Spatiotemporal deep imaging of syncytium induced by the soybean cyst nematode Heterodera glycines
- 615 Downloads
Parasite infections cause dramatic anatomical and ultrastructural changes in host plants. Cyst nematodes are parasites that invade host roots and induce a specific feeding structure called a syncytium. A syncytium is a large multinucleate cell formed by cell wall dissolution-mediated cell fusion. The soybean cyst nematode (SCN), Heterodera glycines, is a major soybean pathogen. To investigate SCN infection and the syncytium structure, we established an in planta deep imaging system using a clearing solution ClearSee and two-photon excitation microscopy (2PEM). Using this system, we found that several cells were incorporated into the syncytium; the nuclei increased in size and the cell wall openings began to be visible at 2 days after inoculation (DAI). Moreover, at 14 DAI, in the syncytium developed in the cortex, there were thickened concave cell wall pillars that resembled “Parthenon pillars.” In contrast, there were many thick board-like cell walls and rarely Parthenon pillars in the syncytium developed in the stele. We revealed that the syncytia were classified into two types based on the pattern of the cell wall structures, which appeared to be determined by the position of the syncytium inside roots. Our results provide new insights into the developmental process of syncytium induced by cyst nematode and a better understanding of the three-dimensional structure of the syncytium in host roots.
KeywordsPlant-parasitic nematode Heterodera Syncytium development Two-photon excitation microscopy (2PEM) Deep imaging
We thank Dr. S. Aiba (National Agriculture and Food Research Organization) and Prof. Dr. K. Kawakita (Nagoya University) for kindly providing cyst of H. glycines and Prof. Dr. M.G.K. Jones (Murdoch University) for kindly providing methods of plant-parasitic nematodes. This work was supported by a grant from the Integrative Graduate Education and Research Program in Green Natural Sciences of Nagoya University, the Japan Society for the Promotion of Science (JSPS) Fellowship (15J04623 for M. O.), the Japan Advanced Plant Science Research Network, the JSPS Grant-in-Aid for challenging Exploratory Research (15K14542 for Y. S., 15K14541 for D. M.), the Japan Science and Technology Agency (ERATO project to T. H.), Toyoaki Scholarship Foundation (for D. M.), the JSPS Grant-in-Aid for Young Scientists (A) (16H06173 for D. M.), and the JSPS KAKENHI (16H06465 for T. H.).
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest.
- Chen S, Lang P, Chronis D, Zhang S, De Jong WS, Mitchum MG, Wang X (2015) In planta processing and glycosylation of a nematode CLAVATA3/ENDOSPERM SURROUNDING REGION-like effector and its interaction with a host CLAVATA2-like receptor to promote parasitism. Plant Physiol 167:262–272CrossRefPubMedGoogle Scholar
- de Almeida Engler J, De Vleesschauwer V, Burssens S, Celenza JL, Inzé D, Van Montagu M, Engler G, Gheysen G (1999) Molecular markers and cell cycle inhibitors show the importance of cell cycle progression in nematode-induced galls and syncytia. Plant Cell 11:793–808CrossRefPubMedPubMedCentralGoogle Scholar
- Endo BY (1964) Penetration and development of Heterodera glycines in soybean roots and related anatomical changes. Phytopathology 54:79–88Google Scholar
- Endo BY (1991) Ultrastructure of initial responses of resistant and susceptible soybean roots to infection by Heterodera glycines. Rev Nématol 14:73–94Google Scholar
- Hewezi T, Howe P, Maier TR, Hussey RS, Mitchum MG, Davis EL, Baum TJ (2008) Cellulose binding protein from the parasitic nematode Heterodera schachtii interacts with Arabidopsis pectin methylesterase: cooperative cell wall modification during parasitism. Plant Cell 20:3080–3093CrossRefPubMedPubMedCentralGoogle Scholar
- Hussey RS, Grundler FMW (1998) Nematode parasitism of plants. In: Perry RN, Wright DJ (eds) The physiology and biochemistry of free-living and plant-parasitic nematodes. CABI Publishing, London, pp 213–243Google Scholar
- Kadam S, Vuong TD, Qiu D, Meinhardt CG, Song L, Deshmukh R, Patil G, Wan J, Valliyodan B, Scaboo AM, Shannon JG, Nguyen HT (2016) Genomic-assisted phylogenetic analysis and marker development for next generation soybean cyst nematode resistance breeding. Plant Sci 242:342–350CrossRefPubMedGoogle Scholar
- Müller J, Rehbock K, Wyss U (1981) Growth of Heterodera schachtii with remarks on amounts of food consumed. Rev Nématol 4:227–234Google Scholar
- Raski DJ (1950) The life history and morphology of the sugar-beet nematode, Heterodera schachtii Schmidt. Phytopathology 40:135–152Google Scholar
- Siddique S, Radakovic ZS, De La Torre CM, Chronis D, Novák O, Ramireddy E, Holbein J, Matera C, Hütten M, Gutbrod P, Anjam MS, Rozanska E, Habash S, Elashry A, Sobczak M, Kakimoto T, Strnad M, Schmülling T, Mitchum MG, Grundler FM (2015) A parasitic nematode releases cytokinin that controls cell division and orchestrates feeding site formation in host plants. Proc Natl Acad Sci U S A 112:12669–16674CrossRefPubMedPubMedCentralGoogle Scholar
- Wan J, Vuong T, Jiao Y, Joshi T, Zhang H, Xu D, Nguyen HT (2015) Whole-genome gene expression profiling revealed genes and pathways potentially involved in regulating interactions of soybean with cyst nematode (Heterodera glycines Ichinohe). BMC Genomics 16:148CrossRefPubMedPubMedCentralGoogle Scholar
- Wyss U, Zunke U (1986) Observations on the behavior of second stage juveniles of Heterodera schachtii inside host roots. Rev Nématol 9:153–165Google Scholar