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Chromosome Organization and Dynamics in Plants Wojciech P Pawlowski

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Chromosome Organization and Dynamics in Plants Wojciech P Pawlowski COPLBI-811; NO. OF PAGES 6 Available online at www.sciencedirect.com Chromosome organization and dynamics in plants Wojciech P Pawlowski The past few years have brought renewed interest in are conducted in a variety of taxa but plants, because of understanding the dynamics of chromosomes in interphase their large and conspicuous chromosomes, are excellent cells as well as during cell division, particularly meiosis. This systems for studying chromosome dynamics. research has been fueled by new imaging methods, particularly three-dimensional, high-resolution, and live Chromosome organization and dynamics in microscopy. Major contributors are also new genetic tools that interphase cells allow elucidation of mechanisms controlling chromosome During interphase, chromosomes become largely decon- behavior. Recent studies in plants have explored chromatin densed but they still exhibit a high level of organization arrangement in interphase nuclei, chromosome interactions within the nucleus. In large-genome eukaryotes, such as and movement during meiotic prophase I, and mechanisms mammals and plants, chromatin threads from individual that ensure correct segregation of chromosomes during chromosomes, instead of freely mixing, form distinct anaphase. These studies shed light on chromosome dynamics chromosome territories [1]. The existence of chromosome in a small-genome plant Arabidopsis thaliana,aswellasin territories was proposed over 100 years ago [2] but only plants with large and complex genomes of polyploid origin, demonstrated conclusively with the advent of the fluor- such as wheat and maize. escence in situ hybridization (FISH) technology [3]. In Arabidopsis thaliana, interphase chromosomes exhibit Address rosette-like structures. In these structures, heterochro- Department of Plant Breeding and Genetics, Cornell University, Ithaca, matic chromosome segments form condensed chromo- NY 14853, United States centers while euchromatic segments remain as loops 0.2– Corresponding author: Pawlowski, Wojciech P ([email protected]) 2 Mb in length that emanate from the chromocenters (Figure 1a) [4]. The heterochromatic centromeric regions are located within the chromocenters. The chro- Current Opinion in Plant Biology 2010, 13:1–6 mocenters are positioned near the nuclear periphery [4] This review comes from a themed issue on and their arrangement relative to each other is predomi- Cell biology nantly random [5–7] and can change following cell Edited by Christian Luschnig and Claire Grierson division [7,8]. No evidence has been found for associ- ations between homologous chromosomes in Arabidopsis interphase nuclei. However, chromosomes that bear 1369-5266/$ – see front matter nuclear organizer regions (NORs) tend to be associated # 2010 Elsevier Ltd. All rights reserved. more often, probably by virtue of their attachment to the nucleolus [5,7]. Telomeres in Arabidopsis interphase cells DOI 10.1016/j.pbi.2010.09.015 show persistent clustering at the nucleolus [9], a unique arrangement that has not been observed in other plants. Introduction In contrast to Arabidopsis, in plants with large genomes, Behavior of chromosomes is a result of interplay between such as wheat, chromosomes in interphase frequently their two conflicting functions: firstly, providing access to exhibit Rabl orientation, in which clustered centromeres the DNA-encoded genetic information, which is required and telomeres are located on the opposite sides of the for transcription and for exchange of genetic information nucleus (Figure 1b) [10]. This arrangement is a remnant during meiotic recombination, and secondly, protecting of the preceding anaphase. Centromere clustering in the structural integrity of the genome and its faithful somatic cells has been investigated in hexaploid and segregation to daughter cells during cell division. These tetraploid wheat, where it is regulated by the Ph1 locus diverse roles of chromosomes are reflected in changes of [11–13]. However, centromere clustering has also been their appearance during the cell cycle. Although it has reported in small-genome plant species that do not exhi- been known for decades that chromosomes undergo bit Rabl orientation. For example, centromere clustering profound alterations in their morphology and arrange- has been found in somatic cells of rice [14]. However, ment in the nucleus, it is only recently that the dynamic while in wheat, centromeres of non-homologous chromo- nature of these changes is being uncovered. The mol- somes cluster, in rice the centromere associations involve ecular mechanisms controlling chromosome behavior and homologous chromosomes. the consequences that chromosome dynamic patterns have for gene expression and chromosome segregation Studies in Arabidopsis have shown that chromosome are also subjects of intense investigations. These studies organization in interphase nuclei not only is genetically www.sciencedirect.com Current Opinion in Plant Biology 2010, 13:1–6 Please cite this article in press as: Pawlowski WP. Chromosome organization and dynamics in plants, Curr Opin Plant Biol (2010), doi:10.1016/j.pbi.2010.09.015 COPLBI-811; NO. OF PAGES 6 2 Cell biology Figure 1 constrained) increases as well, although the movement speed decreases [20]. In contrast to endoreduplication, which increases the copy number of all chromosomes, increasing the number of copies of individual chromo- somes, that is, trisomy, does not substantially alter the chromosome organization in interphase nuclei [22]. Overall, studies revealed a large degree of variation in the patterns of chromosome arrangements and behavior in interphase cells in different plant species and among different tissues. It is quite likely that these diverse patterns reflect diverse roles of interphase chromosome Chromosome arrangement in interphase nuclei. (a) The chromocenter- dynamics. In yeast and mammals, detailed three-dimen- loop organization observed in Arabidopsis. Six chromosomes (black) sional maps of chromosome arrangements in interphase with chromocenters (black dots) are depicted. Chromocenters are nuclei have been constructed [1,23] that allow func- frequently located near the nuclear envelope (blue). Red = centromeres. Green = telomeres. One of the chromosomes (boxed in purple) is tional analyses of interphase chromosome organization magnified in inset. (b) Rabl orientation observed in wheat and other plant and dynamics. However, in plants such studies are still in species with large genomes. Centromeres (red) of all chromosomes their infancy and much more work is needed in this area. (black) are located on the opposite side of the nucleus from telomeres (green). Blue = nuclear envelope. Chromosome interactions in the prophase of meiosis I During the prophase of meiosis, a specialized cell division controlled but also changes during plant development leading to the production of gametes, homologous chromo- and as a response to environmental conditions. Chromo- somes find each other, pair, and recombine (see [24]fora centers show extensive reduction in size in cells of review). In contrast to the somewhat static behavior of Arabidopsis leaves before bolting, as some heterochro- interphase chromosomes, chromosomes during meiotic matic segments relocate away from chromocenters. How- prophase I are extremely dynamic [25]. Meiotic prophase ever, the chromocenter size recovers after elongation of chromosome interactions have two distinct functions, the floral stem [15]. These processes are controlled by the firstly, facilitating genetic exchanges through the process light signaling pathway. Furthermore, ecotypes accli- of crossing-over and secondly, ensuring proper chromo- mated to different latitudes exhibit varying, genetically some segregation in anaphase I. These interactions exhibit programmed, levels of chromatin compaction, depending high levels of complexity [26]. on the light intensity in their habitats [16]. During the past few years, several critical mechanisms New imaging tools, such as fluorescently tagged centro- involved in controlling pairing of homologous chromo- meric proteins and genomic sites marked using bacterial somes have been identified. In plants, similarly to mam- operator/repressor systems, have enabled investigations mals and yeast, homologous chromosome pairing has of interphase chromosome dynamics in live cells been found to be tightly linked to the progression of [8,17,18,19]. These studies demonstrated that Arabidop- meiotic recombination [27]. Meiotic recombination starts sis centromeres during interphase display a rather static by programmed formation of double-stand breaks (DSBs) behavior, exhibiting only diffusive movements with fairly in chromosomal DNA at the onset of meiosis [28]. Ara- low speeds when compared to the velocities of chromo- bidopsis and maize mutations that eliminate the for- some movements in anaphase or meiotic prophase [8]. mation of meiotic DSBs, or affect early stages of their Interstitial chromosome regions are also fairly static, processing and repair, have been shown to also cause although they are less restricted in their movements than severe chromosome pairing defects [29–33]. For example, centromeres [20]. Arabidopsis mutants lacking the SPO11-1 and SPO11-2 proteins, which are responsible for meiotic DSB for- Many tissues in plants become polyploid as a result of mation, exhibit unpaired chromosomes (univalents) DNA endoreduplication, a phenomenon observed in during pachytene, instead of chromosome pairs (biva- species with relatively small genomes, such as Arabidop-
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