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1

Ribeiro, Ana, Inês Graça, Katharina Pawlowski, and Patrícia Santos. "Actinorhizal plant defence-related genes in response to symbiotic Frankia." Functional Plant Biology 38, no. 9 (2011): 639. http://dx.doi.org/10.1071/fp11012.

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Actinorhizal plants have become increasingly important as climate changes threaten to remake the global landscape over the next decades. These plants are able to grow in nutrient-poor and disturbed soils, and are important elements in plant communities worldwide. Besides that, most actinorhizal plants are capable of high rates of nitrogen fixation due to their capacity to establish root nodule symbiosis with N2-fixing Frankia strains. Nodulation is a developmental process that requires a sequence of highly coordinated events. One of these mechanisms is the induction of defence-related events, whose precise role in a symbiotic interaction remains to be elucidated. This review summarises what is known about the induction of actinorhizal defence-related genes in response to symbiotic Frankia and their putative function during symbiosis.
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2

Weidmann, Stéphanie, Lisa Sanchez, Julie Descombin, Odile Chatagnier, Silvio Gianinazzi, and Vivienne Gianinazzi-Pearson. "Fungal Elicitation of Signal Transduction-Related Plant Genes Precedes Mycorrhiza Establishment and Requires the dmi3 Gene in Medicago truncatula." Molecular Plant-Microbe Interactions® 17, no. 12 (December 2004): 1385–93. http://dx.doi.org/10.1094/mpmi.2004.17.12.1385.

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Suppressive subtractive hybridization and expressed sequence tag sequencing identified 29 plant genes which are upregulated during the appressorium stage of mycorrhiza establishment between Medicago truncatula J5 (Myc+) and Glomus mosseae. Eleven genes coding plant proteins with predicted functions in signal transduction, transcription, and translation were investigated in more detail for their relation to early events of symbiotic interactions. Expression profiling showed that the genes are activated not only from the appressorium stage up to the fully established symbiosis in the Myc+ genotype of M. truncatula, but also when the symbionts are not in direct cell contact, suggesting that diffusible fungal molecules (Myc factors) play a role in the induction of a signal-transduction pathway. Transcript accumulation in roots of a mycorrhiza-defective Myc- dmi3 mutant of M. truncatula is not modified by appressorium formation or diffusible fungal molecules, indicating that the signal transduction pathway is required for a successful G. mosseae-M. truncatula interaction leading to symbiosis development. The symbiotic nodulating bacterium Sinorhizobium meliloti does not activate the 11 genes, which supposes early discrimination by plant roots between the microbial symbionts.
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Liu, Zhilei, Yuanjing Li, Lina Ma, Haichao Wei, Jianfeng Zhang, Xingyuan He, and Chunjie Tian. "Coordinated Regulation of Arbuscular Mycorrhizal Fungi and Soybean MAPK Pathway Genes Improved Mycorrhizal Soybean Drought Tolerance." Molecular Plant-Microbe Interactions® 28, no. 4 (April 2015): 408–19. http://dx.doi.org/10.1094/mpmi-09-14-0251-r.

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Mitogen-activated protein kinase (MAPK) cascades play important roles in the stress response in both plants and microorganisms. The mycorrhizal symbiosis established between arbuscular mycorrhizal fungi (AMF) and plants can enhance plant drought tolerance, which might be closely related to the fungal MAPK response and the molecular dialogue between fungal and soybean MAPK cascades. To verify the above hypothesis, germinal Glomus intraradices (syn. Rhizophagus irregularis) spores and potted experiments were conducted. The results showed that AMF GiMAPKs with high homology with MAPKs from Saccharomyces cerevisiae had different gene expression patterns under different conditions (nitrogen starvation, abscisic acid treatment, and drought). Drought stress upregulated the levels of fungi and soybean MAPK transcripts in mycorrhizal soybean roots, indicating the possibility of a molecular dialogue between the two symbiotic sides of symbiosis and suggesting that they might cooperate to regulate the mycorrhizal soybean drought-stress response. Meanwhile, the changes in hydrogen peroxide, soluble sugar, and proline levels in mycorrhizal soybean as well as in the accelerated exchange of carbon and nitrogen in the symbionts were contributable to drought adaptation of the host plants. Thus, it can be preliminarily inferred that the interactions of MAPK signals on both sides, symbiotic fungus and plant, might regulate the response of symbiosis and, thus, improve the resistance of mycorrhizal soybean to drought stress.
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4

Valverde, Angel, Encarna Velázquez, Emilio Cervantes, José M. Igual, and Peter van Berkum. "Evidence of an American Origin for Symbiosis-Related Genes in Rhizobium lusitanum." Applied and Environmental Microbiology 77, no. 16 (June 24, 2011): 5665–70. http://dx.doi.org/10.1128/aem.02017-10.

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ABSTRACTRandomly amplified polymorphic DNA (RAPD) analysis was used to investigate the diversity of 179 bean isolates recovered from six field sites in the Arcos de Valdevez region of northwestern Portugal. The isolates were divided into 6 groups based on the fingerprint patterns that were obtained. Representatives for each group were selected for sequence analysis of 4 chromosomal DNA regions. Five of the groups were placed withinRhizobium lusitanum, and the other group was placed withinR. tropicitype IIA. Therefore, the collection of Portuguese bean isolates was shown to include the two speciesR. lusitanumandR. tropici. In plant tests, the strains P1-7, P1-1, P1-2, and P1-16 ofR. lusitanumnodulated and formed nitrogen-fixing symbioses both withPhaseolus vulgarisandLeucaena leucocephala. A methyltransferase-encodingnodSgene identical with theR. tropicilocus that confers wide host range was detected in the strain P1-7 as well as 24 others identified asR. lusitanum. A methyltransferase-encodingnodSgene also was detected in the remaining isolates ofR. lusitanum, but in this case the locus was that identified with the narrow-host-rangeR. etli. Representatives of isolates with thenodSofR. etliformed effective nitrogen-fixing symbioses withP. vulgarisand did not nodulateL. leucocephala. From sequence data ofnodS, theR. lusitanumgenes for symbiosis were placed within those of eitherR. tropiciorR. etli. These results would support the suggestion thatR. lusitanumwas the recipient of the genes for symbiosis with beans from bothR. tropiciandR. etli.
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Miozzi, Laura, Anna Maria Vaira, Federico Brilli, Valerio Casarin, Mara Berti, Alessandra Ferrandino, Luca Nerva, Gian Paolo Accotto, and Luisa Lanfranco. "Arbuscular Mycorrhizal Symbiosis Primes Tolerance to Cucumber Mosaic Virus in Tomato." Viruses 12, no. 6 (June 22, 2020): 675. http://dx.doi.org/10.3390/v12060675.

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Tomato plants can establish symbiotic interactions with arbuscular mycorrhizal fungi (AMF) able to promote plant nutrition and prime systemic plant defenses against pathogens attack; the mechanism involved is known as mycorrhiza-induced resistance (MIR). However, studies on the effect of AMF on viral infection, still limited and not conclusive, indicate that AMF colonization may have a detrimental effect on plant defenses against viruses, so that the term “mycorrhiza-induced susceptibility” (MIS) has been proposed for these cases. To expand the case studies to a not yet tested viral family, that is, Bromoviridae, we investigated the effect of the colonization by the AMF Funneliformis mosseae on cucumber mosaic virus (CMV) infection in tomato by phenotypic, physiological, biochemical, and transcriptional analyses. Our results showed that the establishment of a functional AM symbiosis is able to limit symptoms development. Physiological and transcriptomic data highlighted that AMF mitigates the drastic downregulation of photosynthesis-related genes and the reduction of photosynthetic CO2 assimilation rate caused by CMV infection. In parallel, an increase of salicylic acid level and a modulation of reactive oxygen species (ROS)-related genes, toward a limitation of ROS accumulation, was specifically observed in CMV-infected mycorrhizal plants. Overall, our data indicate that the AM symbiosis influences the development of CMV infection in tomato plants and exerts a priming effect able to enhance tolerance to viral infection.
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6

Pawlowski, Katharina, Susan Swensen, Changhui Guan, Az-Eddine Hadri, Alison M. Berry, and Ton Bisseling. "Distinct Patterns of Symbiosis-Related Gene Expression in Actinorhizal Nodules from Different Plant Families." Molecular Plant-Microbe Interactions® 16, no. 9 (September 2003): 796–807. http://dx.doi.org/10.1094/mpmi.2003.16.9.796.

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Phylogenetic analyses suggest that, among the members of the Eurosid I clade, nitrogen-fixing root nodule symbioses developed multiple times independently, four times with rhizobia and four times with the genus Frankia. In order to understand the degree of similarity between symbiotic systems of different phylogenetic subgroups, gene expression patterns were analyzed in root nodules of Datisca glomerata and compared with those in nodules of another actinorhizal plant, Alnus glutinosa, and with the expression patterns of homologous genes in legumes. In parallel, the phylogeny of actinorhizal plants was examined more closely. The results suggest that, although relationships between major groups are difficult to resolve using molecular phylogenetic analysis, the comparison of gene expression patterns can be used to inform evolutionary relationships. In this case, stronger similarities were found between legumes and intracellularly infected actinorhizal plants (Alnus) than between actinorhizal plants of two different phylogenetic subgroups (Alnus/Datisca).
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7

Alloisio, Nicole, Clothilde Queiroux, Pascale Fournier, Petar Pujic, Philippe Normand, David Vallenet, Claudine Médigue, Masatoshi Yamaura, Kentaro Kakoi, and Ken-ichi Kucho. "The Frankia alni Symbiotic Transcriptome." Molecular Plant-Microbe Interactions® 23, no. 5 (May 2010): 593–607. http://dx.doi.org/10.1094/mpmi-23-5-0593.

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The actinobacteria Frankia spp. are able to induce the formation of nodules on the roots of a large spectrum of actinorhizal plants, where they convert dinitrogen to ammonia in exchange for plant photosynthates. In the present study, transcriptional analyses were performed on nitrogen-replete free-living Frankia alni cells and on Alnus glutinosa nodule bacteria, using whole-genome microarrays. Distribution of nodule-induced genes on the genome was found to be mostly over regions with high synteny between three Frankia spp. genomes, while nodule-repressed genes, which were mostly hypothetical and not conserved, were spread around the genome. Genes known to be related to nitrogen fixation were highly induced, nif (nitrogenase), hup2 (hydrogenase uptake), suf (sulfur-iron cluster), and shc (hopanoids synthesis). The expression of genes involved in ammonium assimilation and transport was strongly modified, suggesting that bacteria ammonium assimilation was limited. Genes involved in particular in transcriptional regulation, signaling processes, protein drug export, protein secretion, lipopolysaccharide, and peptidoglycan biosynthesis that may play a role in symbiosis were also identified. We also showed that this Frankia symbiotic transcriptome was highly similar among phylogenetically distant plant families Betulaceae and Myricaceae. Finally, comparison with rhizobia transcriptome suggested that F. alni is metabolically more active in symbiosis than rhizobia.
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8

Wang, Yen-Wen, Jaqueline Hess, Jason C. Slot, and Anne Pringle. "De Novo Gene Birth, Horizontal Gene Transfer, and Gene Duplication as Sources of New Gene Families Associated with the Origin of Symbiosis in Amanita." Genome Biology and Evolution 12, no. 11 (September 14, 2020): 2168–82. http://dx.doi.org/10.1093/gbe/evaa193.

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Abstract By introducing novel capacities and functions, new genes and gene families may play a crucial role in ecological transitions. Mechanisms generating new gene families include de novo gene birth, horizontal gene transfer, and neofunctionalization following a duplication event. The ectomycorrhizal (ECM) symbiosis is a ubiquitous mutualism and the association has evolved repeatedly and independently many times among the fungi, but the evolutionary dynamics enabling its emergence remain elusive. We developed a phylogenetic workflow to first understand if gene families unique to ECM Amanita fungi and absent from closely related asymbiotic species are functionally relevant to the symbiosis, and then to systematically infer their origins. We identified 109 gene families unique to ECM Amanita species. Genes belonging to unique gene families are under strong purifying selection and are upregulated during symbiosis, compared with genes of conserved or orphan gene families. The origins of seven of the unique gene families are strongly supported as either de novo gene birth (two gene families), horizontal gene transfer (four), or gene duplication (one). An additional 34 families appear new because of their selective retention within symbiotic species. Among the 109 unique gene families, the most upregulated gene in symbiotic cultures encodes a 1-aminocyclopropane-1-carboxylate deaminase, an enzyme capable of downregulating the synthesis of the plant hormone ethylene, a common negative regulator of plant-microbial mutualisms.
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9

Miura, Chihiro, Katsushi Yamaguchi, Ryohei Miyahara, Tatsuki Yamamoto, Masako Fuji, Takahiro Yagame, Haruko Imaizumi-Anraku, Masahide Yamato, Shuji Shigenobu, and Hironori Kaminaka. "The Mycoheterotrophic Symbiosis Between Orchids and Mycorrhizal Fungi Possesses Major Components Shared with Mutualistic Plant-Mycorrhizal Symbioses." Molecular Plant-Microbe Interactions® 31, no. 10 (October 2018): 1032–47. http://dx.doi.org/10.1094/mpmi-01-18-0029-r.

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Achlorophylous and early developmental stages of chorolophylous orchids are highly dependent on carbon and other nutrients provided by mycorrhizal fungi, in a nutritional mode termed mycoheterotrophy. Previous findings have implied that some common properties at least partially underlie the mycorrhizal symbioses of mycoheterotrophic orchids and that of autotrophic arbuscular mycorrhizal (AM) plants; however, information about the molecular mechanisms of the relationship between orchids and their mycorrhizal fungi is limited. In this study, we characterized the molecular basis of an orchid-mycorrhizal (OM) symbiosis by analyzing the transcriptome of Bletilla striata at an early developmental stage associated with the mycorrhizal fungus Tulasnella sp. The essential components required for the establishment of mutual symbioses with AM fungi or rhizobia in most terrestrial plants were identified from the B. striata gene set. A cross-species gene complementation analysis showed one of the component genes, calcium and calmodulin-dependent protein kinase gene CCaMK in B. striata, retains functional characteristics of that in AM plants. The expression analysis revealed the activation of homologs of AM-related genes during the OM symbiosis. Our results suggest that orchids possess, at least partly, the molecular mechanisms common to AM plants.
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10

Djordjevic, MA, and JJ Weinman. "Factors Determining Host Recognition in the Clover-Rhizobium Symbiosis." Functional Plant Biology 18, no. 5 (1991): 543. http://dx.doi.org/10.1071/pp9910543.

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Rhizobia are microbes that exploit host plants as a nutritional source but cause little or no host damage. They may provide, through biological nitrogen fixation, a valuable source of nitrogen for plant growth. Different rhizobia nodulate a limited range of plants. In this review we will show that host range specificity is determined by the success or otherwise of communication events between the interacting partners. To infect different plant species, a distinct cocktail of phenolic compounds (flavonoids) is recognised. Flavonoids of the correct structure induce the expression of several bacterial nodulation (nod) and other genes required for plant infection. Flavonoids of the incorrect, but related, structure can antagonise nod gene induction. Some nod genes are responsible for the synthesis of a small family of lipo-oligosaccharides necessary for the triggering of a defined but complex series of morphological responses in the host plant including root hair curling and cortical cell division. Lipo-oligosaccharides are active at concentrations of between 10-8 and 10-12 M. The appropriate lipo-oligosaccharide required for infection of one plant host can have antagonistic effects on other non-host plants and this effect appears to be determined by minor chemical changes to the basic lipo-oligosaccharide structure. Apart from host specificity operating at the genus level, other interdependent nod gene functions determine host specificity at the cultivar level. A complex interplay between positively and negatively acting nod genes and a single host gene affects cultivar specificity in a manner analogous to, but more complex than, the gene-for-gene interactions common amongst plant-pathogen interactions.
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11

Paparokidou, Christina, Jonathan R. Leake, David J. Beerling, and Stephen A. Rolfe. "Phosphate availability and ectomycorrhizal symbiosis with Pinus sylvestris have independent effects on the Paxillus involutus transcriptome." Mycorrhiza 31, no. 1 (November 16, 2020): 69–83. http://dx.doi.org/10.1007/s00572-020-01001-6.

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AbstractMany plant species form symbioses with ectomycorrhizal fungi, which help them forage for limiting nutrients in the soil such as inorganic phosphate (Pi). The transcriptional responses to symbiosis and nutrient-limiting conditions in ectomycorrhizal fungal hyphae, however, are largely unknown. An artificial system was developed to study ectomycorrhizal basidiomycete Paxillus involutus growth in symbiosis with its host tree Pinus sylvestris at different Pi concentrations. RNA-seq analysis was performed on P. involutus hyphae growing under Pi-limiting conditions, either in symbiosis or alone. We show that Pi starvation and ectomycorrhizal symbiosis have an independent effect on the P. involutus transcriptome. Notably, low Pi availability induces expression of newly identified putative high-affinity Pi transporter genes, while reducing the expression of putative organic acid transporters. Additionally, low Pi availability induces a close transcriptional interplay between P and N metabolism. GTP-related signalling was found to have a positive effect in the maintenance of ectomycorrhizal symbiosis, whereas multiple putative cytochrome P450 genes were found to be downregulated, unlike arbuscular mycorrhizal fungi. We provide the first evidence of global transcriptional changes induced by low Pi availability and ectomycorrhizal symbiosis in the hyphae of P. involutus, revealing both similarities and differences with better-characterized arbuscular mycorrhizal fungi.
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12

Seddas, Pascale M. A., Cecilia M. Arias, Christine Arnould, Diederik van Tuinen, Olivier Godfroy, Hassan Aït Benhassou, Jérome Gouzy, Dominique Morandi, Fabrice Dessaint, and Vivienne Gianinazzi-Pearson. "Symbiosis-Related Plant Genes Modulate Molecular Responses in an Arbuscular Mycorrhizal Fungus During Early Root Interactions." Molecular Plant-Microbe Interactions® 22, no. 3 (March 2009): 341–51. http://dx.doi.org/10.1094/mpmi-22-3-0341.

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To gain further insight into the role of the plant genome in arbuscular mycorrhiza (AM) establishment, we investigated whether symbiosis-related plant genes affect fungal gene expression in germinating spores and at the appressoria stage of root interactions. Glomus intraradices genes were identified in expressed sequence tag libraries of mycorrhizal Medicago truncatula roots by in silico expression analyses. Transcripts of a subset of genes, with predicted functions in transcription, protein synthesis, primary or secondary metabolism, or of unknown function, were monitored in spores and germinating spores and during interactions with roots of wild-type or mycorrhiza-defective (Myc–) mutants of M. truncatula. Not all the fungal genes were active in quiescent spores but all were expressed when G. intraradices spores germinated in wild-type M. truncatula root exudates or when appressoria or arbuscules were formed in association with wild-type M. truncatula roots. Most of the fungal genes were upregulated or induced at the stage of appressorium development. Inactivation of the M. truncatula genes DMI1, DMI2/MtSYM2, or DMI3/MtSYM13 was associated with altered fungal gene expression (nonactivation or inhibition), modified appressorium structure, and plant cell wall responses, providing first evidence that cell processes modified by symbiosis-related plant genes impact on root interactions by directly modulating AM fungal activity.
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13

Velázquez, Encarna, Alvaro Peix, José Luis Zurdo-Piñiro, José Luis Palomo, Pedro F. Mateos, Raúl Rivas, Estefanía Muñoz-Adelantado, Nicolás Toro, Pablo García-Benavides, and Eustoquio Martínez-Molina. "The Coexistence of Symbiosis and Pathogenicity-Determining Genes in Rhizobium rhizogenes Strains Enables Them to Induce Nodules and Tumors or Hairy Roots in Plants." Molecular Plant-Microbe Interactions® 18, no. 12 (December 2005): 1325–32. http://dx.doi.org/10.1094/mpmi-18-1325.

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Bacteria belonging to the family Rhizobiaceae may establish beneficial or harmful relationships with plants. The legume endosymbionts contain nod and nif genes responsible for nodule formation and nitrogen fixation, respectively, whereas the pathogenic strains carry vir genes responsible for the formation of tumors or hairy roots. The symbiotic and pathogenic strains currently belong to different species of the genus Rhizobium and, until now, no strains able to establish symbiosis with legumes and also to induce tumors or hairy roots in plants have been reported. Here, we report for the first time the occurrence of two rhizobial strains (163C and ATCC11325T) belonging to Rhizobium rhizogenes able to induce hairy roots or tumors in plants and also to nodulate Phaseolus vulgaris under natural environmental conditions. Symbiotic plasmids (pSym) containing nod and nif genes and pTi- or pRi-type plasmids containing vir genes were found in these strains. The nodD and nifH genes of the strains from this study are phylogenetically related to those of Sinorhizobium strains nodulating P. vulgaris. The virA and virB4 genes from strain 163C are phylogenetically related to those of R. tumefaciens C58, whereas the same genes from strain ATCC 11325T are related to those of hairy root-inducing strains. These findings may be of high relevance for the better understanding of plant-microbe interactions and knowledge of rhizobial phylogenetic history.
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14

Karlo, Magda, Clarissa Boschiero, Katrine Gram Landerslev, Gonzalo Sancho Blanco, Jiangqi Wen, Kirankumar S. Mysore, Xinbin Dai, Patrick X. Zhao, and Thomas C. de Bang. "The CLE53–SUNN genetic pathway negatively regulates arbuscular mycorrhiza root colonization in Medicago truncatula." Journal of Experimental Botany 71, no. 16 (April 20, 2020): 4972–84. http://dx.doi.org/10.1093/jxb/eraa193.

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Abstract Plants and arbuscular mycorrhizal fungi (AMF) engage in mutually beneficial symbioses based on a reciprocal exchange of nutrients. The beneficial character of the symbiosis is maintained through a mechanism called autoregulation of mycorrhization (AOM). AOM includes root-to-shoot-to-root signaling; however, the molecular details of AOM are poorly understood. AOM shares many features of autoregulation of nodulation (AON) where several genes are known, including the receptor-like kinase SUPER NUMERIC NODULES (SUNN), root-to-shoot mobile CLAVATA3/ENDOSPERM SURROUNDING REGION (ESR)-RELATED (CLE) peptides, and the hydroxyproline O-arabinosyltransferase ROOT DETERMINED NODULATION1 (RDN1) required for post-translational peptide modification. In this work, CLE53 was identified to negatively regulate AMF symbiosis in a SUNN- and RDN1-dependent manner. CLE53 expression was repressed at low phosphorus, while it was induced by AMF colonization and high phosphorus. CLE53 overexpression reduced AMF colonization in a SUNN- and RDN1 dependent manner, while cle53, rdn1, and sunn mutants were more colonized than the wild type. RNA-sequencing identified 700 genes with SUNN-dependent regulation in AMF-colonized plants, providing a resource for future identification of additional AOM genes. Disruption of AOM genes in crops potentially constitutes a novel route for improving AMF-derived phosphorus uptake in agricultural systems with high phosphorus levels.
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Bazin, Jérémie, Pilar Bustos-Sanmamed, Caroline Hartmann, Christine Lelandais-Brière, and Martin Crespi. "Complexity of miRNA-dependent regulation in root symbiosis." Philosophical Transactions of the Royal Society B: Biological Sciences 367, no. 1595 (June 5, 2012): 1570–79. http://dx.doi.org/10.1098/rstb.2011.0228.

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The development of root systems may be strongly affected by the symbiotic interactions that plants establish with soil organisms. Legumes are able to develop symbiotic relationships with both rhizobial bacteria and arbuscular mycorrhizal fungi leading to the formation of nitrogen-fixing nodules and mycorrhizal arbuscules, respectively. Both of these symbiotic interactions involve complex cellular reprogramming and profound morphological and physiological changes in specific root cells. In addition, the repression of pathogenic defence responses seems to be required for successful symbiotic interactions. Apart from typical regulatory genes, such as transcription factors, microRNAs (miRNAs) are emerging as riboregulators that control gene networks in eukaryotic cells through interactions with specific target mRNAs. In recent years, the availability of deep-sequencing technologies and the development of in silico approaches have allowed for the identification of large sets of miRNAs and their targets in legumes . A number of conserved and legume-specific miRNAs were found to be associated with symbiotic interactions as shown by their expression patterns or actions on symbiosis-related targets. In this review, we combine data from recent literature and genomic and deep-sequencing data on miRNAs controlling nodule development or restricting defence reactions to address the diversity and specificity of miRNA-dependent regulation in legume root symbiosis. Phylogenetic analysis of miRNA isoforms and their potential targets suggests a role for miRNAs in the repression of plant defence during symbiosis and revealed the evolution of miRNA-dependent regulation in legumes to allow for the modification of root cell specification, such as the formation of mycorrhized roots and nitrogen-fixing nodules.
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Wang, Chun-Mei, Martin Ekman, and Birgitta Bergman. "Expression of Cyanobacterial Genes Involved in Heterocyst Differentiation and Dinitrogen Fixation Along a Plant Symbiosis Development Profile." Molecular Plant-Microbe Interactions® 17, no. 4 (April 2004): 436–43. http://dx.doi.org/10.1094/mpmi.2004.17.4.436.

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Members of the cyanobiont genus Nostoc, forming an endosymbiosis with members of the angiosperm genus Gunnera, undergo a number of characteristic phenotypic changes during the development of the symbiosis, the genetic background of which is largely unknown. Transcription patterns of genes related to heterocyst differentiation and dinitrogen fixation and corresponding protein profiles were examined, using reverse transcription-polymerase chain reaction and Western blots, along a developmental (apex to mature parts) sequence in Gunnera magellanica and G. manicata and under mimicked symbiotic conditions in a free-living Gunnera isolate (Nostoc strain 0102). The hetR gene was highly expressed and correlated positively with an increase in heterocyst frequency and with ntcA expression, whereas nifH expression was already high close to the growing apex and glnB (PII) expression decreased along the symbiotic profile. Although gene expression appeared to be regulated to a large extent in the same fashion as in free-living cyanobacteria, significant differences were apparent, such as the overexpression of both hetR and ntcA and the contrasting down-regulation of glnB, features indicating important regulatory differences between symbiotic and free-living cyanobacteria. The significance of these findings is discussed in a symbiotic context.
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17

Bárzana, Gloria, Ricardo Aroca, Gerd Patrick Bienert, François Chaumont, and Juan Manuel Ruiz-Lozano. "New Insights into the Regulation of Aquaporins by the Arbuscular Mycorrhizal Symbiosis in Maize Plants Under Drought Stress and Possible Implications for Plant Performance." Molecular Plant-Microbe Interactions® 27, no. 4 (April 2014): 349–63. http://dx.doi.org/10.1094/mpmi-09-13-0268-r.

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The relationship between modulation by arbuscular mycorrhizae (AM) of aquaporin expression in the host plant and changes in root hydraulic conductance, plant water status, and performance under stressful conditions is not well known. This investigation aimed to elucidate how the AM symbiosis modulates the expression of the whole set of aquaporin genes in maize plants under different growing and drought stress conditions, as well as to characterize some of these aquaporins in order to shed further light on the molecules that may be involved in the mycorrhizal responses to drought. The AM symbiosis regulated a wide number of aquaporins in the host plant, comprising members of the different aquaporin subfamilies. The regulation of these genes depends on the watering conditions and the severity of the drought stress imposed. Some of these aquaporins can transport water and also other molecules which are of physiological importance for plant performance. AM plants grew and developed better than non-AM plants under the different conditions assayed. Thus, for the first time, this study relates the well-known better performance of AM plants under drought stress to not only the water movement in their tissues but also the mobilization of N compounds, glycerol, signaling molecules, or metalloids with a role in abiotic stress tolerance. Future studies should elucidate the specific function of each aquaporin isoform regulated by the AM symbiosis in order to shed further light on how the symbiosis alters the plant fitness under stressful conditions.
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18

Pawlowski, Katharina, Didier Bogusz, Ana Ribeiro, and Alison M. Berry. "Progress on research on actinorhizal plants." Functional Plant Biology 38, no. 9 (2011): 633. http://dx.doi.org/10.1071/fp11066.

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In recent years, our understanding of the plant side of actinorhizal symbioses has evolved rapidly. No homologues of the common nod genes from rhizobia were found in the three Frankia genomes published so far, which suggested that Nod factor-like molecules would not be used in the infection of actinorhizal plants by Frankia. However, work on chimeric transgenic plants indicated that Frankia Nod factor equivalents signal via the same transduction pathway as rhizobial Nod factors. The role of auxin in actinorhizal nodule formation differs from that in legume nodulation. Great progress has been made in the analysis of pathogenesis-related and stress-related gene expression in nodules. Research on nodule physiology has shown the structural and metabolic diversity of actinorhizal nodules from different phylogenetic branches. The onset of large-scale nodule transcriptome analysis in different actinorhizal systems will provide access to more information on the symbiosis and its evolution.
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19

Humann, Jodi L., Hope T. Ziemkiewicz, Svetlana N. Yurgel, and Michael L. Kahn. "Regulatory and DNA Repair Genes Contribute to the Desiccation Resistance of Sinorhizobium meliloti Rm1021." Applied and Environmental Microbiology 75, no. 2 (November 21, 2008): 446–53. http://dx.doi.org/10.1128/aem.02207-08.

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ABSTRACT Sinorhizobium meliloti can form a nitrogen-fixing symbiotic relationship with alfalfa after bacteria in the soil infect emerging root hairs of the growing plant. To be successful at this, the bacteria must be able to survive in the soil between periods of active plant growth, including when conditions are dry. The ability of S. meliloti to withstand desiccation has been known for years, but genes that contribute to this phenotype have not been identified. Transposon mutagenesis was used in combination with novel screening techniques to identify four desiccation-sensitive mutants of S. meliloti Rm1021. DNA sequencing of the transposon insertion sites identified three genes with regulatory functions (relA, rpoE2, and hpr) and a DNA repair gene (uvrC). Various phenotypes of the mutants were determined, including their behavior on several indicator media and in symbiosis. All of the mutants formed an effective symbiosis with alfalfa. To test the hypothesis that UvrC-related excision repair was important in desiccation resistance, uvrA, uvrB, and uvrC deletion mutants were also constructed. These strains were sensitive to DNA damage induced by UV light and 4-NQO and were also desiccation sensitive. These data indicate that uvr gene-mediated DNA repair and the regulation of stress-induced pathways are important for desiccation resistance.
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Debellé, F., L. Moulin, B. Mangin, J. Dénarié, and C. Boivin. "Nod genes and Nod signals and the evolution of the Rhizobium legume symbiosis." Acta Biochimica Polonica 48, no. 2 (June 30, 2001): 359–65. http://dx.doi.org/10.18388/abp.2001_3921.

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The establishment of the nitrogen-fixing symbiosis between rhizobia and legumes requires an exchange of signals between the two partners. In response to flavonoids excreted by the host plant, rhizobia synthesize Nod factors (NFs) which elicit, at very low concentrations and in a specific manner, various symbiotic responses on the roots of the legume hosts. NFs from several rhizobial species have been characterized. They all are lipo-chitooligosaccharides, consisting of a backbone of generally four or five glucosamine residues N-acylated at the non-reducing end, and carrying various O-substituents. The N-acyl chain and the other substituents are important determinants of the rhizobial host specificity. A number of nodulation genes which specify the synthesis of NFs have been identified. All rhizobia, in spite of their diversity, possess conserved nodABC genes responsible for the synthesis of the N-acylated oligosaccharide core of NFs, which suggests that these genes are of a monophyletic origin. Other genes, the host specific nod genes, specify the substitutions of NFs. The central role of NFs and nod genes in the Rhizobium-legume symbiosis suggests that these factors could be used as molecular markers to study the evolution of this symbiosis. We have studied a number of NFs which are N-acylated by alpha,beta-unsaturated fatty acids. We found that the ability to synthesize such NFs does not correlate with taxonomic position of the rhizobia. However, all rhizobia that produce NFs such nodulate plants belonging to related tribes of legumes, the Trifolieae, Vicieae, and Galegeae, all of them being members of the so-called galegoid group. This suggests that the ability to recognize the NFs with alpha-beta-unsaturated fatty acids is limited to this group of legumes, and thus might have appeared only once in the course of legume evolution, in the galegoid phylum.
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Rivas, Raul, Encarna Velázquez, Anne Willems, Nieves Vizcaíno, Nanjappa S. Subba-Rao, Pedro F. Mateos, Monique Gillis, Frank B. Dazzo, and Eustoquio Martínez-Molina. "A New Species of Devosia That Forms a Unique Nitrogen-Fixing Root-Nodule Symbiosis with the Aquatic Legume Neptunia natans (L.f.) Druce." Applied and Environmental Microbiology 68, no. 11 (November 2002): 5217–22. http://dx.doi.org/10.1128/aem.68.11.5217-5222.2002.

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ABSTRACT Rhizobia are the common bacterial symbionts that form nitrogen-fixing root nodules in legumes. However, recently other bacteria have been shown to nodulate and fix nitrogen symbiotically with these plants. Neptunia natans is an aquatic legume indigenous to tropical and subtropical regions and in African soils is nodulated by Allorhizobium undicola. This legume develops an unusual root-nodule symbiosis on floating stems in aquatic environments through a unique infection process. Here, we analyzed the low-molecular-weight RNA and 16S ribosomal DNA (rDNA) sequence of the same fast-growing isolates from India that were previously used to define the developmental morphology of the unique infection process in this symbiosis with N. natans and found that they are phylogenetically located in the genus Devosia, not Allorhizobium or Rhizobium. The 16S rDNA sequences of these two Neptunia-nodulating Devosia strains differ from the only species currently described in that genus, Devosia riboflavina. From the same isolated colonies, we also located their nodD and nifH genes involved in nodulation and nitrogen fixation on a plasmid of approximately 170 kb. Sequence analysis showed that their nodD and nifH genes are most closely related to nodD and nifH of Rhizobium tropici, suggesting that this newly described Neptunia-nodulating Devosia species may have acquired these symbiotic genes by horizontal transfer.
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Liu, Yuan Hui, Yin Shan Jiao, Li Xue Liu, Dan Wang, Chang Fu Tian, En Tao Wang, Lei Wang, et al. "Nonspecific Symbiosis Between Sophora flavescens and Different Rhizobia." Molecular Plant-Microbe Interactions® 31, no. 2 (February 2018): 224–32. http://dx.doi.org/10.1094/mpmi-05-17-0117-r.

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We explored the genetic basis of the promiscuous symbiosis of Sophora flavescens with diverse rhizobia. To determine the impact of Nod factors (NFs) on the symbiosis of S. flavescens, nodulation-related gene mutants of representative rhizobial strains were generated. Strains with mutations in common nodulation genes (nodC, nodM, and nodE) failed to nodulate S. flavescens, indicating that the promiscuous nodulation of this plant is strictly dependent on the basic NF structure. Mutations of the NF decoration genes nodH, nodS, nodZ, and noeI did not affect the nodulation of S. flavescens, but these mutations affected the nitrogen-fixation efficiency of nodules. Wild-type Bradyrhizobium diazoefficiens USDA110 cannot nodulate S. flavescens, but we obtained 14 Tn5 mutants of B. diazoefficiens that nodulated S. flavescens. This suggested that the mutations had disrupted a negative regulator that prevents nodulation of S. flavescens, leading to nonspecific nodulation. For Ensifer fredii CCBAU 45436 mutants, the minimal NF structure was sufficient for nodulation of soybean and S. flavescens. In summary, the mechanism of promiscuous symbiosis of S. flavescens with rhizobia might be related to its nonspecific recognition of NF structures, and the host specificity of rhizobia may also be controlled by currently unknown nodulation-related genes.
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23

Lebedeva, Maria, Mahboobeh Azarakhsh, Yaroslavna Yashenkova, and Lyudmila Lutova. "Nitrate-Induced CLE Peptide Systemically Inhibits Nodulation in Medicago truncatula." Plants 9, no. 11 (October 28, 2020): 1456. http://dx.doi.org/10.3390/plants9111456.

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Legume plants form nitrogen-fixing nodules in symbiosis with soil bacteria rhizobia. The number of symbiotic nodules is controlled at the whole-plant level with autoregulation of nodulation (AON), which includes a shoot-acting CLV1-like receptor kinase and mobile CLE (CLAVATA3/ENDOSPERM SURROUNDING REGION-related) peptides that are produced in the root in response to rhizobia inoculation. In addition to rhizobia-induced CLE peptides, nitrate-induced CLE genes have been identified in Lotus japonicus and Glycine max, which inhibited nodulation when overexpressed. However, nitrate-induced CLE genes that systemically suppress nodulation in AON-dependent manner have not been identified in Medicago truncatula. Here, we found that MtCLE35 expression is activated by both rhizobia inoculation and nitrate treatment in M. truncatula, similarly to L. japonicus CLE genes. Moreover, we found that MtCLE35 systemically suppresses nodulation in AON-dependent manner, suggesting that MtCLE35 may mediate nitrate-induced inhibition of nodulation in M. truncatula.
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24

Deschamps, Philippe. "Primary endosymbiosis: have cyanobacteria and Chlamydiae ever been roommates?" Acta Societatis Botanicorum Poloniae 83, no. 4 (2014): 291–302. http://dx.doi.org/10.5586/asbp.2014.048.

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Eukaryotes acquired the ability to process photosynthesis by engulfing a cyanobacterium and transforming it into a genuine organelle called the plastid. This event, named primary endosymbiosis, occurred once more than a billion years ago, and allowed the emergence of the Archaeplastida, a monophyletic supergroup comprising the green algae and plants, the red algae and the glaucophytes. Of the other known cases of symbiosis between cyanobacteria and eukaryotes, none has achieved a comparable level of cell integration nor reached the same evolutionary and ecological success than primary endosymbiosis did. Reasons for this unique accomplishment are still unknown and difficult to comprehend. The exploration of plant genomes has revealed a considerable amount of genes closely related to homologs of Chlamydiae bacteria, and probably acquired by horizontal gene transfer. Several studies have proposed that these transferred genes, which are mostly involved in the functioning of the plastid, may have helped the settlement of primary endosymbiosis. Some of these studies propose that Chlamydiae and cyanobacterial symbionts coexisted in the eukaryotic host of the primary endosymbiosis, and that Chlamydiae provided solutions for the metabolic symbiosis between the cyanobacterium and the host, ensuring the success of primary endosymbiosis. In this review, I present a reevaluation of the contribution of Chlamydiae genes to the genome of Archaeplastida and discuss the strengths and weaknesses of this tripartite model for primary endosymbiosis.
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25

Mateus, Ivan D., Edward C. Rojas, Romain Savary, Cindy Dupuis, Frédéric G. Masclaux, Consolée Aletti, and Ian R. Sanders. "Coexistence of genetically different Rhizophagus irregularis isolates induces genes involved in a putative fungal mating response." ISME Journal 14, no. 10 (June 8, 2020): 2381–94. http://dx.doi.org/10.1038/s41396-020-0694-3.

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Abstract Arbuscular mycorrhizal fungi (AMF) are of great ecological importance because of their effects on plant growth. Closely related genotypes of the same AMF species coexist in plant roots. However, almost nothing is known about the molecular interactions occurring during such coexistence. We compared in planta AMF gene transcription in single and coinoculation treatments with two genetically different isolates of Rhizophagus irregularis in symbiosis independently on three genetically different cassava genotypes. Remarkably few genes were specifically upregulated when the two fungi coexisted. Strikingly, almost all of the genes with an identifiable putative function were known to be involved in mating in other fungal species. Several genes were consistent across host plant genotypes but more upregulated genes involved in putative mating were observed in host genotype (COL2215) compared with the two other host genotypes. The AMF genes that we observed to be specifically upregulated during coexistence were either involved in the mating pheromone response, in meiosis, sexual sporulation or were homologs of MAT-locus genes known in other fungal species. We did not observe the upregulation of the expected homeodomain genes contained in a putative AMF MAT-locus, but observed upregulation of HMG-box genes similar to those known to be involved in mating in Mucoromycotina species. Finally, we demonstrated that coexistence between the two fungal genotypes in the coinoculation treatments explained the number of putative mating response genes activated in the different plant host genotypes. This study demonstrates experimentally the activation of genes involved in a putative mating response and represents an important step towards the understanding of coexistence and sexual reproduction in these important plant symbionts.
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Fukudome, Mitsutaka, Eri Watanabe, Ken-ichi Osuki, Nahoko Uchi, and Toshiki Uchiumi. "Ectopic or Over-Expression of Class 1 Phytoglobin Genes Confers Flooding Tolerance to the Root Nodules of Lotus japonicus by Scavenging Nitric Oxide." Antioxidants 8, no. 7 (July 4, 2019): 206. http://dx.doi.org/10.3390/antiox8070206.

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Flooding limits biomass production in agriculture. Leguminous plants, important agricultural crops, use atmospheric dinitrogen gas as nitrogen nutrition by symbiotic nitrogen fixation with rhizobia, but this root-nodule symbiosis is sometimes broken down by flooding of the root system. In this study, we analyzed the effect of flooding on the symbiotic system of transgenic Lotus japonicus lines which overexpressed class 1 phytoglobin (Glb1) of L. japonicus (LjGlb1-1) or ectopically expressed that of Alnus firma (AfGlb1). In the roots of wild-type plants, flooding increased nitric oxide (NO) level and expression of senescence-related genes and decreased nitrogenase activity; in the roots of transgenic lines, these effects were absent or less pronounced. The decrease of chlorophyll content in leaves and the increase of reactive oxygen species (ROS) in roots and leaves caused by flooding were also suppressed in these lines. These results suggest that increased levels of Glb1 help maintain nodule symbiosis under flooding by scavenging NO and controlling ROS.
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27

Frenzel, André, Katja Manthey, Andreas M. Perlick, Folker Meyer, Alfred Pühler, Helge Küster, and Franziska Krajinski. "Combined Transcriptome Profiling Reveals a Novel Family of Arbuscular Mycorrhizal-Specific Medicago truncatula Lectin Genes." Molecular Plant-Microbe Interactions® 18, no. 8 (August 2005): 771–82. http://dx.doi.org/10.1094/mpmi-18-0771.

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The large majority of plants are capable of undergoing a tight symbiosis with arbuscular mycorrhizal (AM) fungi. During this symbiosis, highly specialized new structures called arbuscules are formed within the host cells, indicating that, during interaction with AM fungi, plants express AM-specific genetic programs. Despite increasing efforts, the number of genes known to be induced in the AM symbiosis is still low. In order to identify novel AM-induced genes which have not been listed before, 5,646 expressed sequence tags (ESTs) were generated from two Medicago truncatula cDNA libraries: a random cDNA library (MtAmp) and a suppression subtractive hybridization (SSH) library (MtGim), the latter being designed to enhance the cloning of mycorrhiza-upregulated genes. In silico expression analysis was applied to identify those tentative consensus sequences (TCs) of The Institute for Genomic Research M. truncatula gene index (MtGI) that are composed exclusively of ESTs deriving from the MtGim or MtAmp library, but not from any other cDNA library of the MtGI. This search revealed 115 MtAmp- or MTGim-specific TCs. For the majority of these TCs with sequence similarities to plant genes, the AM-specific expression was verified by quantitative reverse-transcription polymerase chain reaction. Annotation of the novel genes induced in mycorrhizal roots suggested their involvement in different transport as well as signaling processes and revealed a novel family of AM-specific lectin genes. The expression of reporter gene fusions in transgenic roots revealed an arbuscule-related expression of two members of the lectin gene family, indicating a role for AM-specific lectins during arbuscule formation or functioning.
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28

Shigenobu, Shuji, and David L. Stern. "Aphids evolved novel secreted proteins for symbiosis with bacterial endosymbiont." Proceedings of the Royal Society B: Biological Sciences 280, no. 1750 (January 7, 2013): 20121952. http://dx.doi.org/10.1098/rspb.2012.1952.

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Aphids evolved novel cells, called bacteriocytes, that differentiate specifically to harbour the obligatory mutualistic endosymbiotic bacteria Buchnera aphidicola . The genome of the host aphid Acyrthosiphon pisum contains many orphan genes that display no similarity with genes found in other sequenced organisms, prompting us to hypothesize that some of these orphan genes are related to lineage-specific traits, such as symbiosis. We conducted deep sequencing of bacteriocytes mRNA followed by whole mount in situ hybridizations of over-represented transcripts encoding aphid-specific orphan proteins. We identified a novel class of genes that encode small proteins with signal peptides, which are often cysteine-rich, that are over-represented in bacteriocytes. These genes are first expressed at a developmental time point coincident with the incorporation of symbionts strictly in the cells that contribute to the bacteriocyte and this bacteriocyte-specific expression is maintained throughout the aphid's life. The expression pattern suggests that recently evolved secretion proteins act within bacteriocytes, perhaps to mediate the symbiosis with beneficial bacterial partners, which is reminiscent of the evolution of novel cysteine-rich secreted proteins of leguminous plants that regulate nitrogen-fixing endosymbionts.
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29

Ruiz-Lozano, Juan M., Hélène Roussel, Silvio Gianinazzi, and Vivienne Gianinazzi-Pearson. "Defense Genes Are Differentially Induced by a Mycorrhizal Fungus and Rhizobium sp. in Wild-Type and Symbiosis-Defective Pea Genotypes." Molecular Plant-Microbe Interactions® 12, no. 11 (November 1999): 976–84. http://dx.doi.org/10.1094/mpmi.1999.12.11.976.

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Mycorrhiza-resistant and non-nodulating pea mutants provide a model system for identifying common genes regulated during the early events in mycorrhiza and nodule establishment. Inoculation of pea roots with Glomus mosseae or Rhizobium leguminosarum can induce overex-pression of seven defense-related genes (pI 206, pI 49, pI 176, PR 10, basic A1-chitinase, transcinnamic acid 4-hydroxylase, chalcone isomerase), depending on the plant genotype and the time point of interaction between the plant and the microsymbiont. Expression of the pI 206 gene is closely correlated with appressorium formation by the mycorrhizal fungus on both mutant and wild-type pea roots. The gene is also induced by the pathogen Aphanomyces euteiches. Transcript accumulation was higher in mutant than in wild-type genotypes for five and six of the studied genes during early stages of root interactions with G. mosseae and R. leguminosarum, respectively, and this is discussed in relation to the symbiotic-defective phenotype of Myc-1Nod¯ pea. The early induction of similar plant defense genes in response to arbuscular mycorrhizal fungi and rhizobia reinforces the hypothesis of common regulatory steps in both root symbioses.
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Campos, Catarina, Tânia Nobre, Michael J. Goss, Jorge Faria, Pedro Barrulas, and Mário Carvalho. "Transcriptome Analysis of Wheat Roots Reveals a Differential Regulation of Stress Responses Related to Arbuscular Mycorrhizal Fungi and Soil Disturbance." Biology 8, no. 4 (December 11, 2019): 93. http://dx.doi.org/10.3390/biology8040093.

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Symbioses with soil microorganisms are central in shaping the diversity and productivity of land plants and provide protection against a diversity of stresses, including metal toxicity. Arbuscular mycorrhizal fungi (AMF) can form extensive extraradical mycelial networks (ERM), which are very efficient in colonizing a new host. We quantified the responses of transcriptomes of wheat and one AMF partner, Rhizoglomus irregulare, to soil disturbance (Undisturbed vs. Disturbed) and to two different preceding mycotrophic species (Ornithopus compressus and Lolium rigidum). Soil disturbance and preceding plant species engender different AMF communities in wheat roots, resulting in a differential tolerance to soil manganese (Mn) toxicity. Soil disturbance negatively impacted wheat growth under manganese toxicity, probably due to the disruption of the ERM, and activated a large number of stress and starvation-related genes. The O. compressus treatment, which induces a greater Mn protection in wheat than L. rigidum, activated processes related to cellular division and growth, and very few related to stress. The L. rigidum treatment mostly induced genes that were related to oxidative stress, disease protection, and metal ion binding. R. irregulare cell division and molecular exchange between nucleus and cytoplasm were increased by O. compressus. These findings are highly relevant for sustainable agricultural systems, when considering a fit-for-purpose symbiosis.
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31

Zhang, N., M. Raftery, Richardson Christensen, and J. Schmid. "Neotyphodium lolii induces a limited host defence response by Lolium perenne." NZGA: Research and Practice Series 13 (January 1, 2007): 199–202. http://dx.doi.org/10.33584/rps.13.2006.3050.

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We have identified three proteins specifically expressed during the interaction between N. lolii and L. perenne in natural compatible associations. Two are pathogenesis-related PR-10 proteins, part of a ubiquitous plant response to pathogens. We have identified seven different L. perenne PR-10 genes and found that endophyte infection increases PR-10 transcript levels, but only mildly. Furthermore, PR-10 mRNA levels also increase in a dysfunctional symbiosis, but the two identified PR-10 proteins are absent. This suggests that part of the regulation of protein expression is at the level of translation and that PR-10 proteins could be required for the symbiosis to be functional. A third symbiosis-specific protein is a very highly expressed N. lolii superoxide dismutase. Such enzymes neutralise superoxide formed by plants as a defence mechanism. Our results suggest that N. lolii elicits a limited host defence, comparable to that elicited by arbuscular mycorrhiza. Keywords: Neotyphodium lolii, Lolium perenne, host response, proteomics, gene expresion, pathogenesis related protein PR-10, fungal superoxide dismutase
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32

Sundaram, S., S. J. Kim, H. Suzuki, C. J. Mcquattie, S. T. Hiremath, and G. K. Podila. "Isolation and Characterization of a Symbiosis-Regulated ras from the Ectomycorrhizal Fungus Laccaria bicolor." Molecular Plant-Microbe Interactions® 14, no. 5 (May 2001): 618–28. http://dx.doi.org/10.1094/mpmi.2001.14.5.618.

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Ectomycorrhizae formed by the symbiotic interaction between ectomycorrhizal fungi and plant roots play a key role in maintaining and improving the health of a wide range of plants. Mycorrhizal initiation, development, and functional maintenance involve morphological changes that are mediated by activation and suppression of several fungal and plant genes. We identified a gene, Lbras, in the ectomycorrhizal fungus Laccaria bicolor that belongs to the ras family of genes, which has been shown in other systems to be associated with signaling pathways controlling cell growth and proliferation. The Lbras cDNA complemented ras2 function in Saccharomyces cerevisiae and had the ability to transform mammalian cells. Expression of Lbras, present as a single copy in the genome, was dependent upon interaction with host roots. Northern analysis showed that expression was detectable in L. bicolor 48 h after interaction as well as in the established mycorrhizal tissue. Phylogenetic analysis with other Ras proteins showed that Lbras is related most closely to Aras of Aspergillus nidulans.
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33

Safronova, Vera I., Polina V. Guro, Anna L. Sazanova, Irina G. Kuznetsova, Andrey A. Belimov, Valentin V. Yakubov, Elizaveta R. Chirak, et al. "Rhizobial Microsymbionts of Kamchatka Oxytropis Species Possess Genes of the Type III and VI Secretion Systems, Which Can Affect the Development of Symbiosis." Molecular Plant-Microbe Interactions® 33, no. 10 (October 2020): 1232–41. http://dx.doi.org/10.1094/mpmi-05-20-0114-r.

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A collection of rhizobial strains isolated from root nodules of the narrowly endemic legume species Oxytropis erecta, O. anadyrensis, O. kamtschatica, and O. pumilio originating from the Kamchatka Peninsula (Russian Federation) was obtained. Analysis of the 16S ribosomal RNA gene sequence showed a significant diversity of isolates belonging to families Rhizobiaceae (genus Rhizobium), Phyllobacteriaceae (genera Mesorhizobium, Phyllobacterium), and Bradyrhizobiaceae (genera Bosea, Tardiphaga). A plant nodulation assay showed that only strains belonging to genus Mesorhizobium could form nitrogen-fixing nodules on Oxytropis plants. The strains M. loti 582 and M. huakuii 583, in addition to symbiotic clusters, possessed genes of the type III and type VI secretion systems (T3SS and T6SS, respectively), which can influence the host specificity of strains. These strains formed nodules of two types (elongated and rounded) on O. kamtschatica roots. We suggest this phenomenon may result from Nod factor–dependent and –independent nodulation strategies. The obtained strains are of interest for further study of the T3SS and T6SS gene function and their role in the development of rhizobium-legume symbiosis. The prospects of using rhizobia having both gene systems related to symbiotic and nonsymbiotic nodulation strategies to enhance the efficiency of plant-microbe interactions by expanding the host specificity and increasing nodulation efficiency are discussed.
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Yang, Ling-Ling, Zhao Jiang, Yan Li, En-Tao Wang, and Xiao-Yang Zhi. "Plasmids Related to the Symbiotic Nitrogen Fixation Are Not Only Cooperated Functionally but Also May Have Evolved over a Time Span in Family Rhizobiaceae." Genome Biology and Evolution 12, no. 11 (July 20, 2020): 2002–14. http://dx.doi.org/10.1093/gbe/evaa152.

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Abstract Rhizobia are soil bacteria capable of forming symbiotic nitrogen-fixing nodules associated with leguminous plants. In fast-growing legume-nodulating rhizobia, such as the species in the family Rhizobiaceae, the symbiotic plasmid is the main genetic basis for nitrogen-fixing symbiosis, and is susceptible to horizontal gene transfer. To further understand the symbioses evolution in Rhizobiaceae, we analyzed the pan-genome of this family based on 92 genomes of type/reference strains and reconstructed its phylogeny using a phylogenomics approach. Intriguingly, although the genetic expansion that occurred in chromosomal regions was the main reason for the high proportion of low-frequency flexible gene families in the pan-genome, gene gain events associated with accessory plasmids introduced more genes into the genomes of nitrogen-fixing species. For symbiotic plasmids, although horizontal gene transfer frequently occurred, transfer may be impeded by, such as, the host’s physical isolation and soil conditions, even among phylogenetically close species. During coevolution with leguminous hosts, the plasmid system, including accessory and symbiotic plasmids, may have evolved over a time span, and provided rhizobial species with the ability to adapt to various environmental conditions and helped them achieve nitrogen fixation. These findings provide new insights into the phylogeny of Rhizobiaceae and advance our understanding of the evolution of symbiotic nitrogen fixation.
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Zou, Hang, Ni-Na Zhang, Qing Pan, Jian-Hua Zhang, Juan Chen, and Ge-Hong Wei. "Hydrogen Sulfide Promotes Nodulation and Nitrogen Fixation in Soybean–Rhizobia Symbiotic System." Molecular Plant-Microbe Interactions® 32, no. 8 (August 2019): 972–85. http://dx.doi.org/10.1094/mpmi-01-19-0003-r.

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The rhizobium–legume symbiotic system is crucial for nitrogen cycle balance in agriculture. Hydrogen sulfide (H2S), a gaseous signaling molecule, may regulate various physiological processes in plants. However, whether H2S has regulatory effect in this symbiotic system remains unknown. Herein, we investigated the possible role of H2S in the symbiosis between soybean (Glycine max) and rhizobium (Sinorhizobium fredii). Our results demonstrated that an exogenous H2S donor (sodium hydrosulfide [NaHS]) treatment promoted soybean growth, nodulation, and nitrogenase (Nase) activity. Western blotting analysis revealed that the abundance of Nase component nifH was increased by NaHS treatment in nodules. Quantitative real-time polymerase chain reaction data showed that NaHS treatment upregulated the expressions of symbiosis-related genes nodA, nodC, and nodD of S. fredii. In addition, expression of soybean nodulation marker genes, including early nodulin 40 (GmENOD40), ERF required for nodulation (GmERN), nodulation signaling pathway 2b (GmNSP2b), and nodulation inception genes (GmNIN1a, GmNIN2a, and GmNIN2b), were upregulated. Moreover, the expressions of glutamate synthase (GmGOGAT), asparagine synthase (GmAS), nitrite reductase (GmNiR), ammonia transporter (GmSAT1), leghemoglobin (GmLb), and nifH involved in nitrogen metabolism were upregulated in NaHS-treated soybean roots and nodules. Together, our results suggested that H2S may act as a positive signaling molecule in the soybean–rhizobia symbiotic system and enhance the system’s nitrogen fixation ability.
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Branscheid, Anja, Daniela Sieh, Bikram Datt Pant, Patrick May, Emanuel A. Devers, Anders Elkrog, Leif Schauser, Wolf-Rüdiger Scheible, and Franziska Krajinski. "Expression Pattern Suggests a Role of MiR399 in the Regulation of the Cellular Response to Local Pi Increase During Arbuscular Mycorrhizal Symbiosis." Molecular Plant-Microbe Interactions® 23, no. 7 (July 2010): 915–26. http://dx.doi.org/10.1094/mpmi-23-7-0915.

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Many plants improve their phosphate (Pi) availability by forming mutualistic associations with arbuscular mycorrhizal (AM) fungi. Pi-repleted plants are much less colonized by AM fungi than Pi-depleted plants. This indicates a link between plant Pi signaling and AM development. MicroRNAs (miR) of the 399 family are systemic Pi-starvation signals important for maintenance of Pi homeostasis in Arabidopsis thaliana and might also qualify as signals regulating AM development in response to Pi availability. MiR399 could either represent the systemic low-Pi signal promoting or required for AM formation or they could act as counter players of systemic Pi-availability signals that suppress AM symbiosis. To test either of these assumptions, we analyzed the miR399 family in the AM-capable plant model Medicago truncatula and could experimentally confirm 10 novel MIR399 genes in this species. Pi-depleted plants showed increased expression of mature miR399 and multiple pri-miR399, and unexpectedly, levels of five of the 15 pri-miR399 species were higher in leaves of mycorrhizal plants than in leaves of nonmycorrhizal plants. Compared with nonmycorrhizal Pi-depleted roots, mycorrhizal roots of Pi-depleted M. truncatula and tobacco plants had increased Pi contents due to symbiotic Pi uptake but displayed higher mature miR399 levels. Expression levels of MtPho2 remained low and PHO2-dependent Pi-stress marker transcript levels remained high in these mycorrhizal roots. Hence, an AM symbiosis-related signal appears to increase miR399 expression and decrease PHO2 activity. MiR399 overexpression in tobacco suggested that miR399 alone is not sufficient to improve mycorrhizal colonization supporting the assumption that, in mycorrhizal roots, increased miR399 are necessary to keep the MtPho2 expression and activity low, which would otherwise increase in response to symbiotic Pi uptake.
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37

Vald�s-L�pez, Oswaldo, Dhileepkumar Jayaraman, Junko Maeda, Pierre-Marc Delaux, Muthusubramanian Venkateshwaran, Mariel C. Isidra-Arellano, Mar�a del Roc�o Reyero-Saavedra, et al. "A Novel Positive Regulator of the Early Stages of Root Nodule Symbiosis Identified by Phosphoproteomics." Plant and Cell Physiology 60, no. 3 (November 23, 2018): 575–86. http://dx.doi.org/10.1093/pcp/pcy228.

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Abstract Signals and signaling pathways underlying the symbiosis between legumes and rhizobia have been studied extensively over the past decades. In a previous phosphoproteomic study on the Medicago truncatula–Sinorhizobium meliloti symbiosis, we identified plant proteins that are differentially phosphorylated upon the perception of rhizobial signals, called Nod factors. In this study, we provide experimental evidence that one of these proteins, Early Phosphorylated Protein 1 (EPP1), is required for the initiation of this symbiosis. Upon inoculation with rhizobia, MtEPP1 expression was induced in curled root hairs. Down-regulation of MtEPP1 in M. truncatula roots almost abolished calcium spiking, reduced the expression of essential symbiosis-related genes (MtNIN, MtNF-YB1, MtERN1 and MtENOD40) and strongly decreased nodule development. Phylogenetic analyses revealed that orthologs of MtEPP1 are present in legumes and specifically in plant species able to host arbuscular mycorrhizal fungi, suggesting a possible role in this association too. Short chitin oligomers induced the phosphorylation of MtEPP1 like Nod factors. However, the down-regulation of MtEPP1 affected the colonization of M. truncatula roots by arbuscular mycorrhizal fungi only moderately. Altogether, these findings indicate that MtEPP1 is essential for the establishment of the legume–rhizobia symbiosis but might plays a limited role in the arbuscular mycorrhizal symbiosis.
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38

Muñoz, Jose A., Carmen Coronado, Javier Pérez-Hormaeche, Adam Kondorosi, Pascal Ratet, and Antonio J. Palomares. "MsPG3, aMedicago sativapolygalacturonase gene expressed during the alfalfa–Rhizobium melilotiinteraction." Proceedings of the National Academy of Sciences 95, no. 16 (August 4, 1998): 9687–92. http://dx.doi.org/10.1073/pnas.95.16.9687.

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Polygalacturonase (PG) is one of the most important enzymes associated with plant cell wall degradation. It has been proposed to participate in the early steps of theRhizobium–legume interaction. We have identified two classes of cDNA fragments corresponding to two classes of PG genes in theMedicagogenome. One of this class, represented by E2inM. truncatulaand Pl1inM. sativa, seems to be related to previously characterized plant PG genes expressed in pollen. We have isolated the genomic clone containing the entire gene corresponding to the second class (E3). We showed thatMsPG3is a single gene in theMedicagogenome coding for PG. By reverse transcription-PCR,MsPG3expression was detected in roots 1 day afterRhizobiuminoculation. The early induction of theMsPG3, as also seen byin situhybridization experiments, supports its involvement in the early stages of theRhizobium-legume infection process. In addition, by analyzing the expression of aMsPG3promoter-gusconstruct inVicia hirsuta-transgenic root nodules, we showed thatMsPG3was expressed in all cells of nodule primordia and in the cells of the invasion zone. By Northern blot,MsPG3transcripts are not detected in variousMedicagotissues, indicating that the function of this gene is related closely to symbiosis. Thus, our results strongly suggest the involvement ofMsPG3gene during meristem formation and/or in the infection process, probably by facilitating cell wall rearrangement, penetration of the bacteria through the root hair wall, or infection thread formation and release of bacteria in plant cells.MsPG3represents a class of PG genes, distinct from the pollen-specific genes, and it is the first pectic encoded enzyme demonstrated to be involved inRhizobium-legume symbiosis.
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39

van Velzen, Robin, Rens Holmer, Fengjiao Bu, Luuk Rutten, Arjan van Zeijl, Wei Liu, Luca Santuari, et al. "Comparative genomics of the nonlegume Parasponia reveals insights into evolution of nitrogen-fixing rhizobium symbioses." Proceedings of the National Academy of Sciences 115, no. 20 (May 1, 2018): E4700—E4709. http://dx.doi.org/10.1073/pnas.1721395115.

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Nodules harboring nitrogen-fixing rhizobia are a well-known trait of legumes, but nodules also occur in other plant lineages, with rhizobia or the actinomycete Frankia as microsymbiont. It is generally assumed that nodulation evolved independently multiple times. However, molecular-genetic support for this hypothesis is lacking, as the genetic changes underlying nodule evolution remain elusive. We conducted genetic and comparative genomics studies by using Parasponia species (Cannabaceae), the only nonlegumes that can establish nitrogen-fixing nodules with rhizobium. Intergeneric crosses between Parasponia andersonii and its nonnodulating relative Trema tomentosa demonstrated that nodule organogenesis, but not intracellular infection, is a dominant genetic trait. Comparative transcriptomics of P. andersonii and the legume Medicago truncatula revealed utilization of at least 290 orthologous symbiosis genes in nodules. Among these are key genes that, in legumes, are essential for nodulation, including NODULE INCEPTION (NIN) and RHIZOBIUM-DIRECTED POLAR GROWTH (RPG). Comparative analysis of genomes from three Parasponia species and related nonnodulating plant species show evidence of parallel loss in nonnodulating species of putative orthologs of NIN, RPG, and NOD FACTOR PERCEPTION. Parallel loss of these symbiosis genes indicates that these nonnodulating lineages lost the potential to nodulate. Taken together, our results challenge the view that nodulation evolved in parallel and raises the possibility that nodulation originated ∼100 Mya in a common ancestor of all nodulating plant species, but was subsequently lost in many descendant lineages. This will have profound implications for translational approaches aimed at engineering nitrogen-fixing nodules in crop plants.
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40

Acosta-Jurado, Sebastián, Cynthia Alias-Villegas, Pilar Navarro-Gómez, Susanne Zehner, Piedad del Socorro Murdoch, Miguel A. Rodríguez-Carvajal, María J. Soto, et al. "The Sinorhizobium fredii HH103 MucR1 Global Regulator Is Connected With the nod Regulon and Is Required for Efficient Symbiosis With Lotus burttii and Glycine max cv. Williams." Molecular Plant-Microbe Interactions® 29, no. 9 (September 2016): 700–712. http://dx.doi.org/10.1094/mpmi-06-16-0116-r.

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Sinorhizobium fredii HH103 is a rhizobial strain showing a broad host range of nodulation. In addition to the induction of bacterial nodulation genes, transition from a free-living to a symbiotic state requires complex genetic expression changes with the participation of global regulators. We have analyzed the role of the zinc-finger transcriptional regulator MucR1 from S. fredii HH103 under both free-living conditions and symbiosis with two HH103 host plants, Glycine max and Lotus burttii. Inactivation of HH103 mucR1 led to a severe decrease in exopolysaccharide (EPS) biosynthesis but enhanced production of external cyclic glucans (CG). This mutant also showed increased cell aggregation capacity as well as a drastic reduction in nitrogen-fixation capacity with G. max and L. burttii. However, in these two legumes, the number of nodules induced by the mucR1 mutant was significantly increased and decreased, respectively, with respect to the wild-type strain, indicating that MucR1 can differently affect nodulation depending on the host plant. RNA-Seq analysis carried out in the absence and the presence of flavonoids showed that MucR1 controls the expression of hundreds of genes (including some related to EPS production and CG transport), some of them being related to the nod regulon.
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41

Nelson, Matthew S., Chan Lan Chun, and Michael J. Sadowsky. "Type IV Effector Proteins Involved in the Medicago-Sinorhizobium Symbiosis." Molecular Plant-Microbe Interactions® 30, no. 1 (January 2017): 28–34. http://dx.doi.org/10.1094/mpmi-10-16-0211-r.

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In this study, we investigated genetic elements of the type IV secretion system (T4SS) found in Sinorhizobium spp. and the role they play in symbiosis. Sinorhizobium meliloti and S. medicae each contain a putative T4SS similar to that used by Agrobacterium tumefaciens during pathogenesis. The Cre reporter assay for translocation system was used to validate potential effector proteins. Both S. meliloti and S. medicae contained the effector protein TfeA, which was translocated into the host plant. Sequence analysis revealed the presence of a nod box involved in transcriptional activation of symbiosis-related genes, upstream of the transcriptional regulator (virG) in the Sinorhizobium T4SS. Replicate quantitative reverse transcription-polymerase chain reaction analyses indicated that luteolin, released by roots and seeds of Medicago truncatula, upregulated transcription of tfeA and virG. Mutations in the T4SS apparatus or tfeA alone resulted in reduced numbers of nodules formed on M. truncatula genotypes. In addition, S. meliloti KH46c, which contains a deletion in the T4SS, was less competitive for nodule formation when coinoculated with an equal number of cells of the wild-type strain. To our knowledge, TfeA is the first T4SS effector protein identified in Sinorhizobium spp. Our results indicate that Sinorhizobium i) uses a T4SS during initiation of symbiosis with Medicago spp., and ii) alters Medicago cells in planta during symbiosis. This study also offers additional bioinformatic evidence that several different rhizobial species may use the T4SS in symbiosis with other legumes.
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42

Takeda, Naoya, Kristina Haage, Shusei Sato, Satoshi Tabata, and Martin Parniske. "Activation of a Lotus japonicus Subtilase Gene During Arbuscular Mycorrhiza Is Dependent on the Common Symbiosis Genes and Two cis-Active Promoter Regions." Molecular Plant-Microbe Interactions® 24, no. 6 (June 2011): 662–70. http://dx.doi.org/10.1094/mpmi-09-10-0220.

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The subtilisin-like serine protease SbtM1 is strongly and specifically induced during arbuscular mycorrhiza (AM) symbiosis in Lotus japonicus. Another subtilase gene, SbtS, is induced during early stages of nodulation and AM. Transcript profiling in plant symbiosis mutants revealed that the AM-induced expression of SbtM1 and the gene family members SbtM3 and SbtM4 is dependent on the common symbiosis pathway, whereas an independent pathway contributes to the activation of SbtS. We used the specific spatial expression patterns of SbtM1 promoter β-d-glucuronidase (GUS) fusions to isolate cis elements that confer AM responsiveness. A promoter deletion and substitution analysis defined two cis regions (region I and II) in the SbtM1 promoter necessary for AM-induced GUS activity. 35S minimal promoter fusions revealed that either of the two regions is sufficient for AM responsiveness when tested in tandem repeat arrangement. Sequence-related regions were found in the promoters of AM-induced subtilase genes in Medicago truncatula and rice, consistent with an ancient origin of these elements predating the divergence of the angiosperms.
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43

Kuznetsova, Elena, Pascale M. A. Seddas-Dozolme, Christine Arnould, Marie Tollot, Diederik van Tuinen, Alexey Borisov, Silvio Gianinazzi, and Vivienne Gianinazzi-Pearson. "Symbiosis-related pea genes modulate fungal and plant gene expression during the arbuscule stage of mycorrhiza with Glomus intraradices." Mycorrhiza 20, no. 6 (January 22, 2010): 427–43. http://dx.doi.org/10.1007/s00572-009-0292-8.

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44

Gamas, Pascal, Françoise de Billy, and Georges Truchet. "Symbiosis-Specific Expression of Two Medicago truncatula Nodulin Genes, MtN1 and MtN13, Encoding Products Homologous to Plant Defense Proteins." Molecular Plant-Microbe Interactions® 11, no. 5 (May 1998): 393–403. http://dx.doi.org/10.1094/mpmi.1998.11.5.393.

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Two Medicago truncatula nodulin genes putatively encoding proteins structurally related to two classes of proteins commonly associated with plant defense reactions have been characterized. MtN1 is homologous to two small, cysteine-rich, pathogen-inducible proteins from pea (pI39 and pI230), whereas MtN13 is closely related to the PR10 family of pathogenesis-related proteins. We show that neither MtN1 nor MtN13 is induced in leaves in response to pathogenic bacteria, and that both are exclusively expressed during nodulation. In situ hybridization experiments as well as Northern (RNA) studies of interactions between M. truncatula and either wild-type Rhizobium meliloti or mutants deficient in infection establish that MtN1 is associated with the infection process, while MtN13 represents the first specific marker described for the nodule outer cortex. Possible roles for MtN1 and MtN13 are discussed. We also present the identification of another member of the PR10 family, designated as MtPR10-1, whose regulation is strikingly different from that observed for MtN13, being constitutively expressed in roots and pathogen-inducible in leaves.
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45

Garrido, José Manuel García, Rafael Jorge León Morcillo, José Ángel Martín Rodríguez, and Juan Antonio Ocampo Bote. "Variations in the Mycorrhization Characteristics in Roots of Wild-Type and ABA-Deficient Tomato Are Accompanied by Specific Transcriptomic Alterations." Molecular Plant-Microbe Interactions® 23, no. 5 (May 2010): 651–64. http://dx.doi.org/10.1094/mpmi-23-5-0651.

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Abscissic acid (ABA) determines mycorrhiza functionality and arbuscule development. In this study, we performed transcriptome analysis in response to different mycorrhization status according to the ABA content in the root to identify genes that may play a role in arbuscule functionality. Affymetrix Tomato GeneChip (approximately 10,000 probes) allowed us to detect and compare the transcriptional root profiling of tomato (Solanum lycopersicum) wild-type and ABA-deficient sitiens plants colonized by Glomus intraradices. A number of identified genes in tomato belong to a category of genes already described as “mycorrhizal core-set” in other host plants. The impairment in arbuscular mycorrhiza (AM) formation in ABA-deficient mutants was associated with upregulation of genes related to defense and cell wall modification, whereas functional mycorrhization in wild-type plants was associated with activation of genes related to isoprenoid metabolism. The oxylipin pathway was activated in tomato mycorrhizal roots at late stages of interaction, and was related to the control of fungal spread in roots, not with the establishment of the symbiosis. Induction of selected genes, representing a range of biological functions and representative of the three sets of genes specifically upregulated in the different plant phenotype, was confirmed by quantitative reverse-transcription polymerase chain reaction, and their response to phythohormone treatment was tested, showing that ethylene and jasmonic acid are key regulators of gene expression during AM development. Comparative analysis of mycorrhiza upregulated functional categories revealed significant changes in gene expression associated with the different mycorrhization status according to the ABA content in the roots.
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46

Medeiros, Camila de, Gilberto Aguiar Pereira, Janyeli Dorini Silva de Freitas, Olavo Bilac Quaresma de Oliveira Filho, Juliana Silveira do Valle, Giani Andrea Linde, Luzia Doretto Paccola-Meirelles, Nelson Barros Colauto, and Fernando Gomes Barcellos. "Gene characterization of Bradyrhizobium spp. strains contrasting in biological nitrogen fixation efficiency in soybean." Semina: Ciências Agrárias 41, no. 6supl2 (November 6, 2020): 3067–80. http://dx.doi.org/10.5433/1679-0359.2020v41n6supl2p3067.

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Bacteria from genus Bradyrhizobium can establish symbiosis with soybean and supply the plant nitrogen demands via biological nitrogen fixation (BNF). This study aimed to characterize genes related to BNF efficiency in B. japonicum strains contrasting in BNF efficiency. These gene sequences were previously identified in B. japonicum (strain S370) as probably related to the BNF efficiency in soybean using a DNA subtractive technique. These genes were amplified with primers based on B. japonicum USDA110 genome. The PCR products were digested with restriction endonucleases and the RFLP products were analyzed by horizontal electrophoresis. Among the four genes, only blr3208 and blr4511 amplified for most of the strains. Neither polymorphism of the restriction profile of blr3208 and blr4511 genes nor with endonuclease for PCR-RFLP was observed. The contrasting strains had blr3208 and blr4511 genes sequenced and the multiple alignment analysis of nucleotide sequences showed the presence of preserved internal regions, confirming the analysis with PCR-RFLP. The blr3208 and blr4511 genes are highly conserved among B. japonicum strains, which may be related to adaptive function during the evolutionary process of Bradyrhizobium genus.
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47

Brito, Belén, Annita Toffanin, Rosa-Isabel Prieto, Juan Imperial, Tomás Ruiz-Argüeso, and Jose M. Palacios. "Host-Dependent Expression of Rhizobium leguminosarum bv. viciae Hydrogenase Is Controlled at Transcriptional and Post-Transcriptional Levels in Legume Nodules." Molecular Plant-Microbe Interactions® 21, no. 5 (May 2008): 597–604. http://dx.doi.org/10.1094/mpmi-21-5-0597.

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The legume host affects the expression of Rhizobium leguminosarum hydrogenase activity in root nodules. High levels of symbiotic hydrogenase activity were detected in R. leguminosarum bacteroids from different hosts, with the exception of lentil (Lens culinaris). Transcription analysis showed that the NifA-regulated R. leguminosarum hydrogenase structural gene promoter (P1) is poorly induced in lentil root nodules. Replacement of the P1 promoter by the FnrN-dependent promoter of the fixN gene restored transcription of hup genes in lentil bacteroids, but not hydrogenase activity. In the PfixN-hupSL strain, additional copies of the hup gene cluster and nickel supplementation to lentil plants increased bacteroid hydrogenase activity. However, the level of activity in lentil still was significantly lower than in pea bacteroids, indicating that an additional factor is impairing hydrogenase expression inside lentil nodules. Immunological analysis revealed that lentil bacteroids contain reduced levels of both hydrogenase structural subunit HupL and nickel-binding protein HypB. Altogether, results indicate that hydrogenase expression is affected by the legume host at the level of both transcription of hydrogenase structural genes and biosynthesis or stability of nickel-related proteins HypB and HupL, and suggest the existence of a plant-dependent mechanism that affects hydrogenase activity during the symbiosis by limiting nickel availability to the bacteroid.
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48

Menna, Pâmela, and Mariangela Hungria. "Phylogeny of nodulation and nitrogen-fixation genes in Bradyrhizobium: supporting evidence for the theory of monophyletic origin, and spread and maintenance by both horizontal and vertical transfer." International Journal of Systematic and Evolutionary Microbiology 61, no. 12 (December 1, 2011): 3052–67. http://dx.doi.org/10.1099/ijs.0.028803-0.

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Bacteria belonging to the genus Bradyrhizobium are capable of establishing symbiotic relationships with a broad range of plants belonging to the three subfamilies of the family Leguminosae ( = Fabaceae), with the formation of specialized structures on the roots called nodules, where fixation of atmospheric nitrogen takes place. Symbiosis is under the control of finely tuned expression of common and host-specific nodulation genes and also of genes related to the assembly and activity of the nitrogenase, which, in Bradyrhizobium strains investigated so far, are clustered in a symbiotic island. Information about the diversity of these genes is essential to improve our current poor understanding of their origin, spread and maintenance and, in this study, we provide information on 40 Bradyrhizobium strains, mostly of tropical origin. For the nodulation trait, common (nodA), Bradyrhizobium-specific (nodY/K) and host-specific (nodZ) nodulation genes were studied, whereas for fixation ability, the diversity of nifH was investigated. In general, clustering of strains in all nod and nifH trees was similar and the Bradyrhizobium group could be clearly separated from other rhizobial genera. However, the congruence of nod and nif genes with ribosomal and housekeeping genes was low. nodA and nodY/K were not detected in three strains by amplification or hybridization with probes using Bradyrhizobium japonicum and Bradyrhizobium elkanii type strains, indicating the high diversity of these genes or that strains other than photosynthetic Bradyrhizobium must have alternative mechanisms to initiate the process of nodulation. For a large group of strains, the high diversity of nod genes (with an emphasis on nodZ), the low relationship between nod genes and the host legume, and some evidence of horizontal gene transfer might indicate strategies to increase host range. On the other hand, in a group of five symbionts of Acacia mearnsii, the high congruence between nod and ribosomal/housekeeping genes, in addition to shorter nodY/K sequences and the absence of nodZ, highlights a co-evolution process. Additionally, in a group of B. japonicum strains that were symbionts of soybean, vertical transfer seemed to represent the main genetic event. In conclusion, clustering of nodA and nifH gives additional support to the theory of monophyletic origin of the symbiotic genes in Bradyrhizobium and, in addition to the analysis of nodY/K and nodZ, indicates spread and maintenance of nod and nif genes through both vertical and horizontal transmission, apparently with the dominance of one or other of these events in some groups of strains.
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49

Petersen, G., H. Darby, V. K. Y. Lam, H. Æ. Pedersen, V. S. F. T. Merckx, A. Zervas, O. Seberg, and S. W. Graham. "Mycoheterotrophic Epirixanthes (Polygalaceae) has a typical angiosperm mitogenome but unorthodox plastid genomes." Annals of Botany 124, no. 5 (July 26, 2019): 791–807. http://dx.doi.org/10.1093/aob/mcz114.

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Abstract Background and Aims Fully mycoheterotrophic plants derive carbon and other nutrients from root-associated fungi and have lost the ability to photosynthesize. While mycoheterotroph plastomes are often degraded compared with green plants, the effect of this unusual symbiosis on mitochondrial genome evolution is unknown. By providing the first complete organelle genome data from Polygalaceae, one of only three eudicot families that developed mycoheterotrophy, we explore how both organellar genomes evolved after loss of photosynthesis. Methods We sequenced and assembled four complete plastid genomes and a mitochondrial genome from species of Polygalaceae, focusing on non-photosynthetic Epirixanthes. We compared these genomes with those of other mycoheterotroph and parasitic plant lineages, and assessed whether organelle genes in Epirixanthes experienced relaxed or intensified selection compared with autotrophic relatives. Key Results Plastomes of two species of Epirixanthes have become substantially degraded compared with that of autotrophic Polygala. Although the lack of photosynthesis is presumably homologous in the genus, the surveyed Epirixanthes species have marked differences in terms of plastome size, structural rearrangements, gene content and substitution rates. Remarkably, both apparently replaced a canonical plastid inverted repeat with large directly repeated sequences. The mitogenome of E. elongata incorporated a considerable number of fossilized plastid genes, by intracellular transfer from an ancestor with a less degraded plastome. Both plastid and mitochondrial genes in E. elongata have increased substitution rates, but the plastid genes of E. pallida do not. Despite this, both species have similar selection patterns operating on plastid housekeeping genes. Conclusions Plastome evolution largely fits with patterns of gene degradation seen in other heterotrophic plants, but includes highly unusual directly duplicated regions. The causes of rate elevation in the sequenced Epirixanthes mitogenome and of rate differences in plastomes of related mycoheterotrophic species are not currently understood.
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50

Nogales, Joaquina, Rosario Campos, Hanaa BenAbdelkhalek, José Olivares, Carmen Lluch, and Juan Sanjuan. "Rhizobium tropici Genes Involved in Free-Living Salt Tolerance are Required for the Establishment of Efficient Nitrogen-Fixing Symbiosis with Phaseolus vulgaris." Molecular Plant-Microbe Interactions® 15, no. 3 (March 2002): 225–32. http://dx.doi.org/10.1094/mpmi.2002.15.3.225.

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Characterization of nine transposon-induced mutants of Rhizobium tropici with decreased salt tolerance (DST) allowed the identification of eight gene loci required for adaptation to high external NaCl. Most of the genes also were involved in adaptation to hyperosmotic media and were required to overcome the toxicity of LiCl. According to their possible functions, genes identified could be classified into three groups. The first group included two genes involved in regulation of gene expression, such as ntrY, the sensor element of the bacterial ntrY/ntrX two-component regulatory system involved in regulation of nitrogen metabolism, and greA, which encodes a transcription elongation factor. The second group included genes related to synthesis, assembly, or maturation of proteins, such as alaS coding for alanine-tRNA synthetase, dnaJ, which encodes a molecular chaperone, and a nifS homolog probably encoding a cysteine desulfurase involved in the maturation of Fe-S proteins. Genes related with cellular build-up and maintenance were in the third group, such as a noeJ-homolog, encoding a mannose-1-phosphate guanylyltransferase likely involved in lipopolysaccharide biosynthesis, and kup, specifying an inner-membrane protein involved in potassium uptake. Another gene was identified that had no homology to known genes but that could be conserved in other rhizobia. When inoculated on Phaseolus vulgaris growing under nonsaline conditions, all DST mutants displayed severe symbiotic defects: ntrY and noeJ mutants were impaired in nodulation, and the remaining mutants formed symbiosis with very reduced nitrogenase activity. The results suggest that bacterial ability to adapt to hyper-osmotic and salt stress is important for the bacteroid nitrogen-fixing function inside the legume nodule and provide genetic evidence supporting the suggestion that rhizobia face severe environmental changes after their release into plant cells.
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