Gametocidal genes: biological mechanisms owing to hybrid dysgenesis in crop breeding, challenges and innovation

Climate change and population growth are major threats to global food security. Many cultivated crops remain vulnerable due to reduced genetic variation. Wild relatives and diverse accessions of crop species are being used to reintroduce diversity into their genomes to help contend with these issues. However, in some species, notably Triticum aestivum, Oryza spp., Solanum lycopersicum, Zea mays and Nicotiana spp., Arabidopsis thaliana and their wild relatives, gamete-killing genes may be responsible for the occurrence of hybrid dysgenesis through the targeting of reproductive cells that do not contain the gene.

This article explores gametocidal genes, 'pollen killers' or 'gamete killers', and toxin-antidote systems that result in sterility, alongside potential biological mechanisms. Gametocidal genes from wheat wild relatives significantly impact breeding programmes: wild relatives may contain useful germplasm but also gametocidal genes resulting in disastrous effects, including yield reductions. Due to their preferential transmission, gametocidal genes are extremely difficult to remove, therefore gene characterization is necessary. Hybrid sterility loci in Oryza spp. have been addressed, highlighting those that function similarly to gametocidal genes. We collate recent evidence to appraise the merit of biological mechanism hypotheses and suggest how recent innovations may improve characterization. Additionally, the challenges that they contribute to breeding programmes and subsequent successes are highlighted. In light of genetic innovation, we suggest contexts where a revival of using gametocidal genes may be beneficial, alongside novel techniques for research.

Past research has identified unique characteristics of gametocidal genes, leading to theories such as the dual-mechanism and restriction-modification models to explain the mechanisms. However, recent research suggests that complex genetic factors such as transposable elements and epigenetics may account for the phenomenon. Future work towards mapping these genes is hopeful: innovations in sequencing, bioinformatics and genomic data have improved the ability to precisely identify the elusive gametocidal genes.