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Gene expression of PLAT and ATS3 proteins increases plant resistance to insects

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Abstract

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Genes of the PLAT protein family, including PLAT and ATS3 subfamilies of higher plants and homologs of liverwort, are involved in plant defense against insects.

Abstract

Laticifer cells in plants contain large amounts of anti-microbe or anti-insect proteins and are involved in plant defense against biotic stresses. We previously found that PLAT proteins accumulate in laticifers of fig tree (Ficus carica) at comparable levels to those of chitinases, and the transcript level of ATS3, another PLAT domain-containing protein, is highest in the transcriptome of laticifers of Euphorbia tirucalli. In this study, we investigated whether the PLAT domain-containing proteins are involved in defense against insects. Larvae of the lepidopteran Spodoptera litura showed retarded growth when fed with Nicotiana benthamiana leaves expressing F. carica PLAT or E. tirucalli ATS3 genes, introduced by agroinfiltration using expression vector pBYR2HS. Transcriptome analysis of these leaves indicated that ethylene and jasmonate signaling were activated, leading to increased expression of genes for PR-1, β-1,3-glucanase, PR5 and trypsin inhibitors, suggesting an indirect mechanism of PLAT- and ATS3-induced resistance in the host plant. Direct cytotoxicity of PLAT and ATS3 to insects was also possible because heterologous expression of the corresponding genes in Drosophila melanogaster caused apoptosis-mediated cell death in this insect. Larval growth retardation of S. litura occurred when they were fed radish sprouts, a good host for agroinfiltration, expressing any of nine homologous genes of dicotyledon Arabidopsis thaliana, monocotyledon Brachypodium distachyon, conifer Picea sitchensis and liverwort Marchantia polymorpha. Of these nine genes, the heterologous expression of A. thaliana AT5G62200 and AT5G62210 caused significant increases in larval death. These results indicated that the PLAT protein family has largely conserved anti-insect activity in the plant kingdom (249 words).

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Abbreviations

DEG:

Differentially expressed (uni)gene

dph:

Days post-harvest

EGFP:

Enhanced green fluorescent protein

GO:

Gene ontology

PR:

Pathogenesis-related

rpkm:

Read counts per kilobase of unigene per million mapped reads

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Acknowledgements

This study was supported by a Grant-in-Aid for Scientific Research from the Ministry of Education, Science, Sports, Culture and Technology of Japan (to SK, No. 20K05768), the research grant for Mission Research on Sustainable Humanosphere from the Research Institute for Sustainable Humanosphere (RISH), Kyoto University (to SK), and Cooperative Research Grant of the Plant Transgenic Design Initiative (PTraD) by Gene Research Center, Tsukuba-Plant Innovation Research Center, University of Tsukuba (to SK, No 2002). We wish to thank Dr. Junji Shimabukuro, Kyoto Institute of Technology, for his generous aid in rearing S. litura.

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Correspondence to Sakihito Kitajima.

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Communicated by Dorothea Bartels.

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Savadogo, E.H., Shiomi, Y., Yasuda, J. et al. Gene expression of PLAT and ATS3 proteins increases plant resistance to insects. Planta 253, 37 (2021). https://doi.org/10.1007/s00425-020-03530-y

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  • DOI: https://doi.org/10.1007/s00425-020-03530-y

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