Hybridization Alters Spontaneous Mutation Rates in a Parent-of-Origin-Dependent Fashion in Arabidopsis  

Abstract

Over 70 years ago, increased spontaneous mutation rates were observed in Drosophila spp. hybrids, but the genetic basis of this phenomenon is not well understood. The model plant Arabidopsis (Arabidopsis thaliana) offers unique opportunities to study the types of mutations induced upon hybridization and the frequency of their occurrence. Understanding the mutational effects of hybridization is important, as many crop plants are grown as hybrids. Besides, hybridization is important for speciation and its effects on genome integrity could be critical, as chromosomal rearrangements can lead to reproductive isolation. We examined the rates of hybridizationinduced point and frameshift mutations as well as homologous recombination events in intraspecific Arabidopsis hybrids using a set of transgenic mutation detector lines that carry mutated or truncated versions of a reporter gene. We found that hybridization alters the frequency of different kinds of mutations. In general, Columbia (Col) 3 Cape Verde Islands and Col 3 C24 hybrid progeny had decreased T→G and T→A transversion rates but an increased C→T transition rate. Significant changes in frameshift mutation rates were also observed in some hybrids. In Col 3 C24 hybrids, there is a trend for increased homologous recombination rates, except for the hybrids from one line, while in Col 3 Cape Verde Islands hybrids, this rate is decreased. The overall genetic distance of the parents had no influence on mutation rates in the progeny, as closely related accessions on occasion displayed higher mutation rates than accessions that are separated farther apart. However, reciprocal hybrids had significantly different mutation rates, suggesting parentof-origin-dependent effects on the mutation frequency.In plants, somatic mutations are an important source of genetic variability, which can, in principle, be passed on as heritable changes to the progeny of an individual (Baake and Gabriel, 1999). Plants have higher point mutation rates than animals (Kovalchuk et al., 2000) and do not have a fixed germline, such that there is a chance for somatic mutations to be transmitted to the next generation (Walbot and Evans, 2003). In contrast, animals cannot transmit somatic mutations to their progeny, as their germline cells are set aside early during development.Mutation rates have been estimated in several organisms, including bacteria and mammals (Kovalchuk et al., 2000). The easiest phenotype for estimating mutation rates in plants is chlorophyll deficiency or albinism. In barley (Hordeum vulgare), it was estimated that albino phenotypes can result from mutations in about 300 different nuclear genes (Klekowski, 1992). Mutations leading to chlorophyll deficiency in barley and buckwheat (Fagopyrum esculentum) occur at rates of 3.2 3 10 24 and 3.1 3 10 24 events per nuclear genome per generation, respectively. In long-lived red mangrove (Rhizophora mangle) plants, this rate was found to be 25 times higher, which led to the prediction that long-lived plants have higher mutation rates per...

Mutation rate analysis via parent–progeny sequencing of the perennial peach. I. A low rate in woody perennials and a higher mutagenicity in hybrids

“…While Duncan found few mutations and considered the hypothesis thus unlikely, his analysis was influential. Indeed, what several more recent authors [15–17] now consider the seminal paper on the hybridization–mutation hypothesis, that of Sturtevant [18], was directly influenced by Duncan [9] and Belgovsky [19]. Both Sturtevant and Belgovsky found increased mutation rates in hybrids in flies.…”

“…Both Sturtevant and Belgovsky found increased mutation rates in hybrids in flies. Intraspecific mating between populations [15,20] can also affect the mutation rate. The extent to which these effects are observed outside of flies (where the effect is probably owing to P element hybrid dysgenesis) is poorly resolved (but see e.g.…”

Parental Age Affects Somatic Mutation Rates in the Progeny of Flowering Plants

“…Also, hybridization has been shown to alter the cell number and average ploidy per nucleus (Bashir et al, 2014). Therefore, it is important to normalize mutation rates by factoring in cell number, cell size, and average ploidy per nucleus in the progenies derived from parents of different age.…”

“…Taking advantage of the plant model system Arabidopsis, in which various somatic mutation rates can readily be assessed (Bashir et al, 2014), we investigated the effects of parental reproductive age on somatic mutation rates in the progeny. We report that there is a pronounced effect of parental age on somatic mutation rates in their offspring in a parent-of-origin-dependent fashion.…”

Susceptibility pays off: insights into the mlo-based powdery mildew resistance

“…Spontaneous mutations in Arabidopsis are known to take place at a rate of 10 -7 to 10 -8 bp/generation (Kovalchuk et al, 2000;Bashir et al, 2014). Anyway, it is reported that the large majority of spontaneous mutations are G/ CA/T transitions (Ossowski et al, 2009).…”