Are the effects of elevated temperature on meiotic recombination and thermotolerance linked via the axis and synaptonemal complex?

Meiosis is unusual among cell divisions in shuffling genetic material by crossovers among homologous chromosomes and partitioning the genome into haploid gametes. Crossovers are critical for chromosome segregation in most eukaryotes, but are also an important factor in evolution, as they generate novel genetic combinations. The molecular mechanisms that underpin meiotic recombination and chromosome segregation are well conserved across kingdoms, but are also sensitive to perturbation by environment, especially temperature. Even subtle shifts in temperature can alter the number and placement of crossovers, while at greater extremes, structural failures can occur in the linear axis and synaptonemal complex structures which are essential for recombination and chromosome segregation. Understanding the effects of temperature on these processes is important for its implications in evolution and breeding, especially in the context of global warming. In this review, we first summarize the process of meiotic recombination and its reliance on axis and synaptonemal complex structures, and then discuss effects of temperature on these processes and structures. We hypothesize that some consistent effects of temperature on recombination and meiotic thermotolerance may commonly be two sides of the same coin, driven by effects of temperature on the folding or interaction of key meiotic proteins. This article is part of the themed issue ‘Evolutionary causes and consequences of recombination rate variation in sexual organisms’.

• Publication year

  2017

• Venue

  Philosophical Transactions of the Royal Society B: Biological Sciences

• Publication date

  2017-11-06

• Fields of study

  Biology, Medicine, Environmental Science

• Identifiers
  DOI 10.1098/rstb.2016.0470PMID 29109229PMCID 5698628
• External record

  Open on Semantic Scholar

• Source metadata

  Semantic Scholar, PubMed

• No claims are published for this paper.

• No concepts are published for this paper.

• The synaptonemal complex has liquid crystalline properties and spatially regulates meiotic recombination factors

  2017cited by this paper
• A few of our favorite things: Pairing, the bouquet, crossover interference and evolution of meiosis.

  2016cited by this paper
• Control of Meiotic Crossovers: From Double-Strand Break Formation to Designation.

  2016cited by this paper
• The challenge of evolving stable polyploidy: could an increase in “crossover interference distance” play a central role?

  2016cited by this paper
• Oxidative stress in oocytes during midprophase induces premature loss of cohesion and chromosome segregation errors

  2016cited by this paper
• The effect of temperature on the male and female recombination landscape of barley.

  2015cited by this paper
• Selection on meiosis genes in diploid and tetraploid Arabidopsis arenosa.

  2015cited by this paper
• Essential and Checkpoint Functions of Budding Yeast ATM and ATR during Meiotic Prophase Are Facilitated by Differential Phosphorylation of a Meiotic Adaptor Protein, Hop1

  2015cited by this paper
• Meiosis evolves: adaptation to external and internal environments.

  2015cited by this paper
• Recombination, Pairing, and Synapsis of Homologs during Meiosis.

  2015cited by this paper
• Transcription dynamically patterns the meiotic chromosome-axis interface

  2015cited by this paper
• Meiotic cohesin STAG3 is required for chromosome axis formation and sister chromatid cohesion

  2014cited by this paper
• Chromosome segregation in plant meiosis

  2014cited by this paper
• Interference-mediated synaptonemal complex formation with embedded crossover designation

  2014cited by this paper
• Crossover Patterning by the Beam-Film Model: Analysis and Implications

  2014cited by this paper
• CDKG1 protein kinase is essential for synapsis and male meiosis at high ambient temperature in Arabidopsis thaliana

  2014cited by this paper
• Topoisomerase II mediates meiotic crossover interference

  2014influential reference
• Mechanism and regulation of meiotic recombination initiation.

  2014cited by this paper
• Homologue engagement controls meiotic DNA break number and distribution

  2014cited by this paper
• Factors underlying restricted crossover localization in barley meiosis.

  2014cited by this paper
• A Quality Control Mechanism Coordinates Meiotic Prophase Events to Promote Crossover Assurance

  2014cited by this paper
• Meiotic chromosome structures constrain and respond to designation of crossover sites

  2013cited by this paper
• Assembly of the Synaptonemal Complex Is a Highly Temperature-Sensitive Process That Is Supported by PGL-1 During Caenorhabditis elegans Meiosis

  2013cited by this paper
• Diversity in the origins of proteostasis networks — a driver for protein function in evolution

  2013cited by this paper
• Protein disorder, prion propensities, and self-organizing macromolecular collectives.

  2013cited by this paper
• The impact of environmental stress on male reproductive development in plants: biological processes and molecular mechanisms

  2013cited by this paper
• Molecular chaperone functions in protein folding and proteostasis.

  2013cited by this paper
• What limits meiotic crossovers?

  2012cited by this paper
• Meiotic cohesin complexes are essential for the formation of the axial element in mice

  2012cited by this paper
• Inter-Homolog Crossing-Over and Synapsis in Arabidopsis Meiosis Are Dependent on the Chromosome Axis Protein AtASY3

  2012cited by this paper
• Delineation of joint molecule resolution pathways in meiosis identifies a crossover-specific resolvase.

  2012cited by this paper
• Control of meiotic recombination frequency in plant genomes.

  2012cited by this paper
• Spatiotemporal Asymmetry of the Meiotic Program Underlies the Predominantly Distal Distribution of Meiotic Crossovers in Barley[W]

  2012cited by this paper
• The role of SYN1 in early Arabidopsis meiosis

  2011cited by this paper
• Molecular chaperones in protein folding and proteostasis

  2011cited by this paper
• Spo11-accessory proteins link double-strand break sites to the chromosome axis in early meiotic recombination.

  2011cited by this paper
• Recombination rate variation in closely related species

  2011cited by this paper
• Roles of Hop1 and Mek1 in Meiotic Chromosome Pairing and Recombination Partner Choice in Schizosaccharomyces pombe

  2010cited by this paper
• Cellular strategies for controlling protein aggregation

  2010cited by this paper
• A C. elegans eIF4E-family member upregulates translation at elevated temperatures of mRNAs encoding MSH-5 and other meiotic crossover proteins

  2010cited by this paper
• DNA end resection: many nucleases make light work.

  2009cited by this paper
• The axial element protein HTP-3 promotes cohesin loading and meiotic axis assembly in C. elegans to implement the meiotic program of chromosome segregation.

  2009cited by this paper
• Phosphorylation of the axial element protein Hop1 by Mec1/Tel1 ensures meiotic interhomolog recombination.

  2008cited by this paper
• Coupling meiotic chromosome axis integrity to recombination.

  2008cited by this paper
• Rad51-Independent Interchromosomal Double-Strand Break Repair by Gene Conversion Requires Rad52 but Not Rad55, Rad57, or Dmc1

  2007cited by this paper
• ZMM proteins during meiosis: Crossover artists at work

  2007cited by this paper
• Premature progression of anther early developmental programs accompanied by comprehensive alterations in transcription during high-temperature injury in barley plants

  2007cited by this paper
• ASY1 mediates AtDMC1-dependent interhomolog recombination during meiosis in Arabidopsis.

  2007cited by this paper
• SUMO modifications control assembly of synaptonemal complex and polycomplex in meiosis of Saccharomyces cerevisiae.

  2006cited by this paper
• Alleles of afd1 dissect REC8 functions during meiotic prophase I

  2006cited by this paper
• Identification of CT46/HORMAD1, an immunogenic cancer/testis antigen encoding a putative meiosis-related protein.

  2005cited by this paper
• Endonucleolytic processing of covalent protein-linked DNA double-strand breaks

  2005cited by this paper
• The Arabidopsis synaptonemal complex protein ZYP1 is required for chromosome synapsis and normal fidelity of crossing over.

  2005cited by this paper
• HTP-1 coordinates synaptonemal complex assembly with homolog alignment during meiosis in C. elegans.

  2005cited by this paper
• Crossover/noncrossover differentiation, synaptonemal complex formation, and regulatory surveillance at the leptotene/zygotene transition of meiosis.

  2004cited by this paper
• An insertional mutation in the rice PAIR2 gene, the ortholog of Arabidopsis ASY1, results in a defect in homologous chromosome pairing during meiosis

  2004cited by this paper
• The genetics and molecular biology of the synaptonemal complex.

  2004cited by this paper
• Chiasma formation in Arabidopsis thaliana accession Wassileskija and in two meiotic mutants

  2004cited by this paper
• Temperature effect on chiasma frequency in the bluebell endymion nonscriptus

  2004cited by this paper
• A meiotic time-course for Arabidopsis thaliana

  2003cited by this paper
• Fission yeast Mus81.Eme1 Holliday junction resolvase is required for meiotic crossing over but not for gene conversion.

  2003cited by this paper
• Abnormal spermatogenesis at low temperatures in the Japanese red‐bellied newt, Cynops pyrrhogaster: Possible biological significance of the cessation of spermatocytogenesis

  2003cited by this paper
• The Arabidopsis SYN1 cohesin protein is required for sister chromatid arm cohesion and homologous chromosome pairing

  2003cited by this paper
• Adaptation of Drosophila to temperature extremes: bringing together quantitative and molecular approaches

  2003cited by this paper
• A Drosophila melanogaster strain from sub-equatorial Africa has exceptional thermotolerance but decreased Hsp70 expression.

  2001cited by this paper
• A census of glutamine/asparagine-rich regions: implications for their conserved function and the prediction of novel prions.

  2000cited by this paper
• A homologue of the yeast HOP1 gene is inactivated in the Arabidopsis meiotic mutant asy1

  2000cited by this paper
• A central role for cohesins in sister chromatid cohesion, formation of axial elements, and recombination during yeast meiosis.

  1999cited by this paper
• The Yeast Red1 Protein Localizes to the Cores of Meiotic Chromosomes

  1997cited by this paper
• An atypical topoisomerase II from archaea with implications for meiotic recombination

  1997cited by this paper
• Interhomolog bias during meiotic recombination: meiotic functions promote a highly differentiated interhomolog-only pathway.

  1997cited by this paper
• Meiosis-specific DNA double-strand breaks are catalyzed by Spo11, a member of a widely conserved protein family.

  1997cited by this paper
• Zip1-induced changes in synaptonemal complex structure and polycomplex assembly

  1995cited by this paper
• ZIP1 is a synaptonemal complex protein required for meiotic chromosome synapsis.

  1993cited by this paper
• Evolutionary Genetics and Environmental Stress

  1991cited by this paper
• The HOP1 gene encodes a meiosis-specific component of yeast chromosomes.

  1990cited by this paper
• Effects of elevated temperature on meiotic chromosome synapsis in Allium ursinum

  1989cited by this paper
• The effect of temperature on recombination activity in testes of rodents.

  1988cited by this paper
• Four effects of elevated temperature on chiasma formation in the locust Schistocerca gregaria

  1988cited by this paper
• Evolutionary rates: effects of stress upon recombination

  1988cited by this paper
• Stage dependency of high-temperature effect on homoeologous chromosome pairing in wheat-rye F1 plants

  1982cited by this paper
• Inferences from genetical evidence on the course of meiotic chromosome pairing in plants.

  1977cited by this paper
• Species of the subgenus Schizotrypanum other than Trypanosoma cruzi and their potential usefulness in the laboratory.

  1976cited by this paper
• An analysis of temperature-dependent asynapsis in Triticum aestivum

  1972cited by this paper
• Related and unrelated changes in conversion and recombination frequencies with temperature in Sordaria fimicola, and their relevance to hybrid-DNA models of recombination.

  1969cited by this paper
• GENETIC RECOMBINATION IN COPRINUS. I. ITS PRECISE TIMING AS REVEALED BY TEMPERATURE TREATMENT EXPERIMENTS

  1969cited by this paper
• Temperature and chiasma formation in Schistocerca gregaria

  1963cited by this paper
• Temperature and chiasma formation in Schistocerca gregaria

  1962cited by this paper
• Temperature effect on chiasma frequency in the bluebell endymion nonscriptus

  1959cited by this paper
• The influence of temperature on meiosis

  1957cited by this paper
• The effect of temperature on chiasma frequency

  1955cited by this paper
• Mechanism of Crossing-over

  1946cited by this paper
• Influence of Temperature on Crossing-over in Drosophila

  1936cited by this paper
• The Mechanism of Crossing-Over

  1916cited by this paper
• Rothamsted Repository Download

  year unknowncited by this paper

• Meiosis in bulbous flower species Lycoris: dances underground

  2026cites this paper
• Regulatory mechanisms of plant meiosis.

  2025cites this paper
• Recombination plasticity in response to temperature variation in reptiles

  2025cites this paper
• Impacts of temperature on recombination rate and meiotic success in thermotolerant and cold-tolerant yeast species

  2025cites this paper
• Multiple Autopolyploid Arabidopsis lyrata Populations Stabilized by Long-Range Adaptive Introgression Across Eurasia

  2025cites this paper
• TempGA: A Temperature-Inspired Adaptive Genetic Algorithm for Solving 7DOF Inverse Kinematics Problems

  2025cites this paper
• Cohesin variants and meiotic timing shape chromosome segregation accuracy.

  2025cites this paper
• Unprecedented chromosome ring formation at anaphase poles during first reduction division in Tradescantia spathacea Sw.

  2025cites this paper
• Heat shock protein 101 safeguards meiotic thermotolerance of male germlines in rice and Arabidopsis

  2025cites this paper
• Expanding horizons of ecological and evolutionary research in urban heat islands.

  2025cites this paper
• The interplay of recombination landscape and a transposable element in European populations of Chironomus riparius

  2025cites this paper
• Diversification and recurrent adaptation of the synaptonemal complex in Drosophila

  2024cites this paper
• Pinpointing the timing of meiosis: a critical factor in evaluating the impact of abiotic stresses on the fertility of cereal crops

  2024cites this paper
• Histone methyltransferase NSD modulates gene silencing mechanisms on Drosophila chromosome 4.

  2024cites this paper
• Temperature affects recombination rate plasticity and meiotic success between thermotolerant and cold tolerant yeast species

  2024cites this paper
• Multiple polyploidizations in Arabidopsis lyrata stabilized by long-range adaptive introgression across Eurasia

  2024cites this paper
• Temperature regulates negative supercoils to modulate meiotic crossovers and chromosome organization

  2024cites this paper
• GLUTAMYL-tRNA SYNTHETASE 1 deficiency confers thermo-sensitive male sterility in rice by affecting ROS homeostasis.

  2024cites this paper
• Simulated climate change and atrazine contamination can synergistically impair zebrafish testicular function.

  2024cites this paper
• Meiosis through three centuries

  2024cites this paper
• Molecular Mechanisms of Male Sterility in Maize

  2024cites this paper
• Asynapsis and meiotic restitution in tomato male meiosis induced by heat stress

  2023cites this paper
• Meiosis: Dances Between Homologs.

  2023cites this paper
• Meiotic instability and irregular chromosome pairing underpin heat-induced infertility in bread wheat carrying the Rht-B1b or Rht-D1b Green Revolution genes.

  2023cites this paper
• DMC1 stabilizes crossovers at high and low temperatures during wheat meiosis

  2023cites this paper
• Meiotic chromosome organization and its role in recombination and cancer.

  2023cites this paper
• Sexual dimorphic regulation of recombination by the synaptonemal complex in C. elegans

  2022cites this paper
• Transcriptomic Analysis on the Effects of Altered Water Temperature Regime on the Fish Ovarian Development of Coreius guichenoti under the Impact of River Damming

  2022cites this paper
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  2022cites this paper
• Temperature sensitivity of DNA double-strand break repair underpins heat-induced meiotic failure in mouse spermatogenesis

  2022cites this paper
• Adaptive Control of the Meiotic Recombination Landscape by DNA Site-dependent Hotspots With Implications for Evolution

  2022cites this paper
• Heat shock protein 101 contributes to the thermotolerance of male meiosis in maize.

  2022cites this paper
• Eco-evolution from deep time to contemporary dynamics: The role of timescales and rate modulators.

  2022cites this paper
• Interfered Chromosome Pairing Promotes Meiosis Instability of Autotetraploid Arabidopsis by High Temperatures

  2021cites this paper
• Interplay between Pds5 and Rec8 in regulating chromosome axis length and crossover frequency

  2021cites this paper
• Heat stress interferes with formation of double-strand breaks and homolog synapsis.

  2021cites this paper
• Male meiotic recombination rate varies with seasonal temperature fluctuations in wild populations of autotetraploid Arabidopsis arenosa

  2021cites this paper
• Mechanistic Insights of High Temperature-Interfered Meiosis in Autotetraploid Arabidopsis thaliana

  2021cites this paper
• Loss of obligate crossovers, defective cytokinesis and male sterility in barley caused by short-term heat stress

  2021cites this paper
• SYP-5 regulates meiotic thermotolerance in Caenorhabditis elegans

  2021cites this paper
• Heat stress reveals the existence of a specialized variant of the pachytene checkpoint in meiosis of Arabidopsis thaliana

  2021influential citation
• Evolution and Plasticity of Genome-Wide Meiotic Recombination Rates.

  2021cites this paper
• Heat stress reveals a specialized variant of the pachytene checkpoint in meiosis of Arabidopsis thaliana

  2021cites this paper
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  2021cites this paper
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  2021cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2020cites this paper
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  2019cites this paper
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  2019cites this paper
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  2019cites this paper
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  2019cites this paper
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  2019cites this paper
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  2019cites this paper
• Leagues of their own: sexually dimorphic features of meiotic prophase I

  2019cites this paper
• Cold Influences Male Reproductive Development in Plants: A Hazard to Fertility, but a Window for Evolution

  2019cites this paper
• A common genomic code for chromatin architecture and recombination landscape

  2018cites this paper
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  2018influential citation
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  2018cites this paper
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  2018cites this paper
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  2018cites this paper
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  2018cites this paper
• Elevated temperature increases meiotic crossover frequency via the interfering (Type I) pathway in Arabidopsis thaliana

  2018cites this paper
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  2017influential citation
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  2017cites this paper
• Low recombination rates in sexual species and sex–asex transitions

  2017cites this paper
• Investigation of natural genetic modifiers of meiotic crossover frequency in Arabidopsis thaliana

  2017cites this paper
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  2017influential citation