An official website of the United States government
SUMMARY Root systems are uniquely adapted to fluctuations in external nutrient availability. In response to suboptimal nitrogen conditions, plants adopt a root foraging strategy that favors a deeper and more branched root architecture, enabling them to explore and acquire soil resources. This response is gradually suppressed as nitrogen conditions improve. However, the root hairless mutantbuzzinBrachypodium distachyonshows a constitutive nitrogen‐foraging phenotype with increased root growth and root branching under nitrate‐rich conditions. To investigate how this unique root structure and root hair morphology in thebuzzmutant affects nitrate metabolism, we measured the expression of nitrate‐responsive genes, nitrate uptake and accumulation, nitrate reductase activity, and nitrogen use efficiency. We found that nitrate responses were upregulated by low nitrate conditions inbuzzrelative to wild type and correlated with increased expression of nitrate transport genes. In addition,buzzmutants showed increased nitrate uptake and a higher accumulation of nitrate in shoots. Thebuzzmutant also showed increased nitrate reductase activity in the shoots under low nitrate conditions. However, developmentally mature wild‐type andbuzzplants grown under low nitrate had similar nitrogen use efficiencies. These findings suggest thatBUZZinfluences nitrate signaling and that enhanced responsiveness to nitrate is required inbuzzseedlings to compensate for the lack of root hairs. These data question the importance of root hairs in enhancing nitrate uptake and expand our understanding of how root hairs in grasses affect physiological responses to low nitrate availability.
more »
« less
The small peptide CEP1 and the NIN-like protein NLP1 regulate NRT2.1 to mediate root nodule formation across nitrate concentrations
Abstract Legumes acquire fixed nitrogen (N) from the soil and through endosymbiotic association with diazotrophic bacteria. However, establishing and maintaining N2-fixing nodules are expensive for the host plant, relative to taking up N from the soil. Therefore, plants suppress symbiosis when N is plentiful and enhance symbiosis when N is sparse. Here, we show that the nitrate transporter MtNRT2.1 is required for optimal nodule establishment in Medicago truncatula under low-nitrate conditions and the repression of nodulation under high-nitrate conditions. The NIN-like protein (NLP) MtNLP1 is required for MtNRT2.1 expression and regulation of nitrate uptake/transport under low- and high-nitrate conditions. Under low nitrate, the gene encoding the C-terminally encoded peptide (CEP) MtCEP1 was more highly expressed, and the exogenous application of MtCEP1 systemically promoted MtNRT2.1 expression in a compact root architecture 2 (MtCRA2)-dependent manner. The enhancement of nodulation by MtCEP1 and nitrate uptake were both impaired in the Mtnrt2.1 mutant under low nitrate. Our study demonstrates that nitrate uptake by MtNRT2.1 differentially affects nodulation at low- and high-nitrate conditions through the actions of MtCEP1 and MtNLP1.
more »
« less
- Award ID(s):
- 2233714
- PAR ID:
- 10507231
- Publisher / Repository:
- Oxford Academic
- Date Published:
- Journal Name:
- The Plant Cell
- Volume:
- 35
- Issue:
- 2
- ISSN:
- 1040-4651
- Page Range / eLocation ID:
- 776 to 794
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
null (Ed.)Symbiotic nitrogen fixation is a complex and regulated process that takes place in root nodules of legumes and allows legumes to grow in soils that lack nitrogen. Nitrogen is mostly acquired from the soil as nitrate and its level in the soil affects nodulation and nitrogen fixation. The mechanism(s) by which legumes modulate nitrate uptake to regulate nodule symbiosis remain unclear. In Medicago truncatula , the MtNPF1.7 transporter has been shown to control nodulation, symbiosis, and root architecture. MtNPF1.7 belongs to the nitrate/peptide transporter family and is a symporter with nitrate transport driven by proton(s). In this study we combined in silico structural predictions with in planta complementation of the severely defective mtnip-1 mutant plants to understand the role of a series of distinct amino acids in the transporter’s function. Our results support hypotheses about the functional importance of the ExxE(R/K) motif including an essential role for the first glutamic acid of the motif in proton(s) and possibly substrate transport. Results reveal that Motif A, a motif conserved among major facilitator transport (MFS) proteins, is essential for function. We hypothesize that it participates in intradomain packing of transmembrane helices and stabilizing one conformation during transport. Our results also question the existence of a putative TMH4-TMH10 salt bridge. These results are discussed in the context of potential nutrient transport functions for MtNPF1.7. Our findings add to the knowledge of the mechanism of alternative conformational changes as well as symport transport in NPFs and enhance our knowledge of the mechanisms for nitrate signaling.more » « less
-
Purpose Legumes form root nodules to gain fixed nitrogen from rhizobia and can also access nitrogen in soil. Data suggest that plants might discriminate among these sources to optimize growth, but recogni- tion of symbiotically fixed nitrogen and its regulation remain poorly understood. Methods A greenhouse inoculation study manipu- lated the molecular form and concentration of nitro- gen available using two Lotus japonicus genotypes and the nitrogen-fixing symbiont, Mesorhizobium loti. Plants were supplied with sole organic and inorganic nitrogen sources to simulate forms that plants might receive from symbiotic nitrogen fixation or from the soil. Host benefit from and regulation of symbiosis was investigated by quantifying symbiotic trait varia- tion and isotopic analysis of nitrogen fixation. Results Host growth varied in response to fertili- zation with alanine, aspartic acid, ammonium, and nitrate, suggesting differences in catabolism effi- ciency. Net benefits of nodulation were reduced or eliminated under all forms of extrinsic fertilization. However, even when symbiosis imposed significant costs, hosts did not reduce investment into nodulation or nitrogen fixation when exposed to aspartic acid, unlike with other nitrogen sources. Conclusions L. japonicus can adaptively down- regulate investment into symbiosis in the presence of some but not all nitrogen sources. Failure to down- regulate any aspect of symbiosis in the presence of aspartic acid suggests that it might be jamming the main signal used by L. japonicus to detect nitrogen fixation.more » « less
-
Summary Establishment of symbiosis between plants and arbuscular mycorrhizal (AM) fungi depends on fungal chitooligosaccharides (COs) and lipo‐chitooligosaccharides (LCOs). The latter are also produced by nitrogen‐fixing rhizobia to induce nodules on leguminous roots. However, host enzymes regulating structure and levels of these signals remain largely unknown.Here, we analyzed the expression of a β‐N‐acetylhexosaminidase gene ofMedicago truncatula(MtHEXO2) and biochemically characterized the enzyme. Mutant analysis was performed to study the role ofMtHEXO2during symbiosis.We found that expression ofMtHEXO2is associated with AM symbiosis and nodulation.MtHEXO2expression in the rhizodermis was upregulated in response to applied chitotetraose, chitoheptaose, and LCOs.M. truncatulamutants deficient in symbiotic signaling did not show induction ofMtHEXO2. Subcellular localization analysis indicated that MtHEXO2 is an extracellular protein. Biochemical analysis showed that recombinant MtHEXO2 does not cleave LCOs but can degrade COs intoN‐acetylglucosamine (GlcNAc).Hexo2mutants exhibited reduced colonization by AM fungi; however, nodulation was not affected inhexo2mutants.In conclusion, we identified an enzyme, which inactivates COs and promotes the AM symbiosis. We hypothesize that GlcNAc produced by MtHEXO2 may function as a secondary symbiotic signal.more » « less
-
Kalcsits, Lee (Ed.)Abstract Many plant species form symbiotic associations with nitrogen-fixing bacteria. Through this symbiosis, plants allocate photosynthate belowground to the bacteria in exchange for nitrogen fixed from the atmosphere. This symbiosis forms an important link between carbon and nitrogen cycles in many ecosystems. However, the economics of this relationship under soil nitrogen availability gradients is not well understood, as plant investment toward symbiotic nitrogen fixation tends to decrease with increasing soil nitrogen availability. Here, we used a manipulation experiment to examine how costs of nitrogen acquisition vary under a factorial combination of soil nitrogen availability and inoculation with Bradyrhizobium japonicum in Glycine max L. (Merr.). We found that inoculation decreased belowground biomass carbon costs to acquire nitrogen and increased total leaf area and total biomass, but these patterns were only observed under low fertilization and were the result of increased plant nitrogen uptake and no change in belowground carbon allocation. These results suggest that symbioses with nitrogen-fixing bacteria reduce carbon costs of nitrogen acquisition by increasing plant nitrogen uptake, but only when soil nitrogen is low, allowing individuals to increase nitrogen allocation to structures that support aboveground growth. This pattern may help explain the prevalence of plants capable of forming these associations in less fertile soils and provides useful insight into understanding the role of nutrient acquisition strategy on plant nitrogen uptake across nitrogen availability gradients.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1093/plcell/koac340
