Meiosis is a special type of cell division by which sexually reproducing organisms maintain their chromosome number across generations. This process produces haploid gametes by two successive rounds of cell division preceded by a unique DNA replication event. During the first meiotic prophase, the homologous chromosomes form stable bivalents, a process which implies their recognition, with a subsequent step of intimate alignment (pairing), synapsis (physical association of paired chromosomes by the synaptonemal complex, SC), and recombination (exchange of chromosomal regions).
Usually, homologous chromosomes are physically separated at initiation of prophase I. In many organisms, telomeres initiate a non-random movement at the entrance of meiosis that brings homologs together tethering at the inner surface of the nuclear envelope (NE).
Sad1/UNC-84 (SUN)-domain proteins are inner NE proteins involved in complexes that link cytoskeletal elements with the nucleoskeleton. In this sense, the SUN proteins connect the telomeres in order to generate the chromosome arrangements, acting as the strings for puppet movements. This telomere attachment to the NE and telomere clustering at the transition between leptotene and zygotene (defining a stage called the “bouquet”) are well-known meiotic phenomena (Zickler and Kleckner, ). Numerous lines of evidence obtained in several non-plant model species suggest that they are driven by the meiotic cytoskeleton (Figure 1). Also, it has been shown that disruption of the telomere/nuclear envelope attachment during meiosis induces alterations in pairing and synapsis (Kracklauer et al., ).
Figure 1
The existence of several SUN domain proteins in plants has been described. Graumann et al. () and Murphy et al. (). However, the specific role of these proteins during plant meiosis remained largely enigmatic (Figure 1; Roberts et al., ). In this issue of Frontiers in Plant Sci. Murphy et al. () provide new evidences that the SUN proteins could be factors involved in facilitating the chromosome movements during the first meiotic prophase. Observations from the Hank Bass laboratory are focused on cytological analyses of maize SUN domain proteins during meiotic prophase. The authors have developed a new antibody against the two SUN proteins from maize and they demonstrate the existence of a characteristic “SUN belt” around the NE. Furthermore, their data suggest interactions between these SUN proteins and the telomeres when the bouquet formation occurs. The work of Murphy et al. () using three classic maize meiotic mutants, provides further insights into the role of SUN proteins in controlling the chromosome movements in plant meiosis. This study is a first step toward a better understanding of chromosome dynamics during the meiotic program.
Statements
Acknowledgments
The authors thank Mónica Pradillo (Universidad Complutense) for her critical reading of the manuscript. Javier Varas is supported at Juan Santos Group by the European Union FP7 grant (Meiosys-KBBE-2009-222883).
Conflict of interest
The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
References
1
GraumannK.RunionsJ.EvansD. E. (2010). Characterization of SUN-domain proteins at the higher plant nuclear envelope. Plant J. 61, 134–144. 10.1111/j.1365-313X.2009.04038.x
2
KracklauerM. P.LinkJ.AlsheimerM. (2013). LINCing the nuclear envelope to gametogenesis. Curr. Top. Dev. Biol. 102, 127–157. 10.1016/B978-0-12-416024-8.00005-2
3
MurphyS. P.GumberH. K.MaoY.BassH. W. (2014). A dynamic meiotic SUN belt includes the zygotene-stage telomere bouquet and is disrupted in chromosome segregation mutants of maize (Zea mays L.). Front. Plant Sci. 5:314. 10.3389/fpls.2014.00314
4
MurphyS. P.SimmonsC. R.BassH. W. (2010). Structure and expression of the maize (Zea mays L.) SUN-domain protein gene family: evidence for the existence of two divergent classes of SUN proteins in plants. BMC Plant Biol. 10:269. 10.1186/1471-2229-10-269
5
RobertsN. Y.OsmanK.ChrisF.FranklinH.PradilloM.VarasJ.et al. (2013). Telomeres in plant meiosis: their structure, dynamics and function in Annual Plant Reviews: Plant Nuclear Structure, Genome Architecture and Gene Regulation, Vol. 46, eds EvansD. E.GraumannK.BryantJ. A. (Oxford, UK: John Wiley and Sons Ltd), 191–228. 10.1002/9781118472507.ch7
6
ZicklerD.KlecknerN. (1998). The leptotene-zygotene transition of meiosis. Annu. Rev. Genet. 32, 619–697. 10.1146/annurev.genet.32.1.619
Summary
Keywords
telomere, SUN, nuclear envelope, bouquet, meiosis
Citation
Varas J and Baroux C (2014) Meiotic chromosome movements in plants, a puppet show?. Front. Plant Sci. 5:502. doi: 10.3389/fpls.2014.00502
Received
22 August 2014
Accepted
09 September 2014
Published
29 September 2014
Volume
5 - 2014
Edited by
Katja Graumann, Oxford Brookes University, UK
Reviewed by
Veit Schubert, Leibniz Institute of Plant Genetics and Crop Plant Research, Germany; Emmanuel Vanrobays, Blaise Pascal University, France
Copyright
© 2014 Varas and Baroux.
This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
*Correspondence: j.varas@pdi.ucm.es
This article was submitted to Plant Cell Biology, a section of the journal Frontiers in Plant Science.
Disclaimer
All claims expressed in this article are solely those of the authors and do not necessarily represent those of their affiliated organizations, or those of the publisher, the editors and the reviewers. Any product that may be evaluated in this article or claim that may be made by its manufacturer is not guaranteed or endorsed by the publisher.