Significance: Meiotic crossovers (COs) are required for accurate chromosome segregation and mix parental genomes to generate genetically diversified gametes. The distribution of COs among chromosomes is not random. In most organisms, at least one CO is formed between each chromosome pair. However, the molecular mechanisms controlling CO distribution are not well understood. Here, we found that Arabidopsis AtFANCD2, AtFANCM, AtFIGL1, and AtRMI1 promote normal distribution of Class I CO to maintain CO assurance in addition to their previously described roles in regulating Class II CO number. These factors, alone or in combination, appear to control ∼50% of the variation between wild-type and random distributions. These discoveries provide genetic insights into understanding of the regulation of CO distribution among chromosomes.

Meiotic recombination increases genetic diversity and manipulation of its frequency and distribution holds great promise in crop breeding. In Arabidopsis thaliana, FANCM (a homolog of mammalian Fanconi anemia complementation group M) suppresses recombination and its function seems conserved in other species including the rosids Brassica spp. and pea (Pisum sativum), and the monocot rice (Oryza sativa). To examine the role of FANCM during meiotic recombination in lettuce (Lactuca sativa, an asterid), we characterized the function of lettuce LsFANCM and found that it can functionally substitute for AtFANCM in transgenic Arabidopsis plants. Moreover, three independent CRISPR/Cas9-edited lettuce Lsfancm mutants showed reduced pollen viability and seed setting. Unexpectedly, analyses of chromosome behavior revealed that 77.8% of Lsfancm meiocytes exhibited univalents. The normal formation of double-strand breaks in DNA and the discontinuous assembly of synaptonemal complex in Lsfancm mutants supports the hypothesis that LsFANCM might be dispensable for the initiation of meiotic recombination but required for normal synapsis. Furthermore, the frequency of lettuce HEI10 (Human Enhancer of Invasion 10) foci, a marker for Class-I crossovers (COs), was similar between wild-type (WT) and Lsfancm. Strikingly, the distribution of LsHEI10 foci and chiasmata in Lsfancm meiotic chromosomes was markedly different from the WT. A similar alteration in the distribution of Class-I COs was also observed in the Arabidopsis Atfancm mutant. Taken together, these results demonstrate that FANCM is important for shaping the distribution of meiotic Class-I COs in plants, and reveal an evolutionarily divergent role for FANCM in meiotic bivalent formation between Arabidopsis and lettuce.

Melon (Cucumis melo) includes more than ten botanical groups, many of which feature netting ornamentation on the surface of mature fruit. Ripe melons display a netted skin that signifies their ripeness and readiness for consumption. Previously, we identified SKIN NETTING (CmSN), which encodes an EamA-like transporter family protein, as the candidate gene controlling fruit skin netting formation in melon, while its biological functions remain unclear. In this study, we demonstrated that the expression of the CmSN gene was considerably lower in netted melons compared to smooth-skinned melons, indicating a negative correlation between CmSN expression and netting formation. Subsequently, we employed transient overexpression and virus-induced gene silencing (VIGS) experiments to explore the role of CmSN gene during fruit development. Overexpression of the CmSN gene inhibited netting development, whereas silencing it promoted netting formation. Using heterologous transformation in tomato, we further confirmed the effect of the CmSN gene on rind texture and toughness, as these tomatoes exhibited rougher and tougher skins. Analysis with near-isogenic lines (NILs) revealed that CmSN gene-bearing fruits (NIL_CmSN) possessed significantly harder rinds than the control smooth-skinned variety HB42, underscoring the role of CmSN in enhancing rind protection. Together, our research offers essential insights into the netting formation and genetic improvement of melon fruits.