Elevated temperature increases meiotic crossover frequency via the interfering (Type I) pathway in Arabidopsis thaliana

Autor: Hong Ma, Hongkuan Wang, Gregory P. Copenhaver, Jiyue Huang, Yingxiang Wang, Scott M. Lewis, Alexander R. Bennett, Ashley R. Albright, Jennifer L. Modliszewski
Rok vydání: 2018
Předmět:
0301 basic medicine
Cancer Research
Arabidopsis
Plant Science
Interference (genetic)
Biochemistry
Chromosomal crossover
Chromosome segregation
Gene Expression Regulation
Plant

Plant Resistance to Abiotic Stress
Chromosome Segregation
Arabidopsis thaliana
Cell Cycle and Cell Division
Crossing Over
Genetic

Homologous Recombination
Genetic Interference
Genetics (clinical)
Ecology
biology
Chromosome Biology
Plant Anatomy
Physics
Temperature
Eukaryota
Classical Mechanics
Plants
Cell biology
Nucleic acids
Meiosis
Phenotype
Experimental Organism Systems
Cell Processes
Plant Physiology
Physical Sciences
Pollen
Mechanical Stress
Research Article
lcsh:QH426-470
DNA recombination
Arabidopsis Thaliana
Brassica
Research and Analysis Methods
Chromosomes
Plant

03 medical and health sciences
Model Organisms
Plant and Algal Models
Plant-Environment Interactions
Genetics
Homologous chromosome
Plant Defenses
Molecular Biology
Ecology
Evolution
Behavior and Systematics

Plant Ecology
Ecology and Environmental Sciences
Organisms
Biology and Life Sciences
Cell Biology
DNA
Plant Pathology
biology.organism_classification
lcsh:Genetics
Thermal Stresses
030104 developmental biology
Mutation
Homologous recombination
Zdroj: PLoS Genetics
PLoS Genetics, Vol 14, Iss 5, p e1007384 (2018)
ISSN: 1553-7404
DOI: 10.1371/journal.pgen.1007384
Popis: For most eukaryotes, sexual reproduction is a fundamental process that requires meiosis. In turn, meiosis typically depends on a reciprocal exchange of DNA between each pair of homologous chromosomes, known as a crossover (CO), to ensure proper chromosome segregation. The frequency and distribution of COs are regulated by intrinsic and extrinsic environmental factors, but much more is known about the molecular mechanisms governing the former compared to the latter. Here we show that elevated temperature induces meiotic hyper-recombination in Arabidopsis thaliana and we use genetic analysis with mutants in different recombination pathways to demonstrate that the extra COs are derived from the major Type I interference sensitive pathway. We also show that heat-induced COs are not the result of an increase in DNA double-strand breaks and that the hyper-recombinant phenotype is likely specific to thermal stress rather than a more generalized stress response. Taken together, these findings provide initial mechanistic insight into how environmental cues modulate plant meiotic recombination and may also offer practical applications.
Author summary Meiosis is the cell division used by sexually reproducing species to produce sperm and egg cells. During meiosis, programmed Double Strand Breaks (DSBs) occur on each chromosome, which allows DNA to be exchanged between chromosome pairs, resulting in crossovers (COs). COs are necessary to ensure faithful chromosome segregation during meiosis, and thus fertility, but are also an important source of genetic variation. As such, CO formation is tightly regulated. Despite this, CO frequency can be altered by external factors, such as temperature. In Arabidopsis thaliana, COs are formed through two pathways: interference-sensitive (Type I) and interference-insensitive (Type II). An increase in temperature results in an increase in CO frequency. Using a pollen based assay, we show that COs are formed in the Type I pathway, which accounts for approximately 85% of the COs in Arabidopsis. To investigate whether temperature-dependent COs are the result of additional DSBs, we used immunological staining to examine protein foci, which mark the sites of DSBs. We discovered that temperature likely increases CO frequency by shifting alternative repair outcomes, called non-crossovers, to favor additional COs, rather than by increasing DSBs. Lastly, we found that temperature is not a general stress response, as plants subject to salt stress did not exhibit an increase in CO frequency. Our results may prove valuable in aiding plant breeding by enhancing our ability to rapidly introgress suites of elite traits from wild-plants into their crop relatives, a method that is particularly attractive as it does not require genetic modifications.
Databáze: OpenAIRE