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A legume kinesin controls vacuole morphogenesis for rhizobia endosymbiosis

Nature Plants volume 8, pages 1275–1288 (2022)Cite this article

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Abstract

Symbioses between legumes and rhizobia require establishment of the plant-derived symbiosome membrane, which surrounds the rhizobia and accommodates the symbionts by providing an interface for nutrient and signal exchange. The host cytoskeleton and endomembrane trafficking systems play central roles in the formation of a functional symbiotic interface for rhizobia endosymbiosis; however, the underlying mechanisms remain largely unknown. Here we demonstrate that the nodulation-specific kinesin-like calmodulin-binding protein (nKCBP), a plant-specific microtubule-based kinesin motor, controls central vacuole morphogenesis in symbiotic cells in Medicago truncatula. Phylogenetic analysis further indicated that nKCBP duplication occurs solely in legumes of the clade that form symbiosomes. Knockout of nKCBP results in central vacuole deficiency, defective symbiosomes and abolished nitrogen fixation. nKCBP decorates linear particles along microtubules, and crosslinks microtubules with the actin cytoskeleton, to control central vacuole formation by modulating vacuolar vesicle fusion in symbiotic cells. Together, our findings reveal that rhizobia co-opted nKCBP to achieve symbiotic interface formation by regulating cytoskeletal assembly and central vacuole morphogenesis during nodule development.

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Fig. 1: Expression patterns of M. truncatula nKCBP, and phylogenetic analysis of KCBP proteins in flowering plants.
Fig. 2: M. truncatula nkcbp mutants exhibited nitrogen starvation symptoms and nodule developmental defects.
Fig. 3: Loss of nKCBP function disrupts the formation of the central vacuole in symbiotic cells.
Fig. 4: The nkcbp mutant shows defects of symbiosome development and bacteroid differentiation.
Fig. 5: Localization of nKCBP and cytoskeletal organization in symbiotic cells.
Fig. 6: nKCBP regulates cytoskeletal organization to control central vacuole formation during symbiotic nodule development.

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Data availability

All data generated in this study are included within the main text and supplementary information. The MtnKCBP gene can be found at Phytozome (https://phytozome-next.jgi.doe.gov/report/gene/Mtruncatula_Mt4_0v1/Medtr5g025100). Protein sequences in Fig. 1d for the phylogenetic analysis and in Supplementary Fig. 6 for the pairwise sequence alignment are accessible either at NCBI (https://blast.ncbi.nlm.nih.gov/Blast.cgi) or at Phytozome (https://phytozome-next.jgi.doe.gov/), with gene IDs provided in Fig. 1d and Supplementary Fig. 6 legends. All experimental materials generated in this work are available from the corresponding author upon request. Source data are provided with this paper.

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Acknowledgements

We thank R. Li (Southern University of Science and Technology) for helpful discussion. We are grateful to H. Wang, L. Su and Y. Wu (Institute of Microbiology, Chinese Academy of Sciences), for providing technical assistance in imaging. We are grateful to X. Li and X. Tan for helping with sample preparation and taking SEM images at the Center for Biological Imaging (CBI), Institute of Biophysics, Chinese Academy of Science. We are grateful to T. Zhao (Institute of Microbiology, Chinese Academy of Sciences) for the technical assistance of flow cytometry. This study was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (grant no. XDB27040210), the Strategic Priority Research Program of Chinese Academy of Sciences (grant no. XDA26030105), the Key Research Program from the Chinese Academy of Sciences (grant no. ZDRW-ZS-2019-2), National Transgenic Major Program (grant no. 2019ZX08010-004), CAS Project for Young Scientists in Basic Research (YSBR-011), the National Science Fund for Distinguished Young Scholars (grant no. 31925003), the National Science Foundation of China (grant no. 32000142) and the grants from the State Key Laboratory of Plant Genomics.

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Authors and Affiliations

  1. State Key Laboratory of Plant Genomics, Institute of Microbiology, Innovative Academy of Seed Design, Chinese Academy of Sciences, Beijing, China

    Xiaxia Zhang, Qi Wang, Jingxia Wu, Chen Zhang, Yige Huang, Guangda Wang, Huan Wang, Juan Tian, Yanjun Yu & Zhaosheng Kong

  2. State Key Laboratory of Plant Molecular Genetics, Center for Excellence in Molecular Plant Science, Chinese Academy of Sciences, Shanghai, China

    Meifang Qi & Yijing Zhang

  3. State Key Laboratory of Agricultural Microbiology, Huazhong Agricultural University, Wuhan, China

    Dasong Chen & Youguo Li

  4. Department of Biochemistry and Molecular Biology, University of Massachusetts, Amherst, MA, USA

    Dong Wang

  5. State Key Laboratory of Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing, China

    Yongbiao Xue

  6. Houji Laboratory in Shanxi Province, Academy of Agronomy, Shanxi Agricultural University, Taiyuan, China

    Zhaosheng Kong

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  1. Xiaxia Zhang
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Contributions

X.Z. designed and performed experiments, analysed the data, prepared figures and videos, and wrote the manuscript. Q.W. participated in experimental design and technical troubleshooting. J.W. participated in the complementary vector constructions. M.Q. participated in sequence blast and phylogenetic analysis. C.Z., Y.H., G.W., H.W., Y.Y., J.T., D.C. and Y.L. provided essential technical assistances. D.W., Y.Z. and Y.X. participated in data interpretation and manuscript organization. Z.K. conceived the project, interpreted the data, and wrote and revised the article.

Corresponding author

Correspondence to Zhaosheng Kong.

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Supplementary information

Supplementary Information

Supplementary Figs. 1–7 and Table 1.

Reporting Summary

Supplementary Video 1

3D reconstruction of vacuoles in nodule nitrogen-fixing cells using confocal microscopy. Related to Fig. 3g,h.

Supplementary Video 2

3D reconstruction of vacuoles in WT nodule nitrogen-fixing cells. Related to Fig. 3i.

Supplementary Video 3

The whole side-view micrographs of central vacuoles in WT nodule nitrogen-fixing cells. Related to Fig. 3i.

Supplementary Video 4

3D reconstruction of vacuoles in nkcbp nodule nitrogen-fixing cells. Related to Fig. 3j.

Supplementary Video 5

The whole side-view micrographs of central vacuole in nkcbp nodule nitrogen-fixing cells. Related to Fig. 3j.

Supplementary Video 6

3D reconstruction of nKCBP localization in nodule infected cells. Related to Fig. 5a.

Source data

Source Data Fig. 1

Statistical source data for Fig. 1a.

Source Data Fig. 2

Statistical source data for Fig. 2c–e.

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Zhang, X., Wang, Q., Wu, J. et al. A legume kinesin controls vacuole morphogenesis for rhizobia endosymbiosis. Nat. Plants 8, 1275–1288 (2022). https://doi.org/10.1038/s41477-022-01261-4

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