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Acta Agronomica Sinica ›› 2024, Vol. 50 ›› Issue (3): 576-589.doi: 10.3724/SP.J.1006.2024.31025

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

Cloning, expression, and functional analysis of wheat (Triticum aestivum L.) TaSPX1 gene in low nitrogen stress tolerance

ZHANG Bao-Hua1,2(), LIU Jia-Jing1,2, TIAN Xiao1,2, TIAN Xu-Zhao1,2, DONG Kuo1, WU Yu-Jie1, XIAO Kai3,*(), LI Xiao-Juan1,2,*()   

  1. 1College of Life Sciences, Hebei Agricultural University, Baoding 071001, Hebei, China
    2Key Laboratory of Plant Physiology and Molecular Pathology, Baoding 071001, Hebei, China
    3College of Agronomy, Hebei Agricultural University, Baoding 071001, Hebei, China
  • Received:2023-04-06 Accepted:2023-09-13 Online:2024-03-12 Published:2023-10-09
  • Contact: *E-mail: xiaokai@hebau.edu.cn; E-mail: lxjlixiaojuan@126.com
  • Supported by:
    National Natural Science Foundation of China(32071935)

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Abstract:

The SPX gene family includes four subgroups: SPX, SPX-EXS, SPX-MFS, and SPX-RING, which play an important role in phosphate signal response, but so far, little is known about the functions of this family in wheat. Previously, we identified a gene TaSPX1 (GenBank No. Ak332300), belonged to SPX subfamily from wheat (Triticum aestivum). Subcellular localization analysis showed that it targeted onto nucleus. Phylogenetic tree of TaSPX1 and its homologous proteins from the wheat, Arabidopsis, and rice SPX families showed that it was closely related to OsSPX1, a member of rice SPX subfamily. The relative expression level of TaSPX1 significantly increased under low nitrogen (low-N) stress when investigated by RT-qPCR. Transgenic tobacco (Nicotiana tabacum) overexpression lines were generated. Using the culture methods of Murashige & Skoog (MS) hydroponic solution, the phenotype of WT and OE under low-N stress treatment was investigated. We found that the plants of OE3 and OE4, two OE lines overexpressing TaSPX1, displayed increased growth vigor and leaf area, together with the enhanced plant fresh weight and root weight, and elevated photosynthetic parameters including photosynthetic rate (Pn), intercellular carbon dioxide concentration (Ci), stomatal conductance (Gs), and transpiration rate (Tr), along with the increased contents of nitrogen, soluble sugar, soluble protein, and chlorophyll content upon low-N stress with respect to WT. Studies on transport and assimilation related parameters showed that under low-N stress, the relative expression level of some related genes and the activities of nitrogen assimilation-related enzymes were increased. Assays on the SOD, POD, and CAT, the enzymes functional as cellular protector, revealed the higher activities of them in OE plants than those in WT. On the contrary, MDA content was decreased. Further RT-qPCR analysis indicated the expression levels of several protection enzymes mentioned above were higher in OE plants than those of WT under low-N stress. Therefore, TaSPX1 played an important role in mediating plant resistance to low-N stress by improving photosynthetic parameters, enhancing nitrogen absorption and transport, and strengthening the protective enzyme system. The results enrich new understanding on the function of wheat SPX family members involved in abiotic stress, and provide a theoretical basis for genetic improvement of crops against low-N stress.

Key words: wheat, TaSPX1, subcellular localization, low nitrogen stress, functional analysis

Table 1

Primers used for RT-qPCR analysis"

引物名称
Primer name		 登录号
Accession number		 上游引物
Forward sequence (5′-3′)		 下游引物
Reverse sequence (5′-3′)
Ntaction U91563 ATTACGAGGATGAAGAGGAAGC TAAAAGCCTGAAGTTTGAAGA
Tatubulin U76558 CATGCTATCCCTCGTCTCGACCT CGCACTTCATGATGGAGTTGTAT
TaSPX1 Ak332300 ACTGGGGCTCTTATCCGTCT CAGCCTGCTCGATCACAGAT
NtSOD1 KJ874395 GGACAAGGAGTTCCGGATGATT CCATATTGACTTGAGCCAAGCG
NtSOD2 EU123521 TTGGGGAAGATGGTACTGCATC TCATCAGGATCAGCGTGAACAA
NtFeSOD KF724056 CAGGCCTGGAATCATCAGTT TTTCACCAAGGCAAGCTTTT
NtMnSOD1 X14482 ACCACCAGAATCACCATCAGAC CTATGCAATTTGGCGACGGTAG
NtMnSOD2 AB093097 AAGCCCTTGAACAGCTACATGA TCGAGTGGTTAATGTGACCTCC
NtCAT NTU07627 CAAGGATCTCTACGACTCGATT CTTGAGGGCAAATAATCCACCT
NtCAT1 EF532799 TCGGAGGATAAGCTTCTCCAGA ATGAGCACACTTGGGAGCATTA
NtCAT1;1 NTU93244 CAATGCTTGCCGATTTCTCT AGCAGGATCGGTATGGTCAG
NtCAT1;2 HF564632 GAAGTTCCCTGACATGGTCCAT AAGTGAACATGTGCAGGCTTTC
NtCAT1;3 HF564631 TGGCAAACGAGAGAAGTGTG AAGCAAGCTTTTGACCCAGA
NtCAT3 HF564633 GACCCCAGAGGATTTGCTGTAA ACCATGTCAGGGAACTTCATCC
NtPOD1;1 L02124 ATTAGGCTAAAGGTCCGTCGTG GCAAGTGTTTCAAAGGGGCTAG
NtPOD1;2 AB044154 GAAGGTTCAGACGCTGAGAGAA CAGGAAACAACTCCAGGACAGA
NtPOD1;3 AB044153 ATGGTCGTGGAGTTCTGGAATC GAATGTCAACCCAAGCAATCCC
NtPOD1;4 D11396 TCCTAATGTAGGTGCAGGAGGA CTCCAATTTCAGATGCAAGGGC
NtPOD1;5 AB178953 AGACCTCACCACCCAACAAC GCATCTCTTCTCCCAAGTGC
NtPOD1;6 AB027753 CTTACTGGTGCGCACACTATTG GCTGAGGAAGAAAGGTTGCATC
NtPOD1;7 AB027752 AATGGGTGCTTCTCTTCTTCGT CCCTTTTCTCTCCTGTGAAGCT
NtPOD4 AY032675 TTCCATCAGGGGATTTGAAG TGGTGCAGGAATGTTTGTGT
NtPOD9 AY032674 GAAACCCTAGCCAACCTTCC TCGTGTTCGTGGAGTTTGAG
NtNRT1.1-s AB102805 TACCGGTTTGTCGACGTGTC TCTCTTCTCCTTGTACACATAC
NtNRT1.1-t AB102806 CCGGCTTCATTGACACTCTT CCTCTTCTCCTTGTACACATAC
NtNRT1.2-s AB102807 GGGTTATCGTTCCCATTTGTCG TCAGCAAGTCTCTTCTCCTTGT
NtNRT1.2-t AB102808 GCCCTAACAGAGGTTAAGAGG TCCCCATTTCAGCAAGTCTC
NtNRT2.1 AJ557583 TAGCCGTCACATTCATGATCCT GATCGGCAGTTCTCGGCGAA
NtNRT2.2 AJ557584 CGTCGATCGTTAGGTATAATC ATTAACTACTCACACTTGGGTAA
NtNR1 X06134 ATCAGGTGGATGGATGGCGA ACAACCAACTCGAAGTACCC
NtNR2 X14059 ATGACTGGACCGTGGAAGTC AAAACACCGCACCGTTTTAG
NtNR3 JN384020 GGACGAAGGTACCGCTGATA GACTTCCACGGTCCAGTCAT
NtNR4 JN384019 TGTTTGAGCATCCGACTCAAC GGAGGTGGTCCACAAGCCA
NtNR5 XM_016606384 ATGGATATTACCGGCCGGCA TTACGTACCATCAGCATTAACA
NtNR6 XM_016583028 TTGAGGCACTGCTCAAAGAGC TCCCAAATGTGAATCACTCCC
NtNIR1 NM_001324935 ATGGCATCTTTTTCTGTTAAAT TTAATCTTCTGCTTCTTCTCTT
NtNIR2 X66145 GGGTTCCAGCTGATGATGTT TGGCATTCTCTTCTCGACCT
NtNIR3 X66147 TGGCAATTCACGAGGCAATC TCGTGGAACTGCACCAAAGT
NtNIR4 XR_001649867 AGTTGGGTTGACCAGTTTGC ACACGGATTCCACTTCCTTG
NtNIR5 XM_016583028 AGCATCTCCAGAAGACTTGG CCCAAATGTGAATCACTCCC
NtGS1 NM_001325250 ATTATGTCTCCGCTTTCAGATC ATTGAGCAAACCAGAAACAAGC
NtGS2 X95932 TCTTGGTGGTTTTCCTGGAC TGCTGAAATGCCAACTGAAG
NtGS3 XM_016584731 AAGATGGCTCAGATCTTGGCTC CTTTAAACATTCAATGCGAGCT
NtGS4 XM_016579636 GATGTGCAAACCCACACCTT CTGCAAATTCCTCGTCTGGT
NtGS5 XM_016640903 CGGGCATGATCAGAATTATTC AGATTGGTCGGGATATGAACC
NtGS6 XM_016640901 AACTAGGCTGGGATTGACG AGTCCCTCTCAGGCTCACAA
NtGS7 XM_016631331 CATTATGTCTCTGCTTTCAGAT TCATGGCAGTAACGACGTATGG

Fig. 1

Phylogenetic analysis of TaSPX1 and homologous from wheat, rice, and Arabidopsis thaliana The sequences of SPX proteins from Triticum aestivum L. (TaSAPs), Oryza sativa L. (OsSPXs), and Arabidopsis thaliana (L.) Heynh. (AtSPXs). The grey dot represents TaSPX1."

Fig. 2

Subcellular location of the TaSPX1-GFP fusion in epidermis cells of transformed tobacco (50 μm)"

Fig. 3

Relative expression pattern of TaSPX1 of wheat seedlings under low-N stress ** indicates significantly different at P < 0.01."

Table 2

Analysis of putative cis-acting elements in the promoter region of TaSPX1"

顺式元件
Cis-element		 目标序列
Target sequence (5′-3′)		 数目
Number		 功能
Function
TATA-BOX TATATA 23 胁迫响应元件和核心启动元件
Stress response elements and core promoter element
CAAT-BOX CAAT 39 MYBHv1结合位点
MYBHv1 binding site
MYC CATGTG/CATTTG 4 干旱和盐响应元件
Drought and salt response element
MYB CAACAG/CAACTG/CAACCA 2 干旱和盐响应元件
Drought and salt response element
ABRE TACGTGTC/ACGTG 7 ABA响应元件
ABA-responsive element
Root motif ATATT 2 根系生长
Root growth
G-box CACGTT/TACGTG/GCCACGTGGA 4 参与光响应顺式作用调节元件
cis-acting regulatory element involved in light responsiveness
LTRE AGTCGG 2 低氮胁迫响应元件
Response to low nitrogen stress
/ NANGAG 4 低氮胁迫响应元件
Response to low nitrogen stress

Fig. 4

Relative expression level of TaSPX1 in overexpression tobacco lines ** indicates significantly different at P < 0.01 compared with the control (WT)."

Fig. 5

Phenotype of WT, OE3, and OE4 plants under low-Pi and low-N treatments and physiological and biochemical characteristics under low-N treatment A: growth status; B: whole plant phenotypic characteristics (Bar: 9 cm); C: fresh weight; D: root weight; E: leaf area; F: chlorophyll content; G: transpiration rate; H: photosynthetic rate; I: stomatal conductance; J: intercellular CO2 concentration. * and ** indicate significantly different at P<0.05 and P<0.01 compared with the control (WT), respectively."

Fig. 6

Contents of nitrogen (A), soluble sugar (B), and soluble protein (C) in WT, OE3, and OE4 under low-N treatment ** indicates significantly different at P < 0.01 compared with the control (WT)."

Fig. 7

Activities of nitrogen anabolases and relative expression of NIRs, NRs, NRTs, and GSs in WT, OE3, and OE4 lines under low-N treatment A: the activities of NIR enzyme; B: the activities of NR enzyme; C: the activities of GS enzyme; D: the relative expression of NRTs; E: the relative expression of NIRs; F: the relative expression of NRs; G: the relative expression of GSs. ** indicates significantly different at P < 0.01 compared with the control (WT)."

Fig. 8

Activity of protection enzymes, MDA content, and the relative expression level of protection enzyme genes in WT, OE3, and OE4 lines under low-N treatment A: the activity of SOD enzyme. B: the activity of POD enzyme. C: the activity of CAT enzyme. D: MDA content. E: the relative expression level of SOD genes. F: the relative expression of POD genes; G: the relative expression of CAT genes. ** indicates significantly different at P < 0.01 compared with the control (WT)."

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