Comparative Analysis of the Symbiotic Efficiency of  Medicago truncatula and Medicago sativa under  Phosphorus Deficiency

Sulieman, Saad; Schulze, Joachim; Tran, Lam‐Son Phan

doi:10.3390/ijms14035198

Cited by 31 publications

(24 citation statements)

References 42 publications

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“…S6) imply that the substantial accumulation of identified amino acids in McCP-31-induced nodules may be the result of the higher SNF capacity and N assimilation under low Pi conditions (Fig. 5A) (40). Indeed, the significant increase in total soluble protein content observed in McCP-31-induced nodules under low Pi treatment (Fig.…”

Section: Discussionmentioning

confidence: 87%

Adaptation of the symbiotic Mesorhizobium –chickpea relationship to phosphate deficiency relies on reprogramming of whole-plant metabolism

Esfahani

Kusano

Nguyen

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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Low inorganic phosphate (Pi) availability is a major constraint for efficient nitrogen fixation in legumes, including chickpea. To elucidate the mechanisms involved in nodule acclimation to low Pi availability, two Mesorhizobium-chickpea associations exhibiting differential symbiotic performances, Mesorhizobium ciceri CP-31 (McCP-31)-chickpea and Mesorhizobium mediterranum SWRI9 (MmSWRI9)-chickpea, were comprehensively studied under both control and low Pi conditions. MmSWRI9-chickpea showed a lower symbiotic efficiency under low Pi availability than McCP-31-chickpea as evidenced by reduced growth parameters and down-regulation of nifD and nifK. These differences can be attributed to decline in Pi level in MmSWRI9-induced nodules under low Pi stress, which coincided with up-regulation of several key Pi starvation-responsive genes, and accumulation of asparagine in nodules and the levels of identified amino acids in Pi-deficient leaves of MmSWRI9-inoculated plants exceeding the shoot nitrogen requirement during Pi starvation, indicative of nitrogen feedback inhibition. Conversely, Pi levels increased in nodules of Pi-stressed McCP-31-inoculated plants, because these plants evolved various metabolic and biochemical strategies to maintain nodular Pi homeostasis under Pi deficiency. These adaptations involve the activation of alternative pathways of carbon metabolism, enhanced production and exudation of organic acids from roots into the rhizosphere, and the ability to protect nodule metabolism against Pi deficiency-induced oxidative stress. Collectively, the adaptation of symbiotic efficiency under Pi deficiency resulted from highly coordinated processes with an extensive reprogramming of whole-plant metabolism. The findings of this study will enable us to design effective breeding and genetic engineering strategies to enhance symbiotic efficiency in legume crops.phosphate deficiency | nitrogen fixation | metabolomics | carbon and nitrogen metabolism | phosphate homeostasis P hosphorus plays a critical role in numerous plant metabolic processes and contributes to the biosynthesis of cellular macromolecules, such as ATP, nucleic acids, phospholipids, and phosphorylated sugars (1). Thus, phosphorus has been established as one of the most important elements required for normal plant growth and development (1). Unfortunately, limited availability of inorganic phosphate (Pi), which is the only absorbable form of phosphorus for plants, in soils is nearly universal, because Pi readily forms various insoluble compounds with metals, such as calcium and iron in alkaline and acidic soils, respectively (1, 2). Pi deficiency can be overcome by the application of Pi fertilizers; however, the excessive use of chemical fertilizers can have serious environmental consequences, including the contamination of soil and water resources (1). Additionally, the global demand for and use of Pi fertilizers are projected to increase significantly with the explosive growth of the global population.Thus, it has been predicted that global Pi res...

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Section: Discussionmentioning

confidence: 87%

Adaptation of the symbiotic Mesorhizobium –chickpea relationship to phosphate deficiency relies on reprogramming of whole-plant metabolism

Esfahani

Kusano

Nguyen

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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“…Plants engaged in symbiotic N 2 fixation are known to have high P demand (Vance et al ., 2003; Sulieman et al ., 2013). This is related to the high energy that is required for nitrogenase to function at a high level.…”

Section: Discussionmentioning

confidence: 99%

“…This premise was necessary for identifying the better symbiotic partner for M. truncatula between both strains, as well as characterizing the reasons for the suboptimal efficiency for M. truncatula × S. meliloti under low P supply. Indeed, little is known about how M. truncatula × S. meliloti is affected by P deficiency at the whole-plant level (Sulieman et al ., 2013). The present data revealed that under conditions of suboptimal P supply (1 μM P), the symbiotic performance of M. truncatula – S. meliloti 102F51 plants was more sensitively affected when compared with that derived from combination with S. meliloti 2011 (Tables 2, 3).…”

Section: Discussionmentioning

confidence: 99%

“…On the 63rd day of growth, the nodulated root system of the plants was sealed within their dark glass cylinders and connected to a computer-controlled, open-flow gas analysis system. This time frame corresponds to the maximum potential nitrogenase activity in M. truncatula and other plant species, such as soybean (Fabre and Planchon, 2000; Sulieman et al ., 2013). Apparent nitrogenase activity (ANA) was measured as H 2 evolution in an N 2 :O 2 (80:20) mixture, and total nitrogenase activity (TNA) was determined as the peak value of H 2 evolution in an Ar:O 2 (80:20) mixture.…”

Section: Methodsmentioning

confidence: 99%

“…The precise understanding of factors affecting M. truncatula –bacterial association will enable improvement of the symbiotic efficiency by genetic engineering. In this regard, it has recently been reported that the model S. meliloti 2011 strain formed a less effective symbiotic association with M. truncatula than with M. sativa under normal growing conditions (Sulieman and Schulze, 2010 a ), while the reverse was revealed under P deprivation (Sulieman et al ., 2013). However, a comparison of S. meliloti 2011 and the most frequently used S. meliloti 102F51 strain in terms of symbiotic efficiency has not been performed with M. truncatula under various levels of P limitation.…”

Section: Introductionmentioning

confidence: 99%

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Growth and nodulation of symbiotic Medicago truncatula at different levels of phosphorus availability

Sulieman

Schulze

et al. 2013

Journal of Experimental Botany

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110

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Medicago truncatula is an important model plant for characterization of P deficiency on leguminous plants at the physiological and molecular levels. Growth optimization of this plant with regard to P supply is the first essential step for elucidation of the role of P in regulation of nodulation. Hence, a study was carried out to address the growth pattern of M. truncatula hydroponically grown at different gradual increases in P levels. The findings revealed that M. truncatula had a narrow P regime, with an optimum P level (12 μM P) which is relatively close to the concentration that induces P toxicity. The accumulated P concentration (2.7 mg g–1 dry matter), which is normal for other crops and legumes, adversely affected the growth of M. truncatula plants. Under P deficiency, M. truncatula showed a higher symbiotic efficiency with Sinorhizobium meliloti 2011 in comparison with S. meliloti 102F51, partially as a result of higher electron allocation to N2 versus H+. The total composition of free amino acids in the phloem was significantly affected by P deprivation. This pattern was found to be almost exclusively the result of the increase in the asparagine level, suggesting that asparagine might be the shoot-derived signal that translocates to the nodules and exerts the down-regulation of nitrogenase activity. Additionally, P deprivation was found to have a strong influence on the contents of the nodule carbon metabolites. While levels of sucrose and succinate tended to decrease, a higher accumulation of malate was observed. These findings have provided evidence that N2 fixation of M. truncatula is mediated through an N feedback mechanism which is closely related to nodule carbon metabolism.

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Databases of Transcription Factors in Legumes

Mochida

Sulieman

et al. 2015

Biological Nitrogen Fixation

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Comparative Analysis of the Symbiotic Efficiency of Medicago truncatula and Medicago sativa under Phosphorus Deficiency

Cited by 31 publications

References 42 publications

Adaptation of the symbiotic Mesorhizobium –chickpea relationship to phosphate deficiency relies on reprogramming of whole-plant metabolism

Adaptation of the symbiotic Mesorhizobium –chickpea relationship to phosphate deficiency relies on reprogramming of whole-plant metabolism

Growth and nodulation of symbiotic Medicago truncatula at different levels of phosphorus availability

Databases of Transcription Factors in Legumes

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