Abstract
Main conclusion
The NAC transcription factor ATAF2 suppresses its own transcription via self-promoter binding. ATAF2 genetically interacts with the circadian regulator CCA1 and phytochrome A to modulate seedling photomorphogenesis in Arabidopsis thaliana.
Abstract
ATAF2 (ANAC081) is a NAC (NAM, ATAF and CUC) transcription factor (TF) that participates in the regulation of disease resistance, stress tolerance and hormone metabolism in Arabidopsis thaliana. We previously reported that ATAF2 promotes Arabidopsis hypocotyl growth in a light-dependent manner via transcriptionally suppressing the brassinosteroid (BR)-inactivating cytochrome P450 genes BAS1 (CYP734A1, formerly CYP72B1) and SOB7 (CYP72C1). Assays using low light intensities suggest that the photoreceptor phytochrome A (PHYA) may play a more critical role in ATAF2-regulated photomorphogenesis than phytochrome B (PHYB) and cryptochrome 1 (CRY1). In addition, ATAF2 is also regulated by the circadian clock. The core circadian TF CIRCADIAN CLOCK ASSOCIATED 1 (CCA1) physically interacts with ATAF2 at the DNA–protein and protein–protein levels, and both differentially suppress BAS1- and SOB7-mediated BR catabolism. In this research, we show that ATAF2 can bind its own promoter as a transcriptional self-repressor. This self-feedback-suppression loop is a typical feature of multiple circadian-regulated genes. Additionally, ATAF2 and CCA1 synergistically suppress seedling photomorphogenesis as reflected by the light-dependent hypocotyl growth analysis of their single and double gene knock-out mutants. Similar fluence-rate response assays using ATAF2 and photoreceptor (PHYB, CRY1 and PHYA) knock-out mutants demonstrate that PHYA is required for ATAF2-regulated photomorphogenesis in a wide range of light intensities. Furthermore, disruption of PHYA can suppress the BR-insensitive hypocotyl-growth phenotype of ATAF2 loss-of-function seedlings in the light, but not in darkness. Collectively, our results provide a genetic interaction synopsis of the circadian-clock-photomorphogenesis-BR integration node involving ATAF2, CCA1 and PHYA.
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Abbreviations
- BL:
-
Brassinolide
- BR:
-
Brassinosteroid
- CBS:
-
CIRCADIAN CLOCK ASSOCIATED 1-binding site
- CCA1:
-
CIRCADIAN CLOCK ASSOCIATED 1
- CRY1:
-
Cryptochrome 1
- EMSA:
-
Electrophoretic mobility shift assay
- NAC:
-
NAM ATAF and CUC
- PHYA:
-
Phytochrome A
- PHYB:
-
Phytochrome B
- TF:
-
Transcription factor
- Y1H:
-
Yeast one-hybrid
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Acknowledgements
We thank Dr. James N. Culver (University of Maryland) for the pATAF2::GUS construct. This research was supported by the United States National Science Foundation project #1656265 (to MMN) and the USDA National Institute of Food and Agriculture, Hatch Umbrella Project #1015621 (to MMN).
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425_2020_3456_MOESM1_ESM.eps
Supplementary Fig. S1 Sucrose significantly promotes Arabidopsis seedling growth in red light. Col-0 and ATAF2ox-1 seedlings grown in low fluence rates of red light were no longer taller than their dark-grown counterparts in the absence of sucrose in the growth media. Three-day-old seedlings were used for the assay. Each data point represents the average of measurements from 30 seedlings (n = 30). Error bars denote the SE The significance of differences was determined by one-way ANOVA with Tukey’s HSD test. Groups with significant differences (P < 0.05) at a given fluence rate were labeled by different letters (EPS 1128 kb)
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Supplementary Fig. S2 Neither PHYB nor CRY1 is essential for ATAF2-regulated seedling photomorphogenesis. Fluence-rate (0–80 μmol m−2 s−1) response assays in white light were performed for phyB-9 versus phyB-9 ataf2-1 and cry1-103 versus cry1-103 ataf2-1. a phyB-9 ataf2-1 hypocotyls were shorter than those of phyB-9 even in the dark, and this short-hypocotyl phenotype was unchanged in low fluence rates (10 and 20 μmol m−2 s−1) of white light. b Similar trends were observed from hypocotyl growth comparisons between cry1-103 ataf2-1 and cry1-103 in the dark and most tested fluence rates (10–60 μmol m−2 s−1) of white light. Four-day-old seedlings were used for both fluence-rate response assays. Each data point represents the average of measurements from 30 seedlings (n = 30). Error bars denote the SE. Two-tailed Student’s t-test was used to determine the significance of differences at a given fluence rate. *P < 0.05, **P < 0.01, ***P < 0.001 (EPS 1234 kb)
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Supplementary Fig. S3 Neither PHYB nor CRY1 is involved in ATAF2-regulated BR homeostasis in the light. a phyB-9 ataf2-1 seedlings are less sensitive to exogenous BL treatment when compared to phyB-9. b cry1-103 ataf2-1 seedlings are less sensitive to exogenous BL treatment when compared to cry1-103 in absolute hypocotyl lengths. c cry1-103 ataf2-1 seedlings are less sensitive to exogenous BL treatment when compared to cry1-103 in relative hypocotyl length percent changes. Four-day-old seedlings were used for both BL response assays. Each data point represents the average of measurements from 30 seedlings (n = 30). Error bars denote the SE. Two-tailed Student’s t-test was used to determine the significance of differences at a given BL concentration. *P < 0.05, ***P < 0.001 (EPS 1316 kb)
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Peng, H., Phung, J., Zhai, Y. et al. Self-transcriptional repression of the Arabidopsis NAC transcription factor ATAF2 and its genetic interaction with phytochrome A in modulating seedling photomorphogenesis. Planta 252, 48 (2020). https://doi.org/10.1007/s00425-020-03456-5
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DOI: https://doi.org/10.1007/s00425-020-03456-5