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PATRONUS1 is expressed in meiotic prophase I to regulate centromeric cohesion in Arabidopsis and shows synthetic lethality with OSD1.

Singh DK, Spillane C, Siddiqi I - BMC Plant Biol. (2015)

Bottom Line: Retention of sister centromere cohesion during meiosis I and its dissolution at meiosis II is necessary for balanced chromosome segregation and reduction of chromosome number.We show here that PANS1 protein is found mainly in prophase I of meiosis, with its level declining late in prophase I during diplotene.PANS1 also shows expression in dividing tissues.

View Article: PubMed Central - PubMed

Affiliation: Centre for Cellular and Molecular Biology (CSIR), Uppal Road, Hyderabad, 500007, India. dipesh@ccmb.res.in.

ABSTRACT

Background: Retention of sister centromere cohesion during meiosis I and its dissolution at meiosis II is necessary for balanced chromosome segregation and reduction of chromosome number. PATRONUS1 (PANS1) has recently been proposed to regulate centromere cohesion in Arabidopsis after meiosis I, during interkinesis. pans1 mutants lose centromere cohesion prematurely during interkinesis and segregate randomly at meiosis II. PANS1 protein interacts with components of the Anaphase Promoting Complex/Cyclosome (APC/C).

Results: We show here that PANS1 protein is found mainly in prophase I of meiosis, with its level declining late in prophase I during diplotene. PANS1 also shows expression in dividing tissues. We demonstrate that, in addition to the previously reported premature loss of centromere cohesion during interkinesis, pans1 mutants show partially penetrant defects in centromere cohesion during meiosis I. We also determine that pans1 shows synthetic lethality at the level of the sporophyte, with Omission of Second Division 1 (osd1), which encodes a known inhibitor of the APC/C that is required for cell cycle progression during mitosis, as well as meiosis I and II.

Conclusions: Our results show that PANS1 is expressed mainly in meiosis I where it has an important function and together with previous studies indicate that PANS1 and OSD1 are part of a network linking centromere cohesion and cell cycle progression through control of APC/C activity.

No MeSH data available.


Related in: MedlinePlus

Loss of centromeric cohesion in pans1 male meiocytes during Meiosis I. FISH on male meiotic chromosome spreads using a centromeric repeat probe showing DAPI (blue) and probe (red). Left column: merged images of DAPI and the probe; middle column: probe alone; right column: DAPI. a-c wild type metaphase I. d-ipans1 metaphase I. d-f mild phenotype showing split centromere signal on one chromosome indicated by arrow head. (g-i) strong phenotype showing univalents of one chromosome and split centromere signals on four chromosomes. Scale bar 10 μm
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Fig2: Loss of centromeric cohesion in pans1 male meiocytes during Meiosis I. FISH on male meiotic chromosome spreads using a centromeric repeat probe showing DAPI (blue) and probe (red). Left column: merged images of DAPI and the probe; middle column: probe alone; right column: DAPI. a-c wild type metaphase I. d-ipans1 metaphase I. d-f mild phenotype showing split centromere signal on one chromosome indicated by arrow head. (g-i) strong phenotype showing univalents of one chromosome and split centromere signals on four chromosomes. Scale bar 10 μm

Mentions: Loss of centromeric cohesion in pans1 during meiosis II could be due to defects in regulation of cohesion specifically during meiosis II, or alternatively could also be connected to defects in centromere organization during meiosis I. The small number of meiocytes that we observed exhibiting a phenotype in meiosis I prompted us to further examine centromere organization. To probe centromere structure during meiosis I, we carried out fluorescence in situ hybridization on meiotic chromosome spreads using a pAL1 centromere repeat probe that hybridizes to pericentromeric repeats [22]. Centromeres in wild type gave regular and compact signals at metaphase I and showed five bivalents, with two signals per bivalent, each signal representing a pair of sister centromeres. In contrast, differences were observed for pans1 wherein about 21 % of the metaphase I stages showed four centromere signals in a bivalent (Fig. 2; Table 1), indicating that sister centromeres were not closely connected. We did not observe splitting of sister centromere signals in midprophase I from zygotene to pachytene in pans1 (0/102 meiocytes; Additional file 1: Figure S2). Our interpretation is that although the sister centromeres are still connected at metaphase I, the connection is not as tight as for wild type and separation of the sister centromere signals occurs following attachment of sister centromeres to the meiosis I spindle. The presence of two or more univalent chromosomes was also seen in 5/8 meiocytes showing split centromere signals at metaphase I and the univalent chromosomes showed bipolar attachment to the meiosis I spindle (Fig. 2G-I). A mixture of reductional and equational segregation therefore appears to be taking place in these meiocytes. These results indicate that in addition to the major phenotype which reflects a requirement for PANS1 in retention of centromere cohesion after meiosis I and up to metaphase of meiosis II (in agreement with earlier reports [19, 20]) there is a requirement for PANS1 in centromere cohesion during meiosis I, as reflected in a partially penetrant pans1 phenotype with regard to centromere cohesion in meiosis I.Fig. 2


PATRONUS1 is expressed in meiotic prophase I to regulate centromeric cohesion in Arabidopsis and shows synthetic lethality with OSD1.

Singh DK, Spillane C, Siddiqi I - BMC Plant Biol. (2015)

Loss of centromeric cohesion in pans1 male meiocytes during Meiosis I. FISH on male meiotic chromosome spreads using a centromeric repeat probe showing DAPI (blue) and probe (red). Left column: merged images of DAPI and the probe; middle column: probe alone; right column: DAPI. a-c wild type metaphase I. d-ipans1 metaphase I. d-f mild phenotype showing split centromere signal on one chromosome indicated by arrow head. (g-i) strong phenotype showing univalents of one chromosome and split centromere signals on four chromosomes. Scale bar 10 μm
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4536785&req=5

Fig2: Loss of centromeric cohesion in pans1 male meiocytes during Meiosis I. FISH on male meiotic chromosome spreads using a centromeric repeat probe showing DAPI (blue) and probe (red). Left column: merged images of DAPI and the probe; middle column: probe alone; right column: DAPI. a-c wild type metaphase I. d-ipans1 metaphase I. d-f mild phenotype showing split centromere signal on one chromosome indicated by arrow head. (g-i) strong phenotype showing univalents of one chromosome and split centromere signals on four chromosomes. Scale bar 10 μm
Mentions: Loss of centromeric cohesion in pans1 during meiosis II could be due to defects in regulation of cohesion specifically during meiosis II, or alternatively could also be connected to defects in centromere organization during meiosis I. The small number of meiocytes that we observed exhibiting a phenotype in meiosis I prompted us to further examine centromere organization. To probe centromere structure during meiosis I, we carried out fluorescence in situ hybridization on meiotic chromosome spreads using a pAL1 centromere repeat probe that hybridizes to pericentromeric repeats [22]. Centromeres in wild type gave regular and compact signals at metaphase I and showed five bivalents, with two signals per bivalent, each signal representing a pair of sister centromeres. In contrast, differences were observed for pans1 wherein about 21 % of the metaphase I stages showed four centromere signals in a bivalent (Fig. 2; Table 1), indicating that sister centromeres were not closely connected. We did not observe splitting of sister centromere signals in midprophase I from zygotene to pachytene in pans1 (0/102 meiocytes; Additional file 1: Figure S2). Our interpretation is that although the sister centromeres are still connected at metaphase I, the connection is not as tight as for wild type and separation of the sister centromere signals occurs following attachment of sister centromeres to the meiosis I spindle. The presence of two or more univalent chromosomes was also seen in 5/8 meiocytes showing split centromere signals at metaphase I and the univalent chromosomes showed bipolar attachment to the meiosis I spindle (Fig. 2G-I). A mixture of reductional and equational segregation therefore appears to be taking place in these meiocytes. These results indicate that in addition to the major phenotype which reflects a requirement for PANS1 in retention of centromere cohesion after meiosis I and up to metaphase of meiosis II (in agreement with earlier reports [19, 20]) there is a requirement for PANS1 in centromere cohesion during meiosis I, as reflected in a partially penetrant pans1 phenotype with regard to centromere cohesion in meiosis I.Fig. 2

Bottom Line: Retention of sister centromere cohesion during meiosis I and its dissolution at meiosis II is necessary for balanced chromosome segregation and reduction of chromosome number.We show here that PANS1 protein is found mainly in prophase I of meiosis, with its level declining late in prophase I during diplotene.PANS1 also shows expression in dividing tissues.

View Article: PubMed Central - PubMed

Affiliation: Centre for Cellular and Molecular Biology (CSIR), Uppal Road, Hyderabad, 500007, India. dipesh@ccmb.res.in.

ABSTRACT

Background: Retention of sister centromere cohesion during meiosis I and its dissolution at meiosis II is necessary for balanced chromosome segregation and reduction of chromosome number. PATRONUS1 (PANS1) has recently been proposed to regulate centromere cohesion in Arabidopsis after meiosis I, during interkinesis. pans1 mutants lose centromere cohesion prematurely during interkinesis and segregate randomly at meiosis II. PANS1 protein interacts with components of the Anaphase Promoting Complex/Cyclosome (APC/C).

Results: We show here that PANS1 protein is found mainly in prophase I of meiosis, with its level declining late in prophase I during diplotene. PANS1 also shows expression in dividing tissues. We demonstrate that, in addition to the previously reported premature loss of centromere cohesion during interkinesis, pans1 mutants show partially penetrant defects in centromere cohesion during meiosis I. We also determine that pans1 shows synthetic lethality at the level of the sporophyte, with Omission of Second Division 1 (osd1), which encodes a known inhibitor of the APC/C that is required for cell cycle progression during mitosis, as well as meiosis I and II.

Conclusions: Our results show that PANS1 is expressed mainly in meiosis I where it has an important function and together with previous studies indicate that PANS1 and OSD1 are part of a network linking centromere cohesion and cell cycle progression through control of APC/C activity.

No MeSH data available.


Related in: MedlinePlus