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Local inhibition of nitrogen fixation and nodule metabolism in drought-stressed soybean.

ABSTRACT: Drought stress is a major factor limiting symbiotic nitrogen fixation (NF) in soybean crop production. However, the regulatory mechanisms involved in this inhibition are still controversial. Soybean plants were symbiotically grown in a split-root system (SRS), which allowed for half of the root system to be irrigated at field capacity while the other half remained water deprived. NF declined in the water-deprived root system while nitrogenase activity was maintained at control values in the well-watered half. Concomitantly, amino acids and ureides accumulated in the water-deprived belowground organs regardless of transpiration rates. Ureide accumulation was found to be related to the decline in their degradation activities rather than increased biosynthesis. Finally, proteomic analysis suggests that plant carbon metabolism, protein synthesis, amino acid metabolism, and cell growth are among the processes most altered in soybean nodules under drought stress. Results presented here support the hypothesis of a local regulation of NF taking place in soybean and downplay the role of ureides in the inhibition of NF.

SUBMITTER: Gil-Quintana E

PROVIDER: S-EPMC3654410 | biostudies-literature | 2013 May

REPOSITORIES: biostudies-literature

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Local inhibition of nitrogen fixation and nodule metabolism in drought-stressed soybean.

Gil-Quintana Erena E Larrainzar Estíbaliz E Seminario Amaia A Díaz-Leal Juan Luis JL Alamillo Josefa M JM Pineda Manuel M Arrese-Igor Cesar C Wienkoop Stefanie S González Esther M EM

Journal of experimental botany 20130411 8

Drought stress is a major factor limiting symbiotic nitrogen fixation (NF) in soybean crop production. However, the regulatory mechanisms involved in this inhibition are still controversial. Soybean plants were symbiotically grown in a split-root system (SRS), which allowed for half of the root system to be irrigated at field capacity while the other half remained water deprived. NF declined in the water-deprived root system while nitrogenase activity was maintained at control values in the well ...[more]

PMID: 23580751

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Project description:It has been reported that supply of nitrate to culture solution rapidly and reversibly inhibits nodule growth and nitrogen fixation activity of soybean. In this study, the effects of ammonium, urea, or glutamine on nodule growth and nitrogen fixation activity are compared with that for nitrate. Soybean plants were cultivated with a nitrogen-free nutrient solution, then 1 mM-N of nitrate, ammonium, glutamine, or urea were supplied from 12 DAP until 17 DAP. Repression of nodule growth and nitrogen fixation activity at 17 DAP were observed by ammonium, urea, and glutamine like nitrate, although the inhibitory effects were milder than nitrate. The removal of nitrogen from the culture solutions after nitrogen treatments resulted in a recovery of the nodule growth. It was found that the glutamine treatment followed by N-free cultivation gave highest nitrogen fixation activity about two times of the control. Tracer experiments with 15N and 13C were performed to evaluate the translocation of N and C to the different tissues. Culture solutions containing a 15N-labeled nitrogen source were supplied from 21 DAP, and the whole shoots were exposed to 13CO2 for 60 min on 23 DAP, and plants were harvested on 24 DAP. The percentage distribution of 15N in nodules was highest for ammonium (1.4%) followed by glutamine (0.78%), urea (0.32%) and nitrate (0.25%). The percentage distribution of 13C in the nodules was highest for the control (11.5%) followed by urea (5.8%), glutamine (2.6%), ammonium (2.3%), and nitrate (2.3%). The inhibitory effects of nitrogen compounds appeared to be related to a decrease in photoassimilate partitioning in the nodules, rather than 15N transport into the nodules. The free amino acid concentrations after nitrogen treatments were increased in the nodules and leaves by nitrate, in the roots by ammonium, in the stems by urea, and the roots, stems, and leaves by glutamine treatment. The concentrations of asparagine, aspartate, and glutamine were increased after nitrogen treatments. By the long-term supply of nitrogen for 2-weeks, nitrate significantly increased the lateral roots and leaf growth. The long-term supply of urea and glutamine also promoted the lateral roots and leaf growth, but ammonium suppressed them.

Project description:Nodulation process in legume plants is essential for biological nitrogen fixation during which process a large amount of phosphorus (P) is required. Under P deficiency, nodule formation is greatly affected, and induction of purple acid phosphatases (PAPs) is an adaptive strategy for nodules to acquire more P. However, regulation roles of PAPs in nodules remain largely understood. In this study, by transcriptome sequencing technology, five PAP genes were found to be differentially expressed, which led to the greatly increased acid phosphatase (APase) and phytase activities in soybean mature nodules under P starvation conditions; and among the five PAP genes, GmPAP12 had the highest transcript level, and RT-PCR indicated expression of GmPAP12 was gradually increasing during nodule development. GUS activity driven by GmPAP12 promoter was also significantly induced in low phosphorus conditions. Further functional analysis showed that under low phosphorus stress, overexpression of GmPAP12 resulted in higher nodule number, fresh weight, and nitrogenase activity as well as the APase activity than those of control plant nodules, whereas the growth performance and APase activity of nodules on hairy roots were greatly lower when GmPAP12 was suppressed, indicating that GmPAP12 may promote P utilization in soybean nodules under low P stress, which thus played an important role in nodulation and biological nitrogen fixation. Moreover, P1BS elements were found in the promoter of GmPAP12, and yeast one-hybrid experiment further proved the binding of P1BS by transcription factor GmPHR1 in the promoter of GmPAP12. At last, overexpression and suppression of GmPHR1 in nodules indeed caused highly increased and decreased expression of GmPAP12, respectively, indicating that GmPAP12 is regulated by GmPHR1 in soybean nodules. Taken together, these data suggested that GmPAP12 was a novel soybean PAP involved in the P utilization and metabolism in soybean root nodules and played an important role in the growth and development of root nodules and biological nitrogen fixation.

Dataset Information

Local inhibition of nitrogen fixation and nodule metabolism in drought-stressed soybean.

Publications

Local inhibition of nitrogen fixation and nodule metabolism in drought-stressed soybean.

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