Pollen sequencing reveals barriers and aberrant patterns of recombination in interspecific tomato hybrids

Abstract

Tomato is the most consumed vegetable in the world. Increasing its natural resistance and resilience is key for ensuring food security within a changing climate. Plant breeders improve those traits by generating crosses of cultivated tomatoes with their wild relatives. Specific allele introgression relying on meiotic recombination, is hampered by structural divergence between parental genomes. However, previous studies of interspecific tomato hybridization focused in single cross or lacked resolution due to prohibitive sequencing costs of large segregating populations. Here, we used pooled-pollen sequencing to reveal unprecedented details of recombination patterns in five interspecific tomato hybrids. We detected hybrid-specific recombination coldspots that underscore the influence of structural divergence in shaping recombination landscape. Crossover regions and coldspots show strong association with specific TE superfamilies exhibiting differentially accessible chromatin between somatic and meiotic cells. We also found gene complexes associated with metabolic processes, stress resistance and domestication syndrome traits, revealing undesired consequences of recombination suppression to phenotypes. Finally, we demonstrate that by using resequencing data of wild and domesticated tomato populations, we can screen for alternative parental genomes to overcome recombination barriers. Overall, our results will allow breeders better informed decisions on generating disease-resistant and climate-resilient tomato.

The role of recombination landscape in species hybridisation and speciation

“…Introgression in barley is rapidly driven to fixed homozygosity, as expected for a strictly self-fertilising species (Dreissig et al, 2020). Crossovers, recombination and introgression were also found to be nearly absent in the centromeric and pericentromeric regions in Mimulus cardinalis (Nelson et al, 2021) and tomatoes (Demirci et al, 2017;Fuentes et al, 2020) (with the exception of scattered recombination hotspots in these regions: Fuentes et al, 2022b).…”

“…Many plant studies have also demonstrated that recombination rate is lower in pericentromeric regions, including in common beans (Bhakta et al, 2015), wheat (Jordan et al, 2018), barley (Dreissig et al, 2019;Dreissig et al, 2020), rice (Fayos et al, 2022) and white campion (Filatov, 2023). Others have shown that crossover rate (which is directly correlated with recombination rate) is lower in these regions in tomatoes (Demirci et al, 2017;Fuentes et al, 2020, Fuentes et al, 2022b and wheat (Jordan et al, 2018). Nyine et al (2020) also showed that introgression is less frequent in lowrecombining regions in winter wheat and its relatives.…”

“…The concept of suppression of recombination as the basis of divergence maintenance is not new, with studies examining both collinear genomes (Butlin, 2005;Feder et al, 2012a, b), and genomes with rearrangements in form of structural variants and chromosomal inversions (e.g. Roesti et al, 2014;Twyford and Friedman, 2015;Moyers et al, 2018;Todesco et al, 2020;Fuentes et al, 2022b). Felsenstein (1981) had proposed that in the speciation with gene flow model, the role of suppressed recombination is to secure linkage disequilibrium between locally adaptive alleles and those for non-random mating.…”

Genes involved in auxin biosynthesis, transport and signalling underlie the extreme adventitious root phenotype of the tomato aer mutant

“…On the other hand, the large BSA peak on chromosome 9 overlaps with the Tm-2 a introgression of S. peruvianum in AC- Tm-2 a and the long causative region of aer on chromosome 4 appears to be related to S. pimpinellifolium . These two regions with a distant genetic origin possess abundant polymorphisms between the parental lines, which can lead to recombination “cold spots” (Chetelat et al 2000 ; Fuentes et al 2022 ) and result in very few recombination events through these regions (Figure S5 ). The pool of 45 AR + lines did not show the extreme AR phenotype of aer , since the additional causative loci segregated randomly in the F 2 lines.…”