Abstract
Main conclusion
The foxtail millet NAC transcription factor NAC1, an ortholog of Arabidopsis NAP, is induced by ABA and senescence and accelerates leaf senescence by promoting ABA biosynthesis.
Leaf senescence, a unique developmental stage involving macromolecule degradation and nutrient remobilization, is finely tuned and tightly controlled by different gene families. NO APICAL MERISTEM, ARABIDOPSIS ATAF1, and CUP-SHAPED COTYLEDON (NAC) transcription factors have been demonstrated to be involved in the modulation of leaf senescence in many land plant species. Foxtail millet (Setaria italica L.), an important food and fodder crop, has been studied for its strong stress tolerance and potential to be a biofuel model plant. However, the functional roles of senescence-associated NACs in foxtail millet are still unknown. In this study, we characterized a nuclear localized NAC transcription factor, SiNAC1, which is induced by senescence and concentrated in senescent leaves in foxtail millet. SiNAC1 also positively responds to abscisic acid (ABA) treatment in foxtail millet. Moreover, SiNAC1 promotes the natural and dark-induced leaf senescence by an ABA-dependent manner in Arabidopsis thaliana. NCED2 and NCED3 are elevated by SiNAC1 overexpression, which subsequently promotes ABA biosynthesis in Arabidopsis. Finally, as a homolog of AtNAP, SiNAC1 can partially rescue the delayed leaf senescence phenotype in atnap mutants. Overall, our results demonstrate that SiNAC1 functions as a positive regulator of leaf senescence and is involved in a positive feedback loop via ABA biosynthesis and leaf senescence.
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Abbreviations
- AAO3:
-
ABSCISIC ALDEHYDE OXIDASE 3
- NAP:
-
NAC-LIKE, ACTIVATED BY AP3/PI
- NCED:
-
9-Cis-epoxycarotenoid dioxygenase
- SAGs:
-
Senescence-associated genes
- senTFs:
-
Senescence-associated transcriptional factors
- TRR:
-
Transcription regulatory region
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Acknowledgements
Arabidopsis T-DNA insertion mutants were provided by ABRC. Seeds of foxtail millet were obtained from Dr. Xianmin Diao (Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing, China). This work was supported by the grants from the National Science Foundation of China (Grant no. 31671694 to CZ, and Grant no. 31600227 to GW), the Natural Science Fund for Distinguished Young Scholars of Hebei Province (Grant no. 2014C2014205165), the Support Program for Hundreds of Outstanding Innovative Talents in Higher Education Institutions of Hebei Province (III) (Grant no. SLRC2017043) to CZ, and the Youth Foundation of Hebei Education Department (Grant no. QN2015215) to GW.
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425_2017_2770_MOESM1_ESM.pptx
Supplementary material 1 (PPTX 285 kb) Fig. S1 Amino acid analysis between AtNAP and five SiNACs. a Protein sequence alignment of AtNAP and five SiNACs using DNAMAN. b Model of five NAC sub-domain, nuclear localization sequence (NLS) and cis-elements in SiNAC1 coding sequence region and promoter region
425_2017_2770_MOESM2_ESM.pptx
Supplementary material 2 (PPTX 838 kb) Fig. S2 Phylogenetic analysis of SiNACs with other genes related to leaf senescence. The phylogenetic tree was constructed using MEGA based on the multiple alignments of 35 NAP protein sequences. Si, Setaria italic; Os, Oryza sativa; Ta, Triticum aestivum; Hv, Hordeum vulgare; Bd, Brachypodium distachyon; Zm, Zea mays; At, Arabidopsis thaliana
425_2017_2770_MOESM3_ESM.pptx
Supplementary material 3 (PPTX 604 kb) Fig. S3 Expression of SiNAC2, SiNAC3, SiNAC4, SiNAC5 in four developmental stages, different tissues and different senescing parts in one leaf in foxtail millet. Error bars indicate the ± SE. All experiments were repeated at least three times, with similar results
425_2017_2770_MOESM4_ESM.pptx
Supplementary material 4 (PPTX 16069 kb) Fig. S4 Subcellular localization and Transcriptional activation analysis of SiNAC2-SiNAC5. a Subcellular localization of SiNAC2-SiNAC5. Column 1 is the signal of GFP; column 2 is bright field of a same cell; columns 3 are overlaps in the same cell. Scale bars=20 μm. b Transcriptional activation analysis of SiNAC2-SiNAC5.All experiments were repeated at least three times, with similar results
425_2017_2770_MOESM5_ESM.pptx
Supplementary material 5 (PPTX 24760 kb) Fig. S5 Altered sensitivity of SiNAC1-OE plants in response to ABA at the germination and cotyledon greening stages compared with Col-0. Seeds of Col and SiNAC1 overexpression plants were sown on petri dishes with or without ABA. The concentration of ABA were 0.25 μM, 0.5 μM and 0.75 μM, respectively. a The different seed germination and cotyledon greening phenotype of Col and transgenic seedlings when incubation in growth chamber after 5 days. b Seed germination rate under different ABA concentration was calculated after vernalization. c Cotyledon greening rate was calculated from the 2nd day to the 7th day after vernalization. Error bars indicate the ± SE. All experiments were repeated at least three times, with similar results
425_2017_2770_MOESM6_ESM.pptx
Supplementary material 6 (PPTX 274 kb) Fig. S6 A model for the role of SiNAC1 in participating a positive feedback loop during leaf senescence. Under natural and dark condition, the onset of leaf senescence was induced by various hormones including ABA. When leaf senescence initiation, ABA biosynthesis and ABA signaling pathway were also activated, which further magnified the senescence signals. During this process, SiNAC1 was a senescence induced transcription factor which could also up-regulated by ABA. Moreover, SiNAC1 promoted expression of two key enzymes in ABA biosynthesis NCED2 and NCED3, which subsequently lead ABA accumulation. Therefore, SiNAC1 involved in a ternary positive feedback module and was response for mediating the leaf senescence signaling to ABA biosynthesis
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Ren, T., Wang, J., Zhao, M. et al. Involvement of NAC transcription factor SiNAC1 in a positive feedback loop via ABA biosynthesis and leaf senescence in foxtail millet. Planta 247, 53–68 (2018). https://doi.org/10.1007/s00425-017-2770-0
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DOI: https://doi.org/10.1007/s00425-017-2770-0