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Molecular interactions between Arabidopsis and an oomycete that increases seed yield and protects the host from insect larvae
Molecular interactions between Arabidopsis and an oomycete that increases seed yield and protects the host from insect larvae
Intracellular accommodation of microbes by plant cells is a shared feature of arbuscular mycorrhiza (AM) and the nitrogen-fixing root nodule symbiosis (RNS). Curiously, it is also the foundation of specific pathogenic interactions with biotrophic oomycetes (downy mildew) and leaf rust fungi. Despite of the central relevance of all these intracellular interactions in agriculture, commonalties between the underlying molecular programs are only superficially studied. In this work I explored potential overlaps between early plant signal transduction processes leading to AM and RNS in legumes and those involved in haustoria development by obligate biotrophic oomycete Hyaloperonospora arabidopsidis (Hpa) in Arabidopsis. In legumes, calcium-spiking is one of the earliest responses of root cells to symbiotic stimulation and depends on the so-called common symbiosis genes Symbiosis Receptor Kinase SymRK and Pollux, encoding a cation-channel localized in the nuclear envelope. Arabidopsis has lost the ability to form root symbioses but still carries multiple SymRK homologous receptor kinase (ShRK) genes and an ortholog of Pollux. I investigated the role of ShRKs and Pollux in the interaction of Arabidopsis with Hpa. Five to six days post inoculation (dpi), Hpa formed a reduced number of sporangiophores and an increased frequency of typically non-encased multilobed haustoria on Arabidopsis pollux and shrk1 x shrk2 mutants. By using R-GECO transgenic lines, I observed cytoplasmic calcium waves and nuclear calcium spiking responses coinciding with the timeframe of massive haustoria development. The frequency and number of nuclear calcium spikes was strongly reduced in shrk1 x shrk2 double and pollux single mutants. To unravel the consequences of these mutations at the transcriptome level, we performed large scale (96 libraries) RNA-sequencing in collaboration with the laboratory of Wolfgang Enard. CAMTA3-regulated and salicylic acid-mediated immune responses were weaker in the mutants, suggesting that Hpa-induced calcium spiking might be decoded by CAMTA3 and might mediate SA-induced defense signaling. In parallel experiments, I obtained evidence that Hpa can be beneficial for Arabidopsis growth and seed yield. Caterpillar-type larvae of Spodoptera littoralis were feeding on non-infected but were repelled by Hpa-infected Arabidopsis. Taken together, our data redefine the biological role of Hpa in the compatible interaction with Arabidopsis as a beneficial symbiont.
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Hwu, Fang-Yu
2022
English
Universitätsbibliothek der Ludwig-Maximilians-Universität München
Hwu, Fang-Yu (2022): Molecular interactions between Arabidopsis and an oomycete that increases seed yield and protects the host from insect larvae. Dissertation, LMU München: Faculty of Biology
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Abstract

Intracellular accommodation of microbes by plant cells is a shared feature of arbuscular mycorrhiza (AM) and the nitrogen-fixing root nodule symbiosis (RNS). Curiously, it is also the foundation of specific pathogenic interactions with biotrophic oomycetes (downy mildew) and leaf rust fungi. Despite of the central relevance of all these intracellular interactions in agriculture, commonalties between the underlying molecular programs are only superficially studied. In this work I explored potential overlaps between early plant signal transduction processes leading to AM and RNS in legumes and those involved in haustoria development by obligate biotrophic oomycete Hyaloperonospora arabidopsidis (Hpa) in Arabidopsis. In legumes, calcium-spiking is one of the earliest responses of root cells to symbiotic stimulation and depends on the so-called common symbiosis genes Symbiosis Receptor Kinase SymRK and Pollux, encoding a cation-channel localized in the nuclear envelope. Arabidopsis has lost the ability to form root symbioses but still carries multiple SymRK homologous receptor kinase (ShRK) genes and an ortholog of Pollux. I investigated the role of ShRKs and Pollux in the interaction of Arabidopsis with Hpa. Five to six days post inoculation (dpi), Hpa formed a reduced number of sporangiophores and an increased frequency of typically non-encased multilobed haustoria on Arabidopsis pollux and shrk1 x shrk2 mutants. By using R-GECO transgenic lines, I observed cytoplasmic calcium waves and nuclear calcium spiking responses coinciding with the timeframe of massive haustoria development. The frequency and number of nuclear calcium spikes was strongly reduced in shrk1 x shrk2 double and pollux single mutants. To unravel the consequences of these mutations at the transcriptome level, we performed large scale (96 libraries) RNA-sequencing in collaboration with the laboratory of Wolfgang Enard. CAMTA3-regulated and salicylic acid-mediated immune responses were weaker in the mutants, suggesting that Hpa-induced calcium spiking might be decoded by CAMTA3 and might mediate SA-induced defense signaling. In parallel experiments, I obtained evidence that Hpa can be beneficial for Arabidopsis growth and seed yield. Caterpillar-type larvae of Spodoptera littoralis were feeding on non-infected but were repelled by Hpa-infected Arabidopsis. Taken together, our data redefine the biological role of Hpa in the compatible interaction with Arabidopsis as a beneficial symbiont.