Scientia Agricultura Sinica ›› 2024, Vol. 57 ›› Issue (3): 442-453.doi: 10.3864/j.issn.0578-1752.2024.03.002

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Function Analysis of the Soybean Transcription Factor NAC1 in Tolerance to Low Phosphorus

XIONG ChuWen(), GUO ZhiBin(), ZHOU QiangHua, CHENG YanBo, MA QiBin, CAI ZhanDong, NIAN Hai()   

  1. College of Agriculture, South China Agricultural University/Guangdong Subcenter of National Center for Soybean Improvement, Guangzhou 510642
  • Received:2023-06-14 Accepted:2023-07-28 Online:2024-02-01 Published:2024-02-05

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Abstract:

【Objective】The productivity of acid soil crops is severely impacted by the limited availability of phosphorus. Soybean (Glycine max) is an important grain and oil crop, known for its preference for phosphorus. Phosphorus deficiency significantly affect both the yield and quality of soybean. While the NAC (NAM, ATAF1/2, CUC2) transcription factor family has been recognized for its involvement in regulating plant responses to various biotic and abiotic stresses, its role in soybean under low phosphorus stress remains largely unexplored. In this study, we focused on the low-phosphorus-tolerant wild soybean variety BW69 as our material, with the objective of cloning and analyzing the expression patterns and functions of the low-phosphorus-tolerant gene GsNAC1. This investigation lays the foundation for a deeper understanding the mechanisms behind the regulation of GsNAC1 response to low phosphorus stress. 【Method】The full-length sequence of GsNAC1 was cloned from BW69, and the characteristics of its encoded amino acid sequence were explored by bioinformatics analysis. In addition, the tissue expression patterns of GsNAC1 were examined through quantitative real-time PCR (qRT-PCR). The subcellular localization of GsNAC1 was observed using laser confocal microscopy. Furthermore, soybean genetic transformation experiments were conducted for further phenotype analysis, and RNA-seq analysis was performed to identify differentially expressed genes (DEGs) related to low phosphorus stress. 【Result】The GsNAC1 gene was successfully cloned, with a full-length coding region of 876 bp. Phylogenetic analysis showed a 62.46% sequence similarity between GsNAC1 and AtATAF1, and no difference was observed with the GmNAC1 sequence from the Williams 82 reference genome. Subcellular localization experiments further revealed that GsNAC1 was localized in the nucleus. Using qRT-PCR, it was discovered that GsNAC1 is expressed in roots, stems, leaves, apes, flowers and pods, with the highest relative expression level found in the roots. Notably, GsNAC1 exhibited significant upregulation in response to low pH and low phosphorus conditions. To assess the phenotypic effects, we performed experiments using both hydroponic and soil cultivation methods under low phosphorus conditions. The transgenic lines showed notable increases in root/shoot ratio, total root length, root surface area, root volume, and phosphorus content compared to the wild type (WT). Transcriptome analysis revealed that GsNAC1 may enhance tolerance to low phosphorus stress by promoting the expression of genes such as GmALMT6, GmALMT27, GmPAP27, and GmWRKY21. 【Conclusion】The expression of GsNAC1 was up-regulated by low pH and low phosphorus, and overexpression of GsNAC1 significantly enhanced the tolerance to low phosphorus stress in soybean, playing a promoting role in the response to low phosphorus stress. Besides, GsNAC1 may enhance the tolerance to low phosphorus stress in soybean by regulating the expression of downstream genes.

Key words: Glycine soja, low phosphorus tolerance, GsNAC1, root system configuration, RNA-seq

Table 1

Primer sequence used in this study"

引物名称
Primer name		 序列
Sequences (5′-3′)
GsNAC1-F ACGTTTCAAATCGCAGTCGC
GsNAC1-R CTTGGCCTAGCCCACATCAC
PTF101-GsNAC1-F gagaacacgggggactctagaATGAAGGGAGAATTAGAGTTGCCA
PTF101-GsNAC1-R cgatcggggaaattcgagctcTCACATCTTCTGTAGGTACATGAACATG
GsNAC1-GFP-F acgggggactcttgaccatggATGAAGGGAGAATTAGAGTTGCCA
GsNAC1-GFP-R aagttcttctcctttactagtCCATCTTCTGTAGGTACATGAACATG
RT-GsNAC1-F CGATCGGAAAACCGAAAGCG
RT-GsNAC1-R TCAACATTGGCGAGGCGATA
Actin3-F GCACCACCGGAGAGAAAATA
Actin3-R GTGCACAATTGATGGACCAG
qGmALMT6-F CCTTGAAGCATCAAAAGAGCCCA
qGmALMT6-R CCCATTGTGACTGCCTCAAAGAT
qGmALMT27-F TTTGAGTTTACCGCAGGGGC
qGmALMT27-R TACGCGGTCAGATCCATTGTC
qGmPAP27-F ACATGTCCTGACACTGACGG
qGmPAP27-R TTGCCACAAGTCTAGGATCGG
qGmWRKY21-F ACAATCCCAACCCAAGGAACT
qGmWRKY21-R GCACCAAGGGAATTTGGCTG
35S CGGATTCCATTGCCCAGCTA
NOS-R CACCGCGCGCGATAATTT

Fig. 1

Analysis of GsNAC1 gene expression profile a: Relative expression of GsNAC1 in roots, stems, leaves, tops, flowers, pods and seeds. b: Relative expression of GsNAC1 at pH 5.8, 5.0, 4.5 and 4.0 treatments. c: Relative expression of GsNAC1 in low phosphorus treatment for 0, 1, 3, 5 and 7 days. Different small letters indicated significant difference at 5% level. The data are expressed as the mean ± standard deviation of three biological repetitions"

Fig. 2

Homology analysis and subcellular localization of the GsNAC1 a: Phylogenetic tree analysis of NAC family of soybean and other species protein. b: Alignment of the amino acid sequences of GsNAC1, GmNAC1 and Arabidopsis thaliana AtATAF1 protein. c: Subcellular localization of GsNAC1 in epidermal cells of tobacco. DAPI: 4′, 6-Diamidinyl-2-phenylindole, a nuclear specific fluorescent dye. GFP: Green fluorescent protein. Mergard: Overlapping images of DAPI, GFP and Bright field"

Fig. 3

Long-term hydroponic phenotypic identification of WT and transgenic strains under LP and NP treatments a: Growth performance of WT and transgenic lines in long-term hydroponic experiments. Morphological parameters of shoot fresh weight (b), root fresh weight (c), root/shoot ratio (d), total root length (e), total root surface (f), total root volume (g) and average diameter (h) were analyzed using RhizoVision Explorer software after 15 days of treatment. WT: Wild type (HuaChun 6), Transgenic Lines: OEGsNAC1-A, OEGsNAC1-B and OEGsNAC1-C, A: OEGsNAC1-A, B: OEGsNAC1-B, C: OEGsNAC1-C. ns: indicates insignificant. *: Significant difference at P<0.05, **: Significant difference at P<0.01. Data are presented as mean ± standard deviation of three biological replicates. The same as below"

Fig. 4

Long-term soil culture phenotyping of WT and transgenic strains under LP and NP treatments a: Phenogram of WT and transgenic plants grown in nutrient soil with normal phosphorus and in acidic red loam with low phosphorus treatment. b: Shoot fresh weight. c: Shoot phosphorus content. d: Roots fresh weight. e: Root phosphorus content"

Fig. 5

Transcriptome profile analysis a: Scatter plot of differentially expressed genes between transgenic and wild-type strains in the absence of low phosphorus stress (red: Up-regulated genes, gray: No differentially expressed genes, blue: Down-regulated genes). b: Wayne diagram showing the overlap of GsNAC1-overexpressed and low phosphorus-induced DEGs. c: Relative expression of GmALMT6 (Glyma.03G152700). d: Relative expression of GmALMT27 (Glyma.17G154300). e: Relative expression of GmPAP27 (Glyma.06G170300). f: Relative expression of GmWRKY21 (Glyma.04G218700)"

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