Peas and other legumes develop spherical or cylindrical structures -- called nodules -- in their roots to establish a mutually beneficial relationship with bacteria that convert atmospheric nitrogen into a useable nutrient for the legume plant. Root nodule symbiosis enables legumes to grow under nitrogen-limiting conditions where most of non-leguminous plants cannot survive.
Researchers in Japan now have a better understanding of how the symbiotic relationship evolved. Gov't Research Support, U. Gov't, Non-P. On the contrary, major crops such as rice, wheat, corn etc. It is highly demanding for agriculture to establish strategies not depending on too much chemical fertilizers because of possible depletion of underground resources, food security caused by soaring fertilizer prices, and environmental effects such as emission of greenhouse gases.
In order to generate nitrogen-fixing non-legumes, we investigate molecular mechanisms in root nodule development. If we identify symbiotic genes that had been involved in legume evolution for acquiring abilities of root nodule development, then we can transfer the genes into non-legumes, to confer nodule formation on non-legumes. Thus, given the vital roles of P in both plant and bacterial metabolism, screening for P-solubilizing traits in N 2 -fixing rhizobia can be a cheaper and useful strategy to ameliorate the negative effects of soil P stress on plants for improved crop yields and food security.
Immobilization of P can occur in inorganic and organic forms Rodriguez and Fraga, During microbial P transformation, the carboxyl and hydroxyl ion containing organic acids release their protons and bind to cations Bergkemper et al. In low-P soils, rhizobia can solubilize soil-bound P in the rhizosphere through acidification by synthesizing gluconic acid under the control of pyrroloquinoline quinone PQQ genes Yadav et al. Of all the organic acids, gluconic acid is most potent in P solubilization and the oxidation of glucose to gluconic acid by rhizobia is an important step in the solubilization of soil P Richardson et al.
Gene gcd in rhizobia encodes quinoprotein glucose dehydrogenase PQQGDH , which is involved in the release of organic anions to solubilize inorganic P Rodriguez et al. In addition to organic acids, inorganic acids and mycorrhizal fungi in soil can also enhance phosphorus solubilization Alori et al. Whereas rhizobia are largely known for their N 2 -fixing traits, mycorrhizal fungi are particularly known for their role in the acquisition of phosphorus and other nutrients required by plants Bolan, A synergistic interaction was observed when faba bean was treated with Rhizobium leguminosarum bv.
The activity of microbial P-enzymes on the huge P reservoir in soils largely accounts for P supply to terrestrial plants. P assimilation under P-poor soil conditions is usually achieved using high-affinity P transporters, in contrast to P-rich soils where low-affinity P transporters are involved Hsieh and Wanner, The expression of genes phoU, phoR , and phoB in soil microbes largely regulates the P-starvation response in cropping systems for increased use of external P sources Eder et al.
For example, what are the cues for low-P sensing in soil by plants and microbes, and what is the timeframe required for biological processes such gene expression to occur? And what are the regulatory mechanisms underlying the build-up of P pool in response to its demand by plants? The successful induction of root nodules and their subsequent colonization by rhizobia require the production of rhizobial Nod factors that allow for their recognition by the host legume Via et al.
Aside their growth promoting effects, rhizobia have been implicated in processes leading to induced systemic resistance ISR in host plants which is governed by complex mechanisms; for example, inoculating common bean with Rhizobium etli led to enhanced resistance to infection by Pseudomonas syringae pv.
The response of host plants to pathogen infection can include a molecular cross-talk between salicylic acid and jasmonates, both of which play key roles in the activation of plant defense related genes Pieterse et al.
Upon attack by insects for instance, intricate processes which include the synthesis of salicylic acid and jasmonates occur leading to the activation of genes responsible for plant defense Hettenhausen et al.
Moreover, siderophores produced by symbiotic rhizobia and other microbes do not only enhance Fe nutrition for healthy plant growth and grain yield in legumes, but also serve as biocontrol agents against pathogens Table 1. For example, siderophores produced by Sinorhizobium meliloti were shown to suppress Macrophomina phaseolina , the causal agent of charcoal rot in groundnut Arora et al. Similarly, co-inoculation of groundnut with Rhizobium and Trichoderma harzianum successfully inhibited infection by Sclerotium rolfsii , the fungal pathogen that causes stem rot disease Ganesan et al.
A Rhizobium species was also found to protect soybean from root rot caused by Phytophthora megasperma , while a Sinorhizobium sp. Rhizobitoxine-producing strains of Bradyrhizobium japonicum were also able to successfully block infection of soybean by Macrophomina phaseolina , the causal pathogen of charcoal rot Deshwal et al.
In addition to their roles as signal molecules in the legume-rhizobia symbiosis, rhizobial metabolites such as riboflavin and lumichrome, as well as vitamins which include thiamine, biotin, niacin and ascorbic acid have been implicated in legume plant defense against pathogens Mehboob et al. For instance, spraying riboflavin on tobacco and Arabidopsis caused resistance to Peronospora parasitica, Pseudomonas syringae pv. In Arabidopsis, riboflavin was similarly found to induce the priming of plant defense response toward infection by Pseudomonas syringae pv.
Moreover, Mesorhizobium loti induced the expression of the Phenylalanine Ammonia lyase LjPAL1 gene responsible for the synthesis of salicylic acid, and consequently altered the response of Lotus japonicum to infection by Pseudomonas syringae Chen et al. Legumes are also reported to protect themselves against pathogens using isoflavonoids, phytoalexins and phytoanticipins Dakora and Phillips, It is therefore possible that the health of a legume plant is dependent on a molecular cross-talk involving several defense molecules such as isoflavones, riboflavin, thiamine and other yet unknown molecules Subramanian et al.
In Arabidopsis for example, infection with Sclerotinia scleroticum increased the expression of the IFS1 gene that codes for isoflavone synthase and highlights the involvement of isoflavones as plant defense molecules Subramanian et al.
Also, a thiamine treatment led to the accumulation of hydrogen peroxide H 2 O 2 and a build-up of lignin in roots of rice following infection with the root-knot nematode Meloidogyne graminicola ; this was associated with the increased transcription of the OsPAL1 and OsC4H genes involved in the phenylpropanoid pathway Huang et al.
Clearly, plants have diverse ways of overcoming biotic and abiotic stress within their environments through the synthesis of novel molecules. For example, following the infection of Arabidopsis by Pieris rapae , one branch of the jasmonate signaling pathway regulated by the MYC2 gene was expressed Santino et al. Clearly, a lot remains to be unraveled regarding the complex chemical cross-talks involved in plant adaptation to disease infection and pathogen attack.
Plant growth and productivity is dependent on multiple factors, which include mineral nutrition, resistance to insect pests and diseases.
Fortunately, symbiotic rhizobia are capable of triggering biological pathways that cause outcomes with direct and indirect effects on plant growth promotion and protection. Studying the interlinkages of outcomes from the legume-rhizobia symbioses has the potential to identify microsymbionts for use as inoculants due to the multiplicity of functions that they elicit.
Whereas, some of the outcomes triggered by rhizobia may be tied to their symbiotic interactions with legumes, the effects of some of the signal molecules produced often extends to non-legumes, thus indicating a wider distribution of these traits among diverse bacterial genera.
SJ and MM drafted the manuscript. FI produced the photo used in Figure 1. The photo was shot by her from her glasshouse studies. Some of the ideas in the manuscript are also from her Master's thesis. FD conceived the idea, edited, and approved the final version of the paper. All authors contributed to the article and approved the submitted version. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.
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