Running head: A central regulator of symbiotic gene ...€¦ · 13/05/2015 · 136 infected from nurse-plants exhibited exaggerated AM fungal colonization in root tips, 137 indicating

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1 Running head: A central regulator of symbiotic gene expression 2

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Research Area: Signaling and Response 7 8 9 10 11 12

13 For correspondence: 14 15 Didier Reinhardt 16 Dept. of Biology 17 Rte Albert Gockel 3 18 CH-1700 Fribourg 19 Switzerland 20 Tel.: ++41 26 300 88 18 21 Fax: ++41 26 300 97 40 22 email: [email protected] 23 24 25

Plant Physiology Preview. Published on May 13, 2015, as DOI:10.1104/pp.15.00310

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26 A petunia GRAS transcription factor controls 27

symbiotic gene expression and fungal 28 morphogenesis in arbuscular mycorrhiza 29

30 Mélanie K. Rich1, Martine Schorderet1, Laure Bapaume1, Laurent Falquet1,2, Patrice 31 Morel3, Michiel Vandenbussche3, Didier Reinhardt1 32 33 1Dept. of Biology, University of Fribourg, Switzerland 34 2Swiss Institute of Bioinformatics, University of Fribourg, Switzerland 35 3Dept. of Reproduction and Plant Development, CNRS/INRA/ENS Lyon, France 36 37

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Summary: The petunia GRAS transcription factor ATA/RAM1 regulates symbiotic 40 gene expression and is required for arbuscule development and restriction of fungal 41 colonization in the root tip. 42 43 44



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Abstract 45 Arbuscular mycorrhiza (AM) is a mutual symbiosis that involves a complex 46

symbiotic interface over which nutrients are exchanged between the plant host and the 47 AM fungus. Dozens of genes in the host are required for the establishment and 48 functioning of the interaction, among them nutrient transporters that mediate the 49 uptake of mineral nutrients delivered by the fungal arbuscules. We have isolated in a 50 genetic mutant screen a petunia GRAS-type transcription factor, ATYPICAL 51 ARBUSCULE (ATA), that acts as the central regulator of AM-related genes and is 52 required for the morphogenesis of arbuscules. Forced mycorrhizal inoculations from 53 neighbouring wild type plants revealed an additional role of ATA in restricting 54 mycorrhizal colonization of the root meristem. The lack of ATA, which represents the 55 orthologue of RAM1 in Medicago truncatula, renders the interaction completely 56 ineffective, hence demonstrating the central role of AM-related genes for arbuscule 57 development and function. 58

59 60 61 62 Abbreviations: 63 AM Arbuscular mycorrhiza 64 RNS Root nodule symbiosis 65 ATA Atypical arbuscule 66 RAM1 Required for arbuscular mycorrhiza1 67

GRAS GIBBERELLIC ACID INSENSITIVE (GAI), REPRESSOR of 68 GAI (RGA) and SCARECROW (SCR) 69

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Introduction 72 Most land plants live in a symbiotic association known as arbuscular 73

mycorrhiza (AM) with soil fungi (Glomeromycota), which provide them with mineral 74 nutrients and improve their stress resistance (George, 2000; Pozo and Azcon-Aguilar, 75 2007; Smith and Read, 2008). In return, the strictly biotrophic fungal partner receives 76 photoassimilates (Douds et al., 2000), and perhaps other vital factors from the host 77 plant. At the core of the interaction is the symbiotic interface, over which the nutrients 78 are exchanged. The interface comprises a highly branched fungal feeding structure, 79 the arbuscule, and the surrounding host membrane in which the arbuscule is 80 accommodated. Establishment of AM interactions requires the mutual recognition of 81 the two partners and the activation of a symbiosis-specific pathway (Harrison, 2012; 82 Gutjahr and Parniske, 2013; Oldroyd, 2013), which relies on a series of so-called 83 common symbiosis (SYM) genes, because their function is required for both, AM and 84 the root nodule symbiosis (RNS) of the legumes (Kistner and Parniske, 2002). The 85 shared signaling pathway entails a nuclear calcium signal, Ca-spiking, which is 86 thought to lead to transcriptional reprogramming of symbiotic cells by a mechanism 87 that involves the calcium and calmodulin-dependent protein kinase (CCaMK), and the 88 transcriptional activator CYCLOPS (Singh and Parniske, 2012; Singh et al., 2014). 89

The common SYM genes were discovered in legumes by surveying 90 nodulation-defective mutants for their mycorrhizal phenotypes (Duc et al., 1989), 91 however, most plants do not engage in mutual symbioses with bacteria, hence their 92 equivalents of common SYM genes function only in AM, and could therefore be 93 compared with the ancient AM-related signaling pathway before it got adopted by 94 rhizobia (Kistner and Parniske, 2002). Although the leguminous species Medicago 95 truncatula and Lotus japonicus are among the leading model systems for root 96 symbioses (Udvardi et al., 2005; Jones et al., 2007), it is important to also consider 97 non-nodulating species such as rice (Oryza sativa) or petunia (Petunia hybrida), in 98 which the symbiosis-related pathways have not been influenced by the evolution of 99 RNS and therefore may resemble the ancestral mechanisms evolved for AM. 100

One of the downstream consequences of signalling through the symbiosis 101 signalling pathway is the activation of a symbiosis-related transcriptional program, 102 which involves the activation of dozens of genes that are thought to be required for 103 the establishment of the symbiotic interface, and for symbiotic functioning (Liu et al., 104 2003; Güimil et al., 2005; Hohnjec et al., 2005; Fiorilli et al., 2009; Gomez et al., 105



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2009; Guether et al., 2009; Breuillin et al., 2010; Gaude et al., 2012; Tromas et al., 106 2012; Hogekamp and Küster, 2013). Comparison between transcriptomic studies in 107 dicots (such as M. truncatula, L. japonicus, P. hybrida, Solanum lycopersicum), and 108 in the monocot model system rice have revealed a conserved set of AM-induced 109 genes (Breuillin et al., 2010). However, only few of them have been functionally 110 elucidated, among them phosphate and nitrate transporters (Maeda et al., 2006; Javot 111 et al., 2007; Guether et al., 2009), proteases (Takeda et al., 2009; Rech et al., 2013), 112 ABC transporters (Zhang et al., 2010; Gutjahr et al., 2012; Kretzschmar et al., 2012), 113 and transcription factors such as CYCLOPS (Singh et al., 2014), RAM1 (Gobbato et 114 al., 2012) and RAD1 (Xue et al., 2015). 115

A number of transcription factors involved in AM and/or RNS have been 116 identified in forward genetic mutant screens and some of them are strongly induced in 117 AM interactions. Besides CYCLOPS (Singh et al., 2014), symbiosis-related TFs 118 belong primarily to the large family of GRAS transcription factors (Smit et al., 2005; 119 Gobbato et al., 2012; Xue et al., 2015). Both, RNS and AM rely on specific GRAS-120 type TFs, which are thought to mediate specific transcriptional read-outs related to 121 AM (Gobbato et al., 2012; Xue et al., 2015) and RNS (Kalo et al., 2005; Smit et al., 122 2005), respectively. However, detailed characterization of mutants revealed 123 overlapping functions of some GRAS-type TFs in AM and RNS (Kalo et al., 2005; 124 Maillet et al., 2011; Lauressergues et al., 2012). 125 126 Here we report the isolation and characterization of a mutant, atypical arbuscule (ata) 127 in Petunia hybrida that is defective in arbuscule development and, as a consequence, 128 cannot establish functional interactions with diverse AM fungi. Infection from 129 colonized wild type plants (nurse-plants) is possible, however, the arbuscule 130 phenotype remains. ATA encodes a GRAS-type transcription factor and represents the 131 orthologue of RAM1 in M. truncatula. Gene expression analysis revealed that the 132 induction of all tested arbuscule-related marker genes in petunia depends on 133 ATA/RAM1, with the notable exception of VAPYRIN, which appears to be involved 134 upstream of ATA/RAM1 or in a parallel pathway. Interestingly, ata/ram1 mutants 135 infected from nurse-plants exhibited exaggerated AM fungal colonization in root tips, 136 indicating that ATA/RAM1 plays a double role in promoting arbuscule morphogenesis 137 and in preventing colonization of the root meristem. 138



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139 140 Results: 141 Isolation of the ata mutant 142 In a forward genetic mutant screen in the transposon-mutagenized Petunia hybrida 143 line W138, an AM-defective mutant has been isolated based on its strongly reduced 144 levels of mycorrhizal colonization in the interaction with the AM fungus Rhizophagus 145 irregularis (Figure 1A,B). Rare infection events were observed in the mutant at early 146 time points (Figure 1B), however, the fungal colonies never reached the same density 147 as in the wild type, and they were characterized by malformed arbuscules (Figure 148 1C,D). In cases where the fungus was able to penetrate the root surface, the first 149 hyphal coil in the epidermis appeared normal, however, in the root cortex the fungus 150 developed profuse hyphal material with many septa, an indication for stress (Figure 151 1E). Based on the prominent defect in arbuscule morphogenesis, the mutant was 152 termed atypical arbuscule (ata). The ata phenotype segregated as a recessive 153 monogenic trait with 98 mutants among 378 segregating F2 plants (25.93% mutants, 154 p<0.05 chi-square test). 155 To test whether the AM-defect in ata exhibits race- or species-specificity towards 156 different AM-fungi, three fungal isolates with relatively distant phylogenetic 157 relationships were compared for their ability to colonize ata, namely R. irregularis, 158 Simiglomus hoi, and Acaulospora scrobicularia (Stockinger et al., 2010; Krueger et 159 al., 2012). All three fungi reached low degrees of transient infection up to 4 weeks 160 after inoculation, but eventually remained unsuccessful in colonizing ata (Figure S1). 161 Hence, the mutation in the ATA gene results in a general defect in AM symbiosis. 162 The initial transient infections (Figure 1B,D,E) indicate that ata can be penetrated, 163 but cannot entertain a functional interaction with AM fungi. In such cases, nutrition 164 from a nearby growing wild type plant can potentially enable the fungus to colonize 165 AM-defective mutants, a system known as nurse-plant inoculation. Nurse-plants 166 represent a very strong inoculum, from which highly AM-resistant mutants 167 (Feddermann et al., 2010), and even non-host plants (Veiga et al., 2013) can be 168 colonized. Indeed, nurse-plant inoculation of ata resulted in rapid and efficient 169 colonization (Figure 2A,B), however, the defect in arbuscule development was 170 retained (Figure 2C,D). These results show that the ATA gene is essential for 171 arbuscule development, whereas infection and colonization as such are independent 172



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from ATA function. Hence, the function of ATA in AM development is relatively late, 173 compared to the function of common SYM genes in infection (Harrison, 2012; 174 Gutjahr and Parniske, 2013). 175 176 Characterization of the ATA locus and the encoded protein 177 We carried out transposon display (Van den Broeck et al., 1998; Vandenbussche et 178 al., 2013) to identify the gene mutated in ata. Using this technique, we identified and 179



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cloned a transposon flanking sequence that strictly cosegregated with the ata 180 phenotype (Figure S2A). The sequence represented a short fragment from the coding 181 region of a GRAS transcription factor gene that contains two exons of 970 and 1121 182 nucleotides, respectively, separated by an intron of 783 nucleotides, and encodes a 183



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predicted protein of 697 amino acids. The transposon had inserted in the second 184 predicted exon 1384 nucleotides downstream of the ATG start codon (Figure S2B). 185 In order to verify that the mutation in this GRAS transcription factor gene is 186 responsible for the AM-defective phenotype in ata mutants, we searched for 187 phenotypic revertants in the progeny of a homozygous ata mutant plant. Such 188 revertants can result from excision of the transposon and from restauration of the open 189 reading frame. Most transposon excisions leave an 8-bp footprint that results from the 190 target site duplication (TSD) during transposon insertion (Gerats et al., 1990), and 191 therefore cause an irreversible shift in the reading frame. However, in rare cases, the 192 reading frame is restored by partial or complete removal of the TSD, resulting in 193 restored gene function. We isolated a phenotypic revertant plant that carried an altered 194 ata allele, in which not only the TSD, but additional 6 bp had been removed at the site 195 of the transposon insertion. Although this results in a deletion of two amino acids, it 196 restores the reading frame and therefore leads to a functional protein (Figure S2C). 197 The simultaneous recovery of the ata phenotype and the nearly perfect restauration of 198 the gene sequence in the revertant suggest that the ata phenotype is caused by the 199 transposon insertion in the GRAS gene. The GRAS transcription factor encoded by 200 the ATA gene exhibits close homology to MtRAM1, and to predicted GRAS proteins 201 from various dicots and monocots, but no close homologs were found in the non-202 mycorrhizal species from the Brassicaceae family, such as Arabidopsis thaliana and 203 Brassica rapa (Figure S2D) (Gobbato et al., 2012; Delaux et al., 2014; Favre et al., 204 2014). Taken together, these results indicate that ATA represents the ortholog of 205 RAM1 in Medicago truncatula, therefore we further refer to it as ATA/RAM1. 206 The ram1-1 mutant in M. truncatula was reported to be defective at a very early point 207 of the interaction, before infection (Gobbato et al., 2012), whereas the defect in 208 ata/ram1 mutants in petunia is at a considerably later stage of the interaction, namely 209 at the stage of arbuscule development (see above). In order to verify the mutant 210 phenotype of our first ata/ram1 allele, we obtained two additional mutant alleles 211 (ram1-2, and ram1-3, respectively) from a large collection of transposon-mutagenized 212 plants characterized by deep sequencing (Vandenbussche et al., 2008). Both new 213 alleles have dTph1 insertions in the first exon after 357 and 381 bp of the coding 214 sequence, respectively (Figure S2B), which completely disrupt the conserved C-215 terminal DNA-binding domain (Figure S3). Inoculation with R. irregularis revealed a 216



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virtually identical phenotype of both new alleles as in ata/ram1-1. In particular, 217 arbuscules were poorly developed and colonization was very low and transient with 218 spore inoculum (Figure S4A). In contrast, nurse-plant inoculation resulted in efficient 219 colonization (Figure S4B), however, the arbuscule-defective phenotype was retained 220 (Figure 2E,F). These results corroborate the essential arbuscule-related function of 221 ATA/RAM1 in petunia, and suggest that all three dTph1 insertion alleles, which are 222 expressed at considerably lower levels than the wild type allele (Figure 3), are strong 223 mutant alleles. This conclusion also follows from the fact that the sequence of dTph 224 carries stop codons in all six reading frames, and therefore, proteins encoded by genes 225



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with dTph insertions are invariably truncated. Since the three dTph insertions in ATA 226 eliminate most (ata/ram1-1) or all (ram1-2, ram1-3) of the conserved C-terminal 227 DNA-binding domain (Figure S3), and since all three alleles exhibit the same strong 228 AM-defective phenotype, they are likely to represent functional null alleles. 229 In order to address the arbuscule phenotype of ram1 mutants in M. truncatula, we 230 inoculated ram1-1 with R. irregularis and performed a time course experiment with 231 samplings after 10, 20, and 30 days from inoculation. As in the case of P. hybrida, the 232 M. truncatula mutant was transiently colonized after 10-20 days (<10% colonization), 233 but at the 30 d time point, the fungus had virtually disappeared, while the wild type 234 had reached >70% colonization (Figure S5A). The rare arbuscules exhibited a deviant 235 shape and structure similar to the ones in ata/ram1 mutants of P. hybrida (Figure 236 S5B,C, compare with Figure 2C-F). These results suggest that the function of RAM1 237 in arbuscule formation is conserved between M. truncatula and P. hybrida. 238 239 ATA/RAM1 is required for the induction of several AM-related genes 240 RAM1 in M. truncatula and in L. japonicus is known to contribute to the induction of 241 several AM-induced transcripts (Gobbato et al., 2012; Xue et al., 2015). In order to 242 assess the role of the petunia RAM1 in AM-related gene induction, we chose a panel 243 of AM-related marker genes, including ATA/RAM1 itself, the VAPYRIN gene that is 244 required for intracellular accommodation of AM fungi (Feddermann et al., 2010; 245 Pumplin et al., 2010; Murray et al., 2011), the two mycorrhizal phosphate transporters 246 PT4 and PT5 (Wegmüller et al., 2008; Breuillin et al., 2010), the closest petunia 247 homologues of the G-type ABC transporter genes STUNTED ARBUSCULE (STR) and 248 STR2 of M. truncatula (Zhang et al., 2010), a glycerol-3-phosphate acyltransferase 249 (GPAT), that is closely related to the AM-specific RAM2 gene in M. truncatula 250 (Wang et al., 2012), and two AM markers with unknown function, subtilase and blue-251 copper-binding protein (BCP) (Breuillin et al., 2010). In order to achieve comparable 252 colonization levels in all genotypes (wt and the three ram1 alleles), the plants were 253 inoculated with nurse-plants. 254 Expression of ATA/RAM1 and of all AM marker genes, except for VAPYRIN, was 255 undetectable or very low in non-mycorrhizal control roots, but was strongly induced 256 in mycorrhizal wild type roots, whereas the induction was abolished in the ata/ram1-1 257 mutant (Figure S6). To confirm this molecular phenotype, we compared the 258 expression of all AM markers in all three ram1 alleles in two independent 259



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experiments. Strong induction ratios were observed in the wild type plants, whereas in 260 all three ram1 alleles, the AM marker genes remained very low or undetectable 261 (Figure 3 and Table S1). An exception was VAPYRIN which is constitutively 262 expressed and becomes further induced in mycorrhizal roots (Feddermann et al., 263 2010), and who's expression was only marginally affected by the mutations in 264 ATA/RAM1 (Figure 3 and Table S1). These findings are in contrast to the vapyrin 265 mutant, in which AM-marker genes were still induced, despite the strong AM-266 defective phenotype (Feddermann et al., 2010). These results suggest that RAM1 is a 267 central regulator of AM-related genes. 268 269 Root tip AM colonization in ata/ram1 mutants 270 Unexpectedly, nurse-plant inoculation of ata/ram1-1 resulted in significantly higher 271 colonization levels than in the wild type (Figure 2A,B). Visual inspection suggested 272 colonization of the root tips, hence this aspect was quantified. All three mutant alleles 273 and two comparable wild type accessions were scored in two independent 274 experiments for the presence of fungal structures in 100 μm intervals from the root 275 tip. In the wild type, only 10-20% of the roots were colonized up to the root tip (<100 276 μm), whereas in the three mutant lines, 40-70% of the root tips contained fungal 277 structures (Figure 4A-E). Detailed quantification of the different fungal structures in 278 root tips showed that both, total colonization and the formation of vesicles, were 279 increased in the mutants (Figure 4D-G). The differences in colonization between 280 mutants and wild type were in all cases significant (Figure S7). Taken together these 281 results show that, despite the defect in arbuscule development (Figure 2), ram1 282 mutants colonized from nurse-plants allow the fungus to grow into the root tip, a 283 region that normally remains devoid of any fungal structures. 284 285 286 287



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Discussion 288 289 Requirement of transcription factors in arbuscular mycorrhiza 290 Establishment of mutual symbioses such as AM and RNS requires a fundamental 291 reprogramming of root cells. Epidermal and hypodermal cells are involved in early 292 communication and at the early stages of infection (Oldroyd et al., 2011; Harrison, 293



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2012; Gutjahr and Parniske, 2013). Subsequently, cortical cells are reprogrammed 294 for intracellular accommodation of the endosymbiotic microbes, and for the ultimate 295 goal of the interaction, nutrient exchange. In addition, the establishment of a state of 296 robust and permanent symbiotic compatibility implies that certain defense pathways 297 are kept silent despite the massive AM fungal colonization in mycorrhizal roots 298 (Kloppholz et al., 2011). The acquisition of these multiple new traits entails 299 transcriptional reprogramming of symbiotic plant cells. 300 For most of the AM-induced transcripts, the mechanism of induction is unknown. 301 Although several predicted transcription factors were identified by their defect in AM 302 (Gobbato et al., 2012; Xue et al., 2015) or RNS (Kalo et al., 2005; Smit et al., 2005; 303 Singh et al., 2014), only few of their downstream targets have been determined. For 304 example, RAM1 has been shown to be required for induction of RAM2 (Gobbato et 305 al., 2012; Xue et al., 2015), NSP1 and NSP2 induce the strigolactone biosynthetic 306 gene DWARF27 (Liu et al., 2011), CYCLOPS induces the NODULE-INCEPTION 307 (NIN) gene (Singh et al., 2014), and RAD1 contributes to induction of STR and 308 RAM2 (Xue et al., 2015). Since most of these studies had been carried out in 309 legumes, the question arises to which degree the mentioned transcription factors 310 contribute to the two symbioses, AM and RNS. At least for NSP2 and for CYCLOPS, 311 a dual role in both symbioses has been shown (Yano et al., 2008; Maillet et al., 312 2011). 313 Since the majority of AM-competent plants does not engage in RNS, it is important to 314 learn how symbiotic signalling is translated into a transcriptional response in plant 315 species that were not influenced by the evolution of RNS. The example of petunia is 316 ideally suited for this, because its AM-related transcriptome has been characterized in 317 detail (Breuillin et al., 2010). Here, we show that the ATA/RAM1 gene of petunia 318 encodes a central transcriptional inducer of AM-related genes, and an essential 319 component in the development of the fungal arbuscules. 320 321 Nurse-plant inoculation reveales a central role of ATA/RAM1 in mycorrhizal 322 gene expression 323 Reduced induction of an AM-inducible gene in a mutant such as ata/ram1 can have 324 two reasons: It could be caused by the mutation, or it could be due, indirectly, to the 325 reduced levels of fungal colonization. To distinguish between these possibilities, we 326



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used nurse-plant inoculation to achieve comparable colonization levels in all 327 genotypes. Nurse-plants are well colonized wild type plants that grow nearby the 328 mutants and represent a very strong source of inoculum. Such inoculum can even 329 result in colonization of the non-host plant Arabidopsis thaliana (Veiga et al., 330 2013), and in the strongly AM-resistant vapyrin mutant, nurse-plant inoculation 331 triggered the induction of the AM-marker gene PT4 although at reduced levels 332 (Feddermann et al., 2010). 333 We examined the expression of eight arbuscule-associated marker genes PT4, PT5, 334 RAM2, STR, STR2, VAPYRIN (see references above), as well as subtilase (Takeda et 335 al., 2007), and a blue-copper-binding protein (Paradi et al., 2010), all representing 336 conserved AM-responsive marker genes (Breuillin et al., 2010). Despite efficient 337 colonization from nurse-plants (Figure 2), all these genes remained silent in ata/ram1 338 mutants, with the exception of VAPYRIN, which still showed constitutive expression 339 and mycorrhizal induction (Figure 3, Table S1). VAPYRIN represents a common 340 symbiosis gene that acts downstream of calcium-spiking (Murray et al., 2011), and is 341 required at earlier stages of AM infection than ATA/RAM1, namely at cell penetration 342 (Feddermann et al., 2010; Pumplin et al., 2010). In this sence, VAPYRIN acts 343 upstream, and therefore independently, of the function of ATA/RAM1. 344 345 ATA/RAM1 prevents AM colonization of the root tips 346 Nurse-plant inoculation allowed us to discover a second important aspect of the 347 ata/ram1 phenotype. Ata/ram1 mutants tended to be colonized at higher levels than 348 the wild type (Figure 2). An obvious aspect of the colonized mutant roots was that 349 they often exhibited fungal colonization into the extreme root tip (Figure 4), a region 350 that is normally not colonized. This indicates that ATA/RAM1 is not only involved in 351 the induction of arbuscule-associated genes (Figure 3), but also in a negative 352 feedback loop that protects the root meristems from excessive AM fungal 353 colonization. Colonized root tips had a normal overall shape and appearance, 354 indicating that their function was not significantly affected by fungal colonization. 355 The colonization of ram1 root tips resembles the effect of overexpression of a micro-356 RNA-resistant version of NSP2 in M. truncatula, which also resulted in ectopic AM 357 colonization in root tips (Lauressergues et al., 2012). 358 359



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Why is arbuscule development inhibited in ata/ram1? 360 In ram1 mutants, all the common SYM genes are intact, and accordingly, the initial 361 infection events, such as the formation of hyphopodia on the root surface and hyphal 362 coils in epidermal cells, are normal in ram1 mutants (Figure 1). Differences in the 363 interpretation of the mutant phenotypes in this study and in previous studies (Gobbato 364 et al., 2012; Xue et al., 2015) may be due to differences in the timing of sampling, 365 and/or in differences in the inoculation procedure. In contrast to the early stages of the 366 interaction, infection in the cortex, and in particular arbuscule development, were 367 strongly affected in ram1 mutants (Figure 2). The timing of these relatively late 368 defects are consistent with the molecular defect of ram1 mutants, which is the lack of 369 induction of genes that are expressed in cells with arbuscules, in particular PT4, STR, 370 STR2, and RAM2. We conclude that ram1 has a relatively late defect in AM 371 development, which, however, translates into a strong general AM defect because of 372 the lack of secondary infection events. Therefore, the phenotype of ram1 at later 373 stages appears very strong, even stronger than mutants affected in common SYM 374 genes, which act upstream and are affected at early stages of infection, but permit 375 occasional infection events that can develop into almost normal infection units 376 (Bonfante et al., 2000; Novero et al., 2002; Demchenko et al., 2004). 377 Several of the arbuscule-associated genes were shown to be essential for AM 378 symbiosis. Their mutation results in defective symbiosis which is often associated 379 with incomplete development and/or premature senescence of the fungal arbuscules. 380 This is the case for PT4 (Maeda et al., 2006; Javot et al., 2007), STR and STR2 381 (Zhang et al., 2010; Gutjahr et al., 2012), subtilase (Takeda et al., 2009), and RAM2 382 (Wang et al., 2012). The fact that all these genes fail to be induced in ram1 mutants 383 (Figure 3) can explain the strong defect in arbuscule formation, and, secondarily, the 384 abortion of AM development. Based on the collective evidence described here, we 385 conclude that ATA/RAM1 acts as a general transcriptional activator of arbuscule-386 associated genes in petunia. 387 388 Acknowledgments 389 We thank the Petunia Genome Consortium for access to the P. axillaris draft genome 390 sequence, and Giles E. Oldroyd for providing seeds of the M. truncatula ram1-1 391 mutant. This work was supported by the Swiss National Science Foundation (Grant-392 No.: 31003A_135778) and the University of Fribourg. 393



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394 Supplemental Material 395 396 Supplemental Information and Supplemental Figures are available online at . . . . 397 398 Supplemental Materials and Methods 399 400 401 Supplemental Figures 402 403 Fig. S1. AM-defective phenotype of ata mutant in combination with diverse AM 404 fungi 405 406 Fig. S2. ATA encodes a conserved GRAS transcription factor 407 408 Fig. S3. The GRAS transcription factor encoded by ATA/RAM1 and its closest 409 homologs in M. truncatula, rice, and mayze 410 411 Fig. S4. Colonization of ram1-2 and ram1-3 by R. irregularis 412 413 Fig. S5. AM-defective phenotype of M. truncatula ram1-1 414 415 Fig. S6. Expression of AM marker genes in the ata mutant 416 417 Fig. S7. Statistical analysis of fungal colonization of the root tip 418 419 Table S1. Expression of AM marker genes in the ata/ram1 mutants 420 421 Table S2. Primers for qPCR 422 423 424 Figure legends 425 426 Figure 1. The ata mutant is AM-defective 427



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A) Root colonization in the wild type (Petunia hybrida line W138) colonized by R. 428 irregularis. Total root colonization (blue), occurrence of arbuscules (red), and of 429 abnormal arbuscules (green) is indicated. 430 B) Root colonization in the ata mutant colonized by R. irregularis. Color code as in 431 (A). Asterisks indicate significant differences between the mutant and the wild type. 432 C) and D) colonization pattern in the wild type (C), and in one of the rare colonization 433 units in the ata mutant (D). Arbuscules are indicated by arrowheads. 434 E) Overview of the developmental stages of R. irregularis in ata. A hyphopodium 435 (arrow) and an infected epidermal cell with a fungal hypha (cross) mark a successful 436 infection event. Note the frequent septa in the fungal hyphae (white arrowheads), 437 indicative of stress in the fungus. 438 Columns represent the average of five biological replicates ± standard deviation. 439 Significant differences (Student's t-test) between the mutant and the wild type are 440 indicated with asterisk (*: p<0.05; **: p<0.01). v: vesicles; Size bars: 100 µm in C,D; 441 50 µm in E. 442 443 Figure 2. ata mutants can be colonized from nurse-plant inoculum but retain the 444 arbuscule phenotype 445 A) Root colonization in the wild type (Petunia hybrida line W138) colonized by R. 446 irregularis from nurse-plants. Total root colonization (blue), occurrence of arbuscules 447 (red), and of abnormal arbuscules (green) is indicated. 448 B) Root colonization in the ata mutant colonized by R. irregularis from nurse-plants. 449 Color code as in (A). Asterisks indicate significant differences between the mutant 450 and the wild type. 451 (C-F) Appearance of arbuscules in the wild type (C), ata (D), ram1-2 (E), and ram1-452 3 (F). 453 Columns represent the average of five biological replicates ± standard deviation. 454 Significant differences (Student's t-test) between the mutant and the wild type are 455 indicated with asterisk (*: p<0.05; **: p<0.01; ***: p<0.001). size bars: 25 µm. 456 457 Figure 3. ATA/RAM1 is required for induction of AM marker genes. 458 Gene expression was analyzed by quantitative real time RT-PCR one week after 459 inoculation with R. intraradices from nurse-plants. Two independent experiments are 460 shown in combination: Firstly, wild type (blue) vs. ata/ram1-1 (red), and secondly, 461



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wildtype (green) vs. ram1-2 (purple) and ram1-3 (orange). Columns represent the 462 average of three independent biological replicates ± standard deviation. Gene 463 expression values are expressed relative to the constitutively expressed reference gene 464 GAPDH. Significant differences (Student's t-test) between the mutant and the 465 respective wild type are indicated with asterisk (*: p<0.05; **: p<0.01; ***: p<0.001). 466 467 Figure 4. ata/ram1 mutants allow mycorrhizal colonization of the root tip. 468 A) Non-colonized wild type root. 469 B) Colonized wild type root. 470 C) Colonized ata/ram1-1 root. 471 D) Fungal colonization in wild type (blue; n=36) and ata/ram1-1 roots (red; 39) in the 472 distal 1 mm of the root tip. 473 E) Fungal colonization as in (D) in wild type (blue; n=28), ram1-2 (red; n=32), and 474 ram1-3 (green; n=35). 475 F) Fungal colonization as in (D), but scored only for vesicles. 476 G) Fungal colonization as in (E), but scored only for vesicles. 477 Size bar: 100 µm. 478 479 480 Supplemental Figures 481 482 Figure S1. AM-defective phenotype of ata mutant in combination with diverse 483 AM fungi. 484 Wild type and ata mutants were inoculated with R. irregularis, Simiglomus hoi, and 485 Acaulospora scrobiculata. Total root colonization was assessed after 1, 2, 4, and 8 486 weeks. Columns represent the average of three biological replicates ± standard 487 deviation. Significant differences (Student's t-test) between the mutant and the wild 488 type are indicated with asterisk (*: p<0.05; **: p<0.01; ***: p<0.001). 489 490 Figure S2. ATA encodes a conserved GRAS transcription factor. 491 A) Transposon display revealed a PCR amplicon that cosegregated with the ata 492 mutant phenotype (arrow). 493



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B) Map of the wild type ATA/RAM1 locus and the three ram1 insertion alleles. Thick 494 lines represent exons, the thin line represents the single intron. Arrows indicate the 495 insertion sites of dTPh1 in the alleles ata/ram1-1, ram1-2, and ram1-3, respectively. 496 C) Analysis of the revertant allele of ata/ram1-1 in comparison with the respective 497 sequence stretch of the wild type allele in Petunia axillaris, as well as the closest 498 homologues from M. truncatula, rice (Oryza sativa), and mayze (Zea mays) (compare 499 with Figure S3). Note a deletion of 2 amino acid residues in the revertant allele (Pa-500 ATA-rev). 501 D) Phylogram of the predicted ATA protein from P. axillaris and RAM1 from M. 502 truncatula together with the closest homologs from various monocot (Zea mays, 503 Brachypodium distachyon, Setaria italica, Sorghum bicolor), and dicot species 504 (Capsella rubella, Arabidopsis thaliana, Arabidopsis lyrata, Lotus japonicus, 505 Cucumis sativus, Solanum lycopersicum, Vitis vinifera, Populus trichocarpa, and 506 Ricinus communis). 507 508 Figure S3. The GRAS transcription factor encoded by ATA/RAM1 and its closest 509 homologs in M. truncatula, rice, and mayze. 510 The predicted petunia ATA/RAM1 protein sequence was aligned with MtRAM1 and 511 the closest homologs of rice (Oryza sativa), and mayze (Zea mays) using multalin 512 (http://multalin.toulouse.inra.fr). Arrows indicate the insertion sites of dTph1 in the 513 alleles ata/ram1-1 (arrow 1), ram1-2 (arrow 2), and ram1-3 (arrow 3), respectively. 514 515 Figure S4. Colonization of ram1-2 and ram1-3 by R. irregularis. 516 A) Total root colonization in the wild type (blue), ram1-2 (red), and ram1-3 (green), 517 colonized from R. irregularis spore inoculum. 518 B) Total root colonization in the wild type (blue), ram1-2 (red), and ram1-3 (green), 519 colonized from nurse-plants with R. irregularis. 520 Columns represent the average of five biological replicates ± standard deviation. 521 Significant differences (Student's t-test) between the mutant and the wild type are 522 indicated with asterisk (*: p<0.05). 523 524 Figure S5. AM-defective phenotype of M. truncatula ram1-1. 525 A) Total root colonization of R. irregularis in M. truncatula wild type (Line A17; 526 blue) and in ram1-1 (red). 527



21

B) Wild type root (line A17) colonized by R. irregularis. Arbuscules are indicated by 528 arrow-heads. 529 C) Root of M. truncatula ram1-1 mutant inoculated with R. irregularis. Note the 530 aberrant arbuscules (arrowheads). Size bars: 50 µm in B,C. 531 532 Figure S6. Expression of AM marker genes in the ata mutant. 533 Gene expression was determined by real time RT-PCR in non-mycorrhizal control 534 roots (-), and in colonized roots of the wild type (grey bars), and in ata mutants (black 535 bars). Each bar represents an individual replicate plant. 536 537 Figure S7. Statistical analysis of fungal colonization in the root tip. 538 The data shown in Figure 4D,E was transformed into survival curves. Log-rank test 539 was performed to assess the significance of the difference between the curves. A p-540 value <0.05 is considered statistically significant. From top left to bottom right: 541 ata/ram1-1 vs. wt1, ram1-2 vs. wt2, ram1-3 vs. wt2, mean mutants vs. mean wt, wt1 542 vs wt2. Blue curves represent the wt, red curves represent the mutants. In (E), the blue 543 curve represents wt1, the red curve wt2. 544 545 Table S1. Expression of AM marker genes in the ata/ram1 mutants. 546 Expression of the indicated genes was analyzed in plants inoculated for 1 week with 547 R. irregularis nurse-plant inoculum. Gene expression was analyzed in the wild type 548 and the three petunia ram1 alleles relative to GAPDH expression. Gene expression 549 values represent the mean of three independent biological replicates. Comparison 550 between the mutants and the respective wild type plants revealed to which degree 551 gene expression was reduced due to the respective ram1 mutation (fold less), and p-552 values (t-test) indicate significant differences. 553 554



Parsed CitationsBonfante P, Genre A, Faccio A, Martini I, Schauser L, Stougaard J, Webb J, Parniske M (2000) The Lotus japonicus LjSym4 gene isrequired for the successful symbiotic infection of root epidermal cells. Molecular Plant-Microbe Interactions 13: 1109-1120

Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Breuillin F, Schramm J, Hajirezaei M, Ahkami A, Favre P, Druege U, Hause B, M. B, Kretzschmar T, Bossolini E, Kuhlemeier C,Martinoia E, Franken P, Scholz U, Reinhardt D (2010) Phosphate systemically inhibits development of arbuscular mycorrhiza inPetunia hybrida and represses genes involved in mycorrhizal functioning. Plant Journal 64: 1002-1017


Delaux P-M, Varala K, Edger PP, Coruzzi GM, Pires JC, Ane J-M (2014) Comparative phylogenomics uncovers the impact ofsymbiotic associations on host genome evolution. Plos Genetics 10: e1004487


Demchenko K, Winzer T, Stougaard J, Parniske M, Pawlowski K (2004) Distinct roles of Lotus japonicus SYMRK and SYM15 in rootcolonization and arbuscule formation. New Phytologist 163: 381-392


Douds DD, Pfeffer PE, Shachar-Hill Y (2000) Carbon partitioning, cost, and metabolism of arbuscular mycorrhizas. In Y Kapulnik,DD Douds, eds, Arbuscular Mycorrhizas: Physiology and Function. Kluwer Academic Publishers, Dordrecht


Duc G, Trouvelot A, Gianinazzi-Pearson V, Gianinazzi S (1989) First report of non-mycorrhizal plant mutants (myc-) obtained in pea(Pisum sativum L.) and fababean (Vicia faba L.). Plant Science 60: 215-222


Favre P, Bapaume L, Bossolini E, Delorenzi L, Falquet L, Reinhardt D (2014) A novel bioinformatics pipeline to discover genesrelated to arbuscular mycorrhizal symbiosis based on their evolutionary conservation pattern among higher plants. BMC PlantBiology 14: 333


Feddermann N, Duvvuru Muni RR, Zeier T, Stuurman J, Ercolin F, Schorderet M, Reinhardt D (2010) The PAM1 gene of petunia,required for intracellular accommodation and morphogenesis of arbuscular mycorrhizal fungi, encodes a homologue of VAPYRIN.Plant Journal 64: 470-481


Fiorilli V, Catoni M, Miozzi L, Novero M, Accotto GP, Lanfranco L (2009) Global and cell-type gene expression profiles in tomatoplants colonized by an arbuscular mycorrhizal fungus. New Phytologist 184: 975-987


Gaude N, Bortfeld S, Duensing N, Lohse M, Krajinski F (2012) Arbuscule-containing and non-colonized cortical cells of mycorrhizalroots undergo extensive and specific reprogramming during arbuscular mycorrhizal development. Plant Journal 69: 510-528


George E (2000) Nutrient uptake - Contributions of arbuscular mycorrhizal fungi to plant mineral nutrition. In Y Kapulnik, DDDouds, eds, Arbuscular mycorrhizas: Physiology and function. Kluwer Academic Publishers, Dordrecht, pp 307-343


Gerats AGM, Huits H, Vrijlandt E, Maraña C, Souer E, Beld M (1990) Molecular characterization of a nonautonomous transposableelement (dTph1) of petunia. Plant Cell 2: 1121-1128


Gobbato E, Marsh JF, Vernie T, Wang E, Maillet F, Kim J, Miller JB, Sun J, Bano SA, Ratet P, Mysore KS, Dénarie J, Schultze M,Oldroyd GED (2012) A GRAS-type transcription factor with a specific function in mycorrhizal signaling. Current Biology 22: 2236-https://plantphysiol.orgDownloaded on April 22, 2021. - Published by

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http://search.crossref.org/?page=1&rows=2&q=Demchenko K, Winzer T, Stougaard J, Parniske M, Pawlowski K (2004) Distinct roles of Lotus japonicus SYMRK and SYM15 in root colonization and arbuscule formation. New Phytologist 163: 381-392

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http://search.crossref.org/?page=1&rows=2&q=Douds DD, Pfeffer PE, Shachar-Hill Y (2000) Carbon partitioning, cost, and metabolism of arbuscular mycorrhizas. In Y Kapulnik, DD Douds, eds, Arbuscular Mycorrhizas: Physiology and Function. Kluwer Academic Publishers, Dordrecht

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http://search.crossref.org/?page=1&rows=2&q=Duc G, Trouvelot A, Gianinazzi-Pearson V, Gianinazzi S (1989) First report of non-mycorrhizal plant mutants (myc-) obtained in pea (Pisum sativum L.) and fababean (Vicia faba L.). Plant Science 60: 215-222

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http://search.crossref.org/?page=1&rows=2&q=Gerats AGM, Huits H, Vrijlandt E, Mara�a C, Souer E, Beld M (1990) Molecular characterization of a nonautonomous transposable element (dTph1) of petunia. Plant Cell 2: 1121-1128

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2241Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Gomez SK, Javot H, Deewatthanawong P, Torres-Jerez I, Tang YH, Blancaflor EB, Udvardi MK, Harrison MJ (2009) Medicagotruncatula and Glomus intraradices gene expression in cortical cells harboring arbuscules in the arbuscular mycorrhizalsymbiosis. BMC Plant Biology 9: 10


Guether M, Balestrini R, Hannah M, He J, Udvardi M, Bonfante P (2009) Genome-wide reprogramming of regulatory networks, cellwall and membrane biogenesis during arbuscular-mycorrhizal symbiosis in Lotus japonicus. New Phytologist 182: 200-212


Guether M, Neuhauser B, Balestrini R, Dynowski M, Ludewig U, Bonfante P (2009) A mycorrhizal-specific ammonium transporterfrom Lotus japonicus acquires nitrogen released by arbuscular mycorrhizal fungi. Plant Physiology 150: 73-83


Güimil S, Chang HS, Zhu T, Sesma A, Osbourn A, Roux C, Ionnidis V, Oakeley EJ, Docquier M, Descombes P, Briggs SP,Paszkowski U (2005) Comparative transcriptomics of rice reveals an ancient pattern of response to microbial colonization.Proceedings Of The National Academy Of Sciences Of The United States Of America 102: 8066-8070


Gutjahr C, Parniske M (2013) Cell and developmental biology of arbuscular mycorrhiza symbiosis. Annual Review of Cell andDevelopmental Biology 29: 593-617


Gutjahr C, Radovanovic D, Geoffroy J, Zhang Q, Siegler H, Chiapello M, Casieri L, An K, An G, Guiderdoni E, Kumar CS,Sundaresan V, Harrison MJ, Paszkowski U (2012) The half-size ABC transporters STR1 and STR2 are indispensable formycorrhizal arbuscule formation in rice. Plant Journal 69: 906-920


Harrison MJ (2012) Cellular programs for arbuscular mycorrhizal symbiosis. Current Opinion in Plant Biology 15: 691-698Pubmed: Author and TitleCrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Hogekamp C, Küster H (2013) A roadmap of cell-type specific gene expression during sequential stages of the arbuscularmycorrhiza symbiosis. BMC Genomics 14: 306


Hohnjec N, Vieweg ME, Puhler A, Becker A, Küster H (2005) Overlaps in the transcriptional profiles of Medicago truncatula rootsinoculated with two different Glomus fungi provide insights into the genetic program activated during arbuscular mycorrhiza.Plant Physiology 137: 1283-1301


Javot H, Penmetsa RV, Terzaghi N, Cook DR, Harrison MJ (2007) A Medicago truncatula phosphate transporter indispensable forthe arbuscular mycorrhizal symbiosis. Proceedings of the National Academy of Sciences of the United States of America 104: 1720-1725


Jones KM, Kobayashi H, Davies BW, Taga ME, Walker GC (2007) How rhizobial symbionts invade plants: the Sinorhizobium-Medicago model. Nature Reviews Microbiology 5: 619-633


Kalo P, Gleason C, Edwards A, Marsh J, Mitra RM, Hirsch S, Jakab J, Sims S, Long SR, Rogers J, Kiss GB, Downie JA, OldroydGED (2005) Nodulation signaling in legumes requires NSP2, a member of the GRAS family of transcriptional regulators. Science308: 1786-1789

Pubmed: Author and TitleCrossRef: Author and Title https://plantphysiol.orgDownloaded on April 22, 2021. - Published by


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CrossRef: Author and TitleGoogle Scholar: Author Only Title Only Author and Title

Van den Broeck D, Maes T, Sauer M, Zethof J, De Keukeleire P, D'Hauw M, Van Montagu M, Gerats T (1998) Transposon displayidentifies individual transposable elements in high copy number lines. Plant Journal 13: 121-129


Vandenbussche M, Janssen A, Zethof J, van Orsouw N, Peters J, van Eijk MJT, Rijpkema AS, Schneiders H, Santhanam P, de BeenM, van Tunen A, Gerats T (2008) Generation of a 3D indexed Petunia insertion database for reverse genetics. Plant Journal 54:1105-1114


Vandenbussche M, Zethof J, Gerats A (2013) Transposon display: a versatile method for transposon tagging. Methods in MolecularBiology 1057: 239-250


Veiga RSL, Faccio A, Genre A, Pieterse CMJ, Bonfante P, van der Heijden MGA (2013) Arbuscular mycorrhizal fungi reduce growthand infect roots of the non-host plant Arabidopsis thaliana. Plant Cell and Environment 36: 1926-1937


Wang ET, Schornack S, Marsh JF, Gobbato E, Schwessinger B, Eastmond P, Schultze M, Kamoun S, Oldroyd GED (2012) Acommon signaling process that promotes mycorrhizal and oomycete colonization of plants. Current Biology 22: 2242-2246


Wegmüller S, Svistoonoff S, Reinhardt D, Stuurman J, Amrhein N, Bucher M (2008) A transgenic dTph1 insertional mutagenesissystem for forward genetics in mycorrhizal phosphate transport of Petunia. Plant Journal 54: 1115-1127


Xue L, Cui H, Buer B, Vijayakumar V, Delaux P-M, Junkermann S, Bucher M (2015) Network of GRAS transcription factors involvedin the control of arbuscule development in Lotus japonicus. Plant Physiol 167: 854-871


Yano K, Yoshida S, Muller J, Singh S, Banba M, Vickers K, Markmann K, White C, Schuller B, Sato S, Asamizu E, Tabata S, MurookaY, Perry J, Wang TL, Kawaguchi M, Imaizumi-Anraku H, Hayashi M, Parniske M (2008) CYCLOPS, a mediator of symbioticintracellular accommodation. Proceedings of the National Academy of Sciences of the United States of America 105: 20540-20545


Zhang Q, Blaylock LA, Harrison MJ (2010) Two Medicago truncatula half-ABC transporters are essential for arbuscule developmentin arbuscular mycorrhizal symbiosis. Plant Cell 22: 1483-1497



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http://www.ncbi.nlm.nih.gov/pubmed?term=%28Plant Journal%5BTitle%5D%29 AND 54%5BVolume%5D AND 1105%5BPagination%5D AND Vandenbussche M%2C Janssen A%2C Zethof J%2C van Orsouw N%2C Peters J%2C van Eijk MJT%2C Rijpkema AS%2C Schneiders H%2C Santhanam P%2C de Been M%2C van Tunen A%2C Gerats T%5BAuthor%5D&dopt=abstract

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http://scholar.google.com/scholar?as_q=Two Medicago truncatula half-ABC transporters are essential for arbuscule development in arbuscular mycorrhizal symbiosis&num=10&btnG=Search+Scholar&as_occt=any&as_sauthors=Zhang&as_ylo=2010&as_allsubj=all&hl=en&c2coff=1


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Running head: A central regulator of symbiotic gene ...€¦ · 13/05/2015 · 136 infected from nurse-plants exhibited exaggerated AM fungal colonization in root tips, 137 indicating