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Root-knot nematodes modulate cell walls during root-knot formation in Arabidopsis roots

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Abstract

Phytoparasitic nematodes parasitize many species of rooting plants to take up nutrients, thus causing severe growth defects in the host plants. During infection, root-knot nematodes induce the formation of a characteristic hyperplastic structure called a root-knot or gall on the roots of host plants. Although many previous studies addressed this abnormal morphogenesis, the underlying mechanisms remain uncharacterized. To analyze the plant–microorganism interaction at the molecular level, we established an in vitro infection assay system using the nematode Meloidogyne incognita and the model plant Arabidopsis thaliana. Time-course mRNA-seq analyses indicated the increased levels of procambium-associated genes in the galls, suggesting that vascular stem cells play important roles in the gall formation. Conversely, genes involved in the formation of secondary cell walls were decreased in galls. A neutral sugar analysis indicated that the level of xylan, which is one of the major secondary cell wall components, was dramatically reduced in the galls. These observations were consistent with the hypothesis of a decrease in the number of highly differentiated cells and an increase in the density of undifferentiated cells lead to gall formation. Our findings suggest that phytoparasitic nematodes modulate the developmental mechanisms of the host to modify various aspects of plant physiological processes and establish a feeding site.

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Acknowledgements

We thank Ms. Tomomi Sagara (Kumamoto University) for technical assistance.

Funding

This work was supported by grants from the Japan Society for the Promotion of Science (JSPS) KAKENHI [Grant numbers 26440151, 14J40052, 25440134, 25119713, 24114009, 24370024, 16K14757, 17H03967, and 18H05487 to S.S., 18H04787 and 18H04844 to S.K.], by the MEXT Supported Program for the Strategic Research Foundation at Private Universities from the Ministry of Education, Culture, Sports, Science and Technology of Japan, Grant Number S1511023 to S. K. and partly supported by ALCA program of the Japan Science and Technology Agency (Grant no. JPMJAL1107).

Author information

Author notes

  1. Takeshi Kuroha

    Present address: Division of Applied Genetics, Institute of Agrobiological Sciences, National Agriculture and Food Research Organization (NARO), 2-1-2 Kannondai, Tsukuba, Ibaraki, 305-8518, Japan

  2. Miyuki T. Nakata

    Present address: Division of Biological Science, Graduate School of Science and Technology, Nara Institute of Science and Technology (NAIST), 8916-5 Takayama, Ikoma, Nara, 630-0192, Japan

  3. Takashi Ishida, Reira Suzuki and Satoru Nakagami contributed equally to this work.

Authors and Affiliations

  1. International Research Organization for Advanced Science and Technology (IROAST), Kumamoto University, Kurokami 2-39-1, Kumamoto, 860-8555, Japan

    Takashi Ishida

  2. Graduate School of Science and Technology, Kumamoto University, Kumamoto, Japan

    Reira Suzuki, Satoru Nakagami & Shinichiro Sawa

  3. Graduate School of Life Sciences, Tohoku University, Sendai, Japan

    Takeshi Kuroha, Ryusuke Yokoyama & Kazuhiko Nishitani

  4. Bioproduction Research Institute, National Institute of Advanced Industrial Science and Technology (AIST), Tsukuba, Ibaraki, Japan

    Shingo Sakamoto, Miyuki T. Nakata & Nobutaka Mitsuda

  5. Department of Industrial Life Sciences, Faculty of Life Sciences, Kyoto Sangyo University, Kyoto, Japan

    Seisuke Kimura

  6. Center for Ecological Evolutionary Developmental Biology, Kyoto Sangyo University, Kyoto, Japan

    Seisuke Kimura

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  1. Takashi Ishida
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Contributions

TI and SS initiated the project and designed the experiments. RS perform infection assays. TI, SN and SK performed statistical analyses. RS, SS, MTN and NM performed expression analyses. TK, RY and KN performed neutral sugar measurements. SS advised on the planning of the project and writing. TI wrote the manuscript with input from all authors.

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Correspondence to Takashi Ishida.

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Ishida, T., Suzuki, R., Nakagami, S. et al. Root-knot nematodes modulate cell walls during root-knot formation in Arabidopsis roots. J Plant Res 133, 419–428 (2020). https://doi.org/10.1007/s10265-020-01186-z

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