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Unregulated GmAGL82 due to Phosphorus Deficiency Positively Regulates Root Nodule Growth in Soybean.

ABSTRACT: Nitrogen fixation, occurring through the symbiotic relationship between legumes and rhizobia in root nodules, is crucial in sustainable agriculture. Nodulation and soybean production are influenced by low levels of phosphorus stress. In this study, we discovered a MADS transcription factor, GmAGL82, which is preferentially expressed in nodules and displays significantly increased expression under conditions of phosphate (Pi) deficiency. The overexpression of GmAGL82 in composite transgenic plants resulted in an increased number of nodules, higher fresh weight, and enhanced soluble Pi concentration, which subsequently increased the nitrogen content, phosphorus content, and overall growth of soybean plants. Additionally, transcriptome analysis revealed that the overexpression of GmAGL82 significantly upregulated the expression of genes associated with nodule growth, such as GmENOD100, GmHSP17.1, GmHSP17.9, GmSPX5, and GmPIN9d. Based on these findings, we concluded that GmAGL82 likely participates in the phosphorus signaling pathway and positively regulates nodulation in soybeans. The findings of this research may lay the theoretical groundwork for further studies and candidate gene resources for the genetic improvement of nutrient-efficient soybean varieties in acidic soils.

SUBMITTER: Song J

PROVIDER: S-EPMC10855635 | biostudies-literature | 2024 Feb

REPOSITORIES: biostudies-literature

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Unregulated GmAGL82 due to Phosphorus Deficiency Positively Regulates Root Nodule Growth in Soybean.

Song Jia J Liu Ying Y Cai Wangxiao W Zhou Silin S Fan Xi X Hu Hanqiao H Ren Lei L Xue Yingbin Y

International journal of molecular sciences 20240201 3

Nitrogen fixation, occurring through the symbiotic relationship between legumes and rhizobia in root nodules, is crucial in sustainable agriculture. Nodulation and soybean production are influenced by low levels of phosphorus stress. In this study, we discovered a MADS transcription factor, GmAGL82, which is preferentially expressed in nodules and displays significantly increased expression under conditions of phosphate (Pi) deficiency. The overexpression of GmAGL82 in composite tr ...[more]

PMID: 38339080

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Project description:Phosphorus (P) is a vital macronutrient required for soybean growth and development but is a finite resource in agriculture worldwide. Low inorganic P availability in soil is often a significant constraint for soybean production. However, little is known about the response of P supply on agronomic, root morphology, and physiological mechanisms of contrasting soybean genotypes at various growth stages and the possible effects of different P on soybean yield and yield components. Therefore, we conducted two concurrent experiments using the soil-filled pots with six genotypes (deep-root system: PI 647960, PI 398595, PI 561271, PI 654356; and shallow-root system: PI 595362, PI 597387) and two P levels [0 (P0) and 60 (P60) mg P kg-1 dry soil] and deep PVC columns with two genotypes (PI 561271 and PI 595362) and three P levels [0 (P0), 60 (P60), and 120 (P120) mg P kg-1 dry soil] in a temperature-controlled glasshouse. The genotype × P level interaction showed that increased higher P supply increased leaf area, shoot and root dry weights, total root length, shoot, root, and seed P concentrations and contents, P use efficiency (PUE), root exudation, and seed yield at different growth stages in both experiments. At the vegetative stage (Experiment 1), shallow-rooted genotypes with shorter life cycles had more root dry weight (39%) and total root length (38%) than deep-rooted genotypes with longer life cycles under different P levels. Genotype PI 654356 produced significantly higher (22% more) total carboxylates than PI 647960 and PI 597387 under P60 but not at P0. Total carboxylates positively correlated with root dry weight, total root length, shoot and root P contents, and physiological PUE. The deep-rooted genotypes (PI 398595, PI 647960, PI 654356, and PI 561271) had the highest PUE and root P contents. In Experiment 2, at the flowering stage, genotype PI 561271 had the greatest leaf area (202%), shoot dry weight (113%), root dry weight (143%), and root length (83%) relative to the short-duration, shallow-rooted genotype PI 595362 with external P applied (P60 and P120), with similar trends at maturity. PI 595362 had a greater proportion of carboxylates as malonate (248%), malate (58%), and total carboxylates (82%) than PI 561271 under P60 and P120 but no differences at P0. At maturity, the deep-rooted genotype PI 561271 had greater shoot, root, and seed P contents and PUE than the shallow-rooted genotype PI 595362 under increased P rates but no differences at P0. Further, the genotype PI 561271 had higher shoot (53%), root (165%), and seed yield (47%) than PI 595362 with P60 and P120 than P0. Therefore, inorganic P application enhances plant resistance to the soil P pool and maintains high soybean biomass production and seed yield.

Project description:Soybean root nodules are known to contain a high diversity of both rhizobial endophytes and nonrhizobial endophytes (NREs). Nevertheless, the variation of these bacteria among different root nodules within single plants has not been reported. So far, it is unclear whether the selection of NREs among different root nodules within single plants is a random process or is strictly controlled by the host plant to favor a few specific NREs based on their beneficial influence on plant growth. As well, it is also unknown if the relative frequency of NREs within different root nodules is consistent or if it varies based on the location or size of a root nodule. We assessed the microbiomes of 193 individual soybean root nodules from nine plants using high-throughput DNA sequencing. Bradyrhizobium japonicum strains occurred in high abundance in all root nodules despite the presence of other soybean-compatible rhizobia, such as Ensifer, Mesorhizobium, and other species of Bradyrhizobium in soil. Nitrobacter and Tardiphaga were the two nonrhizobial genera that were uniformly detected within almost all root nodules, though they were in low abundance. DNA sequences related to other NREs that have frequently been reported, such as Bacillus, Pseudomonas, Flavobacterium, and Variovorax species, were detected in a few nodules. Unlike for Bradyrhizobium, the low abundance and inconsistent occurrence of previously reported NREs among different root nodules within single plants suggest that these microbes are not preferentially selected as endophytes by host plants and most likely play a limited part in plant growth as endophytes.IMPORTANCE Soybean (Glycine max L.) is a valuable food crop that also contributes significantly to soil nitrogen by developing a symbiotic association with nitrogen-fixing rhizobia. Bacterial endophytes (both rhizobial and nonrhizobial) are considered critical for the growth and resilience of the legume host. In the past, several studies have suggested that the selection of bacterial endophytes within root nodules can be influenced by factors such as soil pH, nutrient availability, host plant genotype, and bacterial diversity in soil. However, the influence of size or location of root nodules on the selection of bacterial endophytes within soybean roots is unknown. It is also unclear whether the selection of nonrhizobial endophytes within different root nodules of a single plant is a random process or is strictly regulated by the host. This information can be useful in identifying potential bacterial species for developing bioinoculants that can enhance plant growth and soil nitrogen.

Dataset Information

Unregulated GmAGL82 due to Phosphorus Deficiency Positively Regulates Root Nodule Growth in Soybean.

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Unregulated <i>GmAGL82</i> due to Phosphorus Deficiency Positively Regulates Root Nodule Growth in Soybean.

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