Intragenomic Conflict Between the Two Major Knob Repeats of Maize

Abstract

Examples of meiotic drive, the non-Mendelian segregation of a specific genomic region, have been identified in several eukaryotic species. Maize contains the abnormal chromosome 10 (Ab10) drive system that transforms typically inert heterochromatic knobs into centromere-like domains (neocentromeres) that move rapidly poleward along the spindle during meiosis. Knobs can be made of two different tandem repeat sequences (TR-1 and 180-bp repeat), and both repeats have become widespread in Zea species. Here we describe detailed studies of a large knob on chromosome 10 called K10L2. We show that the knob is composed entirely of the TR-1 repeat and is linked to a strong activator of TR-1 neocentromere activity. K10L2 shows weak meiotic drive when paired with N10 but significantly reduces the meiotic drive exhibited by Ab10 (types I or II) in Ab10/K10L2 heterozygotes. These and other data confirm that (1) there are two separate and independent neocentromere activities in maize, (2) that both the TR-1 and knob 180 repeats exhibit meiotic drive (in the presence of other drive genes), and (3) that the two repeats can operate in competition with each other. Our results support the general concept that tandem repeat arrays can engage in arms-race-like struggles and proliferate as an outcome.A S a general rule eukaryotic chromosome movement is mediated by kinetochore proteins, which bridge the interaction between the centromeric DNA and the spindle microtubules. As cell division proceeds, the centromeres move toward spindle poles, while the chromosome arms drag behind. However, genes on a chromosome 10 variant in maize known as Abnormal chromosome 10 (Ab10) change this dynamic by providing heterochromatic regions called knobs the means to move poleward along the microtubule lattice during meiosis. Each knob may be composed of thousands of tandem repeats that are clearly separated into two distinct homology groups, the 350-bp TR-1 repeat and the 180-bp repeat (Peacock et al. 1981;Ananiev et al. 1998). When Ab10 confers activity to knobs they are referred to as neocentromeres (Rhoades 1952). Ab10 contains the genes that activate neocentromeres and other unknown functions that together cause the preferential transmission of knobbed chromosomes to progeny in a process known as meiotic drive (Longley 1945;Kikudome 1959;Rhoades and Dempsey 1988a).Structurally, Ab10 is similar to the canonical chromosome 10 (N10), but contains a large haplotype on the end of its long arm (Mroczek et al. 2006) (Figure 1A). The Ab10 haplotype contains the genes required for neocentromere activity and meiotic drive, as well as long arrays of both types of knob repeats (Hiatt and Dawe 2003a). Hundreds of other genes are present within the haplotype and are allelic with similar genes on N10; however, Ab10 and N10 do not recombine in this area due to the presence of multiple rearrangements (Mroczek et al. 2006). There are two well-studied cytological variants of the Ab10 haplotype that differ primarily by the size and repeat content of their knob...

European maize genomes unveil pan-genomic dynamics of repeats and genes

“…Consistent with fiber-FISH studies, we also detected numerous locations of the 180 bp knob repeat unit throughout the chromosome assemblies [50]. These widespread knob repeats affected gene density and expression levels of adjacent genes adding further complexity to known effects of large-scale knobs in maize on recombination rates, meiotic drive and phenotypic traits like flowering time [29,51,52]. WGAs enabled to identify long runs of pairwise and higher-order combinations of genomic regions with identical haplotypes.…”

Endogenous pararetrovirus sequences associated with 24 nt small RNAs at the centromeres of Fritillaria imperialis L. (Liliaceae), a species with a giant genome

“…Malik and Henikoff () suggested a model for centromeric repeat proliferation involving meiotic drive: the non‐Mendelian segregation of chromosomes bearing certain sequences during meiosis leading to their preferential inheritance (Kanizay and Dawe, ; Kanizay et al ., ). If the presence of FriEPRV sequences at centromeres causes (or at some point during its evolution has caused) meiotic drive, it is likely that FriEPRV will spread (or have spread), as chromosomes with more centromeric FriEPRV sequences will be preferentially inherited.…”

“…If the presence of FriEPRV sequences at centromeres causes (or at some point during its evolution has caused) meiotic drive, it is likely that FriEPRV will spread (or have spread), as chromosomes with more centromeric FriEPRV sequences will be preferentially inherited. This has been reported for heterochromatin in maize ( Zea mays ) and centromeric repeats in other grasses (Kanizay and Dawe, ; Kanizay et al ., ). It also agrees with the theory of ‘boom–burst’ cycles in the evolution of centromere sequences (Zhang et al ., ).…”

Normal Segregation of a Foreign-Species Chromosome During Drosophila Female Meiosis Despite Extensive Heterochromatin Divergence

“…It remains an open question whether meiotic drivers are truly rare in nature, or instead whether higher frequency variants exist that cause lower level drive that is beyond the limit of detection in small-scale experiments. A major hurdle in resolving this question is the difficulty of reliably detecting weak meiotic drive effects, one example being the maize chromosomal knob K10L2 (Kanizay et al 2013).…”