Role of the Nod Factor Hydrolase MtNFH1 in Regulating Nod Factor Levels during Rhizobial Infection and in Mature Nodules of <i>Medicago truncatula</i>

Cai, Jie; Zhang, Lan-Yue; Liu, Wei; Tian, Yongsheng; Xiong, Jinsong; Wang, Yihan; Li, Ru-Jie; Li, Haoming; Wen, Jiangqi; Mysore, Kirankumar S.; Boller, Thomas; Xie, Zhiping; Staehelin, Christian

doi:10.1105/tpc.17.00420

Cited by 42 publications

(43 citation statements)

References 88 publications

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“…TtsI is the transcriptional activator of T3SS genes and effector genes, including nopP, and can be transcriptionally induced by the NodD1-flavonoid complex (38,39), which can also activate the transcription of nod genes involved in the biosynthesis of Nod factors (NFs). Although rhizobial NFs are the key symbiotic signal initiating both infection and nodule organogenesis (40), it was recently demonstrated that excess amounts of NFs negatively regulate the initiation of infection threads in M. truncatula, and NF hydrolase MtNFH1 is involved (41). The abnormal branching of indeterminate nodules, as seen on MtNFH1-deficient M. truncatula plants, was also observed on C. cajan roots inoculated with mutants lacking znu genes of CCBAU45436 in this study.…”

Section: Discussionsupporting

confidence: 58%

Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery

Zhang

Jiao

et al. 2020

mBio

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Pathogenic bacteria need high-affinity zinc uptake systems to counteract the nutritional immunity exerted by infected hosts. However, our understanding of zinc homeostasis in mutualistic systems such as the rhizobium-legume symbiosis is limited. Here, we show that the conserved high-affinity zinc transporter ZnuABC and accessory transporter proteins (Zip1, Zip2, and c06450) made cumulative contributions to nodulation of the broad-host-range strain Sinorhizobium fredii CCBAU45436. Zur acted as a zinc-dependent repressor for the znuC-znuB-zur operon, znuA, and c06450 by binding to the associated Zur box, but did not regulate zip1 and zip2. ZnuABC was the major zinc transporter. Combined mutants lacking znuA and one of the three accessory genes had more severe defects in nodulation and growth under zinc starvation conditions than the znuA mutant, though rhizoplane colonization by these mutants was not impaired. In contrast to the elite strain CCBAU45436, more drastic symbiotic defects were observed for the znuA mutants of other Sinorhizobium strains, which lack at least one of the three accessory genes in their genomes and are characterized by their limited host range and geographical distribution. The znu-derived mutants showed a higher expression level of nod genes involved in Nod factor biosynthesis and a reduced expression of genes encoding a type three secretion system and its effector NopP, which can interfere with the host immune system. Application of exogenous zinc restored the nodulation ability of these znu-derived mutants. Therefore, the conserved ZnuABC and accessory components in the zinc starvation machinery play an important role in modulating symbiotic compatibility. IMPORTANCE The rhizobium-legume symbiosis contributes around 65% of biological nitrogen fixation in agriculture systems and is critical for sustainable agriculture by reducing the amount of chemical nitrogen fertilizer being used. Rhizobial inocula have been commercialized for more than 100 years, but the efficiency of inoculation can vary among legume cultivars, field sites, and years. These long-lasting challenging problems impede the establishment of a sustainable agriculture, particularly in developing countries. Here, we report that rhizobial zinc starvation machinery containing a conserved high-affinity zinc transporter and accessory components makes cumulative contributions to modulating rhizobial symbiotic compatibility. This work highlights a critical role of largely unexplored nutritional immunity in the rhizobium-legume symbiosis, which makes zinc starvation machinery an attractive target for improving rhizobial symbiotic compatibility.

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Section: Discussionsupporting

confidence: 58%

Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery

Zhang

Jiao

et al. 2020

mBio

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“…Downstream of the Nod factor signaling pathway, paralogous Nod factor hydrolases MtNFH1 (NOD FACTOR HYDROLASE1) and LjCHIT5 (CHITINASE5) cleave the lipochitooligosaccharidic backbone of Nod factors produced by their respective symbionts ( Figure 3). This degradation of Nod factors appears to be crucial for rhizobial infection, colonization, and nodule formation (Cai et al, 2018;Malolepszy et al, 2018). Interestingly, delays in nodule formation by aberrant Nod factor-producing strains were abolished in Ljchit5 mutants, implicating Nod factor hydrolysis in partner recognition (Malolepszy et al, 2018).…”

Section: Nod Factor Signaling and The Common Symbiotic Pathwaymentioning

confidence: 99%

Celebrating 20 Years of Genetic Discoveries in Legume Nodulation and Symbiotic Nitrogen Fixation

Roy¹,

Liu²,

Nandety³

et al. 2019

Plant Cell

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512

484

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Since 1999, various forward-and reverse-genetic approaches have uncovered nearly 200 genes required for symbiotic nitrogen fixation (SNF) in legumes. These discoveries advanced our understanding of the evolution of SNF in plants and its relationship to other beneficial endosymbioses, signaling between plants and microbes, the control of microbial infection of plant cells, the control of plant cell division leading to nodule development, autoregulation of nodulation, intracellular accommodation of bacteria, nodule oxygen homeostasis, the control of bacteroid differentiation, metabolism and transport supporting symbiosis, and the control of nodule senescence. This review catalogs and contextualizes all of the plant genes currently known to be required for SNF in two model legume species, Medicago truncatula and Lotus japonicus, and two crop species, Glycine max (soybean) and Phaseolus vulgaris (common bean). We also briefly consider the future of SNF genetics in the era of pan-genomics and genome editing.

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“…Regulation of LCO perception involves their degradation by host hydrolases in the rhizosphere and symbiotic tissues (Tian et al, 2013;Cai et al, 2018;Malolepszy et al, 2018). This might explain why diverse doses of LCOs trigger similar symbiotic responses and Fig.…”

Section: Differential Immunity Suppression By Lcos In Symbiotic and Nmentioning

confidence: 99%

Lipo‐chitooligosaccharide signalling blocks a rapid pathogen‐induced ROS burst without impeding immunity

et al. 2018

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Summary Molecular signals released by microbes at the surface of plant roots and leaves largely determine host responses, notably by triggering either immunity or symbiosis. How these signalling pathways cross‐talk upon coincident perception of pathogens and symbionts is poorly described in plants forming symbiosis. Nitrogen fixing symbiotic Rhizobia spp. and arbuscular mycorrhizal fungi produce lipo‐chitooligosaccharides (LCOs) to initiate host symbiotic programmes. In Medicago truncatula roots, the perception of LCOs leads to reduced efflux of reactive oxygen species (ROS). By contrast, pathogen perception generally triggers a strong ROS burst and activates defence gene expression. Here we show that incubation of M. truncatula seedlings with culture filtrate (CF) of the legume pathogen Aphanomyces euteiches alone or simultaneously with Sinorhizobium meliloti LCOs, resulted in a strong ROS release. However, this response was completely inhibited if CF was added after pre‐incubation of seedlings with LCOs. By contrast, expression of immunity‐associated genes in response to CF and disease resistance to A. euteiches remained unaffected by LCO treatment of M. truncatula roots. Our findings suggest that symbiotic plants evolved ROS inhibition response to LCOs to facilitate early steps of symbiosis whilst maintaining a parallel defence mechanisms toward pathogens.

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Role of the Nod Factor Hydrolase MtNFH1 in Regulating Nod Factor Levels during Rhizobial Infection and in Mature Nodules of Medicago truncatula

Cited by 42 publications

References 88 publications

Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery

Modulation of Symbiotic Compatibility by Rhizobial Zinc Starvation Machinery

Celebrating 20 Years of Genetic Discoveries in Legume Nodulation and Symbiotic Nitrogen Fixation

Lipo‐chitooligosaccharide signalling blocks a rapid pathogen‐induced ROS burst without impeding immunity

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