Absence of SUN1 and SUN2 proteins in Arabidopsis thaliana leads to a delay in meiotic progression and defects in synapsis and recombination

Abstract

These authors contributed equally to this work. SUMMARYThe movement of chromosomes during meiosis involves location of their telomeres at the inner surface of the nuclear envelope. Sad1/UNC-84 (SUN) domain proteins are inner nuclear envelope proteins that are part of complexes linking cytoskeletal elements with the nucleoskeleton, connecting telomeres to the force-generating mechanism in the cytoplasm. These proteins play a conserved role in chromosome dynamics in eukaryotes. Homologues of SUN domain proteins have been identified in several plant species. In Arabidopsis thaliana, two proteins that interact with each other, named AtSUN1 and AtSUN2, have been identified. Immunolocalization using antibodies against AtSUN1 and AtSUN2 proteins revealed that they were associated with the nuclear envelope during meiotic prophase I. Analysis of the double mutant Atsun1-1 Atsun2-2 has revealed severe meiotic defects, namely a delay in the progression of meiosis, absence of full synapsis, the presence of unresolved interlock-like structures, and a reduction in the mean cell chiasma frequency. We propose that in Arabidopsis thaliana, overlapping functions of SUN1 and SUN2 ensure normal meiotic recombination and synapsis.

The F-Box Protein ZYGO1 Mediates Bouquet Formation to Promote Homologous Pairing, Synapsis, and Recombination in Rice Meiosis

“…In zygo1, the telomere clustering deficiency does not fully suppress homologous pairing and recombination. In other bouquetdeficient mutants, such as in ndj1D, pam1, and Atsun1 Atsun2, a level of pairing and recombination are also achieved (TrellesSticken et al, 2000;Golubovskaya et al, 2002;Varas et al, 2015). Therefore, telomere bouquet is not absolutely required for homologous pairing, and the partial pairing observed in zygo1 might be promoted by homologous recombination.…”

“…SUN proteins, such as SUN-1, AtSUN1, AtSUN2, and ZmSUN2, show polarized localization on one side of the nuclear envelope during early prophase I in C. elegans, Arabidopsis, and maize (Penkner et al, 2009;Murphy et al, 2014;Varas et al, 2015). In rice, there are four SUN-domaincontaining proteins, among which OsSAD1 is closely related to AtSUN1 and AtSUN2 (Murphy et al, 2010).…”

“…At diakinesis, a mixture of bivalents and univalents was observed (Supplemental Figure 6H). Therefore, meiocytes in zygo1 during early prophase I were distinguished as being at leptotene or postleptotene stages according to the stage description of Atsun1-1 Atsun2-2, which also lacks typical zygotene and pachytene stage cells (Varas et al, 2015).…”

“…However, so far, the molecular mechanisms underlying telomere bouquet formation in plant species are largely unknown. In Arabidopsis, two SUNdomain proteins (AtSUN1 and AtSUN2) were identified to have overlapping function in telomere dynamics and homologous pairing during meiosis (Varas et al, 2015). In addition, the plural abnormalities of meiosis1 (pam1) and the desynaptic mutants were reported to be defective in telomere clustering in maize (Zea mays) (Golubovskaya et al, 2002;Murphy and Bass, 2012), but the candidate genes of these two mutants are still unknown.…”

Dynamic Changes in Plant Nuclear Organization in Response to Environmental and Developmental Signals

“…Zhou et al (2015c) addressed whether WIP and WIT act in this context as part of a LINC complex. To work around the lethality of the sun1 sun2 double null mutant (Varas et al, 2015), they retargeted remaining SUN proteins in a viable, leaky sun1 sun2 mutant background to the ER and saw a significant effect on both pollen vegetative nuclear movement and fertilization. Taken together, these papers suggest that the entire LINC complex is involved in moving the vegetative nucleus during pollen tube growth.…”