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Title: Catastrophic chromosomal restructuring during genome elimination in plants}
Article:
Abstract:
Genome instability is associated with mitotic errors and cancer. This phenomenon can lead to deleterious rearrangements, but also genetic novelty, and many questions regarding its genesis, fate and evolutionary role remain unanswered. Here, we describe extreme chromosomal restructuring during genome elimination, a process resulting from hybridization of Arabidopsis plants expressing different centromere histones H3. Shattered chromosomes are formed from the genome of the haploid inducer, consistent with genomic catastrophes affecting a single, laggard chromosome compartmentalized within a micronucleus. Analysis of breakpoint junctions implicates breaks followed by repair through non-homologous end joining( NHEJ) or stalled fork repair. Furthermore, mutation of required NHEJ factor DNA Ligase 4 results in enhanced haploid recovery. Lastly, heritability and stability of a rearranged chromosome suggest a potential for enduring genomic novelty. These findings provide a tractable, natural system towards investigating the causes and mechanisms of complex genomic rearrangements similar to those associated with several human disorders.
Introduction:
Nucleosomes containing variant histone( centromeric histone H3, CENH3)( Verdaasdonk and Bloom, 2011)( also known as CENP-A) determine centromeres. In the absence of the endogenous CENH3, Arabidopsis thaliana mitotic and meiotic functions can be complemented by chimeric CENH3( Ravi and Chan, 2010; Ravi et al., 2010) or CENH3 from diverged plant species( Maheshwari et al., 2015), but crossing these strains to wild-type individuals results in frequent loss of the chromosomes marked by the variant CENH3. Following stochastic genome elimination in the early mitotic divisions, the progeny can be haploid, aneuploid or diploid( Ravi and Chan, 2010; Ravi et al., 2014). In nature, similar phenomena involve defective CENH3 loading( Sanei et al., 2011). Thus, mating of individuals that express diverged CENH3s, can lead to mitotic catastrophe. The consequences of mitotic malfunction on genome integrity can be dire( McClintock, 1984; Gordon et al., 2012). Missegregated chromosomes can lead to aneuploidy( Janssen et al., 2011), but also to extensive and catastrophic restructuring resulting in, sequentially, chromosome sequestration in micronuclei, endonucleolytic damage, defective repair, and finally rescue( Crasta et al., 2012; Hatch et al., 2013; Zhang et al., 2013). The resulting structurally rearranged chromosomes may contribute to cancer or developmental syndromes( Hastings et al., 2009; Liu et al., 2011; Stephens et al., 2011; Jones and Jallepalli, 2012). Nevertheless, chromosomal rearrangements are not necessarily deleterious: some may influence fitness by altering recombination or gene dosage( Comai et al., 2003). It is possible that pathways leading to disease and to diversity share a common mechanistic basis( Zhang et al., 2013). Genome elimination in Arabidopsis provides a previously lacking organismal system to investigate genome instability during mitotic catastrophes, connected mechanisms, and consequences.
Discussion:
Taken together, our results provide evidence for the occurrence of chromosome restructuring( Cai et al., 2014; Morrison et al., 2014) when diverged individuals hybridize, identifying a centromere-based mechanism for genomic instability. This phenomenon studied here depends on chimeric CENH3, but a similar effect was observed when the haploid inducer strain expresses CENH3 of a close species( Maheshwari et al., 2015), indicating the effectiveness of natural and artificial variation. While the genesis and fate of restructured chromosomes is difficult to study in humans, their formation, effects, and even transmission in Arabidopsis are within experimental reach, as demonstrated by the enhancing effect of NHEJ mutants on haploid induction. The range of phenotypes, the formation of copy variants and of chimeric genes at junctions, and their occasional meiotic transmission, suggest that catastrophic chromosomal restructuring, could contribute to heritable genetic variation.
The genome of an individual organism contains all the instructions needed to build and maintain that individual . Any changes to the DNA in the genome can alter the instructions that are given to cells , which can lead to cancer and other diseases . However , changes to the genome can sometimes be beneficial as they can introduce more variety into the instructions carried by different individuals , which increases their potential to adapt to changes in their environment . In plants and animals , DNA is arranged into structures called chromosomes . Generally , an individual's genome contains two copies of each chromosome; one inherited from their mother and one from their father . However , occasionally during reproduction , all the chromosomes from one of the parents are left out from the cells of the offspring in a process called ‘genome elimination’ . This makes individuals that carry only half the normal number of chromosomes , known as haploids . Sometimes the process of genome elimination is disrupted , which leads to individuals that have incomplete genomes or chromosomes that carry big rearrangements of the DNA , as if they had been shattered and put back together incorrectly . In a small plant known as Arabidopsis thaliana , genome elimination frequently happens in the offspring of two individuals that carry different versions of a gene called centromeric histone H3 ( CENH3 ) . However , it is not clear how this works , or what roles genome elimination plays in evolution and disease . Here , Tan et al . studied genome elimination by cross-breeding Arabidopsis plants that carried a mutant form of CENH3 with plants that have a normal version of the protein . The experiments found that many of the offspring were haploid . Some of the others carried an extra copy of an entire chromosome or a section of a chromosome . A third group had an extra copy of a chromosome that was missing some sections or had been rearranged . These ‘shattered’ chromosomes were always formed from chromosomes that came from the parent plant with a mutant form of CENH3 . Tan et al . also found that a protein called DNA Ligase 4 , which helps reconnect broken DNA strands , is involved in repairing the breaks in these shattered chromosomes . Some of the genetic rearrangements documented in the experiments were passed on to subsequent generations of plants , which suggests that these genomic changes can be stable enough to be inherited . The genomic rearrangements observed in the Arabidopsis plants are similar to those seen in patients with cancer and other genetic diseases . Tan et al . findings show that Arabidopsis plants provide a useful system for studying these genome rearrangements , which may inform efforts to treat these human diseases .