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An integrated nitrogen utilization gene network and transcriptome analysis reveal candidate genes in response to nitrogen deficiency in Brassica napus.

ABSTRACT: Nitrogen (N) is an essential factor for crop yield. Here, we characterized 605 genes from 25 gene families that form the complex gene networks of N utilization pathway in Brassica napus. We found unequal gene distribution between the A_n- and C_n-sub-genomes, and that genes derived from Brassica rapa were more retained. Transcriptome analysis indicated that N utilization pathway gene activity shifted in a spatio-temporal manner in B. napus. A low N (LN) stress RNA-seq of B. napus seedling leaves and roots was generated, which proved that most N utilization related genes were sensitive to LN stress, thereby forming co-expression network modules. Nine candidate genes in N utilization pathway were confirmed to be significantly induced under N deficiency conditions in B. napus roots, indicating their potential roles in LN stress response process. Analyses of 22 representative species confirmed that the N utilization gene networks were widely present in plants ranging from Chlorophyta to angiosperms with a rapid expansion trend. Consistent with B. napus, the genes in this pathway commonly showed a wide and conserved expression profile in response to N stress in other plants. The network, genes, and gene-regulatory modules identified here represent resources that may enhance the N utilization efficiency or the LN tolerance of B. napus.

SUBMITTER: Li P

PROVIDER: S-EPMC10203523 | biostudies-literature | 2023

REPOSITORIES: biostudies-literature

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An integrated nitrogen utilization gene network and transcriptome analysis reveal candidate genes in response to nitrogen deficiency in Brassica napus.

Li Pengfeng P Du Runjie R Li Zhaopeng Z Chen Zhuo Z Li Jiana J Du Hai H

Frontiers in plant science 20230509

Nitrogen (N) is an essential factor for crop yield. Here, we characterized 605 genes from 25 gene families that form the complex gene networks of N utilization pathway in Brassica napus. We found unequal gene distribution between the An- and Cn-sub-genomes, and that genes derived from Brassica rapa were more retained. Transcriptome analysis indicated that N utilization pathway gene activity shifted in a spatio-temporal manner in B. napus. A low N (LN) s ...[more]

PMID: 37229128

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Project description:Phytohormones play pivotal roles in the response of plants to various biotic and abiotic stresses. Boron (B) is an essential microelement for plants, and Brassica napus (B. napus) is hypersensitive to B deficiency. However, how auxin responds to B deficiency remained a dilemma for many years and little is known about how other phytohormones respond to B deficiency. The identification of B-efficient/inefficient B. napus indicates that breeding might overcome these constraints in the agriculture production. Here, we seek to identify phytohormone-related processes underlying B-deficiency tolerance in B. napus at the physiological and gene expression levels. Our study indicated low-B reduced indole-3-acetic acid (IAA) concentration in both the shoots and roots of B. napus, and affected the expression of the auxin biosynthesis gene BnNIT1 and the efflux gene BnPIN1 in a time-dependent manner. Low-B increased the jasmonates (JAs) and abscisic acid (ABA) concentrations and induced the expression of the ABA biosynthesis gene BnNCED3 and the ABA sensor gene BnPYL4 in the shoot. In two contrasting genotypes, the auxin concentration decreased more drastically in the B-inefficient genotype 'W10,' and together the expression of BnNIT1 and BnPIN1 also decreased more significantly in 'W10' under long-term B deficiency. While the JAs concentration was considerably higher in this genotype, and the ABA concentration was induced in 'W10' compared with the B-efficient genotype 'QY10.' Digital gene expression (DGE) profiling confirmed the differential expression of the phytohormone-related genes, indicating more other phyohormone differences involving in gene regulation between 'QY10' and 'W10' under low-B stress. Additionally, the activity of DR5:GFP was reduced in the root under low-B in Arabidopsis, and the application of exogenous IAA could partly restore the B-defective phenotype in 'W10.' Overall, our data suggested that low-B disturbed phytohormone homeostasis in B. napus, which originated from the change of transcriptional regulation of phytohormones-related genes, and the differences between genotypes may partly account for their difference in tolerance (B-efficiency) to low-B.

Project description:BackgroundNitrogen (N), phosphorus (P) and potassium (K) are critical macronutrients in crops, such that deficiency in any of N, P or K has substantial effects on crop growth. However, the specific commonalities of plant responses to different macronutrient deficiencies remain largely unknown.MethodsHere, we assessed the phenotypic and physiological performances along with whole transcriptome and metabolomic profiles of rapeseed seedlings exposed to N, P and K deficiency stresses.ResultsQuantities of reactive oxygen species were significantly increased by all macronutrient deficiencies. N and K deficiencies resulted in more severe root development responses than P deficiency, as well as greater chlorophyll content reduction in leaves (associated with disrupted chloroplast structure). Transcriptome and metabolome analyses validated the macronutrient-specific responses, with more pronounced effects of N and P deficiencies on mRNAs, microRNAs (miRNAs), circular RNAs (circRNAs) and metabolites relative to K deficiency. Tissue-specific responses also occurred, with greater effects of macronutrient deficiencies on roots compared with shoots. We further uncovered a set of common responders with simultaneous roles in all three macronutrient deficiencies, including 112 mRNAs and 10 miRNAs involved in hormonal signaling, ion transport and oxidative stress in the root, and 33 mRNAs and 6 miRNAs with roles in abiotic stress response and photosynthesis in the shoot. 27 and seven common miRNA-mRNA pairs with role in miRNA-mediated regulation of oxidoreduction processes and ion transmembrane transport were identified in all three macronutrient deficiencies. No circRNA was responsive to three macronutrient deficiency stresses, but two common circRNAs were identified for two macronutrient deficiencies. Combined analysis of circRNAs, miRNAs and mRNAs suggested that two circRNAs act as decoys for miR156 and participate in oxidoreduction processes and transmembrane transport in both N- and P-deprived roots. Simultaneously, dramatic alterations of metabolites also occurred. Associations of RNAs with metabolites were observed, and suggested potential positive regulatory roles for tricarboxylic acids, azoles, carbohydrates, sterols and auxins, and negative regulatory roles for aromatic and aspartate amino acids, glucosamine-containing compounds, cinnamic acid, and nicotianamine in plant adaptation to macronutrient deficiency.ConclusionsOur findings revealed strategies to rescue rapeseed from macronutrient deficiency stress, including reducing the expression of non-essential genes and activating or enhancing the expression of anti-stress genes, aided by plant hormones, ion transporters and stress responders. The common responders to different macronutrient deficiencies identified could be targeted to enhance nutrient use efficiency in rapeseed.

Dataset Information

An integrated nitrogen utilization gene network and transcriptome analysis reveal candidate genes in response to nitrogen deficiency in Brassica napus.

Publications

An integrated nitrogen utilization gene network and transcriptome analysis reveal candidate genes in response to nitrogen deficiency in <i>Brassica napus</i>.

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