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The Fungal Root Endophyte Serendipita Indica Modifies Extracellular 2 Nucleotides to Subvert Plant Immunity

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The Fungal Root Endophyte Serendipita Indica Modifies Extracellular 2 Nucleotides to Subvert Plant Immunity bioRxiv preprint doi: https://doi.org/10.1101/396028; this version posted August 20, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 1 The fungal root endophyte Serendipita indica modifies extracellular 2 nucleotides to subvert plant immunity. 3 Shadab Nizam1,2, Xiaoyu Qiang1,2, Stephan Wawra2, Robin Nostadt1, Felix Getzke2, 4 Florian Schwanke2, Ingo Dreyer3, Gregor Langen2, Alga Zuccaro1,2+ 5 1Max-Planck-Institute for Terrestrial Microbiology, Karl-von-Frisch Strasse 10, 35043 6 Marburg, Germany 7 2University of Cologne, Botanical Institute, Cluster of Excellence on Plant Sciences 8 (CEPLAS), Cologne Biocenter, Zülpicher Str. 47b, 50674 Cologne, Germany 9 3Centro de Bioinformática y Simulación Molecular (CBSM), Universidad de Talca, 10 Chile 11 +Corresponding Author 12 Key words: DORN1; extracellular nucleotides; plant immunity; LecRK-1.9; 13 One sentence abstract: Immune modulation by metabolites in plant fungus 14 interaction 15 Abstract 16 Extracellular adenosine 5′-triphosphate (eATP) is an essential signaling molecule 17 that mediates different cellular processes through its interaction with membrane- 18 associated receptor proteins in animals and plants. eATP regulates plant growth, 19 development and responses to biotic and abiotic stresses. Its accumulation in the 20 apoplast induces ROS production and cytoplasmic calcium increase mediating a 21 defense response to invading microbes. We demonstrate that perception of eATP is 22 important in plant-fungus interaction and that during colonization by the beneficial 23 root endophyte Serendipita indica accumulation of eATP in the apoplast occurs at 24 early symbiotic stages. We show by liquid chromatography-tandem mass 25 spectrometry, cytological and functional analysis that S. indica subvert eATP host 26 response by secreting SiE5’NT, an enzymatically active ecto-5'-nucleotidase capable 27 of hydrolyzing eATP to adenosine. A. thaliana lines producing extracellular SiE5’NT 28 are significantly better colonized and have reduced eATP levels and defense 29 signaling, indicating that SiE5’NT functions as a compatibility factor. Our data show 30 that extracellular bioactive nucleotides play an important role in fungus-root 31 interactions and that fungi can modify plant derived metabolites in the apoplast to 32 modulate host immunity. 33 Introduction 34 ATP is a coenzyme that serves as an universal energy currency and as building 35 block of genetic material and secondary metabolites. Additionally, ATP and 36 adenosine are important extracellular regulators in plants and animals (Burnstock, 37 1972, Burnstock, 2012, Chivasa & Slabas, 2012, Clark, Morgan et al., 2014, Tanaka, 1 bioRxiv preprint doi: https://doi.org/10.1101/396028; this version posted August 20, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 38 Choi et al., 2014). In plants it has been shown that extracellular ATP (eATP) is 39 released during growth, physical injury and in response to various abiotic and biotic 40 stresses and microbe derived elicitors (Cao, Halane et al., 2017, Choi, Tanaka et al., 41 2014, Clark et al., 2014, Dark, Demidchik et al., 2011, Kim, Sivaguru et al., 2006, 42 Roux & Steinebrunner, 2007, Song, Steinebrunner et al., 2006, Tanaka et al., 2014, 43 Tanaka, Gilroy et al., 2010, Wu & Wu, 2008). Accumulation of eATP triggers the 44 production of reactive oxygen species (ROS), nitric oxide, callose deposition, 45 cytoplasmic calcium increase, transient phosphorylation of MPK3 and MPK6, and 46 expression of genes involved in plant stress response and immunity (Choi et al., 47 2014, Lim, Wu et al., 2014). To be physiologically relevant eATP must be sensed by 48 specific receptors at the cell surface. Recently, the Arabidopsis thaliana lectin 49 receptor kinase DORN1 (DOes not Respond to Nucleotides 1, At5g60300), also 50 known as the LecRK-I.9 (lectin receptor kinase I.9), was identified as the first plant 51 purinoceptor essential for the plant response to eATP, unveiling an eATP signaling 52 pathway in plants (Choi et al., 2014). The RXLR-dEER effector protein IPI-O 53 secreted by the oomycete pathogen Phytophthora infestans targets LecRK- 54 I.9/DORN1 (Bouwmeester, de Sain et al., 2011, Gouget, Senchou et al., 2006, 55 Senchou, Weide et al., 2004, Wang, Nsibo et al., 2016), suggesting that some 56 microbes have the tools to manipulate host eATP perception/signaling. LecRK- 57 I.9/DORN1 mutant plants show enhanced susceptibility to pathogenic infection by 58 the oomycete P. brassicae and the bacterium Pseudomonas syringae (Pst). 59 Consistently, overexpression of LecRK-I.9/DORN1 increases plant resistance to 60 Phytophthora spp and Pst (Balague, Gouget et al., 2017). Taken together, these 61 results suggest a role for an eATP-receptor protein in plant immunity. 62 There is increasing evidence that fungi, both pathogenic and mutualistic, have large 63 repertoires of secreted effectors. Some were functionally shown to be able to 64 manipulate the host cell physiology, suppress plant defense and ultimately promote 65 fungal colonization (Rovenich, Boshoven et al., 2014). Among fungi, compatibility 66 factors are mainly reported from biotrophic and hemibiotrophic leaf pathogens (Lo 67 Presti, Lanver et al., 2015). In contrast only few factors have been functionally 68 characterized from root mutualistic fungi (Kloppholz, Kuhn et al., 2011, Plett, 69 Daguerre et al., 2014, Plett, Kemppainen et al., 2011, Wawra, Fesel et al., 2016). 70 Therefore, the basis and mode of action of mutualistic fungal compatibility factors 71 remain poorly understood. The filamentous root endophyte Serendipita indica (syn. 72 Piriformospora indica) belongs to the order Sebacinales (Basidiomycota). S. indica 73 colonizes the root epidermal and cortex cells without penetrating the central cylinder 74 and displays a biphasic colonization strategy (Deshmukh, Huckelhoven et al., 2006, 75 Lahrmann, Ding et al., 2013, Qiang, Zechmann et al., 2012b, Zuccaro, Lahrmann et 76 al., 2011). During the initial phase of biotrophic colonization, the fungus invades the 77 root cells inter- and intracellularly. Subsequently, S. indica switches to a host cell 78 death associated phase, although a defined switch to necrotrophy with massive cell 79 death does not occur (Deshmukh et al., 2006, Lahrmann et al., 2013, Qiang et al., 80 2012b). S. indica colonization exhibits various effects on the host plants such as 2 bioRxiv preprint doi: https://doi.org/10.1101/396028; this version posted August 20, 2018. The copyright holder for this preprint (which was not certified by peer review) is the author/funder. All rights reserved. No reuse allowed without permission. 81 enhanced growth and assimilation of nitrate and phosphate, increased tolerance to 82 abiotic stresses and resistance against pathogens (Lahrmann & Zuccaro, 2012, 83 Oberwinkler, Riess et al., 2013, Qiang, Weiss et al., 2012a, Vahabi, Sherameti et al., 84 2015). Since S. indica establishes symbiotic interactions with a wide range of 85 experimental plants, including the dicot model plant A. thaliana and the monocot 86 cereal crop Hordeum vulgare (barley), it represents an excellent model system to 87 study ATP-mediated plant defense responses in the roots of unrelated hosts. 88 In order to identify S. indica secreted effectors, proteins present in the apoplastic 89 fluid (APF) of colonized barley roots were analyzed at three different symbiotic 90 stages by liquid chromatography-tandem mass spectrometry (LC-MS/MS). One of 91 the most abundant secreted fungal proteins identified at all time points is a predicted 92 5'-nucleotidase. The gene encoding this enzyme is induced during colonization of 93 both, barley and A. thaliana. Animal ecto-5'-nucleotidases (E5'NTs) have been 94 considered to play a key role in the conversion of AMP to adenosine and in 95 counteracting together with ecto-nucleotide pyrophosphatase/phosphodiesterase (E- 96 NPP), ecto-nucleoside triphosphate diphosphohydrolase (E-NTPDase) and alkaline 97 phosphatases (AP), eATP signaling (Antonioli, Pacher et al., 2013, Matsuoka & 98 Ohkubo, 2004). The importance of bioactive nucleotides signaling and fungal 99 extracellular E5'NT activity during plant-fungus interaction is unknown. We show 100 here that S. indica E5'NT is capable of hydrolyzing ATP, ADP and AMP to 101 adenosine, altering eATP levels and defense signaling in planta and plays an 102 important role in fungal accommodation at early symbiotic stages, suggesting that 103 immune modulation by metabolites in the apoplast is a mechanism of compatibility in 104 plant-fungus interactions. 105 Results 106 Identification of fungal proteins in the apoplast of barley roots 107 In order to identify soluble secreted candidate effector proteins during S. indica root 108 colonization, the proteins present in the APF of barley roots at three different 109 symbiotic stages (biotrophic and early and late cell death associated phase 110 corresponding to 5, 10 and 14 day-post-inoculation respectively) were analyzed 111 together with the proteins found in the culture filtrate (CF) obtained from S. indica 112 axenically grown in liquid complex medium (CM). To assess possible cytoplasmic 113 contaminations a strain constitutively expressing an S. indica codon-optimized GFP 114 under the SiGPD promoter (Hilbert, Voll et al., 2012b) was used.
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