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ARF2 positively regulates flavonols and proanthocyanidins biosynthesis in Arabidopsis thaliana

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Abstract

Main conclusion

Auxin response factor 2 acts as a positive regulator to fine-tune the spatial and temporal accumulation of flavonoid compounds, mainly flavonols and proanthocyanidins in Arabidopsis.

Abstract

Auxin response factor (ARF) proteins are reported to involve in auxin-mediated regulation of flavonoid biosynthesis. However, the detailed regulation mechanism of ARF remains still unknown. Here, we provide genetic and molecular evidence that one of the twenty-three ARF members—ARF2—positively regulates flavonoid biosynthesis at multi-level in tissue-specific manner in Arabidopsis thaliana. Loss-of-function mutation of ARF2 led to significant reduction in flavonoid content (e.g., flavonols and proanthocyanidins) in the seedlings and seeds of the Arabidopsis arf2 mutants. Over-expression of ARF2 increased flavonols and proanthocyanidins content in Arabidopsis. Additionally, the changes of flavonoid content correlate well with the transcript abundance of several regulatory genes (e.g., MYB11, MYB12, MYB111, TT2, and GL3), and key biosynthetic genes (e.g., CHS, F3'H, FLS, ANS, ANR, TT12, TT19, and TT15), in the arf2 mutant and ARF2 over-expression lines. Transient transactivation assays with site-directed mutagenesis confirmed that ARF2 directly regulates the expression of MYB12 and FLS genes in the flavonol pathway and ANR in the proanthocyanidin pathway, and indirectly regulates MYB11 and MYB111 genes in the flavonol pathway, and ANS, TT12, TT19 and TT15 genes in the proanthocyanidin pathway. Further genetic results indicated that ARF2 acts upstream of MYB12 to regulate flavonol accumulation, and of TT2 to regulate proanthocyanidins accumulation. In particular, yeast two-hybrid assays revealed that ARF2 physically interacts with TT2, a master regulator of proanthocyanidins biosynthesis. Combined together, these results indicated that ARF2 functions as a positive regulator for the fine-tuned spatial and temporal regulation of flavonoids (mainly flavonols and proanthocyanidins) accumulation in Arabidopsis.

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taken from epidermis cell of transfected leaves 40–48 h after infiltration. Scale bars = 10 μm. c Seed phenotype of the tt2/arf2-8 double mutant lines relative to the single mutant tt2, arf2-8 and the wild type before (left) and after (right) DMACA staining. Bars = 0.5 mm. d Analysis of extractable and non-extractable proanthocyanidins levels in the seeds of the mutant tt2, arf2-8, tt2/arf2-8 and the wild type Arabidopsis. The extractable and non-extractable proanthocyanidins levels in wild type were set as value of 100%, respectively. Data are presented as mean ± SD, Student’s t test (n = 3, **P < 0.01)

Fig. 7

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Data availability

All data generated or analyzed during this study are included in this published article and its supplementary information files.

Abbreviations

ANR:

Anthocyanidin reductase

ANS:

Anthocyanidin synthase

ARFs:

Auxin response factors

AuxREs:

Auxin response elements

CHI:

Chalcone isomerase

CHS:

Chalcone synthase

DFR:

Dihydroflavonol-4-reductase

EGL3:

Enhancer of glabra 3

F3H:

Flavanone 3-hydroxylase

F3’H:

Flavanone 3′-hydroxylase

FLS:

Flavonol synthase

GL3:

Glabra 3

TT:

Transparent testa

TTG1:

Transparent testa glabra 1

TFs:

Transcription factors

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Acknowledgements

We appreciate Professor Zhizhong Gong (China Agricultural University, Beijing, China) for providing ARF2 over-expressing lines (OE-1 and OE-2), and Professor Lei Wang (Institute of Botany, Chinese Academy of Sciences, Beijing, China) for providing pBI-2YC-CAT and pBI-2YN-CAT vectors in the bi-molecular fluorescence complementation assays. This work was supported by the National Nature Science Foundation of China (31370335 and 31870281), and the Major State Basic Research and Development Program (2013CB127002).

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Authors and Affiliations

  1. Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing, 100193, China

    Wenbo Jiang, Yaying Xia, Xiaojia Su & Yongzhen Pang

  2. Key Laboratory of Plant Resources and Beijing Botanical Garden, Institute of Botany, Chinese Academy of Sciences, Beijing, 100093, China

    Yaying Xia & Xiaojia Su

  3. University of Chinese Academy of Sciences, Beijing, 100049, China

    Yaying Xia

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  1. Wenbo Jiang
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Jiang, W., Xia, Y., Su, X. et al. ARF2 positively regulates flavonols and proanthocyanidins biosynthesis in Arabidopsis thaliana. Planta 256, 44 (2022). https://doi.org/10.1007/s00425-022-03936-w

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