Gametophytic and zygotic selection leads to segregation distortion through in vivo induction of a maternal haploid in maize

Abstract

Production of maternal haploids via a male inducer can greatly accelerate maize breeding and is an interesting biological phenomenon in double fertilization. However, the mechanism behind haploid induction remains elusive. Segregation distortion, which is increasingly recognized as a potentially powerful evolutionary force, has recently been observed during maternal haploid induction in maize. The results present here showed that both male gametophytic and zygotic selection contributed to severe segregation distortion of a locus, named segregation distortion 1 (sed1), during maternal haploid induction in maize. Interestingly, analysis of reciprocal crosses showed that sed1 is expressed in the male gametophyte. A novel mapping strategy based on segregation distortion has been used to fine-map this locus. Strong selection for the presence of the sed1 haplotype from inducers in kernels with haploid formation and defects could be detected in the segregating population. Dual-pollination experiments showed that viable pollen grains from inducers had poor pollen competitive ability against pollen from normal genotypes. Although defective kernels and haploids have different phenotypes, they are most probably caused by the sed1 locus, and possible mechanisms for production of maternal haploids and the associated segregation distortion are discussed. This research also provides new insights into the process of double fertilization.

The Genetic Basis of Haploid Induction in Maize Identified with a Novel Genome-Wide Association Method

“…Three of these genes in the qhir12 region, GRMZM2G137502 and GRMZM2G135834, each encoding a DNA binding protein, and GRMZM2G096682, encoding an amino acid binding protein, constitute intuitive candidates for triggering HI in maize. In agreement with both hypotheses for in vivo HI in maize (Sarkar and Coe 1966;Beckert et al 2008;Li et al 2009;Xu et al 2013) and characters associated with HI (Prigge et al 2012;Qiu et al 2014), their mutant versions might be involved in chromosomal segregation distortion. Besides the structural candidates identified in the coding sequences of these genes, we cannot exclude that the causal mutation is located in a regulatory region as has been shown for other genes (e.g., Hanson et al 1996;Clark et al 2006;Salvi et al 2007).…”

“…The success of this new technology became possible, because dozens of maize inducer lines have been developed worldwide (reviewed in Supplemental Material, File S1) which, when used as pollinators, trigger the production of seeds with haploid embryo at an acceptable rate, i.e., .2% . Double fertilization followed by elimination of the inducer chromosomes in the embryo at later developmental stages (Li et al 2009;Xu et al 2013) as well as parthenogenesis (Sarkar and Coe 1966;Beckert et al 2008) HI in maize, but a proof of these hypotheses requires profound knowledge about the genetic and physiological factors underlying this phenomenon. All previous QTL mapping studies for unraveling the genetic architecture of HI detected a major QTL on chromosome 1 (Röber 1999;Beckert et al 2008; Prigge et al 2012).…”

“…If some of these controls have been misclassified and possess HI ability, in contrast to our assumption, this has no effect on the first step of our CHE approach and would merely reduce the power of the test in the second step but would not result in false positives. However, presence of HI in germplasm not selected for this trait is very unlikely for the following reasons: (i) In vivo HI in maize is associated with endosperm abortion, embryo abortion, and segregation distortion (Prigge et al 2012;Xu et al 2013). Maintenance breeding of inducers requires continuous selection for HI to counteract the strong negative effects on fitness of this character (Melchinger et al 2016).…”

Fertilization and Uniparental Chromosome Elimination during Crosses with Maize Haploid Inducers

“…One is using an ig mutant to generate both maternal and paternal haploids (Kermicle, 1969;Evans, 2007), and the other is using Stock6-derived inducers to produce maternal haploids only. The application of Stock6-derived inducers has become the foundation for modern DH technology (Prigge and Melchinger, 2012;Xu et al, 2013). The haploid induction rate (HIR) of inducer line Stock6 is 1% to 2% (Coe, 1959), which is 10 to 20 times higher than the spontaneous HIR in maize.…”

“…The haploidinducing capacity of inducers can be improved by selection (Sarkar et al, 1972). New inducers with improved HIRs have been developed, such as WS14 (2%-5% induction rate; Lashermes et al, 1988), RWS (Röber et al, 2005), and CAU5 (Xu et al, 2013).…”