Recognition of pathogen-derived sphingolipids in Arabidopsis

A paper by Dr. Kato and colleagues was published in Science.

Kato, H., Nemoto, K., Shimizu, M., Abe, A., Asai, S., Ishihama, N., Matsuoka, S., Daimon, T., Ojika, M., Kawakita, K., Onai, K., Shirasu, K., Yoshida, M., Ishiura, M., Takemoto, D., Takano, Y., & Terauchi, R. (2022). Recognition of pathogen-derived sphingolipids in Arabidopsis. Science, 376(6595), 857–860. https://doi.org/10.1126/science.abn0650

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In plants, many invading microbial pathogens are recognized by cell-surface pattern recognition receptors, which induce defense responses. Here, we show that the ceramide Phytophthora infestans–ceramide D (Pi-Cer D) from the plant pathogenic oomycete P. infestans triggers defense responses in Arabidopsis. Pi-Cer D is cleaved by an Arabidopsis apoplastic ceramidase, NEUTRAL CERAMIDASE 2 (NCER2), and the resulting 9-methyl–branched sphingoid base is recognized by a plasma membrane lectin receptor–like kinase, RESISTANT TO DFPM-INHIBITION OF ABSCISIC ACID SIGNALING 2 (RDA2). 9-Methyl–branched sphingoid base is specific to microbes and induces plant immune responses by physically interacting with RDA2. Loss of RDA2 or NCER2 function compromised Arabidopsis resistance against an oomycete pathogen. Thus, we elucidated the recognition mechanisms of pathogen-derived lipid molecules in plants.

A jacalin-like lectin domain-containing protein of Sclerospora graminicola acts as an apoplastic virulence effector in plant–oomycete interactions

A paper has been published in which Prof. Terauchi is the corresponding author.

Kobayashi, M., Utsushi, H., Fujisaki, K., Takeda, T., Yamashita, T., & Terauchi, R. (2022). A jacalin-like lectin domain-containing protein of Sclerospora graminicola acts as an apoplastic virulence effector in plant–oomycete interactions. Molecular Plant Pathology, 23, 845– 854. https://doi.org/https://doi.org/10.1111/mpp.13197

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The plant extracellular space, including the apoplast and plasma membrane, is the initial site of plant–pathogen interactions. Pathogens deliver numerous secreted proteins, called effectors, into this region to suppress plant immunity and establish infection. Downy mildew caused by the oomycete pathogen Sclerospora graminicola (Sg) is an economically important disease of Poaceae crops including foxtail millet (Setaria italica). We previously reported the genome sequence of Sg and showed that the jacalin-related lectin (JRL) gene family has significantly expanded in this lineage. However, the biological functions of JRL proteins remained unknown. Here, we show that JRL from Sg (SgJRL) functions as an apoplastic virulence effector. We identified eight SgJRLs by protein mass spectrometry analysis of extracellular fluid from Sg-inoculated foxtail millet leaves. SgJRLs consist of a jacalin-like lectin domain and an N-terminal putative secretion signal; SgJRL expression is induced by Sg infection. Heterologous expression of three SgJRLs with N-terminal secretion signal peptides in Nicotiana benthamiana enhanced the virulence of the pathogen Phytophthora palmivora inoculated onto the same leaves. Of the three SgJRLs, SG06536 fused with green fluorescent protein (GFP) localized to the apoplastic space in N. benthamiana leaves. INF1-mediated induction of defence-related genes was suppressed by co-expression of SG06536-GFP. These findings suggest that JRLs are novel apoplastic effectors that contribute to pathogenicity by suppressing plant defence responses.

Pathogen-derived 9-methyl sphingoid base is perceived by a lectin receptor kinase in Arabidopsis

Kato, H., Nemoto, K., Shimizu, M., Abe, A., Asai, S., Ishihama, N., Daimon, T., Ojika, M., Kawakita, K., Onai, K., Shirasu, K., Ishiura, M., Takemoto, D., Takano, Y. and Terauchi, R. (2021). Pathogen-derived 9-methyl sphingoid base is perceived by a lectin receptor kinase in Arabidopsis. BioRxiv, 2021.10.18.464766. https://doi.org/10.1101/2021.10.18.464766

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In plants, many invading microbial pathogens are recognized by cell-surface pattern recognition receptors (PRRs), inducing defense responses; yet how PRRs perceive pathogen sphingolipids remains unclear. Here, we show that the ceramide Pi-Cer D from a plant pathogenic oomycete Phytophthora infestans triggers defense responses in Arabidopsis. Pi-Cer D is cleaved by an Arabidopsis apoplastic ceramidase, NCER2, and the resulting 9-methyl-branched sphingoid base is recognized by a plasma membrane lectin receptor-like kinase, RDA2. Importantly, 9-methyl-branched sphingoid base, which is unique to microbes, induces plant immune responses by interacting with RDA2. Loss of RDA2 or NCER2 function compromised Arabidopsis resistance against an oomycete pathogen, indicating that these are crucial for defense. We provide new insights that help elucidate the recognition mechanisms of pathogen-derived lipid molecules in plants.

Fig. 4. A model for the recognition of pathogen-derived ceramide in plants. Pi-Cer D is cleaved by plant apoplastic ceramidase NCER2 into 9-methyl sphingoid base. 9-methyl sphingoid base is recognized by a lectin-receptor kinase, RDA2/SphingR, which then induces defense responses that include WRKY33 gene expression and enhances immunity against pathogen infection.

Population Genomics of Yams: Evolution and Domestication of Dioscorea Species

Sugihara, Y., Kudoh, A., Oli, M. T., Takagi, H., Natsume, S., Shimizu, M., Abe, A., Asiedu, R., Asfaw, A., Adebola, R. & Terauchi, R. (2021). Population Genomics of Yams: Evolution and Domestication of Dioscorea Species. In: Population Genomics. Springer, Cham. https://doi.org/10.1007/13836_2021_94

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Yam is a collective name of tuber crops belonging to the genus Dioscorea. Yam is important not only as a staple food crop but also as an integral component of society and culture of the millions of people who depend on it. However, due to its regional importance, yam has long been regarded as an “orphan crop” lacking a due global attention. Although this perception is changing with recent advances in genomics technologies, domestication processes of most yam species are still ambiguous. This is mainly due to the complicated evolutionary history of Dioscorea species caused by frequent hybridization and polyploidization, which is possibly caused by dioecy that imposed obligate outcrossing to the species of Dioscorea. In this chapter, we provide an overview of the evolution of Dioscorea and address the domestication of yam from population genomics perspectives by focusing on the processes of hybridization and polyploidization. A review is given to the recent population genomics studies on the hybrid origin of D. rotundata in West and Central Africa, the global dispersion of D. alata through human migrations, and the whole-genome duplication of the South America species of D. trifida. In the end, we give a summary of current understanding of sex-determination system in Dioscorea.