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Holocentric Chromosomes: Convergent Evolution, Meiotic Adaptations, and Genomic Analysis

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Holocentric Chromosomes: Convergent Evolution, Meiotic Adaptations, and Genomic Analysis Chromosome Res DOI 10.1007/s10577-012-9292-1 Holocentric chromosomes: convergent evolution, meiotic adaptations, and genomic analysis Daniël P. Melters & Leocadia V. Paliulis & Ian F. Korf & Simon W. L. Chan # Springer Science+Business Media B.V. 2012 Abstract In most eukaryotes, the kinetochore protein trait has arisen at least 13 independent times (four times in complex assembles at a single locus termed the centro- plants and at least nine times in animals). Holocentric mere to attach chromosomes to spindle microtubules. chromosomes have inherent problems in meiosis because Holocentric chromosomes have the unusual property of bivalents can attach to spindles in a random fashion. attaching to spindle microtubules along their entire Interestingly, there are several solutions that have evolved length. Our mechanistic understanding of holocentric to allow accurate meiotic segregation of holocentric chro- chromosome function is derived largely from studies in mosomes. Lastly, we describe how extensive genome the nematode Caenorhabditis elegans, but holocentric sequencing and experiments in nonmodel organisms chromosomes are found over a broad range of animal may allow holocentric chromosomes to shed light on and plant species. In this review, we describe how hol- general principles of chromosome segregation. ocentricity may be identified through cytological and molecular methods. By surveying the diversity of organ- Keywords centromere . holocentric . meiosis . isms with holocentric chromosomes, we estimate that the phylogeny. tandem repeat . chromosome Abbreviations Responsible Editor: Rachel O’Neill and Beth Sullivan. ChIP-seq Chromatin immunoprecipitation Electronic supplementary material The online version of this followed by sequencing article (doi:10.1007/s10577-012-9292-1) contains ChIP-chip Chromatin immunoprecipitation supplementary material, which is available to authorized users. followed by hybridization of isolated D. P. Melters : I. F. Korf DNA to a DNA microarray. Department of Molecular and Cell Biology FISH Fluorescent in situ hybridization. and Genome Center, University of California, cenH3 Centromere specific histone H3 variant Davis, CA, USA (CENP-A in humans Cid in Drosophila D. P. Melters : S. W. L. Chan melanogaster, HCP-3 in Caenorhabditis Department of Plant Biology, University of California, elegans) Davis, CA, USA L. V. Paliulis Biology Department, Bucknell University, Lewisburg, PA 17837, USA “Darwin answers that we must look for imper- fections and oddities, because any perfection in * S. W. L. Chan ( ) organic design or ecology obliterates the paths of Howard Hughes Medical Institute, Chevy Chase, MD, USA history and might have been created as we find e-mail: [email protected] it.” Stephen J. Gould (1986) D.P. Melters et al. Introduction Identification of holocentric chromosomes The centromere is the chromosomal locus bound How can we identify and confirm holocentricity? by kinetochore proteins that connect eukaryotic Ideally, several criteria should be met. In species with chromosomes to spindle microtubules during cell large chromosomes, cytogenetic methods are valuable division. In most eukaryotes, kinetochore proteins and are applicable to any organism in which individual assemble at a single location per chromosome. In mitotic or meiotic chromosomes can be observed. these “monocentric” chromosomes, the centromere First, all chromosomes in a mitotic metaphase spread is visible as the primary constriction in large meta- must lack a primary constriction [a classic hallmark of phase chromosomes. In select taxa, kinetochore (sub-)metacentric chromosomes] (Fig. 1a). Second, proteins bind along the entire length of the chro- during mitotic anaphase, the sister chromatids must mosomes and microtubules can attach along most migrate in parallel to the spindle poles, in contrast to of the poleward facing surface (Dernburg 2001; monocentric species in which pulling forces are Maddox et al. 2004; Guerra et al. 2010). First exerted on a single chromosomal point and chromo- described in cytogenetic experiments dating from some arms trail behind (Fig. 1b). These two criteria are 1935 (Schrader 1935), these “holocentric” chromo- historically the most common methods used to identi- somes have also been called diffuse-kinetochore fy holocentric species. chromosomes, holokinetic chromosomes, and poly- Some species are amenable to detailed cytogenetic kinetic chromosomes. These differences in nomen- manipulations that can diagnose holocentricity more clature may reflect the difficulty of distinguishing definitively. If a holocentric chromosome is frag- chromosomes with evenly distributed kinetochore mented, each individual fragment retains centromere proteins from chromosomes that contain numerous activity and can segregate to the poles (Fig. 1c). but discrete microtubule-binding sites (White 1973). For Chromosomes can be broken by X-ray irradiation the rest of this review, we will use the most common (Hughes-Schrader and Schrader 1961), or more pre- term, i.e., holocentric chromosomes. Although hol- cisely by laser dissection (Fuková et al. 2007). ocentric chromosomes are found in a minority of Chromosomal fragments must persist after breakage, eukaryotes, their prevalence may be underestimated. and micronuclei resulting from a failure to segregate Many species are difficult to study cytologically. In chromosome fragments should not be observed. One addition, there are a large number of uncharacterized problem of chromosome breakage techniques is that insect and nematode species whose phylogenetic posi- DNA damage response pathways can induce cell- tion suggest that they should have holocentric cycle checkpoints or apoptosis, disallowing further chromosomes. studies of such cells. Laser dissection is restricted to The nematode Caenorhabditis elegans is by far a desired cell cycle phase (breaks are usually induced the most well-studied holocentric organism. The during metaphase), which may be beneficial if check- function of kinetochore proteins in this organism point activiation or apoptosis are cell-cycle stage has been reviewed elsewhere (Dernburg 2001; dependent. In select experimental systems such as grass- Maddox et al. 2004). Almost nothing is known hopper spermatocytes, individual chromosomes can be about the biology of other holocentric species. manipulated using microdissection tips, and this could The primary goal of this review is to survey the serve as an ideal test of holocentricity (Paliulis and evolution of holocentric chromosomes throughout Nicklas 2004). In principle, the ends of mitotic meta- eukaryotes, highlighting the fact that this property phase chromosomes should move freely in monocentric has arisen many independent times. A crucial step chromsomes, whereas they should be resistant to such in adapting to the holocentric habit is alterations in physical stimulus in holocentric chromosomes (Doan meiosis, and we describe how the fundamental and Paliulis 2009)(Fig.1d). incompatibility between distributed microtubule- A more precise method to identify holocentric chro- binding sites and crossing-over can be resolved. mosomesisistovisualizekinetochoreproteinsbyimmu- Lastly, we show how widespread genome sequenc- nofluorescence microscopy. Holocentric chromosomes ing can shed light on the function of holocentric will have kinetochore proteins bound along most if not chromosomes. the entire length of a metaphase chromosome, whereas Evolution of holocentric chromosomes R Fig. 1 How to diagnose holocentricity. a Monocentric chromo- somes have a primary constriction. In metacentric chromo- somes, the primary constriction is approximately equidistant from both chromosomal ends, whereas the primary constriction on acrocentric chromosomes is close to one of the ends. In contrast, holocentric chromosomes lack a primary constriction. b During anaphase, monocentric chromosome are pulled by spindle microtubules from a single point where the kinetochore is assembled. In holocentric chromosomes, the kinetochores are assembled along the length of the chromosome, and during anaphase, the two sister chromatids maintain their parallel rela- tionship. c Upon chromosome fragmention, only two fragments of a monocentric chromosome will retain kinetochore function and segregate to the spindle poles. In holocentric chromosomes, all fragments migrate to the poles. d Micromanipulation of monocentric chromosome ends during metaphase results in the movement of just the chromosome end. In contrast, in holocen- tric chromosomes, where spindle microtubules display pulling forces over the length chromosome, the entire chromosome will be perturbed putative holocentric organisms, and this approach is likely to become more widespread. Once a reference genome is available for a given organism, chromatin immunoprecipitation followed by sequencing (ChIP- seq) can reveal whether kinetochore proteins are bound to a single centromere or to multiple locations on each chromosome. This method has recently been pioneered for holocentric organisms in C. elegans (Gassmann et al. 2012). As it is independent of cytology, ChIP-seq will be an especially useful method in the many organisms whose chromosomes are too small for reliable cytoge- netic assays (many deeply diverged single-celled eukar- yotes fall into this category). Broad phylogenetic distribution of holocentric chromosomes Holocentric chromosomes have radically different pat- terns of kinetochore protein deposition compared to monocentric chromosomes and require substantial
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