scholarly journals Nitrate-Induced CLE Peptide Systemically Inhibits Nodulation in Medicago truncatula

Plants ◽  
2020 ◽  
Vol 9 (11) ◽  
pp. 1456
Author(s):  
Maria Lebedeva ◽  
Mahboobeh Azarakhsh ◽  
Yaroslavna Yashenkova ◽  
Lyudmila Lutova
Keyword(s):  
Medicago Truncatula ◽  
Lotus Japonicus ◽  
Dependent Manner ◽  
Receptor Kinase ◽  
Nitrate Treatment ◽  
Whole Plant ◽  
Cle Peptides ◽  
Autoregulation Of Nodulation ◽  
Cle Peptide ◽  
Plant Level

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.

scholarly journals Characterisation of Medicago truncatula CLE34 and CLE35 in nodulation control

2020 ◽  
Author(s):  
Celine Mens ◽  
April H. Hastwell ◽  
Huanan Su ◽  
Peter M. Gresshoff ◽  
Ulrike Mathesius ◽  
...  
Keyword(s):  
Pisum Sativum ◽  
Medicago Truncatula ◽  
Sequence Homology ◽  
Dependent Manner ◽  
Legume Species ◽  
Mature Peptide ◽  
Cle Peptides ◽  
Autoregulation Of Nodulation ◽  
Cle Peptide ◽  
Distinct Role

AbstractLegume plants form a symbiosis with N2-fixing soil rhizobia, resulting in new root organs called nodules that enable N2-fixation. Nodulation is a costly process that is tightly regulated by the host through Autoregulation of Nodulation (AON) and nitrate-dependent regulation of nodulation. Both pathways require legume-specific CLAVATA/ESR-related (CLE) peptides. Nitrogen-induced nodulation-suppressing CLE peptides have not previously been characterised in Medicago truncatula, with only rhizobia-induced MtCLE12 and MtCLE13 identified. Here, we report on novel peptides MtCLE34 and MtCLE35 in nodulation control pathways. The nodulation-suppressing CLE peptides of five legume species were classified into three clades based on sequence homology and phylogeny. This approached identified MtCLE34 and MtCLE35 and four new CLE peptide orthologues of Pisum sativum. Whereas MtCLE12 and MtCLE13 are induced by rhizobia, MtCLE34 and MtCLE35 respond to both rhizobia and nitrate. MtCLE34 was identified as a pseudogene lacking a functional CLE-domain. Overexpression of MtCLE12, MtCLE13 and MtCLE35 inhibits nodulation. Together, our findings indicate that MtCLE12 and MtCLE13 have a distinct role in AON, while MtCLE35 regulates nodule numbers in a rhizobia- and nitrate-dependent manner. MtCLE34 likely had a similar role to MtCLE35 but its function was lost due to a nonsense mutation resulting in the loss of the mature peptide.

scholarly journals Inoculation- and Nitrate-Induced CLE Peptides of Soybean Control NARK-Dependent Nodule Formation

2011 ◽  
Vol 24 (5) ◽  
pp. 606-618 ◽  
Author(s):  
Dugald E. Reid ◽  
Brett J. Ferguson ◽  
Peter M. Gresshoff
Keyword(s):  
Amino Acid ◽  
Nodule Development ◽  
Nodule Formation ◽  
Dependent Manner ◽  
Transgenic Roots ◽  
Nitrate Treatment ◽  
Cle Peptides ◽  
Autoregulation Of Nodulation ◽  
Cle Peptide ◽  
Bradyrhizobium Sp

Systemic autoregulation of nodulation in legumes involves a root-derived signal (Q) that is perceived by a CLAVATA1-like leucine-rich repeat receptor kinase (e.g. GmNARK). Perception of Q triggers the production of a shoot-derived inhibitor that prevents further nodule development. We have identified three candidate CLE peptide-encoding genes (GmRIC1, GmRIC2, and GmNIC1) in soybean (Glycine max) that respond to Bradyrhizobium japonicum inoculation or nitrate treatment. Ectopic overexpression of all three CLE peptide genes in transgenic roots inhibited nodulation in a GmNARK-dependent manner. The peptides share a high degree of amino acid similarity in a 12-amino-acid C-terminal domain, deemed to represent the functional ligand of GmNARK. GmRIC1 was expressed early (12 h) in response to Bradyrhizobium-sp.-produced nodulation factor while GmRIC2 was induced later (48 to 72 h) but was more persistent during later nodule development. Neither GmRIC1 nor GmRIC2 were induced by nitrate. In contrast, GmNIC1 was strongly induced by nitrate (2 mM) treatment but not by Bradyrhizobium sp. inoculation and, unlike the other two GmCLE peptides, functioned locally to inhibit nodulation. Grafting demonstrated a requirement for root GmNARK activity for nitrate regulation of nodulation whereas Bradyrhizobium sp.-induced regulation was contingent on GmNARK function in the shoot.

scholarly journals The structure and activity of nodulation-suppressing CLE peptide hormones of legumes

2015 ◽  
Vol 42 (3) ◽  
pp. 229 ◽  
Author(s):  
April H. Hastwell ◽  
Peter M. Gresshoff ◽  
Brett J. Ferguson
Keyword(s):  
Molecular Mechanisms ◽  
De Novo ◽  
Lotus Japonicus ◽  
Peptide Hormones ◽  
Negative Feedback Loops ◽  
C Terminus ◽  
Cle Peptides ◽  
Autoregulation Of Nodulation ◽  
Cle Peptide ◽  
External Stimuli

Legumes form a highly-regulated symbiotic relationship with specific soil bacteria known as rhizobia. This interaction results in the de novo formation of root organs called nodules, in which the rhizobia fix atmospheric di-nitrogen (N2) for the plant. Molecular mechanisms that regulate the nodulation process include the systemic ‘autoregulation of nodulation’ and the local nitrogen-regulation of nodulation pathways. Both pathways are mediated by novel peptide hormones called CLAVATA/ESR-related (CLE) peptides that act to suppress nodulation via negative feedback loops. The mature peptides are 12–13 amino acids in length and are post-translationally modified from the C-terminus of tripartite-domain prepropeptides. Structural redundancy between the prepropeptides exists; however, variations in external stimuli, timing of expression, tissue specificity and presence or absence of key functional domains enables them to act in a specific manner. To date, nodulation-regulating CLE peptides have been identified in Glycine max (L.) Merr., Medicago truncatula Gaertn., Lotus japonicus (Regel) K.Larsen and Phaseolus vulgaris L. One of the L. japonicus peptides, called LjCLE-RS2, has been structurally characterised and found to be an arabinosylated glycopeptide. All of the known nodulation CLE peptides act via an orthologous leucine rich repeat (LRR) receptor kinase. Perception of the peptide results in the production of a novel, unidentified inhibitor signal that acts to suppress further nodulation events. Here, we contrast and compare the various nodulation-suppressing CLE peptides of legumes.

scholarly journals Αναπρογραμματισμός του μεταβολισμού του Lotus japonicus σε μεταγραφικό, βιοχημικό και μεταβολομικό επίπεδο κατά τη συμβιωτική αζωτοδέσμευση

2016 ◽  
Author(s):  
Χρυσάνθη Καλλονιάτη
Keyword(s):  
Nitrogen Fixation ◽  
Metabolite Profiling ◽  
Symbiotic Nitrogen Fixation ◽  
Sulfur Metabolism ◽  
Lotus Japonicus ◽  
Nitrogen Fixing ◽  
Model Legume ◽  
Whole Plant ◽  
Plant Level ◽  
Molecular And Biochemical Mechanisms

Symbiotic nitrogen fixation in legumes takes place in specialized organs called nodules,which become the main source of assimilated nitrogen for the whole plant. Symbiotic nitro‐gen fixation requires exquisite integration of plant and bacterial metabolism and involvesglobal changes in gene expression and metabolite accumulation in both rhizobia and thehost plant. In order to study the metabolic changes mediated by symbiotic nitrogen fixationon a whole‐plant level, metabolite levels were profiled by gas chromatography–mass spec‐trometry in nodules and non‐symbiotic organs of Lotus japonicus plants uninoculated or in‐oculated with M. loti wt,  ΔnifA or  ΔnifH fix‐ strains. Furthermore, transcriptomic andbiochemical approaches were combined to study sulfur metabolism in nodules, its link tosymbiotic nitrogen fixation, and the effect of nodules on whole‐plant sulfur partitioning andmetabolism. It is well established that nitrogen and sulfur (S) metabolism are tightly en‐twined and sulfur is required for symbiotic nitrogen fixation, however, little is known aboutthe molecular and biochemical mechanisms governing sulfur uptake and assimilation duringsymbiotic nitrogen fixation. Transcript profiling in Lotus japonicus was combined with quan‐tification of S‐metabolite contents and APR activity in nodules and in non‐symbiotic organsof plants uninoculated or inoculated with M. loti wt, ΔnifA or ΔnifH fix‐ strains. Moreover,sulfate uptake and its distribution into different plant organs were analyzed and 35S‐flux intodifferent S‐pools was monitored. Metabolite profiling revealed that symbiotic nitrogen fixa‐tion results in dramatic changes of many aspects of primary and secondary metabolism innodules which leads to global reprogramming of metabolism of the model legume on awhole‐plant level. Moreover, our data revealed that nitrogen fixing nodules represent athiol‐rich organ. Their high APR activity and 35S‐flux into cysteine and its metabolites in com‐bination with the transcriptional up‐regulation of several genes involved in sulfur assimila‐tion highlight the function of nodules as a new site of sulfur assimilation. The higher thiolcontent observed in non‐symbiotic organs of nitrogen fixing plants in comparison touninoculated plants cannot be attributed to local biosynthesis, indicating that nodules couldserve as a novel source of reduced sulfur for the plant, which triggers whole‐plant repro‐gramming of sulfur metabolism. Interestingly, the changes in metabolite profiling and theenhanced thiol biosynthesis in nodules and their impact on the whole‐plant sulfur, carbonand nitrogen economy are dampened in fix‐ plants, which in most respects metabolically re‐sembled uninoculated plants, indicating a strong interaction between nitrogen fixation andsulfur and carbon metabolism.

scholarly journals The CLE53–SUNN genetic pathway negatively regulates arbuscular mycorrhiza root colonization in Medicago truncatula

2020 ◽  
Vol 71 (16) ◽  
pp. 4972-4984 ◽  
Author(s):  
Magda Karlo ◽  
Clarissa Boschiero ◽  
Katrine Gram Landerslev ◽  
Gonzalo Sancho Blanco ◽  
Jiangqi Wen ◽  
...  
Keyword(s):  
Mycorrhizal Fungi ◽  
Phosphorus Uptake ◽  
Arbuscular Mycorrhizal ◽  
Dependent Manner ◽  
High Phosphorus ◽  
Peptide Modification ◽  
Cle Peptides ◽  
Autoregulation Of Nodulation ◽  
Low Phosphorus ◽  
Phosphorus Levels

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.

scholarly journals CLE-HAR1 Systemic Signaling and NIN-Mediated Local Signaling Suppress the Increased Rhizobial Infection in the daphne Mutant of Lotus japonicus

2020 ◽  
Vol 33 (2) ◽  
pp. 320-327 ◽  
Author(s):  
Emiko Yoro ◽  
Takuya Suzaki ◽  
Masayoshi Kawaguchi
Keyword(s):  
Lotus Japonicus ◽  
Constitutive Expression ◽  
Negative Regulation ◽  
Dependent Manner ◽  
Long Distance ◽  
Systemic Signaling ◽  
Putative Receptor ◽  
Autoregulation Of Nodulation ◽  
Local Signaling ◽  
The Relationship

Legumes survive in nitrogen-limited soil by forming a symbiosis with rhizobial bacteria. During root nodule symbiosis, legumes strictly control the development of their symbiotic organs, the nodules, in a process known as autoregulation of nodulation (AON). The study of hypernodulation mutants has elucidated the molecular basis of AON. Some hypernodulation mutants show an increase in rhizobial infection in addition to developmental alteration. However, the relationship between the AON and the regulation of rhizobial infection has not been clarified. We previously isolated daphne, a nodule inception (nin) allelic mutant, in Lotus japonicus. This mutant displayed dramatically increased rhizobial infection, suggesting the existence of NIN-mediated negative regulation of rhizobial infection. Here, we investigated whether the previously isolated components of AON, especially CLAVATA3/ESR (CLE)-RELATED-ROOT SIGNAL1 (CLE-RS1), CLE-RS2, and their putative receptor HYPERNODULATION AND ABERRANT ROOT FORMATION1 (HAR1), were able to suppress increased infection in the daphne mutant. The constitutive expression of LjCLE-RS1/2 strongly reduced the infection in the daphne mutant in a HAR1-dependent manner. Moreover, reciprocal grafting analysis showed that strong reduction of infection in daphne rootstock constitutively expressing LjCLE-RS1 was canceled by a scion of the har1 or klavier mutant, the genes responsible for encoding putative LjCLE-RS1 receptors. These data indicate that rhizobial infection is also systemically regulated by CLE-HAR1 signaling, a component of AON. In addition, the constitutive expression of NIN in daphne har1 double-mutant roots only partially reduced the rhizobial infection. Our findings indicate that the previously identified NIN-mediated negative regulation of infection involves unknown local signaling, as well as CLE-HAR1 long-distance signaling.

Medicago truncatula response to water-deficit stress: whole plant perspectives

2021 ◽  
Author(s):  
◽  
Verónica Castañeda Presa
Keyword(s):  
Water Deficit ◽  
Medicago Truncatula ◽  
Water Status ◽  
Water Deficit Stress ◽  
World Population ◽  
Fibrous Root ◽  
Model Plant ◽  
Whole Plant ◽  
Plant Level

Medicago truncatula is a forage legume with agricultural but also scientifical interest, being used as a model plant for the study of legumes’ biology. Within a climate change context, it is of great importance to maintain/increase plant yield in stressful growth conditions to meet the requirements of the increasing world population. In order to achieve this, it is mandatory to further understand the adaptive response of plants to water-deficit stress, for which the use of this model plant results of great utility. In the present study, the simultaneous study of various plant organs with particular focus on the root system allows us a more integrative understanding of water-deficit response mechanisms from a whole-plant perspective. The root tissue was studied in Chapter 1, distinguishing between the thick taproot and the much thinner fibrous root. The different behaviour of both root types under well-watered as well as under water-deficit conditions was studied from a physiological and metabolic perspec-tive. This study highlighted the active role of the taproot rather than being considered a mere nutrient storage organ. The taproot showed a more resilient nature towards water-deficit stress than the fibrous root, while sucrose cleavage modulation, together with proline metabolism sug-gested a crucial role of these pathways in the root adaptation to water-deficit stress. In Chapter 2 we aimed to address different water-deficit conditions that can affect plant water status, using iso-osmotical conditions of salinity (NaCl and KCl), lack of irrigation and an osmoticum (PEG). This approach allows us to identify the similarities and differences in the mechanisms involved in the response to each stress at the whole-plant level. While PEG was dismissed as a reliable drought-stress mimicker, NaCl and KCl led to similar responses, with a slightly higher negative effect of KCl on plant metabolism. On the other hand, an emphasis on the shoot and root protection was observed for NaCl and no-irrigation stress, respectively. The study of the phloem sap allowed us to better understand the responses to the different water-deficit conditions at a whole-plant level. In summary, this study provides further insight into the response at the whole-plant level of M. truncatula to water-deficit conditions from a biochemical, metabolic and physiological point of view.

Differential responses of the sunn4 and rdn1-1 super-nodulation mutants of Medicago truncatula to elevated atmospheric CO2

2021 ◽  
Author(s):  
Yunfa Qiao ◽  
Shujie Miao ◽  
Jian Jin ◽  
Ulrike Mathesius ◽  
Caixian Tang
Keyword(s):  
Nitrogen Fixation ◽  
Elevated Co2 ◽  
Medicago Truncatula ◽  
N2 Fixation ◽  
Sink Strength ◽  
Wild Type ◽  
Total N ◽  
Autoregulation Of Nodulation ◽  
Nodulation Mutants ◽  
Fixation Capacity

Abstract Background and Aims Nitrogen fixation in legumes requires tight control of carbon and nitrogen balance. Thus, legumes control nodule numbers via an autoregulation mechanism. ‘Autoregulation of nodulation’ mutants super-nodulate and are thought to be carbon-limited due to the high carbon-sink strength of excessive nodules. This study aimed to examine the effect of increasing carbon supply on the performance of super-nodulation mutants. Methods We compared the responses of Medicago truncatula super-nodulation mutants (sunn-4 and rdn1-1) and wild type to five CO2 levels (300-850 μmol mol -1). Nodule formation and N2 fixation were assessed in soil-grown plants at 18 and 42 days after sowing. Key results Shoot and root biomass, nodule number and biomass, nitrogenase activity and fixed-N per plant of all genotypes increased with increasing CO2 concentration and reached the maximum around 700 μmol mol -1. While the sunn-4 mutant showed strong growth-retardation compared to wild-type plants, elevated CO2 increased shoot biomass and total N content of rdn1-1 mutant up to two-fold. This was accompanied by a four-fold increase in nitrogen fixation capacity in the rdn1-1 mutant. Conclusions These results suggest that the super-nodulation phenotype per se did not limit growth. The additional nitrogen fixation capacity of the rdn1-1 mutant may enhance the benefit of elevated CO2 on plant growth and N2 fixation.

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