Skip to main content
Log in

Protoplasts in the analysis of early plant-pathogen interactions: current applications and perspectives

  • Published:
European Journal of Plant Pathology Aims and scope Submit manuscript

Abstract

Transient gene expression in protoplasts has been applied to the analysis of gene expression, promoter activity, subcellular localization of proteins, and genome editing. Its advantages have been realized in recent years in various physiological, biochemical, genetic, and molecular biological studies. The omics and systems biology studies of plant development and their interactions with the environment have revitalized this approach. Early plant-pathogen interaction represents one of the most unique signalling research areas. Here, we try to discuss some developments and current applications of the protoplast system. It is for sure that the system will significantly bridge the gap between high throughput approaches and functional analysis in the study of plant-pathogen interactions in the omics era.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

Abbreviations

CDPK:

Calcium-dependent protein kinase

ETI:

Effector-triggered immunity

FC:

Fusicoccin

GFP:

Green fluorescent protein

HR:

Hypersensitive response

LRR:

Leucine-rich repeat

MAP:

Mitogen-activated protein

PA:

Picolinic acid

PAMP:

Pathogen-associated molecular pattern

PCD:

Programmed cell death

PR:

Pathogenesis-related

PRR:

Pattern recognition receptor

PTI:

PAMP-triggered immunity

ROS:

Reactive oxygen species

SE:

Sieve tube element

TTSS:

Type III secretion system

VIGS:

Virus-induced gene silencing

References

  • Alfano, J. R., & Collmer, A. (2004). Type III secretion system effector proteins: Double agents in bacterial disease and plant defense. Annual Review of Phytopathology, 42, 385–414.

    Article  CAS  PubMed  Google Scholar 

  • Alvarez, M. E., Nota, F., & Cambiagno, D. A. (2010). Epigenetic control of plant immunity. Molecular Plant Pathology, 11, 563–576.

    Article  CAS  PubMed  Google Scholar 

  • Asai, T., Stone, J. M., Heard, J. E., Kovtun, Y., Yorgey, P., Sheen, J., & Ausubel, F. M. (2000). Fumonisin B1-induced cell death in Arabidopsis protoplasts requires jasmonate-, ethylene-, and salicylate-dependent signaling pathways. Plant Cell, 12, 1823–1835.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Asai, T., Tena, G., Plotnikova, J., Willmann, M. R., Chiu, W. L., Gomez-Gomez, L., Boller, T., Ausubel, F. M., & Sheen, J. (2002). MAP kinase signalling cascade in Arabidopsis innate immunity. Nature, 415, 977–983.

    Article  CAS  PubMed  Google Scholar 

  • Baek, D., Nam, J., Koo, Y. D., Kim, D. H., Lee, J., Jeong, J. C., Kwak, S. S., Chung, W. S., Lim, C. O., Bahk, J. D., Hong, J. C., Lee, S. Y., Kawai-Yamada, M., Uchimiya, H., & Yun, D. J. (2004). Bax-induced cell death of Arabidopsis is meditated through reactive oxygen-dependent and -independent processes. Plant Molecular Biology, 56, 15–27.

    Article  CAS  PubMed  Google Scholar 

  • Bahar, O. P., Pruitt, R., Luu, D. D., Schwessinger, B., Daudi, A., Liu, F., Ruan, R., Fontaine-Bodin, L., Koebnik, R., & Ronald, P. C. (2014). The Xanthomonas Ax21 protein is processed by the general secretory system and is secreted in association with outer membrane vesicles. Peer J, 2, e242.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ballio, A., Brufani, M., Casinovi, C. G., Cerrini, S., Fedeli, W., Pellicciari, R., Santurbano, B., & Vaciago, A. (1968). The structure of fusicoccin. Experientia, 24, 631–635.

    Article  CAS  PubMed  Google Scholar 

  • Bart, R., Chern, M., Park, D. J., Bartley, L., & Ronald, P. C. (2006). A novel system for gene silencing using siRNAs in rice leaf and stem-derived protoplasts. Plant Methods, 2, 13. doi:10.1186/1746-4811-2-13.

    Article  PubMed  PubMed Central  Google Scholar 

  • Bradley, D. J., Kjellbom, P., & Lamb, C. J. (1992). Elicitor- and wound-induced oxidative cross-linking of a proline-rich plant cell wall protein: A novel, rapid defense response. Cell, 70, 21–30.

    Article  CAS  PubMed  Google Scholar 

  • Chen, X. M. (2005). Epidemiology and control of stripe rust Puccinia striiformis f. Sp. tritici on wheat. Canadian Journal of Plant Pathology, 27, 314–337.

    Article  Google Scholar 

  • Chen, S. B., Tao, L., Zeng, L. R., Vega-Sanchez, M. E., Umemura, K., & Wang, G. L. (2006). A highly efficient transient protoplast system for analyzing defence gene expression and protein-protein interactions in rice. Molecular Plant Pathology, 7, 417–427.

    Article  CAS  PubMed  Google Scholar 

  • Chisholm, S. T., Coaker, G., Day, B., & Staskawicz, B. J. (2006). Host-microbe interactions: Shaping the evolution of the plant immune response. Cell, 124, 803–814.

    Article  CAS  PubMed  Google Scholar 

  • Coll, N. S., Epple, P., & Dangl, J. L. (2011). Programmed cell death in the plant immune system. Cell Death & Differentiation, 18, 1247–1256.

    Article  CAS  Google Scholar 

  • Daub, E., Herrero, S., & Chung, K. (2005). Photoactivated perylenequinone toxins in fungal pathogenesis of plants. FEMS Microbiology Letters, 252, 197–206.

    Article  CAS  PubMed  Google Scholar 

  • De Sutter, V., Vanderhaeghen, R., Tilleman, S., Lammertyn, F., Vanhoutte, I., Karimi, M., Inze, D., Goossens, A., & Hilson, P. (2005). Exploration of jasmonate signalling via automated and standardized transient expression assays in tobacco cells. Plant Journal, 44, 1065–1076.

    Article  CAS  PubMed  Google Scholar 

  • Dodds, P. N., & Rathjen, J. P. (2010). Plant immunity: Towards an integrated view of plant-pathogen interactions. Nature Reviews Genetics, 11, 539–548.

    Article  CAS  PubMed  Google Scholar 

  • Dowd, P. F. (1999). Relative inhibition of insect phenol oxidase by cyclic fungal metabolites from insect and plant pathogens. Natural Toxins, 7, 337–341.

    Article  CAS  PubMed  Google Scholar 

  • Ek-Ramos, M. J., Avila, J., Cheng, C., Martin, G. B., & Devarenne, T. P. (2010). The T-loop extension of the tomato protein kinase AvrPto-dependent Pto-interacting protein 3 (Adi3) directs nuclear localization for suppression of plant cell death. Journal of Biological Chemistry, 285, 17584–17594.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ek-Ramos, M. J., Avila, J., Nelson Dittrich, A. C., Su, D., Gray, J. W., & Devarenne, T. P. (2014). The tomato cell death suppressor Adi3 is restricted to the endosomal system in response to the Pseudomonas syringae effector protein AvrPto. PloS One, 9, e110807. doi:10.1371/journal.pone.0110807.

    Article  PubMed  PubMed Central  Google Scholar 

  • Faraco, J., Di Sansebastiano, G. P., Spelt, K., Koes, R. E., & Quattrocchio, F. M. (2011). One protoplast is not the other! Plant Physiology, 156, 474–478.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gao, X., Wheeler, T., Li, Z., Kenerley, C. M., He, P., & Shan, L. (2011). Silencing GhNDR1 and GhMKK2 compromises cotton resistance to Verticillium wilt. Plant Journal, 66, 293–305. doi:10.1111/j.1365-313X.2011.04491.x.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Goh, C. H., Oku, T., & Shimazaki, K. (1995). Properties of proton pumping in response to blue light and fusicoccin in guard cell protoplasts isolated from adaxial epidermis of Vicia leaves. Plant Physiology, 109, 187–194.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Greenberg, J. T., & Yao, N. (2004). The role and regulation of programmed cell death in plant-pathogen interactions. Cellular Microbiology, 6, 201–211.

    Article  CAS  PubMed  Google Scholar 

  • Grzebelus, E., Kruk, M., Macko-Podgórni, A., & Grzebelus, D. (2013). Response of carrot protoplasts and protoplast-derived aggregates to selection using a fungal culture filtrate of Alternaria radicina. Plant Cell, Tissue and Organ Culture, 115, 209–222.

    Article  CAS  Google Scholar 

  • Hafke, J. B., Furch, A. C., Reitz, M. U., & van Bel, A. J. (2007). Functional sieve element protoplasts. Plant Physiology, 145, 703–711.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hauck, P., Thilmony, R., & He, S. Y. (2003). A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proceedings of the National Academy of Sciences of the United States of America, 100, 8577–8582.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hématy, K., Cherk, C., & Somerville, S. (2009). Host–pathogen warfare at the plant cell wall. Current Opinion in Plant Biology, 12, 406–413.

    Article  PubMed  Google Scholar 

  • Hlavácková, V., & Naus, J. (2007). Chemical signal as a rapid long-distance information messenger after local wounding of a plant? Plant Signaling & Behavior, 2, 103–105.

    Article  Google Scholar 

  • Hückelhoven, R. (2007). Cell wall–associated mechanisms of disease resistance and susceptibility. Annual Review of Phytopathology, 45, 101–127.

    Article  PubMed  Google Scholar 

  • Iakimoval, E. T., Weltering, E. J., & Yordanova, Z. P. (2007). Toxin- and cadmium-induced cell death events in tomato suspension cells resemble features of hypersensitive response. Journal of Fruit and Ornamental Plant Research, 15, 5–19.

    Google Scholar 

  • Iakovidis, M., Teixeira, P. J., Exposito-Alonso, M., Cowper, M. G., Law, T. F., Liu, Q., Vu, M. C., Dang, T. M., Corwin, J. A., Weigel, D., Dangl, J. L., & Grant, S. R. (2016). Effector-triggered immune response in Arabidopsis thaliana is a quantitative trait. Genetics, 204, 337–353. doi:10.1534/genetics.116.190678.

    Article  PubMed  PubMed Central  Google Scholar 

  • Iwahashi, H., Kawamorim, H., & Fukushima, K. (1999). Quinolinic acid, alphapicolinic acid, fusaric acid, and 2,6-pyridinedicarboxylic acid enhance the Fenton reaction in phosphate buffer. Chemico-Biological Interactions, 118, 201–215.

    Article  CAS  PubMed  Google Scholar 

  • Jacob, F. (1974). The logic of living systems. London: Allen Lane.

    Google Scholar 

  • Jia, Z., Cui, Y., Li, Y., Wang, X., Du, Y., & Huang, S. (2010). Inducible positive screening system to unveil the signaling pathways of late blight resistance. Journal of Integrative Plant Biology, 52, 476–484.

    CAS  PubMed  Google Scholar 

  • Johansson, F., Sommarin, M., & Larsson, C. (1993). Fusicoccin activates the plasma membrane H+-ATPase by a mechanism involving the C-terminal inhibitory domain. Plant Cell, 5, 321–327.

    CAS  PubMed  PubMed Central  Google Scholar 

  • Jones, J. D., & Dangl, J. L. (2006). The plant immune system. Nature, 444, 323–329.

    Article  CAS  PubMed  Google Scholar 

  • Kirsch, C., Takamiya-Wik, M., Schmelzer, E., Hahlbrock, K., & Somssich, I. E. (2000). A novel regulatory element involved in rapid activation of parsley ELI7 gene family members by fungal elicitor or pathogen infection. Molecular Plant Pathology, 1, 243–251.

    Article  CAS  PubMed  Google Scholar 

  • Komarova, T. V., Sheshukova, E. V., & Dorokhov, Y. L. (2014). Cell wall methanol as a signal in plant immunity. Frontier in Plant Science, 5, 101. doi:10.3389/fpls.2014. 00101.

    Google Scholar 

  • Koschmann, J., Machens, F., Becker, M., Niemeyer, J., Schulze, J., Bülow, L., Stahl, D. J., & Hehl, R. (2012). Integration of bioinformatics and synthetic promoters leads to the discovery of novel elicitor-responsive cis-regulatory sequences in Arabidopsis. Plant Physiololgy, 160, 178–191.

    Article  CAS  Google Scholar 

  • Lewis, L. A., Polanski, K., de Torres-Zabala, M., Jayaraman, S., Bowden, L., Moore, J., Penfold, C. A., Jenkins, D. J., Hill, C., Baxter, L., Kulasekaran, S., Truman, W., Littlejohn, G., Prusinska, J., Mead, A., Steinbrenner, J., Hickman, R., Rand, D., Wild, D. L., Ott, S., Buchanan-Wollaston, V., Smirnoff, N., Beynon, J., Denby, K., & Grant, M. (2015). Transcriptional dynamics driving MAMP-triggered immunity and pathogen effector-mediated immuno suppression in Arabidopsis leaves following infection with Pseudomonas syringae pv. Tomato DC 3000. Plant Cell, 27, 3038–3064.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, X., Lin, H., Zhang, W., Zou, Y., Zhang, J., Tang, X., & Zhou, J. M. (2005). Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proceedings of the National Academy of Sciences of the United States of America, 102, 12990–12995.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, J. F., Chung, H. S., Niu, Y., Bush, J., McCormack, M., & Sheen, J. (2013). Comprehensive protein-based artificial microRNA screens for effective gene silencing in plants. Plant Cell, 25, 1507–1522. doi:10.1105/tpc.113.112235.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li, J. F., Zhang, D. D., & Sheen, J. (2014). Epitope-tagged protein-based artificial miRNA screens for optimized gene silencing in plants. Nature Protocols, 9, 939–949. doi:10.1038/nprot. 2014.061.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang, H., Yao, N., Song, J. T., Luo, S., Lu, H., & Greenberg, J. T. (2003). Ceramides modulate programmed cell death in plants. Genes & Development, 17, 2636–2641.

    Article  CAS  Google Scholar 

  • Lu, H., Zhang, C., Albrecht, U., Shimizu, R., Wang, G. F., & Bowman, K. D. (2013). Overexpression of a citrus NDR1 ortholog increases disease resistance in Arabidopsis. Frontiers in Plant Science, 4, 157. doi:10.3389/fpls.2013.00157.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ma, L. S., Lukasik, E., Gawehns, F., & Takken, F. L. W. (2012). The use of Agroinfiltration for transient expression of plant resistance and fungal effector proteins in Nicotiana benthamiana leaves. Methods in Molecular Biology, 835, 61–74. doi:10.1007/978-1-61779-501-5_4.

    Article  CAS  PubMed  Google Scholar 

  • Mukhtar, M. S., Carvunis, A. R., Dreze, M., Epple, P., Steinbrenner, J., Moore, J., Tasan, M., Galli, M., Hao, T., Nishimura, M. T., Pevzner, S. J., Donovan, S. E., Ghamsari, L., Santhanam, B., Romero, V., Poulin, M. M., Gebreab, F., Gutierrez, B. J., Tam, S., Monachello, D., Boxem, M., Harbort, C. J., McDonald, N., Gai, L., Chen, H., He, Y., Consortium, E. U. E., Vandenhaute, J., Roth, F. P., Hill, D. E., Ecker, J. R., Vidal, M., Beynon, J., Braun, P., & Dangl, J. L. (2011). Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science, 333, 596–601. doi:10.1126/science.1203659.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Newman, M. A., Sundelin, T., Nielsen, J. T., & Erbs, G. (2013). MAMP (microbe-associated molecular pattern) triggered immunity in plants. Frontiers in Plant Science, 16(4), 139. doi:10.3389/fpls.2013.00139.

    Google Scholar 

  • O’Brien, J. A., Daudi, A., Butt, V. S., & Bolwell, G. P. (2012). Reactive oxygen species and their role in plant defence and cell wall metabolism. Planta, 236, 765–779.

    Article  PubMed  Google Scholar 

  • Park, C. J., & Ronald, P. C. (2012). Cleavage and nuclear localization of the rice XA21 immune receptor. Nature Communications, 3, 920. doi:10.1038/ncomms1932.

    Article  PubMed  PubMed Central  Google Scholar 

  • Randhawa, H., Puchalski, B. J., Frick, M., Goyal, A., Despins, T., Graf, R., Laroche, A., & Gaudet, D. A. (2012). Stripe rust resistance among western Canadian spring wheat and triticale cultivars. Canadian Journal of Plant Science, 92, 713–722.

    Article  CAS  Google Scholar 

  • Ruiz-Ferrer, V., & Voinnet, O. (2009). Roles of plant small RNAs in biotic stress responses. Annual Review of Plant Biology, 60, 485–510. doi:10.1146/annurev.arplant.043008.092111.

    Article  CAS  PubMed  Google Scholar 

  • Sheen, J. (2001). Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiology, 127, 1466–1475.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stratmann, J. W. (2003). Long distance run in the wound response--jasmonic acid is pulling ahead. Trends in Plant Science, 8, 247–250.

    Article  CAS  PubMed  Google Scholar 

  • Sun, X., Hu, Z., Chen, R., Jiang, Q., Song, G., Zhang, H., & Xi, Y. (2015). Targeted mutagenesis in soybean using the CRISPR-Cas9 system. Scientific Reports, 5, 10342. doi:10.1038/srep10342.

    Article  PubMed  PubMed Central  Google Scholar 

  • Tauzin, A. S., & Giardina, T. (2014). Sucrose and invertases, a part of the plant defense response to the biotic stresses. Frontiers in Plant Science, 5, 293. doi:10.3389/fpls.2014.00293.

    Article  PubMed  PubMed Central  Google Scholar 

  • Vidhyasekaran, P. (2007). Toxins in disease symptom development. In P. Vidhyasekaran (Ed.), Fungal pathogenesis in plants and crops - molecular biology and host defense mechanisms 2nd (pp. 469–488). Boca Raton: CRC Press.

    Chapter  Google Scholar 

  • Vleeshouwers, V. G., Raffaele, S., Vossen, J. H., Champouret, N., Oliva, R., Segretin, M. E., Rietman, H., Cano, L. M., Lokossou, A., Kessel, G., Pel, M. A., & Kamoun, S. (2011). Understanding and exploiting late blight resistance in the age of effectors. Annual Review of Phytopathology, 49, 507–531. doi: 10.1146/annurev-phyto-072910-095326.

  • Wang, Y., Li, J., Hou, S., Wang, X., Li, Y., Ren, D., Chen, S., Tang, X., & Zhou, J. M. (2010). A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell, 22, 2033–2044.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Y. H., Zhang, L. R., Zhang, L. L., Xing, T., Peng, J. Z., Sun, S. L., Chen, G., & Wang, X. J. (2013). A novel stress-associated protein SbSAP14 from Sorghum bicolor confers tolerance to salt stress in transgenic rice. Molecular Breeding, 32, 437–449.

    Article  CAS  Google Scholar 

  • Wodak, S. J., Vlasblom, J., Turinsky, A. L., & Pu, S. (2013). Protein-protein interaction networks: The puzzling riches. Current Opinion in Structural Biology, 23, 941–953. doi:10.1016/j.sbi.2013.08.002.

    Article  CAS  PubMed  Google Scholar 

  • Woo, J. W., Kim, J., Kwon, S. I., Corvalán, C., Cho, S. W., Kim, H., Kim, S. G., Kim, S. T., Choe, S., & Kim, J. S. (2015). DNA-free genome editing in plants with preassembled CRISPR-Cas9 ribonucleoproteins. Nature Biotechnology, 33, 1162–1164.

    Article  CAS  PubMed  Google Scholar 

  • Wu, Y., Wood, M. D., Tao, Y., & Katagiri, F. (2003). Direct delivery of bacterial avirulence proteins into resistant Arabidopsis protoplasts leads to hypersensitive cell death. Plant Journal, 33, 131–137.

    Article  CAS  PubMed  Google Scholar 

  • Xing, T., & Laroche, A. (2011). Revealing plant defense signaling: Getting more sophisticated with phosphoproteomics. Plant Signaling & Behavior, 6, 1469–1474. doi:10.4161/psb. 6.10.17345.

    Article  CAS  Google Scholar 

  • Xing, T., & Wang, X. J. (2015). Protoplasts in plant signaling analysis: Moving forward in the omics era. Botany, 93, 325–332.

    Article  Google Scholar 

  • Xing, T., Malik, K., Martin, T., & Miki, B. L. (2001). Activation of tomato PR and wound-related genes by a mutagenized tomato MAP kinase kinase through divergent pathways. Plant Molecular Biology, 46, 109–120.

    Article  CAS  PubMed  Google Scholar 

  • Xing, T., Wang, X. J., Malik, K., & Miki, B. L. (2003). Guided deletion and mutagenesis analysis identified a tMEK2-responsive region in tomato lepr1b1 promoter. Canadian Journal of Plant Pathology, 25, 209–214.

    Article  CAS  Google Scholar 

  • Xing, H. L., Dong, L., Wang, Z. P., Zhang, H. Y., Han, C. Y., Liu, B., Wang, X. C., & Chen, Q. J. (2014). A CRISPR/Cas9 toolkit for multiplex genome editing in plants. BMC Plant Biology, 14, 327. doi:10.1186/s12870-014-0327-y.

    Article  PubMed  PubMed Central  Google Scholar 

  • Yoo, S. D., Cho, Y. H., & Sheen, J. (2007). Arabidopsis mesophyll protoplasts: A versatile cell system for transient gene expression analysis. Nature Protocols, 2, 1565–1572.

    Article  CAS  PubMed  Google Scholar 

  • Zeng, W., Melotto, M., & He, S. Y. (2010). Plant stomata: A checkpoint of host immunity and pathogen virulence. Current Opinion in Biotechnology, 21, 599–603.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhai, Z., Sooksa-nguan, T., & Vatamaniuk, O. K. (2009). Establishing RNA interference as a reverse-genetic approach for gene functional analysis in protoplasts. Plant Physiology, 149, 642–652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang, K. H., Zhang, X., Mao, B. Z., Qun, L., & Zu, H. H. (2004). Alpha-picolinic acid, a fungal toxin and mammal apoptosis-inducing agent, elicits hypersensitive like response and enhances disease resistance in rice. Cell Research, 14, 27–33.

    Article  PubMed  Google Scholar 

  • Zhang, Y., Su, J., Duan, S., Ao, Y., Dai, J., Liu, J., Wang, P., Li, Y., Liu, B., Feng, D., Wang, J., & Wang, H. (2011). A highly efficient rice green tissue protoplast system for transient gene expression and studying light/chloroplast-related processes. Plant Methods, 30, doi: 10.1186/1746 -4811-7-30

Download references

Acknowledgments

This work was supported by a research grant to T.X. from Natural Sciences and Engineering Research Council of Canada and a research grant to X.J.W. from National Natural Science Foundation of China.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Tim Xing or Xiaojing Wang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Xing, T., Li, XQ., Laroche, A. et al. Protoplasts in the analysis of early plant-pathogen interactions: current applications and perspectives. Eur J Plant Pathol 149, 1001–1010 (2017). https://doi.org/10.1007/s10658-017-1230-9

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10658-017-1230-9

Keywords

Navigation