Abstract
Key messages
Plant PIFs have been characterized, WGDs contributed to the expansion of class II PIFs; BdPIFs localized in the nucleus; BdPIF4/5C most likely response to high temperature and light stress.
Abstract
Phytochrome interacting factors (PIFs) belong to a small subset of basic helix-loop-helix (bHLH) transcription factors (TFs). As cellular signaling hubs, PIFs integrate multiple external and internal signals to orchestrate the regulation of the transcriptional network, thereby actuating the pleiotropic aspects of downstream morphogenesis. Nevertheless, the origin, phylogeny and function of plant PIFs are not well understood. To elucidate their evolution history and biological function, the comprehensive genomic analysis of the PIF genes was conducted using 40 land plant genomes plus additionally four alga lineages and also performed their gene organizations, sequence features and expression patterns in different subfamilies. In this study, phylogenetic analysis displayed that 246 PIF gene members retrieved from all embryophytes could be divided into three main clades, which were further felled into five distinct classes (Class I-V). The duplications of Class II PIFs were associated specially with whole genome duplication (WGD) events during the plant evolution process. Sequence analysis showed that PIF proteins had a conserved APB motif, and its crucial amino acid residues were relatively high proportion in the average abundance. As expected, subcellular localization analysis revealed that all BdPIF proteins were localized to the nucleus. Especially, BdPIF4/5C showed the highest expression level at high temperature, and the most significant hypocotyl elongation phenotype of overexpression of BdPIFs in Arabidopsis, which was consistent with the function and phenotype of AtPIF4. In brief, our findings provide a novel perspective on the origin and evolutionary history of plant PIFs, and lays a foundation for further investigation on its functions in plant growth and development.
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modified from Phytozome (https://phytozome-next.jgi.doe.gov/). Red and blue stars indicate whole-genome duplication and triplication, respectively
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Abbreviations
- PIF (PIL):
-
Phytochrome interacting factor-like
- phys:
-
Phytochromes
- WGDs:
-
Whole genome duplications
- R:
-
Red
- FR:
-
Far-red
- bHLH:
-
Basic helix-loop-helix
- APB:
-
Active phyB binding
- APA:
-
Active phyA binding
- ROS:
-
Reactive oxygen species
- FT:
-
Flowing locus T
- pI:
-
Isoelectric point
- Mw:
-
Molecular weight
- JTT:
-
Jones-Taylor-Thornton
- MEGA:
-
Molecular evolution genetic analysis
- ML:
-
Maximum-likelihood
- Clo-0:
-
Columbia-0
- MS:
-
Murashige and Skoog
- RT-qPCR:
-
Real-time quantitative polymerase chain reaction
- DAPI:
-
4’,6–Diamidino-2–phenylindole
- RL:
-
Rosette leaves
- Days:
-
Flowering time
- SOD:
-
Superoxide dismutase
- POD:
-
Peroxidase
- CAT:
-
Catalase
- ώ = dN/dS :
-
Nonsynonymous-to-synonymous rates ratio
- WGT:
-
Whole-genome triplication
- ORFs:
-
Open reading frames
- pifq :
-
p if1/3/4/5
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This study was supported from the Shanghai Sailing Program (19YF1414800) to MJ. The funding body had no role in study design, analysis, decision to publish, or preparation of the manuscript.
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MJ conceived and designed the work. MJ financially supported this study. MJ, CZ and GW performed the experiments and analyzed the data. MJ wrote and revised the manuscript. All authors read and approved the final manuscript.
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299_2022_2850_MOESM1_ESM.tif
Supplementary file1 (TIF 4938 KB) Fig. S1 Weblogos represents the bHLH domain of each group. The red star indicates the amino acids residues (H-E-R) at positions 5, 9, and 13 are the most critical for binding DNA
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Supplementary file2 (TIF 8665 KB) Fig. S2 Maximum Likelihood phylogenetic tree of plant Class I PIFs. The red circle represents duplication events
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Supplementary file3 (TIF 8331 KB) Fig. S3 Maximum Likelihood phylogenetic tree of plant Class II PIFs. The red circle represents duplication events
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Supplementary file4 (TIF 9193 KB) Fig. S4 Maximum Likelihood phylogenetic tree of plant Class III PIFs. The red circle represents duplication events
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Supplementary file5 (TIF 13733 KB) Fig. S5 Maximum Likelihood phylogenetic tree of plant Class IV PIFs. The red circle represents duplication events
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Supplementary file6 (TIF 16482 KB) Fig. S6 Maximum Likelihood phylogenetic tree of plant Class V PIFs. The red circle represents duplication events
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Supplementary file7 (TIF 1636 KB) Fig. S7 Correlation coefficient analysis of the Class II PIF gene family size and rounds of genome duplication in 9 eudicot species
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Supplementary file8 (TIF 10533 KB) Fig. S8 Semi-quantitative RT-PCR analysis of BdPIFs transgenic plants. Semi-quantitative RT-PCR was performed to analyze their expression patterns and the total RNA for RT-PCR was extracted from B. distachyon fresh leaves. The AtActin gene was served as expression control
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Supplementary file9 (TIF 4676 KB) Fig. S9 Phenotypic analysis of the transgenic Arabidopsis lines expressing B. distachyon PIF4/5C gene under long-day conditions. The statistical significance of differences was assessed using Tukey’s honestly significant difference (HSD) test. Asterisks denote significant differences (P < 0.05) between transgenic and control plants. Days, flowering time from sowing to the first flower opening; RL, numbers of rosette leaves at flowering; 4-6, 35S:: BdPIF4/5C lines 4-6. Bars, 1 cm
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Supplementary file10 (TIF 14948 KB) Fig. S10 Expression profiles of SODs, PODs and CATs. The plants grown in the 22℃ continuous irradiation. Plants were grown at 22℃ for 8 days before transfer to dark for 2 days. Control plants were maintained at light. Data are means ± SD from three independent experiments. * Significant (t test, P < 0.05) difference compared with WT plants. BdPIF4/5A-OX, 35S:: BdPIF4/5A; BdPIF4/5B-OX, 35S:: BdPIF4/5B; BdPIF4/5C-OX, 35S:: BdPIF4/5C; BdPIF3A-OX, 35S:: BdPIF3A; BdPIF3B-OX, 35S:: BdPIF3B; BdPIF8-OX, 35S:: BdPIF8
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Supplementary file11 (TIF 11741 KB) Fig. S11 Correlation analysis between SOD genes expression results and actual activities of SOD under normal (a) and light treatment (b) conditions
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Supplementary file17 (DOCX 49 KB) Table S6 Table showing nomenclatured gene name locus ID detailed genomic information and subcellular localization of plant PIFs
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Jiang, M., Wen, G. & Zhao, C. Phylogeny and evolution of plant Phytochrome Interacting Factors (PIFs) gene family and functional analyses of PIFs in Brachypodium distachyon. Plant Cell Rep 41, 1209–1227 (2022). https://doi.org/10.1007/s00299-022-02850-5
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DOI: https://doi.org/10.1007/s00299-022-02850-5