AtMAC stabilizes the phragmoplast by crosslinking microtubules and actin filaments during cytokinesis.
AtMAC
actin filaments
cytokinesis
microtubules
phragmoplast
Journal
Journal of integrative plant biology
ISSN: 1744-7909
Titre abrégé: J Integr Plant Biol
Pays: China (Republic : 1949- )
ID NLM: 101250502
Informations de publication
Date de publication:
Aug 2023
Aug 2023
Historique:
received:
05
01
2023
accepted:
23
04
2023
medline:
23
8
2023
pubmed:
24
4
2023
entrez:
24
04
2023
Statut:
ppublish
Résumé
The phragmoplast, a structure crucial for the completion of cytokinesis in plant cells, is composed of antiparallel microtubules (MTs) and actin filaments (AFs). However, how the parallel structure of phragmoplast MTs and AFs is maintained, especially during centrifugal phragmoplast expansion, remains elusive. Here, we analyzed a new Arabidopsis thaliana MT and AF crosslinking protein (AtMAC). When AtMAC was deleted, the phragmoplast showed disintegrity during centrifugal expansion, and the resulting phragmoplast fragmentation led to incomplete cell plates. Overexpression of AtMAC increased the resistance of phragmoplasts to depolymerization and caused the formation of additional phragmoplasts during cytokinesis. Biochemical experiments showed that AtMAC crosslinked MTs and AFs in vitro, and the truncated AtMAC protein, N-CC1, was the key domain controlling the ability of AtMAC. Further analysis showed that N-CC1(51-154) is the key domain for binding MTs, and N-CC1(51-125) for binding AFs. In conclusion, AtMAC is the novel MT and AF crosslinking protein found to be involved in regulation of phragmoplast organization during centrifugal phragmoplast expansion, which is required for complete cytokinesis.
Substances chimiques
Microtubule-Associated Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
1950-1965Subventions
Organisme : National Natural Science Foundation of China
ID : 31570323
Organisme : National Natural Science Foundation of China
ID : 91854206
Organisme : National Natural Science Foundation of China
ID : 32200272
Informations de copyright
© 2023 The Authors. Journal of Integrative Plant Biology published by John Wiley & Sons Australia, Ltd on behalf of Institute of Botany, Chinese Academy of Sciences.
Références
Ambrose, J.C., Li, W., Marcus, A., Ma, H., and Cyr, R. (2005). A minus-end-directed kinesin with plus-end tracking protein activity is involved in spindle morphogenesis. Mol. Biol. Cell 16: 1584-1592.
Ambrose, J.C., Shoji, T., Kotzer, A.M., Pighin, J.A., and Wasteneys, G.O. (2007). The Arabidopsis CLASP gene encodes a microtubule-associated protein involved in cell expansion and division. Plant Cell 19: 2763-2775.
Buschmann, H., Green, P., Sambade, A., Doonan, J.H., and Lloyd, C.W. (2011). Cytoskeletal dynamics in interphase, mitosis and cytokinesis analysed through Agrobacterium-mediated transient transformation of tobacco BY-2 cells. New Phytol. 190: 258-267.
Buschmann, H., and Muller, S. (2019). Update on plant cytokinesis: Rule and divide. Curr. Opin. Plant Biol. 52: 97-105.
Chugh, M., Reissner, M., Bugiel, M., Lipka, E., Herrmann, A., Roy, B., Muller, S., and Schaffer, E. (2018). Phragmoplast orienting kinesin 2 is a weak motor switching between processive and diffusive modes. Biophys. J. 115: 375-385.
Gardiner, J., Overall, R., and Marc, J. (2011). Putative Arabidopsis homologues of metazoan coiled-coil cytoskeletal proteins. Cell Biol. Int. 35: 767-774.
Hamada, T., Nagasaki-Takeuchi, N., Kato, T., Fujiwara, M., Sonobe, S., Fukao, Y., and Hashimoto, T. (2013). Purification and characterization of novel microtubule-associated proteins from Arabidopsis cell suspension cultures. Plant Physiol. 163: 1804-1816.
Herrmann, A., Livanos, P., Lipka, E., Gadeyne, A., Hauser, M.T., Van Damme, D., and Muller, S. (2018). Dual localized kinesin-12 POK2 plays multiple roles during cell division and interacts with MAP65-3. EMBO Rep. 19: e46085.
Higaki, T., Kutsuna, N., Sano, T., and Hasezawa, S. (2008). Quantitative analysis of changes in actin microfilament contribution to cell plate development in plant cytokinesis. BMC Plant Biol. 8: 80.
Ho, C.M., Hotta, T., Guo, F., Roberson, R.W., Lee, Y.R., and Liu, B. (2011). Interaction of antiparallel microtubules in the phragmoplast is mediated by the microtubule-associated protein MAP65-3 in Arabidopsis. Plant Cell 23: 2909-2923.
Ho, C.M., Lee, Y.R., Kiyama, L.D., Dinesh-Kumar, S.P., and Liu, B. (2012). Arabidopsis microtubule-associated protein MAP65-3 cross-links antiparallel microtubules toward their plus ends in the phragmoplast via its distinct C-terminal microtubule binding domain. Plant Cell 24: 2071-2085.
Igarashi, H., Orii, H., Mori, H., Shimmen, T., and Sonobe, S. (2000). Isolation of a novel 190 kDa protein from tobacco BY-2 cells: Possible involvement in the interaction between actin filaments and microtubules. Plant Cell Physiol. 41: 920-931.
Ingouff, M., Fitz Gerald, J.N., Guerin, C., Robert, H., Sorensen, M.B., Van Damme, D., Geelen, D., Blanchoin, L., and Berger, F. (2005). Plant formin AtFH5 is an evolutionarily conserved actin nucleator involved in cytokinesis. Nat. Cell Biol. 7: 374-380.
Kawamura, E., Himmelspach, R., Rashbrooke, M.C., Whittington, A.T., Gale, K.R., Collings, D.A., and Wasteneys, G.O. (2006). MICROTUBULE ORGANIZATION 1 regulates structure and function of microtubule arrays during mitosis and cytokinesis in the Arabidopsis root. Plant Physiol. 140: 102-114.
Klotz, J., and Nick, P. (2012). A novel actin-microtubule cross-linking kinesin, NtKCH, functions in cell expansion and division. New Phytol. 193: 576-589.
Larkin, M.A., Blackshields, G., Brown, N.P., Chenna, R., McGettigan, P.A., McWilliam, H., Valentin, F., Wallace, I.M., Wilm, A., Lopez, R., et al. (2007). Clustal W and Clustal X version 2.0. Bioinformatics 23: 2947-2948.
Lechner, B., Rashbrooke, M.C., Collings, D.A., Eng, R.C., Kawamura, E., Whittington, A.T., and Wasteneys, G.O. (2012). The N-terminal TOG domain of Arabidopsis MOR1 modulates affinity for microtubule polymers. J. Cell Sci. 125: 4812-4821.
Lepvrier, E., Doigneaux, C., Moullintraffort, L., Nazabal, A., and Garnier, C. (2014). Optimized protocol for protein macrocomplexes stabilization using the EDC, 1-ethyl-3-(3-(dimethylamino)propyl)carbodiimide, zero-length cross-linker. Anal. Chem. 86: 10524-10530.
Li, H., Sun, B., Sasabe, M., Deng, X., Machida, Y., Lin, H., Julie Lee, Y.R., and Liu, B. (2017). Arabidopsis MAP65-4 plays a role in phragmoplast microtubule organization and marks the cortical cell division site. New Phytol. 215: 187-201.
Li, Y., Shen, Y., Cai, C., Zhong, C., Zhu, L., Yuan, M., and Ren, H. (2010). The type II Arabidopsis formin14 interacts with microtubules and microfilaments to regulate cell division. Plant Cell 22: 2710-2726.
Lin, F., Krishnamoorthy, P., Schubert, V., Hause, G., Heilmann, M., and Heilmann, I. (2019). A dual role for cell plate-associated PI4Kbeta in endocytosis and phragmoplast dynamics during plant somatic cytokinesis. EMBO J. 38: e100303.
Liu, B. (2011). The plant cytoskeleton. Springer, New York. pp. 207-225.
Liu, P.W., Qi, M., Xue, X.H., and Ren, H.Y. (2011). Dynamics and functions of the actin cytoskeleton during the plant cell cycle. Chin. Sci. Bull. 56: 3504-3510.
Livanos, P., and Muller, S. (2019). Division plane establishment and cytokinesis. Annu. Rev. Plant Biol. 70: 239-267.
Moscatiello, R., Baldan, B., and Navazio, L. (2013). Plant cell suspension cultures. Methods Mol. Biol. 953: 77-93.
Murata, T., Sano, T., Sasabe, M., Nonaka, S., Higashiyama, T., Hasezawa, S., Machida, Y., and Hasebe, M. (2013). Mechanism of microtubule array expansion in the cytokinetic phragmoplast. Nat. Commun. 4: 1967.
Oh, S.A., Pal, M.D., Park, S.K., Johnson, J.A., and Twell, D. (2010). The tobacco MAP215/Dis1-family protein TMBP200 is required for the functional organization of microtubule arrays during male germline establishment. J. Exp. Bot. 61: 969-981.
Oka, M., Yanagawa, Y., Asada, T., Yoneda, A., Hasezawa, S., Sato, T., and Nakagawa, H. (2004). Inhibition of proteasome by MG-132 treatment causes extra phragmoplast formation and cortical microtubule disorganization during M/G1 transition in synchronized tobacco cells. Plant Cell Physiol. 45: 1623-1632.
Preuss, M.L., Kovar, D.R., Lee, Y.R., Staiger, C.J., Delmer, D.P., and Liu, B. (2004). A plant-specific kinesin binds to actin microfilaments and interacts with cortical microtubules in cotton fibers. Plant Physiol. 136: 3945-3955.
Sabetta, W., Vannini, C., Sgobba, A., Marsoni, M., Paradiso, A., Ortolani, F., Bracale, M., Viggiano, L., Blanco, E., and de Pinto, M.C. (2016). Cyclic AMP deficiency negatively affects cell growth and enhances stress-related responses in tobacco Bright Yellow-2 cells. Plant Mol. Biol. 90: 467-483.
Smertenko, A. (2018). Phragmoplast expansion: The four-stroke engine that powers plant cytokinesis. Curr. Opin. Plant Biol. 46: 130-137.
Smertenko, A., Hewitt, S.L., Jacques, C.N., Kacprzyk, R., Liu, Y., Marcec, M.J., Moyo, L., Ogden, A., Oung, H.M., Schmidt, S., et al. (2018). Phragmoplast microtubule dynamics - A game of zones. J. Cell Sci. 131: jcs203331.
Sun, H., Furt, F., and Vidali, L. (2018). Myosin XI localizes at the mitotic spindle and along the cell plate during plant cell division in Physcomitrella patens. Biochem. Biophys. Res. Commun. 506: 409-421.
Tamura, K., Stecher, G., Peterson, D., Filipski, A., and Kumar, S. (2013). MEGA6: Molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30: 2725-2729.
Tian, J., Han, L., Feng, Z., Wang, G., Liu, W., Ma, Y., Yu, Y., and Kong, Z. (2015). Orchestration of microtubules and the actin cytoskeleton in trichome cell shape determination by a plant-unique kinesin. eLife 4: e09351.
van Gisbergen, P.A., Li, M., Wu, S.Z., and Bezanilla, M. (2012). Class II formin targeting to the cell cortex by binding PI(3,5)P(2) is essential for polarized growth. J. Cell Biol. 198: 235-250.
van Oostende-Triplet, C., Guillet, D., Triplet, T., Pandzic, E., Wiseman, P.W., and Geitmann, A. (2017). Vesicle dynamics during plant cell cytokinesis reveals distinct developmental phases. Plant Physiol. 174: 1544-1558.
Waadt, R., Schmidt, L.K., Lohse, M., Hashimoto, K., Bock, R., and Kudla, J. (2008). Multicolor bimolecular fluorescence complementation reveals simultaneous formation of alternative CBL/CIPK complexes in planta. Plant J. 56: 505-516.
Wu, S.Z., and Bezanilla, M. (2014). Myosin VIII associates with microtubule ends and together with actin plays a role in guiding plant cell division. eLife 3: e03498.
Xu, T., Qu, Z., Yang, X., Qin, X., Xiong, J., Wang, Y., Ren, D., and Liu, G. (2009). A cotton kinesin GhKCH2 interacts with both microtubules and microfilaments. Biochem. J. 421: 171-180.
Yoneda, A., Akatsuka, M., Kumagai, F., and Hasezawa, S. (2004). Disruption of actin microfilaments causes cortical microtubule disorganization and extra-phragmoplast formation at M/G1 interface in synchronized tobacco cells. Plant Cell Physiol. 45: 761-769.
Zhang, Y., Zhang, W.J., Baluska, F., Menzel, D., and Ren, H.Y. (2009). Dynamics and roles of phragmoplast microfilaments in cell plate formation during cytokinesis of tobacco BY-2 cells. Chin. Sci. Bull. 54: 2051-2061.
Zhou, Y., Yang, S., Mao, T., and Zhang, Z. (2015). MAPanalyzer: A novel online tool for analyzing microtubule-associated proteins. Database (Oxford) 2015: bav108.