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Identification of the cytoplasmic motor–LINC complex involved in rapid chromosome movements during meiotic prophase in Arabidopsis thaliana

Nature Plants volume 11, pages 1608–1627 (2025)Cite this article

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Abstract

Homologous pairing and recombination during meiosis are facilitated by rapid prophase movements (RPMs), which depend on chromosome attachment to the nuclear envelope (NE) and on cytoplasmic forces transmitted to the chromosomes through the NE, mediated by Linker of Nucleoskeleton and Cytoskeleton (LINC) complexes. In plants, only the NE-associated SUN-domain proteins SUN1 and SUN2 have been identified as components of the RPM process. Here we show that, during meiosis, SUN1 and SUN2 form a LINC complex with the KASH-domain protein SINE3, which recruits the meiosis-specific kinesin PSS1 to the NE. These proteins accumulate at telomere-binding sites in the NE, and their loss disrupts telomere attachment and bouquet formation and abolishes RPMs. These defects lead to defective synapsis and clustered crossovers, resulting in chromosome mis-segregation. Our results establish that the mechanism underlying RPMs is conserved in Arabidopsis thaliana, with RPMs primarily facilitating homologous recognition rather than preventing non-homologous interactions.

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Fig. 1: Phenotypic analysis of sine3 and sine4 mutants.
Fig. 2: SINE3 is expressed during meiosis and colocalizes with PSS1 and Cter-SUNs.
Fig. 3: SINE3 interacts with PSS1 and Cter-SUNs to form the cytoplasmic motor–LINC chain.
Fig. 4: Localization dependency between SINE3, PSS1 and Cter-SUNs.
Fig. 5: The PSS1–LINC chain is required for telomere attachment to the NE.
Fig. 6: The PSS1–LINC chain is required for prophase centromere movements.
Fig. 7: The PSS1–LINC chain is required for normal synapsis and class I CO distribution.
Fig. 8: The meiotic kinesin-like protein PSS1 controls CO distribution.

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Data availability

The accession codes are provided in Supplementary Table 1. Source data are provided with this paper.

Code availability

The R software scripts used to perform quantitative analyses of centromere dynamics are available at https://doi.org/10.57745/V1NNFI. The scripts used to analyse the inter-MLH1 distance and calculate the CoC are available via GitHub at https://github.com/mapeuch/Arabidopsis_LINC_paper.

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Acknowledgements

This work has benefited from the support of the Institut Jean-Pierre Bourgin’s Plant Observatory technological platforms PO-Plants and PO-Cyto. This research was funded by the National Natural Science Foundation of China (grant nos 32300296 to B.C. and 32370360 and 32170354 to C.Y.) and the ANR (COPATT ANR-20-CE12-0006 to M.G. and M.T.-A. and MeioMove ANR-21CE12-0042 to M.G., P.A., L.C. and S.L.). The Institute Jean-Pierre Bourgin benefits from the support of Saclay Plant Sciences (ANR-17-EUR0007).

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Author notes

  1. These authors contributed equally: Bowei Cai, Mariana Tiscareno-Andrade.

  2. These authors jointly supervised this work: Chao Yang, Mathilde Grelon.

Authors and Affiliations

  1. National Key Laboratory of Crop Genetic Improvement, Hubei Hongshan Laboratory, Huazhong Agricultural University, Wuhan, China

    Bowei Cai, Yanru Luo, Fei Cao, Xinjie Yuan, Yashi Zhang & Chao Yang

  2. Université Paris-Saclay, INRAE, AgroParisTech, Institute Jean-Pierre Bourgin for Plant Sciences (IJPB), Versailles, France

    Mariana Tiscareno-Andrade, Sandrine Lefranc, Aurélie Chambon, Marion Peuch, Aurélie Hurel, Julie Guérin, Nathalie Vrielynck, Christine Mézard, Philippe Andrey, Laurence Cromer & Mathilde Grelon

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Contributions

M.G., C.M., P.A., L.C. and C.Y. conceived and designed the experiments. B.C., M.T.-A., Y.L., S.L., F.C., A.C., X.Y., M.P., Y.Z., A.H., J.G., N.V., C.M. and L.C. performed the experiments. M.G., B.C., M.T.-A., S.L., A.C., M.P., C.M., P.A., L.C. and C.Y. analysed the data. M.G., B.C., M.T.-A., S.L., M.P., C.M., P.A. and C.Y. wrote the paper.

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Correspondence to Chao Yang or Mathilde Grelon.

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Extended data

Extended Data Fig. 1 Phenotypes and Epistatic Analyses of the sine3 Mutants.

(a) Generation and mutation identification of CRISPR-Cas9 sine3 and sine4 mutants. (b) Vegetative growth of Wt, sine3-1, sine3-4, sine3-5, sine4-1, sine4-2, sine3-1 sine4-1, and sine3-1 sine4-2 plants. Bar: 10 cm. (c) Seed viability quantification. Horizontal magenta lines indicate mean \(\pm \,\)SD. Horizontal black lines indicate the results of an ordinary one-way ANOVA, followed by Tukey’s multiple comparison test (comparing all mean values), ns= non significant, **** indicates p values < 0.0001. (d-f) Pollen viability after Alexander staining in single and multiple mutants. Pollen grains from at least five different plants of each genotype were analyzed. Horizontal magenta lines indicate mean \(\pm \,\)SD. Asterisks indicate differences that were found significant after ordinary one-way ANOVA, followed by Tukey’s multiple comparison test (comparing all mean values) (d, e), or unpaired t test (f). ns= non significant, **** indicates p values < 0.0001. (g) Box plot that shows the quantification of the minimum chiasma number at metaphase/anaphase transition. The boxes extend from the 25th to 75th percentiles, whiskers extend from minimum to maximum values. Asterisks indicate the results of an ordinary one-way ANOVA, followed by Dunnett’s multiple comparison test (comparing each mean value to the Wt mean values). ns= non significant, **** indicates p values < 0.0001.

Source data

Extended Data Fig. 2 Functional validation of SINE3 reporter lines.

(a-b) Expression pattern of SINE3:GFP (a) and GFP:SINE3 (b) in male meiosis of sine3-1 mutant at early and late prophase. Bars: 10 µm. (c) Siliques of Wt, sine3-1, GFP:SINE3 (in sine3-1), SINE3:GFP (in sine3-1), SINE3:interGFP (in sine3-1) plants. Bar: 1 cm. (d) Pollen viability of Wt, sine3-1, GFP:SINE3 (sine3-1), SINE3:GFP (sine3-1), SINE3:interGFP (sine3-1) plants. Asterisks indicate significant difference (one-way ANOVA followed by Tukey’s multiple comparaison test, **** indicate p values < 0.0001, ns= non significant). Magenta lines indicate mean \(\pm \,\)SD. (e) Expression pattern of SINE3:interGFP during male meiosis of sine3-1 mutants at early, mid, and late prophase. Bars: 10 µm. White arrowheads indicate the expression of SINE3:interGFP in some tapetal cells.

Source data

Extended Data Fig. 3 Functional validation of PSS1 reporter lines.

(a) Siliques of Wt, pss1-3, PSS1:GFP (in pss1-3) line1, and PSS1:GFP (in pss1-3) line2 plants. Bar: 1 cm. (b) Pollen viability of Wt, pss1-3, PSS1:GFP (in pss1-3) line1, and PSS1:GFP (in pss1-3) line2 plants. Asterisks indicate significant difference (one-way ANOVA followed by Tukey’s multiple comparaison test, **** indicate p values < 0.0001, ns= non significant). Magenta lines show mean \(\pm \,\)SD. (c) Expression pattern of PSS1:GFP in male meiosis of pss1-3 mutants at early, mid, and late prophase. Bars: 10 µm.

Source data

Extended Data Fig. 4 PSS1 is associated to the meiocyte NE from late leptotene to diplotene.

Co-immunostaining of REC8 (magenta), with HEI10 (yellow) and PSS1 (green) on 3D-preserved male meiocytes from wild-type plants. For each cell from Fig. 2d (main text), the maximum intensity projection of each channel is shown, as well as the DAPI signal (grey). Bars: 2 µm. EL= Early Leptotene, LL= Late Leptotene, Z=Zygotene, P= Pachytene, D= Diplotene. The negative control for anti-PSS1 staining is also shown (pss1-1 mutant).

Extended Data Fig. 5 Interactions between the components of the cytoplasmic motor-LINC chain.

(a-b) Experimental controls for in planta BiFC. (a) The BiFC control testing the interaction of SINE3:interVenusNter with ASY1:VENUSCter. (b) The BiFC control testing the interaction of PSS1:VenusCter with ASY1:VENUSNter. All images were captured from A. thaliana male meiocytes of plants transformed by the relevant combinations of constructs. All bars: 10 µm. (c) The C-terminal region of PSS1 interacts with SINE3 in yeast two-hybrid assay. Monomeric GFP (mGFP) fused with AD or BD domains was used as a negative control. The synthetic dropout media in the absence of Leu, Trp, and His (-L/W/H) or Leu, Trp, His, and Ade (-L/W/H/A) were used for interaction test.

Extended Data Fig. 6 Localization dependency between SINE3, PSS1, and SUN1-Live imaging.

(a, b) Localization of PSS1:GFP in male meiocytes of wild type (a) and sine3-1 (b) during prophase. (c, d) Localization of SUN1:GFP in male meiocytes of wild type (c) and sine3-1 (d) during prophase. (e) Localization of SINE3:GFP in male meiocytes of sun1 sun2. (f) Localization of PSS1:GFP in male meiocytes of sun1 sun2 during prophase. (g) Localization of SINE3:GFP in male meiocytes of pss1. (h) Localization of SUN1:GFP in male meiocytes of pss1. The RFP:TUA5 labels the microtubule and helps to determine the meiotic stages together with bright field (BF) images. All bars: 10 µm.

Extended Data Fig. 7 Localization dependency between SINE3, PSS1, and Cter-SUN proteins – Immunocytology.

Co-immunostaining of REC8 (magenta), with Cter-SUNs or PSS1 or SINE3:interGFP on 3D-preserved male meiocytes from wild-type or mutants. For each cell from Fig. 4d (main text), the maximum intensity projection of each signal is shown. Bars: 2 µm, except for pss1 meiocyte: 3 µm. For the 3D movie stacks, see the following videos:. Movie11_4D_Wt: Wt with anti REC8, and PSS1. Movie12_4D_Wt: Wt with anti REC8, and Cter-SUNs. Movie13_4D_sine3: sine3-1 with anti REC8, and PSS1. Movie14_4D_sine3: sine3-1 with anti REC8, and Cter-SUNs. Movie15_4D_pss1_SINE3interGFP: pss1-1_SINE3:interGFP with anti REC8, GFP, and Cter-SUNs. Movie16_4D_sun1sun2_SINE3interGFP: sun1sun2_SINE3:interGFP with anti REC8, GFP, and PSS1.

Extended Data Fig. 8 Localization dependency between SINE3, PSS1, and Cter-SUNs.

(a) Analysis of the protein intensity of SUN1:GFP on the NE of wild type and sine3-1 mutant plants. Black horizontal lines indicate mean, magenta lines +/− SD. Asterisks indicate significant difference (Students’ t-test, P < 0.01). (b) Examples for the occasionally observed polarization of SINE3:interGFP and SUN1:GFP in pss1-3 mutants. Bars: 10 µm.

Source data

Extended Data Fig. 9 SINE3 and PSS1 are enriched at telomere anchorage sites on the NE and are required for telomere attachment to the NE and bouquet formation.

(a) Maximum intensity projections of each channel for the cells shown in Fig. 5a (main text), Bars: 2 µm. Corresponding 3D movie stacks are: Movie17_5A_Wt_SINE3interGFP and Movie18_5A_Wt_SINE3interGFP. (b) Maximum intensity projections of each channel for the cells shown in Fig. 5b (main text), Bars: 3 µm. Corresponding 3D movie stacks are: Movie19_5B_Wt, Movie20_5B_sine3, and Movie21_5B_pss1. (c) Example of a mutant meiocyte where telomere cluster is observed in the nucleoplasm. Bars: 3 µm. Corresponding 3D movie stacks are Movie22_sine3 and Movie23_pss1. For B and C, and on 3D movie stacks, nucleolus and NE segmentations are shown, with the telomere locations (coloured spheres). The colour code is based on the proximity to the nuclear periphery (the telomeres at the periphery are the pinker).

Extended Data Fig. 10 The cytoskeletal motor-LINC complex chain (PSS1-LINC) is required for class I CO distribution.

(a) Representative example of late diplotene cells on which the MLH1 foci quantification has been performed (data shown in Fig. 7b, main text). Bars: 3 µm. (b) HEI10 immunostaining in male meiocytes of Wt, sine3-1, pss1-3, sine3-1 pss1-3, and sun1 sun2 mutant plants at late pachytene or late pachytene-like stages. Bars: 10 µm. The red rectangles highlight the chromosome regions with closely localized HEI10 foci. The corresponding quantification of the number of HEI10 foci is shown below. Error bars indicate the mean ± SD and asterisks indicate significant difference (Tukey’s multiple comparison test, P < 0.01).

Source data

Supplementary information

Supplementary Information

Supplementary Tables 1–5.

Reporting Summary

Supplementary Video 1

SINE3–interGFP expression patterns in an early leptotene cell.

Supplementary Video 2

SINE3–interGFP expression patterns in a late leptotene cell.

Supplementary Video 3

SINE3–interGFP expression patterns in a zygotene cell.

Supplementary Video 4

SINE3–interGFP expression patterns in a pachytene cell.

Supplementary Video 5

SINE3–interGFP expression patterns in a diplotene cell.

Supplementary Video 6

PSS1 expression patterns in an early leptotene cell.

Supplementary Video 7

PSS1 expression patterns in a late leptotene cell.

Supplementary Video 8

PSS1 expression patterns in a zygotene cell.

Supplementary Video 9

PSS1 expression patterns in a pachytene cell.

Supplementary Video 10

PSS1 expression patterns in a diplotene cell.

Supplementary Video 11

Localization dependency between SINE3, PSS1 and Cter-SUNs in the WT with anti-REC8 and anti-PSS1.

Supplementary Video 12

Localization dependency between SINE3, PSS1 and Cter-SUNs in the WT with anti-REC8 and anti-Cter-SUNs.

Supplementary Video 13

Localization dependency between SINE3, PSS1 and Cter-SUNs in sine3 with anti-REC8 and anti-PSS1.

Supplementary Video 14

Localization dependency between SINE3, PSS1 and Cter-SUNs in sine3 with anti-REC8 and anti-Cter-SUNs.

Supplementary Video 15

Localization dependency between SINE3, PSS1 and Cter-SUNs in pss1-SINE3-interGFP with anti-REC8, anti-GFP and anti-SUNs.

Supplementary Video 16

Localization dependency between SINE3, PSS1 and Cter-SUNs in sun1 sun2-SINE3-interGFP with anti-REC8, anti-GFP and anti-PSS1.

Supplementary Video 17

The PSS1–LINC chain is required for telomere attachment to the NE. SINE3–interGFP with anti-REC8, anti-GFP and anti-Cter-SUNs.

Supplementary Video 18

The PSS1–LINC chain is required for telomere attachment to the NE. SINE3–interGFP with anti-REC8, anti-GFP and anti-PSS1.

Supplementary Video 19

The PSS1–LINC chain is required for telomere attachment to the NE. WT with anti-REC8, anti-ASY1 and anti-ZYP1.

Supplementary Video 20

The PSS1–LINC chain is required for telomere attachment to the NE. sine3 with anti-REC8, anti-ASY1 and anti-ZYP1.

Supplementary Video 21

The PSS1–LINC chain is required for telomere attachment to the NE. pss1 with anti-REC8, anti-ASY1 and anti-ZYP1.

Supplementary Video 22

The PSS1–LINC chain is required for telomere attachment to the NE. sine3 with anti-REC8, anti-ASY1 and anti-ZYP1.

Supplementary Video 23

The PSS1–LINC chain is required for telomere attachment to the NE. pss1 with anti-REC8, anti-ASY1 and anti-ZYP1.

Supplementary Video 24

The PSS1–LINC chain is required for prophase centromere movements. WT_GFP-CENH3_REC8–RFP.

Supplementary Video 25

The PSS1–LINC chain is required for prophase centromere movements. sine3-1_GFP-CENH3_REC8–RFP.

Supplementary Video 26

The PSS1–LINC chain is required for prophase centromere movements. pss1-1_GFP-CENH3_REC8–RFP.

Supplementary Video 27

The PSS1–LINC chain is required for prophase centromere movements. sine4-1_GFP-CENH3_REC8–RFP.

Supplementary Video 28

The PSS1–LINC chain is required for prophase centromere movements. wip123_GFP-CENH3_REC8–RFP.

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Cai, B., Tiscareno-Andrade, M., Luo, Y. et al. Identification of the cytoplasmic motor–LINC complex involved in rapid chromosome movements during meiotic prophase in Arabidopsis thaliana. Nat. Plants 11, 1608–1627 (2025). https://doi.org/10.1038/s41477-025-02043-4

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