Decision letter: Catastrophic chromosomal restructuring during genome elimination in plants

Abstract

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.