Gametocidal genes: from a discovery to the application in wheat breeding

Abstract

Some species of the genus Aegilops, a wild relative of wheat, carry chromosomes that after introducing to wheat exhibit preferential transmission to progeny. Their selective retention is a result of the abortion of gametes lacking them due to induced chromosomal aberrations. These chromosomes are termed Gametocidal (Gc) and, based on their effects, they are categorized into three types: mild, intense or severe, and very strong. Gc elements within the same homoeologous chromosome groups of Aegilops (II, III, or IV) demonstrate similar Gc action. This review explores the intriguing dynamics of Gc chromosomes and encompasses comprehensive insights into their source species, behavioral aspects, mode of action, interactions, suppressions, and practical applications of the Gc system in wheat breeding. By delving into these areas, this work aims to contribute to the development of novel plant genetic resources for wheat breeding. The insights provided herein shed light on the utilization of Gc chromosomes to produce chromosomal rearrangements in wheat and its wild relatives, thereby facilitating the generation of chromosome deletions, translocations, and telosomic lines. The Gc approach has significantly advanced various aspects of wheat genetics, including the introgression of novel genes and alleles, molecular markers and gene mapping, and the exploration of homoeologous relationships within Triticeae species. The mystery lies in why gametes possessing Gc genes maintain their normality while those lacking Gc genes suffer abnormalities, highlighting an unresolved research gap necessitating deeper investigation.

Keywords: Aegilops; Gc factors/elements/genes; Triticum; gametocidal; pollen-killer; segregation distorter; wheat.

Figure 1

A schematic illustration depicting the Gc action on gametogenesis in wheat (2n + 2 = 42 + 1 Gc´ + 1 alien = 44 chromosomes). Both male and female gametes lacking the Gc genes experience failure or exhibit chromosome abnormalities. Green, brown, and orange arrows indicate alien, Gc, and wheat-alien translocated chromosomes, respectively. Gc´, stands for the Gc chromosome in a monosomic state.

Figure 2

A diagram demonstrates how the restriction-modification system explains chromosome breakage occurring during both gametogenesis (A) and in zygotic cells (B) of wheat, adapted from Tsujimoto (2005) with modifications. RE represents the gene for the restriction enzyme (acting like a scissor), while ME represents the gene for the modification enzyme (acting like a stapler). The RE acts by cleaving specific recognition sites on DNA. However, when these sites are shielded by DNA methylation facilitated by the ME, the RE is unable to cleave. This scenario typically occurs in individuals homozygous for the Gc gene, where chromosome breakage does not occur. The incomplete function of ME can result in the inability to protect all restriction sites, leading to chromosome breakage. Following the meiosis of hemizygotes for the Gc gene, haploid cells lacking the Gc gene are produced. Before the initial mitotic division during gametogenesis, DNA undergoes replication. As these cells lack ME, one strand of the replicated DNA remains unmodified at restriction sites. If the RE persists in the cell longer than ME, or if RE is introduced by other cells, it can cleave the unmodified restriction sites. In the following mitosis, unmodified DNA is cleaved similarly. Consequently, gametes lacking the Gc gene become non-viable. In this model, hemi-modified or hemi-methylated DNA is hypothesized to be susceptible to cleavage by RE, as evidenced by chromosome breakage observed during the first pollen mitosis.

Figure 3

Application of Gc action via chromosome 2C^cy from Ae. cylindrica to induce chromosomal breakage in H. chilense in the background of common wheat. GISH on metaphase spreads showing Ae. cylindrica (red arrows) chromosome 2C^cy (A, B) and H. chilense (green arrows) chromosomes 2H^ch and 7H^ch (A) and 7H^ch (B) in CS genetic background. No chromosomal aberrations showed in the cells carrying monosomic 2C^cy (A, B). However, after selfing or backcrossing, mutations are expected in the following generations in the zygotes lacking the 2C^cy chromosome. Homozygous centromeric translocation (green arrows) 7H^chS·5AL (C), adapted from Mattera et al. (2015) with modifications, and Robertsonian translocation (green arrows) 2H^chS·2DL (D), adapted from Palomino and Cabrera (2019) with modifications. FISH red signals are from probes GAA-satellite sequence (C) and repetitive sequence pAs1 (D). Chromosomes were counterstained with DAPI (blue color).

Figure 4

Breakage by Gc action in chromosomes from wild barley (H. chilense) as alien disomic additions in wheat; adapted from Said and Cabrera (2009) and Said et al. (2012) with modifications. The idiograms (left) in (A-C) show the breakpoints (arrows). Double FISH with the pAs1 (red) and GISH (green) probes on mitotic metaphase of chromosome 3H^ch and its deletions in the genetic background of wheat (A, B). FISH with pAs1 (red) probe on mitotic metaphase of chromosome 4H^ch and its deletion in the genetic background of wheat (C) (Said et al., unpublished). The chromosomes were counterstained with DAPI (blue). Chromosome deletion (del), fraction length (FL), short and long arms (S and L, respectively).

Figure 5

A diagram showing the use of wheat aneuploids carrying rearranged alien chromosomes generated by Gc action for physical mapping of DNA markers/genes on alien chromosomes in wheat. Idiograms I, II, III, IV, V, and VI illustrate translocation between alien short (S)/wheat long (L) arms, translocation between wheat short (S)/alien long (L) arms, deletion in the short arm, deletion in the long arm, telocentric long arm, and telocentric short arm, respectively. The + or – signs indicate the presence or absence, respectively, of markers/genes in the wheat aneuploids, which is directly related to the existent or missing chromatin region.