FANCM promotes class I interfering crossovers and suppresses class II non-interfering crossovers in wheat meiosis

Abstract

FANCM suppresses crossovers in plants by unwinding recombination intermediates. In wheat, crossovers are skewed toward the chromosome ends, thus limiting generation of novel allelic combinations. Here, we observe that FANCM maintains the obligate crossover in tetraploid and hexaploid wheat, thus ensuring that every chromosome pair exhibits at least one crossover, by localizing class I crossover protein HEI10 at pachytene. FANCM also suppresses class II crossovers that increased 2.6-fold in fancm msh5 quadruple mutants. These data are consistent with a role for FANCM in second-end capture of class I designated crossover sites, whilst FANCM is also required to promote formation of non-crossovers. In hexaploid wheat, genetic mapping reveals that crossovers increase by 31% in fancm compared to wild type, indicating that fancm could be an effective tool to accelerate breeding. Crossover rate differences in fancm correlate with wild type crossover distributions, suggesting that chromatin may influence the recombination landscape in similar ways in both wild type and fancm.

Characterization and acceleration of genome shuffling and ploidy reduction in synthetic allopolyploids by genome sequencing and editing

“…First, plants are more tolerant to harmful genome variations. For example, the mutation of chromosome recombination-related genes such as Fanconi Anemia Complementation Group M ( FANCM ) causes cancers and other severe syndromes in animals but does not cause obvious vegetative or reproductive growth defects in plants ( 10 , 11 ). Second, plants can produce a large number of descendants that allow us to screen large populations for rare mutants and infrequent characters.…”

Exploring impact of recombination landscapes on breeding outcomes

“…These proteins are not meiosis-specific and are also involved in the repair of spontaneous DNA breaks in somatic cells ( 22 ), suggesting that the class II CO pathway may be primarily utilized to resolve defective recombination intermediates. Several proteins affecting class I as well as II COs have been labeled anti-CO factors, including RecQ helicase 4 (RECQ4) ( 23 ), Fanconi Anemia of Complementation group M (FANCM) ( 24 – 26 ), and AAA-ATPase Fidgetin-like-1 (FIGL1) ( 27 ). RECQ4 and FANCM act by dissolving CO intermediates, while FIGL1 is thought to regulate DSB resection and limit strand invasion during DSB repair in class II CO formation.…”

Unravelling mechanisms that govern meiotic crossover formation in wheat

“…A VIGS approach has been utilised to analyse the effect of FANCM hypomorphs on recombination in F 1 tetraploid wheat hybrids, where silencing had no effect on CO numbers, but altered CO distributions [ 55 ]. We have recently shown that FANCM promotes formation of class I COs, whilst preventing the formation of class II COs in tetraploid and hexaploid wheat [ 56 ]. In tetraploid wheat, the gain in class II COs is equal to the loss of class I COs, thus no net change in recombination occurred in fancm .…”

“…However, in the hexaploid fancm null mutant, the loss of class I COs is relatively less than the tetraploid, giving an overall 31% increase in COs. This gain in COs associates with H3K27me3 and the additional COs are likely to be in the same ‘hot’ regions as wild type [ 56 ].…”