Abstract
Growing evidence indicates that actin cytoskeleton is involved in plant innate immune responses, but the functional mechanism remains largely unknown. Here, we investigated the behavior of a cotton profilin gene (GhPFN2) in response to Verticillium dahliae invasion, and evaluated its contribution to plant defense against this soil-borne fungal pathogen. GhPFN2 expression was up-regulated when cotton root was inoculated with V. dahliae, and the actin architecture was reorganized in the infected root cells, with a clear increase in the density of filamentous actin and the extent of actin bundling. Compared to the wild type, GhPFN2-overexpressing cotton plants showed enhanced protection against V. dahliae infection and the actin cytoskeleton organization in root epidermal cells was clearly altered, which phenocopied that of the wild-type (WT) root cells challenged with V. dahliae. These results provide a solid line of evidence showing that actin cytoskeleton reorganization involving GhPFN2 is important for defense against V. dahliae infection.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Aparicio-Fabre, R., Guillén, G., Estrada, G., Olivares-Grajales, J., Gurrola, G., and Sánchez, F. (2006). Profilin tyrosine phosphorylation in poly-lproline-binding regions inhibits binding to phosphoinositide 3-kinase in Phaseolus vulgaris. Plant J 47, 491–500.
Boldogh, I., Vojtov, N., Karmon, S., and Pon, L.A. (1998). Interaction between mitochondria and the actin cytoskeleton in budding yeast requires two integral mitochondrial outer membrane proteins, Mmm1p and Mdm10p. J Cell Biol 141, 1371–1381.
Boukhelifa, M., Moza, M., Johansson, T., Rachlin, A., Parast, M., Huttelmaier, S., Roy, P., Jockusch, B.M., Carpen, O., Karlsson, R., and Otey, C.A. (2006). The proline-rich protein palladin is a binding partner for profilin. FEBS J 273, 26–33.
Cai, Y., He, X., Mo, J.C., Sun, Q., Yang, J., and Liu, J. (2009). Molecular research and genetic engineering of resistance to Verticillium wilt in cotton: a review. Afr J Biotechnol 8, 7363–7372.
Cheng, H.Q., Han, L.B., Yang, C.L., Wu, X.M., Zhong, N.Q., Wu, J.H., Wang, F.X., Wang, H.Y., and Xia, G.X. (2016). The cotton MYB108 forms a positive feedback regulation loop with CML11 and participates in the defense response against Verticillium dahliae infection. J Exp Bot 67, 1935–1950.
Day, B., Henty, J.L., Porter, K.J., and Staiger, C.J. (2011). The pathogenactin connection: a platform for defense signaling in plants. Annu Rev Phytopathol 49, 483–506.
Evangelista, M., Pruyne, D., Amberg, D.C., Boone, C., and Bretscher, A. (2002). Formins direct Arp2/3-independent actin filament assembly to polarize cell growth in yeast. Nat Cell Biol 4, 32–41.
Fradin, E.F., and Thomma, B.P.H.J. (2006). Physiology and molecular aspects of Verticillium wilt diseases caused by V. dahliae and V. albo-atrum. Mol Plant Pathol 7, 71–86.
Fu, Y., Duan, X., Tang, C., Li, X., Voegele, R.T., Wang, X., Wei, G., and Kang, Z. (2014). TaADF7, an actin-depolymerizing factor, contributes to wheat resistance against Puccinia striiformis f. sp. tritici. Plant J 78, 16–30.
Gaspar, Y.M., McKenna, J.A., McGinness, B.S., Hinch, J., Poon, S., Connelly, A.A., Anderson, M.A., and Heath, R.L. (2014). Field resistance to Fusarium oxysporum and Verticillium dahliae in transgenic cotton expressing the plant defensin NaD1. J Exp Bot 65, 1541–1550.
Van Gestel, K., Le, J., and Verbelen, J.P. (2001). A comparison of F-actin labeling methods for light microscopy in different plant specimens: multiple techniques supplement each other. Micron 32, 571–578.
Gharechahi, J., Khalili, M., Hasanloo, T., and Salekdeh, G.H. (2013). An integrated proteomic approach to decipher the effect of methyl jasmonate elicitation on the proteome of Silybum marianum L. hairy roots. Plant Physiol Biochem 70, 115–122.
Gibbon, B.C., Zonia, L.E., Kovar, D.R., Hussey, P.J., and Staiger, C.J. (1998). Pollen profilin function depends on interaction with proline-rich motifs. Plant Cell 10, 981–994.
Hardham, A.R., Jones, D.A., and Takemoto, D. (2007). Cytoskeleton and cell wall function in penetration resistance. Curr Opin Plant Biol 10, 342–348.
Henty-Ridilla, J.L., Shimono, M., Li, J., Chang, J.H., Day, B., and Staiger, C.J. (2013). The plant actin cytoskeleton responds to signals from microbe-associated molecular patterns. PLoS Pathog 9, e1003290.
Higaki, T., Kutsuna, N., Sano, T., Kondo, N., and Hasezawa, S. (2010). Quantification and cluster analysis of actin cytoskeletal structures in plant cells: role of actin bundling in stomatal movement during diurnal cycles in Arabidopsis guard cells. Plant J 61, 156–165.
Inada, N., Higaki, T., and Hasezawa, S. (2016). Nuclear function of subclass I actin depolymerizing factor contributes to susceptibility in Arabidopsis to an adapted powdery mildew fungus. Plant Physiol 170, 1420–1434.
Jarosch, B., Collins, N.C., Zellerhoff, N., and Schaffrath, U. (2005). RAR1, ROR1, and the actin cytoskeleton contribute to basal resistance to Magnaporthe grisea in barley. Mol Plant Microbe Interact 18, 397–404.
Kang, Y., Jelenska, J., Cecchini, N.M., Li, Y., Lee, M.W., Kovar, D.R., and Greenberg, J.T. (2014). HopW1 from Pseudomonas syringae disrupts the actin cytoskeleton to promote virulence in Arabidopsis. PLoS Pathog 10, e1004232.
Kobayashi, I., and Hakuno, H. (2003). Actin-related defense mechanism to reject penetration attempt by a non-pathogen is maintained in tobacco BY-2 cells. Planta 217, 340–345.
Li, C., He, X., Luo, X., Xu, L., Liu, L., Min, L., Jin, L., Zhu, L., and Zhang, X. (2014). Cotton WRKY1 mediates the plant defense-to-development transition during infection of cotton by Verticillium dahliae by activating JASMONATE ZIM-DOMAIN1 expression. Plant Physiol 166, 2179–2194.
Li, J., Henty-Ridilla, J.L., Staiger, B.H., Day, B., and Staiger, C.J. (2015). Capping protein integrates multiple MAMP signalling pathways to modulate actin dynamics during plant innate immunity. Nat Commun 6, 7206.
Li, Y.B., Han, L.B., Wang, H.Y., Zhang, J., Sun, S.T., Feng, D.Q., Yang, C.L., Sun, Y.D., Zhong, N.Q., and Xia, G.X. (2016). The thioredoxin GbNRX1 plays a crucial role in homeostasis of apoplastic reactive oxygen species in response to Verticillium dahliae infection in cotton. Plant Physiol 170, 2392–2406.
Liao, M., Li, Y., and Wang, Z. (2009). Identification of elicitor-responsive proteins in rice leaves by a proteomic approach. Proteomics 9, 2809–2819.
Lipka, V., and Panstruga, R. (2005). Dynamic cellular responses in plantmicrobe interactions. Curr Opin Plant Biol 8, 625–631.
Miklis, M., Consonni, C., Bhat, R.A., Lipka, V., Schulze-Lefert, P., and Panstruga, R. (2007). Barley MLO modulates actin-dependent and actinindependent antifungal defense pathways at the cell periphery. Plant Physiol 144, 1132–1143.
Porter, K., and Day, B. (2016). From filaments to function: the role of the plant actin cytoskeleton in pathogen perception, signaling and immunity. J Integr Plant Biol 58, 299–311.
Pujol, N., Bonet, C., Vilella, F., Petkova, M.I., Mozo-VillarÃ-as, A., and de la Torre-Ruiz, M.A. (2009). Two proteins from Saccharomyces cerevisiae: Pfy1 and Pkc1, play a dual role in activating actin polymerization and in increasing cell viability in the adaptive response to oxidative stress. FEMS Yeast Res 9, 1196–1207.
Schütz, I., Gus-Mayer, S., and Schmelzer, E. (2006). Profilin and Rop GTPases are localized at infection sites of plant cells. Protoplasma 227, 229–235.
Song, X., Ma, Q., Hao, X., and Li, H. (2012). Roles of the actin cytoskeleton and an actin-binding protein in wheat resistance against Puccinia striiformis f. sp. tritici. Protoplasma 249, 99–106.
Staiger, C.J., and Blanchoin, L. (2006). Actin dynamics: old friends with new stories. Curr Opin Plant Biol 9, 554–562.
Takemoto, D., and Hardham, A.R. (2004). The cytoskeleton as a regulator and target of biotic interactions in plants. Plant Physiol 136, 3864–3876.
Tian, M., Chaudhry, F., Ruzicka, D.R., Meagher, R.B., Staiger, C.J., and Day, B. (2009). Arabidopsis actin-depolymerizing factor AtADF4 mediates defense signal transduction triggered by the Pseudomonas syringae effector AvrPphB. Plant Physiol 150, 815–824.
Underwood, W., and Somerville, S.C. (2008). Focal accumulation of defences at sites of fungal pathogen attack. J Exp Bot 59, 3501–3508.
Wang, J., Wang, H.Y., Zhao, P.M., Han, L.B., Jiao, G.L., Zheng, Y.Y., Huang, S.J., and Xia, G.X. (2010). Overexpression of a Profilin (GhPFN2) promotes the progression of developmental phases in cotton fibers. Plant Cell Physiol 51, 1276–1290.
Wang, J., Zuo, H., Huo, Y., Feng, C., Wang, Y., and Ma, Q. (2015). Evaluation of actin cytoskeleton in non-host resistance of pepper to Puccinia striiformis f. sp. tritici stress. Physiol Mol Plant Pathol 92, 112–118.
Wang, W., Wen, Y., Berkey, R., and Xiao, S. (2009). Specific targeting of the Arabidopsis resistance protein RPW8.2 to the interfacial membrane encasing the fungal haustorium renders broad-spectrum resistance to powdery mildew. Plant Cell 21, 2898–2913.
Wang, Y.Q., Chen, D.J., Wang, D.M., Huang, Q.S., Yao, Z.P., Liu, F.J., Wei, X.W., Li, R.J., Zhang, Z.N., and Sun, Y.R. (2004). Over-expression of Gastrodia anti-fungal protein enhances Verticillium wilt resistance in coloured cotton. Plant Breed 123, 454–459.
Wang, Y., and Riechmann, V. (2008). Microtubule anchoring by cortical actin bundles prevents streaming of the oocyte cytoplasm. Mech Dev 125, 142–152.
Yarmola, E.G., and Bubb, M.R. (2006). Profilin: emerging concepts and lingering misconceptions. Trends Biochem Sci 31, 197–205.
Yuan, H.Y., Yao, L.L., Jia, Z.Q., Li, Y., and Li, Y.Z. (2006). Verticillium dahliae toxin induced alterations of cytoskeletons and nucleoli in Arabidopsis thaliana suspension cells. Protoplasma 229, 75–82.
Zhao, S.S., Zhao, Y.X., and Guo, Y. (2015). 14-3-3 λ protein interacts with ADF1 to regulate actin cytoskeleton dynamics in Arabidopsis. Sci China Life Sci 58, 1142–1150.
Acknowledgements
This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB11040600), the National Natural Science Foundation of China (31671278), and the State Key Laboratory of Plant Genomics of China (2015B0129-02).
Author information
Authors and Affiliations
Corresponding authors
Electronic supplementary material
Rights and permissions
About this article
Cite this article
Wang, W., Sun, Y., Han, L. et al. Overexpression of GhPFN2 enhances protection against Verticillium dahliae invasion in cotton. Sci. China Life Sci. 60, 861–867 (2017). https://doi.org/10.1007/s11427-017-9067-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-017-9067-2