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An autoregulatory feedback loop involving PAP1 and TAS4 in response to sugars in Arabidopsis

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Abstract

miR828 in Arabidopsis triggers the cleavage of Trans-Acting SiRNA Gene 4 (TAS4) transcripts and production of small interfering RNAs (ta-siRNAs). One siRNA, TAS4-siRNA81(−), targets a set of MYB transcription factors including PAP1, PAP2, and MYB113 which regulate the anthocyanin biosynthesis pathway. Interestingly, miR828 also targets MYB113, suggesting a close relationship between these MYBs, miR828, and TAS4, but their evolutionary origins are unknown. We found that PAP1, PAP2, and TAS4 expression is induced specifically by exogenous treatment with sucrose and glucose in seedlings. The induction is attenuated in abscisic acid (ABA) pathway mutants, especially in abi3-1 and abi5-1 for PAP1 or PAP2, while no such effect is observed for TAS4. PAP1 is under regulation by TAS4, demonstrated by the accumulation of PAP1 transcripts and anthocyanin in ta-siRNA biogenesis pathway mutants. TAS4-siR81(−) expression is induced by physiological concentrations of Suc and Glc and in pap1-D, an activation-tagged line, indicating a feedback regulatory loop exists between PAP1 and TAS4. Bioinformatic analysis revealed MIR828 homologues in dicots and gymnosperms, but only in one basal monocot, whereas TAS4 is only found in dicots. Consistent with this observation, PAP1, PAP2, and MYB113 dicot paralogs show peptide and nucleotide footprints for the TAS4-siR81(−) binding site, providing evidence for purifying selection in contrast to monocots. Extended sequence similarities between MIR828, MYBs, and TAS4 support an inverted duplication model for the evolution of MIR828 from an ancestral gymnosperm MYB gene and subsequent formation of TAS4 by duplication of the miR828* arm. We obtained evidence by modified 5′-RACE for a MYB mRNA cleavage product guided by miR828 in Pinus resinosa. Taken together, our results suggest that regulation of anthocyanin biosynthesis by TAS4 and miR828 in higher plants is evolutionarily significant and consistent with the evolution of TAS4 since the dicot—monocot divergence.

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Abbreviations

TAS :

Trans-Acting SiRNA Gene

miRNA:

microRNA

Suc:

Sucrose

Glc:

Glucose

PAP1:

Production of Anthocyanin Pigment1

qRT-PCR:

Quantitative real-time Polymerase Chain Reaction

ABA:

Abscisic acid

sRNA:

Small RNA

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Acknowledgments

The authors thank the Arabidopsis Biological Resource Center at Ohio State University for seeds, the greenhouse staff in the Department of Biological Sciences at Texas Tech University, Ruth Finkelstein for the abi4-103 mutant seeds, Zhixin Xie for the rdr6-15 and dcl4-2 mutant seeds, Xuemei Chen for the hen1-1 mutant seeds, and Hong-Liang Zhu for discussion and technical support. This work was supported by the National Institutes of Health (R21GM077245 to C.D.R.).

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  1. Qing-Jun Luo

    Present address: Department of Pediatrics, Stanford University, Stanford, CA, 94305-5208, USA

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  1. Department of Biological Sciences, Texas Tech University, Lubbock, TX, 79409-3131, USA

    Qing-Jun Luo, Amandeep Mittal, Fan Jia & Christopher D. Rock

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  1. Qing-Jun Luo
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Correspondence to Christopher D. Rock.

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11103_2011_9778_MOESM1_ESM.docx

Fig. S1. Predicted PAP1 cis-regulatory elements (C/T)(A/C)NCCACNN(G/T) in TAS4, MIR828 and PAP1 promoters. Putative promoter sequences for 2,000 bp upstream of the transcription start sites for TAS4, MIR828 and PAP1 (Panels A, B, and C, respectively) were extracted from the TAIR website (www.arabidopsis.org). TATA and CAAT boxes are predicted by the Plant Cis-acting Regulatory DNA Elements Database (PLACE) (Higo et al. 1999), and PAP1 cis-regulatory elements are found manually according to a consensus sequence functionally characterized as described (Dare et al. 2008). The cis-regulatory elements within the putative MIR828 promoter locate in the 3′-untranslated region (3′-UTR) of its upstream gene At4g27750. The annotation for color labels is as follows: white letters in uppercase with blue color background, stop codon; orange letters in uppercase, exon; red letters in lowercase, 3′-UTR; purple letters in lowercase, intron; black letters in lowercase, intergenic regions; white letters in lowercase with red color background, PAP1 cis-regulatory elements; green color, TATA box; yellow color, CAAT box. (DOCX 20 kb)

11103_2011_9778_MOESM2_ESM.tif

Fig. S2. Sequence alignments of MYB family members from dicot and monocot species. The full length cDNA sequences were aligned with T-Coffee and part of the alignments is shown. Panel A: alignment for sequences spanning miR828 complementary site. Panel B: alignment for sequences spanning TAS4-siR81(−) complementary site. Abbreviations correspond to species are listed as follows. Ath, Arabidopsis thaliana; Vvi, Vitis vinifera; Ghy, Gerbera hybrid cultivar; Iba, Ipomoea batatas; Fcy, Fagopyrum cymosum. (TIFF 221 kb)

11103_2011_9778_MOESM3_ESM.tif

Fig. S3. Alternate hairpin structures of the Picea glauca (spruce) pri-miR828 predicted by MFOLD, showing only one “good” DCL substrate per structure. Green color shows mature miR828; red and blue lines indicate putative alternate secondary structures for the same pri-miR828. (TIFF 156 kb)

11103_2011_9778_MOESM4_ESM.tif

Fig. S4. Predicted secondary structure of Euphorbia esula pri-miR828 by MFOLD. The predicted mature miR828 sequences are in green. (TIFF 136 kb)

11103_2011_9778_MOESM5_ESM.tif

Fig. S5. Predicted secondary structure of Pinus contorta pri-miR828 by MFOLD. The predicted mature miR828 sequences are in green. (TIFF 111 kb)

11103_2011_9778_MOESM6_ESM.tif

Fig. S6. Predicted secondary structure of Trillium camschatcense MIR828 gene by MFOLD. The predicted mature miR828 sequences are in green. (TIFF 99 kb)

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Luo, QJ., Mittal, A., Jia, F. et al. An autoregulatory feedback loop involving PAP1 and TAS4 in response to sugars in Arabidopsis. Plant Mol Biol 80, 117–129 (2012). https://doi.org/10.1007/s11103-011-9778-9

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