Genome-Wide Analysis of Poplar SQUAMOSA-Promoter-Binding Protein (SBP) Family under Salt Stress
Abstract
:1. Introduction
2. Materials and Methods
2.1. Identification of SBP Genes
2.2. Phylogenetic Evolution and Gene Structure Analysis
2.3. Chromosome Location and Gene Duplication Analysis
2.4. Promoter and miRNA Analysis
2.5. Plant Materials
2.6. Gene Expression Analysis by RNA-Seq
2.7. Verification of Real-Time Quantitative PCR
2.8. Yeast Two-Hybrid Test
3. Results
3.1. Identification and Sequence Alignment of PtSBPs
3.2. Phylogeny and Gene Structure Analysis
3.3. Chromosome Location and Gene Duplication Events
3.4. Cis-Acting Element and Target miRNA Analysis
3.5. Gene Expression Analysis of PtSBPs in Different Tissues
3.6. Gene Expression Analysis of PtSBPs in Different Tissues under Salt Stress
3.7. PtSBP Protein Interaction Analysis
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Data Availability Statement
Conflicts of Interest
References
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Gene Name | Accession Number | AA | Molecular Weight | Theoretical PI | Instability Index | Aliphatic Index | GRAVY | AtSBP Ortholog | Subcellular Locatioon |
---|---|---|---|---|---|---|---|---|---|
PtSBP1 | Potri.001G055900.1 | 446 | 49008.35 | 8.67 | 52.71 | 61.95 | −0.724 | AT5G43270.3 | Nucleus |
PtSBP2 | Potri.001G058600.1 | 376 | 41280.85 | 9.3 | 54.07 | 56.81 | −0.707 | AT5G50670.1 | Cytoplasm; Nucleus |
PtSBP3 | Potri.001G398200.1 | 244 | 27427.02 | 9.07 | 63.32 | 61.56 | −0.784 | AT3G15270.1 | Nucleus |
PtSBP4 | Potri.002G002400.1 | 1073 | 119091.39 | 8.53 | 59.07 | 76.59 | −0.528 | AT1G20980.1 | Nucleus |
PtSBP5 | Potri.002G142200.1 | 325 | 36132.89 | 9.11 | 57.79 | 58.95 | −0.705 | AT1G02065.1 | Cytoplasm; Nucleus |
PtSBP6 | Potri.002G142400.1 | 398 | 43784.56 | 8.53 | 53.54 | 65.73 | −0.606 | AT1G27360.4 | Nucleus |
PtSBP7 | Potri.002G188700.4 | 1002 | 110900.96 | 5.87 | 53.09 | 79.63 | −0.365 | AT2G47070.1 | Nucleus |
PtSBP8 | Potri.003G169400.1 | 313 | 34232.95 | 9.23 | 53.55 | 58.27 | −0.699 | AT5G50570.2 | Nucleus |
PtSBP9 | Potri.003G172600.1 | 411 | 45630.63 | 9.24 | 47.86 | 60.07 | −0.818 | AT5G43270.3 | Cytoplasm; Nucleus |
PtSBP10 | Potri.004G046700.1 | 148 | 16466.96 | 7.6 | 80.6 | 36.89 | −1.316 | AT2G33810.1 | Nucleus |
PtSBP11 | Potri.005G258700.1 | 1072 | 118587.67 | 8.14 | 58.2 | 77.31 | −0.475 | AT1G20980.1 | Nucleus |
PtSBP12 | Potri.007G138800.1 | 202 | 22709.64 | 9.49 | 47.34 | 51.14 | −0.916 | AT1G53160.1 | Nucleus |
PtSBP13 | Potri.008G097900.1 | 510 | 55865.53 | 7.25 | 46.81 | 68.63 | −0.492 | AT1G69170.1 | Nucleus |
PtSBP14 | Potri.008G098600.1 | 1035 | 115390.06 | 7.3 | 43.54 | 84.11 | −0.373 | AT2G47070.1 | Nucleus |
PtSBP15 | Potri.008G197000.1 | 793 | 88909.58 | 6.43 | 46.93 | 78.89 | −0.358 | AT5G18830.3 | Cytoplasm; Nucleus |
PtSBP16 | Potri.010G026200.1 | 782 | 87604.3 | 6.49 | 49.47 | 81.24 | −0.298 | AT5G18830.3 | Cytoplasm; Nucleus |
PtSBP17 | Potri.010G154000.1 | 1030 | 114785.39 | 8.13 | 45.62 | 82.24 | −0.409 | AT2G47070.1 | Nucleus |
PtSBP18 | Potri.010G154300.1 | 600 | 66181.99 | 8.18 | 47.49 | 75.27 | −0.335 | AT1G69170.1 | Nucleus |
PtSBP19 | Potri.011G055900.1 | 144 | 16188.76 | 6.53 | 85.47 | 44.79 | −1.206 | AT2G33810.1 | Nucleus |
PtSBP20 | Potri.011G116800.1 | 242 | 27239.63 | 8.93 | 70.78 | 56.03 | −0.888 | AT3G15270.1 | Nucleus |
PtSBP21 | Potri.012G100700.1 | 346 | 38302.62 | 8.68 | 55.2 | 51.3 | −0.707 | AT5G50570.2 | Nucleus |
PtSBP22 | Potri.014G057700.1 | 328 | 36449.12 | 8.85 | 59.69 | 55.7 | −0.745 | AT1G02065.1 | Nucleus |
PtSBP23 | Potri.014G057800.1 | 408 | 45197.94 | 6.81 | 60.25 | 62.4 | −0.694 | AT1G27370.4 | Nucleus |
PtSBP24 | Potri.014G114300.1 | 1004 | 111261.28 | 6.13 | 51.82 | 80.3 | −0.393 | AT3G60030.1 | Nucleus |
PtSBP25 | Potri.015G060400.1 | 561 | 61613.62 | 8.39 | 53.58 | 63.62 | −0.562 | AT1G69170.1 | Cytoplasm; Nucleus |
PtSBP26 | Potri.015G098900.1 | 381 | 41809.37 | 8.68 | 56.67 | 60.37 | −0.644 | AT5G50570.2 | Nucleus |
PtSBP27 | Potri.016G048500.1 | 382 | 41034.42 | 9.03 | 59.25 | 57.75 | −0.614 | AT2G42200.1 | Nucleus |
PtSBP28 | Potri.017G012900.1 | 110 | 12592.56 | 9.49 | 35.42 | 56.55 | −0.776 | AT1G53160.2 | Cytoplasm; Nucleus |
PtSBP29 | Potri.018G149900.1 | 472 | 51720.59 | 8.58 | 61.98 | 62.46 | −0.569 | AT5G43270.3 | Cytoplasm; Nucleus |
PtSBP30 | Potri.019G073600.1 | 69 | 8351.57 | 10.62 | 91.51 | 43.91 | −0.916 | AT3G57920.1 | Nucleus |
No. | Paralogous Genes | Ks | Ka | Ka/Ks |
---|---|---|---|---|
1 | PtSBP2 (Chr01)/PtSBP8 (Chr03) | 0.178443215 | 0.061591622 | 0.345160908 |
2 | PtSBP3 (Chr01)/PtSBP20 (Chr11) | 0.342751855 | 0.078286805 | 0.228406656 |
3 | PtSBP4 (Chr02)/PtSBP11 (Chr05) | 0.271895969 | 0.068274383 | 0.2511048 |
4 | PtSBP6 (Chr02)/PtSBP23 (Chr14) | 0.284902171 | 0.071482635 | 0.250902388 |
5 | PtSBP10 (Chr04)/PtSBP19 (Chr11) | 0.25806393 | 0.114291101 | 0.442879023 |
6 | PtSBP12 (Chr07)/PtSBP28 (Chr17) | 0.470500471 | 0.265439967 | 0.564165146 |
7 | PtSBP13 (Chr08)/PtSBP18 (Chr10) | 0.236628628 | 0.100342683 | 0.424051323 |
8 | PtSBP14 (Chr08)/PtSBP17 (Chr10) | 0.224605439 | 0.064208977 | 0.285874541 |
9 | PtSBP15 (Chr08)/PtSBP16 (Chr10) | 0.232984091 | 0.078535107 | 0.33708356 |
10 | PtSBP21 (Chr12)/PtSBP26 (Chr15) | 0.300891016 | 0.112241239 | 0.373029545 |
Cis-element | Sequences | Function | Genes |
---|---|---|---|
3-AF1 binding site | TAAGAGAGGAA | cis-acting regulatory element involved in light responsiveness | PtSBP30 |
AACA_motif | TAACAAACTCCA | involved in endosperm-specific negative expression | PtSBP30 |
ABRE | ACGTG,CACGTG/CGCACGTGTC,GCAACGTGTC,GCCGCGTGGC/CGTACGTGCA,TACGTGTC | cis-acting element involved in the abscisic acid responsiveness | PtSBP13, PtSBP14 |
ACE | CTAACGTATT | cis-acting regulatory element involved in light responsiveness | PtSBP13 |
AE-box | AGAAACAA,AGAAACTT | cis-acting regulatory element involved in light responsiveness | PtSBP17 |
ARE | AAACCA | cis-acting regulatory element essential for the anaerobic induction | PtSBP14, PtSBP15 |
AT1-motif | AATTATTTTTTATT | cis-acting regulatory element involved in light responsiveness | PtSBP16, PtSBP17 |
ATCT-motif | AATCTAATCC | cis-acting regulatory element involved in light responsiveness | PtSBP25, PtSBP26 |
AuxRR-core | GGTCCAT | cis-acting regulatory element involved in auxin responsiveness | PtSBP15 |
Box 4 | ATTAAT | cis-acting regulatory element involved in light responsiveness | PtSBP24-27 |
CAT-box | GCCACT | cis-acting regulatory element related to meristem expression | PtSBP11 |
CGTCA-motif | CGTCA | cis-acting regulatory element involved in the MeJA-responsiveness | PtSBP11 |
chs-CMA1a | TTACTTAA | cis-acting regulatory element involved in light responsiveness | PtSBP21 |
chs-CMA2a | TCACTTGA | cis-acting regulatory element involved in light responsiveness | PtSBP19-20, PtSBP24 |
GA-motif | ATAGATAA | cis-acting regulatory element involved in light responsiveness | PtSBP19, PtSBP20 |
Gap-box | CAAATGAA(A/G)A | cis-acting regulatory element involved in light responsiveness | PtSBP16 |
GARE-motif | TCTGTTG | cis-acting element involved in gibberellin-responsiveness | PtSBP4, PtSBP25, PtSBP30 |
GATA-motif | AAGGATAAGG/GATAGGA/GATAGGG | cis-acting regulatory element involved in light responsiveness | PtSBP20 |
G-box | CACGAC,CACGTC,CACGTT,GCCACGTGGA,TACGTG/TAACACGTAG,ACACGTG(G/T)CACC,TCCACATGGCA | cis-acting regulatory element involved in light responsiveness | PtSBP12, PtSBP15 |
GC-motif | CCCCCG | cis-acting regulatory element essential for the anaerobic induction | PtSBP12, PtSBP13 |
GCN4_motif | TGAGTCA | cis-regulatory element involved in endosperm expression | PtSBP11 |
GT1-motif | GGTTAA,GGTTAAT | cis-acting regulatory element involved in light responsiveness | PtSBP29, PtSBP30 |
HD-Zip 1 | CAAT(A/T)ATTG | element involved in differentiation of the palisade mesophyll cells | PtSBP13, PtSBP16 |
I-box | AAGATAAGGCT/CCATATCCAAT/GGATAAGGTG,TGATAATGT | cis-acting regulatory element involved in light responsiveness | PtSBP19, PtSBP20, PtSBP24 |
LAMP-element | CTTTATCA | cis-acting regulatory element involved in light responsiveness | PtSBP20 |
L-box | ATTCTCACCTACCA | cis-acting regulatory element involved in light responsiveness | PtSBP24 |
LS7 | CAGATTTATTTTTA | cis-acting regulatory element involved in light responsiveness | PtSBP21 |
LTR | CCGAAA | cis-acting element involved in low-temperature responsiveness | PtSBP13 |
MBS | CAACTG | MYB binding site involved in drought-inducibility | PtSBP27, PtSBP28 |
MBSI | AAAAAAC(G/C)GTTA,TTTTTACGGTTA | MYB binding site involved in flavonoid biosynthetic genes regulation | PtSBP27 |
MRE | AACCTAA | MYB binding site involved in light responsiveness | PtSBP27 |
MSA-like | (T/C)C(T/C)AACGG(T/C)(T/C)A | cis-acting element involved in cell cycle regulation | PtSBP18 |
O2-site | GATGATGTGG,GTTGACGTGA | cis-acting regulatory element involved in zein metabolism regulation | PtSBP11 |
P-box | CCTTTTG | cis-acting element involved in gibberellin-responsiveness | PtSBP1, PtSBP4, PtSBP5, PtSBP7, PtSBP9, PtSBP10, PtSBP11, PtSBP24, PtSBP30 |
RY-element | CATGCATG | cis-acting regulatory element involved in seed-specific regulation | PtSBP12 |
Sp1 | GGGCGG | cis-acting regulatory element involved in light responsiveness | PtSBP29 |
TATC-box | TATCCCA | cis-acting element involved in gibberellin-responsiveness | PtSBP13 |
TCA-element | CCATCTTTTT | cis-acting element involved in salicylic acid responsiveness | PtSBP13 |
TCCC-motif | TCTCCCT | cis-acting regulatory element involved in light responsiveness | PtSBP20 |
TC-rich repeats | ATTCTCTAAC/GTTTTCTTAC | cis-acting element involved in defense and stress responsiveness | PtSBP13, PtSBP18 |
TCT-motif | TCTTAC | cis-acting regulatory element involved in light responsiveness | PtSBP16, PtSBP19-21 |
TGACG-motif | TGACG | cis-acting regulatory element involved in the MeJA-responsiveness | PtSBP11, PtSBP12 |
TGA-element | AACGAC | cis-acting regulatory element involved in auxin responsiveness | PtSBP18 |
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Guo, Q.; Li, L.; Zhao, K.; Yao, W.; Cheng, Z.; Zhou, B.; Jiang, T. Genome-Wide Analysis of Poplar SQUAMOSA-Promoter-Binding Protein (SBP) Family under Salt Stress. Forests 2021, 12, 413. https://doi.org/10.3390/f12040413
Guo Q, Li L, Zhao K, Yao W, Cheng Z, Zhou B, Jiang T. Genome-Wide Analysis of Poplar SQUAMOSA-Promoter-Binding Protein (SBP) Family under Salt Stress. Forests. 2021; 12(4):413. https://doi.org/10.3390/f12040413
Chicago/Turabian StyleGuo, Qing, Li Li, Kai Zhao, Wenjing Yao, Zihan Cheng, Boru Zhou, and Tingbo Jiang. 2021. "Genome-Wide Analysis of Poplar SQUAMOSA-Promoter-Binding Protein (SBP) Family under Salt Stress" Forests 12, no. 4: 413. https://doi.org/10.3390/f12040413