The maternal cytoplasmic environment may be involved in the viability selection of gametes and zygotes

Abstract

Segregation distortion is the phenomenon whereby the observed genotypic frequencies of a locus fall outside the expected Mendelian segregation ratio, and it is increasingly recognised as a potentially powerful evolutionary force. The main reason for segregation distortion is a difference in the viability of gametes and zygotes caused by viability loci in the segregating progeny. However, the maternal cytoplasm may also be involved in the viability selection of gametes and zygotes. The objectives of this study were to map the segregation distortion loci (SDL) in maize and to test the hypothesis that the viability of gametes and zygotes may also be associated with the maternal cytoplasmic environment. In the present study, a reciprocal mating design was conducted to generate an F2-segregating population. A linkage map was constructed with 126 microsatellite markers. A whole-genome scan was performed to detect the SDL in segregating populations with different maternal cytoplasm environments. Altogether, 14 SDL with strong LOD (logarithm (base 10) of odds) supports were identified in the specifically designed F2 populations. Interestingly, we found dramatic changes in the genotypic frequencies of the SDL in the two maternal cytoplasmic backgrounds, which indicated a change in the viability of gametes and zygotes in different cytoplasmic environments. Furthermore, in the JB cytoplasmic background, most of the detected SDL and complete distortion markers exhibited similar bias patterns favouring the Y53 alleles. These results suggested that selfish cytoplasmic elements may have an important role in shaping the patterns of segregation distortion in F2 populations through selective viability of gametes and zygotes. Heredity Keywords: segregation distortion; cytoplasm; selection; viability; maize INTRODUCTION Segregation distortion, also called transmission ratio distortion, is the phenomenon whereby alleles at a locus deviate from the Mendelian expectation. This phenomenon has been described in many species, including maize (Lu et al., 2002), rice (Yamagishi et al., 2010), eggplant (Barchi et al., 2010), alfalfa (Li et al., 2011), mouse (Casellas et al., 2010 and drosophila (Orr and Irving, 2005;Phadnis, 2011). These alleles, also called segregation distorters, might alter the transmission ratio in specific cases and are considered selfish genetic elements that manipulate Mendelian transmission to their own advantage (Hurst and Werren, 2001;Phadnis and Orr, 2009;Werren, 2011). Evolutionary research suggests that segregation distorters may be involved in promoting population divergence and, ultimately, speciation (Phadnis and Orr, 2009;McDermott and Noor, 2010). A variety of physiological and genetic factors may explain the observed segregation distortion. For example, meiotic drive, the preferential selection that occurs during meiosis, may cause certain alleles to be overrepresented in the gametes (McDermott and Noor, 2010). As a result, distorted Mendelian ratios may be observed in offspring that have undergone genot...

Identification and Characterization of Segregation Distortion Loci on Cotton Chromosome 18

“…The other SDL likely reflected zygotic selection. These results provided a better understanding of the putative mechanism of SD, which has been reported in many plant species (Anhalt et al, 2008; Fishman et al, 2008; Cai et al, 2011; Castro et al, 2011; Diouf and Mergeai, 2012; Tang et al, 2013). …”

“…Tang et al (2013) showed that the maternal cytoplasmic environment might be involved in the viability selection of gametes and zygotes resulting from dramatic changes in the genotypic frequencies of the SDL in the two reciprocal cross populations. In the present study, six out of eleven SDL on chromosome 18 were dependent on the cytoplasmic environment, but other SDL were not.…”

“…The detailed procedure is available in the PROC QTL manual 2 . In the output result table, the loci were designated as significant SDL with a LOD value of 3.0 (Tang et al, 2013). …”

“…This phenomenon is commonly detected via genetic mapping and has been documented in various species, including mouse (Eversley et al, 2010; Casellas et al, 2012), Drosophila (Phadnis and Orr, 2009; Larracuente and Presgraves, 2012; McDermott and Noor, 2012), Tigriopus (Pritchard et al, 2011), rice (Koide et al, 2012; Reflinur et al, 2014; Xu et al, 2014), maize (Tang et al, 2013), and cotton (Yu et al, 2011; Hulse-Kemp et al, 2015). SD, a powerful evolutionary force, has been suggested as a selection mechanism among different gametophyte and/or sporophyte genotypes (Sandler and Novitski, 1957).…”

Potential Involvement of Maternal Cytoplasm in the Regulation of Flowering Time via Interaction with Nuclear Genes in Maize

“…In our previous study (Tang et al, 2013a), several segregation distortion loci (SDL) were identified in two cytoplasm background PROC QTL procedures proposed by Hu and Xu (2009). In our previous study (Tang et al, 2013a), several segregation distortion loci (SDL) were identified in two cytoplasm background PROC QTL procedures proposed by Hu and Xu (2009).…”