Haploid Induction and Genome Instability

Advances in DNA sequencing and genome analysis enable both reinterpretation of historical data as well as discovery of plant genome instability in the field and in experimental systems. Genome instability, which in animals is associated with cancer, can be triggered in plants by multiple causes, including crosses between parents with incompatible genomes. Mechanisms leading to instability are common across plant and animal kingdoms, involving failure in chromosome partitioning between dividing cells, DNA breaks, and faulty repair. Haploid induction, an important tool in plant breeding, can result from alteration of a chromatin protein that determines centromeres and promotes genome instability. Plant tolerance to genomic imbalance and to aneuploidy may provide increased opportunity for evolutionary success of karyotypic novelty generated by genome instability. The advent of affordable, large-scale DNA sequencing methods, coupled with advanced computing power, is empowering a detailed analysis of the structure and function of chromosomes. Genomic instability, involving chromosome number and structure changes, has been documented in multiple systems. In plants, haploid induction through genome elimination has recently been connected mechanistically to the formation of complex chromosome reorganizations, known collectively as chromoanagenesis. These abnormalities can be triggered by altering the specialized centromeric histone 3, the epigenetic determinant of centromeres, which leads to loss of centromere function and chromosome missegregation. Other historical and recent instances of genomic instability, at the same time, suggest multiple causes. Their study provides a unique opportunity for a synthesis encompassing genome evolution, its response to stress, as well as the possibility of recruiting the connected mechanisms for genome engineering-based plant breeding. The advent of affordable, large-scale DNA sequencing methods, coupled with advanced computing power, is empowering a detailed analysis of the structure and function of chromosomes. Genomic instability, involving chromosome number and structure changes, has been documented in multiple systems. In plants, haploid induction through genome elimination has recently been connected mechanistically to the formation of complex chromosome reorganizations, known collectively as chromoanagenesis. These abnormalities can be triggered by altering the specialized centromeric histone 3, the epigenetic determinant of centromeres, which leads to loss of centromere function and chromosome missegregation. Other historical and recent instances of genomic instability, at the same time, suggest multiple causes. Their study provides a unique opportunity for a synthesis encompassing genome evolution, its response to stress, as well as the possibility of recruiting the connected mechanisms for genome engineering-based plant breeding. an organism or cell with an abnormal chromosome number that involves an incomplete set. a supernumerary, often highly heterochromatic accessory chromosome encoding few or no traits, found occasionally in outcrossing plants and animals. a chromosomal region that becomes attached to spindle fibers during mitosis and meiosis, facilitating the movement of chromosomes to the metaphase plate and subsequently to the poles of the spindle apparatus. (CENH3 in plants, CENP-A in vertebrates, CID in fruit fly). A replacement histone 3 that epigenetically determines centromeric chromatin and promotes formation of the kinetochore. encompasses the various mechanisms that result in highly rearranged chromosomes. We use the general chromoanagenesis term (remodeled chromosomes are thus ‘chromoanagenic’) to define restructuring processes affecting chromosomes, of which there are four classes: chromothripsis, kataegis, chromoplexy, and chromoanansynthesis [5Pellestor F. Chromoanagenesis: cataclysms behind complex chromosomal rearrangements.Mol. Cytogenet. 2019; 12: 6Crossref PubMed Scopus (0) Google Scholar, 116Holland A.J. Cleveland D.W. Chromoanagenesis and cancer: mechanisms and consequences of localized, complex chromosomal rearrangements.Nat. Med. 2012; 18: 1630-1638Crossref PubMed Scopus (129) Google Scholar, 117Zhang C.-Z. et al.Chromothripsis and beyond: rapid genome evolution from complex chromosomal rearrangements.Genes Dev. 2013; 27: 2513-2530Crossref PubMed Scopus (123) Google Scholar]. replication-fork failure followed by unguided repair with amplifications in the form of duplications, triplications, or quadruplications of certain regions. series of rearrangements involving multiple chromosomes. fragmented chromosomes joined up in random fashion. two copies of a given chromosome (normal diploid state). a genetic trait or property heritable through mitosis or meiosis and determined by DNA or chromatin modification without DNA sequence changes. an organism or cell containing a single set the chromosomes constituting the nuclear genome. a plant type that in specific crosses results in uniparental progeny lacking the haploid inducer genome. a visual representation or image of the chromosomes in a cell or organism. clusters of hypermutation within fragmented regions. small clusters of stem cells that form the plant body. The two embryonic meristem types, one in the shoot, the other in the root, are formed very early in embryo development and produce continued growth after germination. cellular bodies that have a defective nuclear membrane and that form around chromatin separated from the proper nucleus as a result of missegration and DNA damage. an abnormal, supernumerary chromosome that can be linear or circular. It is smaller than any in the original set and is formed by deletion of one or multiple segments in a regular chromosome. failure of proper delivery of a chromosome to the designated spindle pole. newly formed centromere appearing at a locus where no centromere was visible in previous cell divisions. a DNA repair pathway that joins broken DNA ends regardless of their sequence. Two types are known: ‘canonical’ and ‘noncanonical’. reunion of previously separated chromosomes by nuclear fusion. Also, reattachment of a broken fragment to the chromosome. three copies of a given chromosome. loss of a terminal chromosome segment.