming the steps of the ladder. Although several components of axial and transverse elements have been identified, how the two are connected to form the SC has remained an enigma. Recent discoveries suggest that SUMO modification underlies protein-protein interactions within the SC of budding yeast. The versatility of SUMO in regulating protein-protein interactions adds an exciting new dimension to our understanding of the SC and suggests that SCs are not homogenous structures throughout the nucleus. We propose that this heterogeneity may allow differential regulation of chromosome structure and function.

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SUMOylation is required for normal development of linear elements and wild-type meiotic recombination in Schizosaccharomyces pombe

Cited by 32 publications

References 46 publications

The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species

The Genomes of Three Uneven Siblings: Footprints of the Lifestyles of Three Trichoderma Species

Synaptonemal complex formation and meiotic checkpoint signaling are linked to the lateral element protein Red1

SUMO meets meiosis: An encounter at the synaptonemal complex

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