Abstract
Main Conclusion
PlARF2 can positively regulate the seed dormancy in Paeonia lactiflora Pall. and bind the RY cis-element.
Abstract
Auxin, a significant phytohormone influencing seed dormancy, has been demonstrated to be regulated by auxin response factors (ARFs), key transcriptional modulators in the auxin signaling pathway. However, the role of this class of transcription factors (TFs) in perennials with complex seed dormancy mechanisms remains largely unexplored. Here, we cloned and characterized an ARF gene from Paeonia lactiflora, named PlARF2, which exhibited differential expression levels in the seeds during the process of seed dormancy release. The deduced amino acid sequence of PlARF2 had high homology with those of other plants and contained typical conserved Auxin_resp domain of the ARF family. Phylogenetic analysis revealed that PlARF2 was closely related to VvARF3 in Vitis vinifera. The subcellular localization and transcriptional activation assay showed that PlARF2 is a nuclear protein possessing transcriptional activation activity. The expression levels of dormancy-related genes in transgenic callus indicated that PlARF2 was positively correlated with the contents of PlABI3 and PlDOG1. The germination assay showed that PlARF2 promoted seed dormancy. Moreover, TF Centered Yeast one-hybrid assay (TF-Centered Y1H), electrophoretic mobility shift assay (EMSA) and dual-luciferase reporter assay analysis (Dual-Luciferase) provided evidence that PlARF2 can bind to the ‘CATGCATG’ motif. Collectively, our findings suggest that PlARF2, as TF, could be involved in the regulation of seed dormancy and may act as a repressor of germination.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Data availability
The data that support the results are included in this article. Other relevant materials are available from the corresponding author upon reasonable request.
Abbreviations
- ARF:
-
Auxin response factor
- CDS:
-
Coding sequence
- FC:
-
Functional complementary
- TF:
-
Transcription factor
- Y1H:
-
Yeast one-hybrid assay
References
Baud S, Kelemen Z, Thevenin J, Boulard C, Blanchet S, To A, Payre M, Berger N, Effroy-Cuzzi D, Franco-Zorrilla JM, Godoy M, Solano R, Thevenon E, Parcy F, Lepiniec L, Dubreucq B (2016) Deciphering the molecular mechanisms underpinning the transcriptional control of gene expression by master transcriptional regulators in Arabidopsis seed. Plant Physiol 171:1099–1112. https://doi.org/10.1104/pp.16.00034
Bewley JD, Black M (1994) Seeds: Physiology of development and germination, 2nd edn. Springer, Boston
Chen N, Wang H, Abdelmageed H, Veerappan V, Tadege M, Allen RD (2020) HSI2/VAL1 and HSL1/VAL2 function redundantly to repress DOG1 expression in Arabidopsis seeds and seedlings. New Phytol 227:840–856. https://doi.org/10.1111/nph.16559
Chen X, He S, Jiang L, Li X, Guo W, Chen B, Zhou J, Skliar V (2021) An efficient transient transformation system for gene function studies in pumpkin (Cucurbita moschata D.). Sci Hortic. https://doi.org/10.1016/j.scienta.2021.110028
Cherenkov P, Novikova D, Omelyanchuk N, Levitsky V, Grosse I, Weijers D, Mironova V (2018) Diversity of cis-regulatory elements associated with auxin response in Arabidopsis thaliana. J Exp Bot 69:329–339. https://doi.org/10.1093/jxb/erx254
Duan S, Xin R, Guan S, Li X, Fei R, Cheng W, Pan Q, Sun X (2022) Optimization of callus induction and proliferation of Paeonia lactiflora Pall. and Agrobacterium-mediated genetic transformation. Front Plant Sci 13:996690. https://doi.org/10.3389/fpls.2022.996690
Ellis CM, Nagpal P, Young JC, Hagen G, Guilfoyle TJ, Reed JW (2005) Auxin response factor1 and auxin response factor2 regulate senescence and floral organ abscission in Arabidopsis thaliana. Development 132:4563–4574. https://doi.org/10.1242/dev.02012
Fei R, Guan S, Duan S, Ge J, Sun T, Sun X (2023) Elucidating biological functions of 9-cis-epoxycarotenoid dioxygenase genes involved in seed dormancy in Paeonia lactiflora. Plants-Basel 12(4):710. https://doi.org/10.3390/plants12040710
Freire-Rios A, Tanaka K, Crespo I, van der Wijk E, Sizentsova Y, Levitsky V, Lindhoud S, Fontana M, Hohlbein J, Boer DR, Mironova V, Weijers D (2020) Architecture of DNA elements mediating ARF transcription factor binding and auxin-responsive gene expression in Arabidopsis. Proc Natl Acad Sci USA 117:24557–24566. https://doi.org/10.1073/pnas.2009554117
Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe WJJ (2012) Molecular mechanisms of seed dormancy. Plant Cell Environ 35:1769–1786. https://doi.org/10.1111/j.1365-3040.2012.02542.x
Guerriero G, Martin N, Golovko A, Sundstrom JF, Rask L, Ezcurra I (2009) The RY/Sph element mediates transcriptional repression of maturation genes from late maturation to early seedling growth. New Phytol 184:552–565. https://doi.org/10.1111/j.1469-8137.2009.02977.x
Guilfoyle TJ, Hagen G (2007) Auxin response factors. Curr Opin Plant Biol 10:453–460. https://doi.org/10.1016/j.pbi.2007.08.014
Hardtke CS, Berleth T (1998) The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J 17:1405–1411. https://doi.org/10.1093/emboj/17.5.1405
Hussain S, Kim SH, Bahk S, Ali A, Nguyen XC, Yun DJ, Chung WS (2020) The auxin signaling repressor IAA8 promotes seed germination through down-regulation of ABI3 transcription in Arabidopsis. Front Plant Sci 11:111. https://doi.org/10.3389/fpls.2020.00111
Israeli A, Reed JW, Ori N (2020) Genetic dissection of the auxin response network. Nature Plants 6:1082–1090. https://doi.org/10.1038/s41477-020-0739-7
Ji X, Wang L, Nie X, He L, Zang D, Liu Y, Zhang B, Wang Y (2014) A novel method to identify the DNA motifs recognized by a defined transcription factor. Plant Mol Biol 86:367–380. https://doi.org/10.1007/s11103-014-0234-5
Jia HY, Suzuki M, McCarty DR (2014) Regulation of the seed to seedling developmental phase transition by the LAFL and VAL transcription factor networks. Wires Dev Biol 3:135–145. https://doi.org/10.1002/wdev.126
Kalluri UC, Difazio SP, Brunner AM, Tuskan GA (2007) Genome-wide analysis of Aux/IAA and ARF gene families in Populus trichocarpa. BMC Plant Biol 7:59. https://doi.org/10.1186/1471-2229-7-59
Kieffer M, Neve J, Kepinski S (2010) Defining auxin response contexts in plant development. Curr Opin Plant Biol 13:12–20. https://doi.org/10.1016/j.pbi.2009.10.006
Kumar R, Tyagi AK, Sharma AK (2011) Genome-wide analysis of auxin response factor (ARF) gene family from tomato and analysis of their role in flower and fruit development. Mol Genet Genom 285:245–260. https://doi.org/10.1007/s00438-011-0602-7
Lee YI, Chen MC, Lin L, Chung MC, Leu WM (2018) Increased expression of 9-cis-epoxycarotenoid dioxygenase, PtNCED1, associated with inhibited seed germination in a terrestrial orchid, Phaius tankervillae. Front Plant Sci 9:1043. https://doi.org/10.3389/fpls.2018.01043
Li HF, Ran K, Sun QR (2016a) Genome-wide identification and expression analysis of peach auxin response factor gene families. J Plant Biochem Biotechnol 25:349–357. https://doi.org/10.1007/s13562-015-0346-2
Li ZH, Zhang J, Liu YL, Zhao JH, Fu JJ, Ren XL, Wang GY, Wang JH (2016b) Exogenous auxin regulates multi-metabolic network and embryo development, controlling seed secondary dormancy and germination in Nicotiana tabacum L. BMC Plant Biol 16:41. https://doi.org/10.1186/s12870-016-0724-5
Li YH, Han SQL, Qi YH (2022) Advances in structure and function of auxin response factor in plants. J Integr Plant Biol 65:617–632. https://doi.org/10.1111/jipb.13392
Liu X, Zhang H, Zhao Y, Feng Z, Li Q, Yang HQ, Luan S, Li J, He ZH (2013) Auxin controls seed dormancy through stimulation of abscisic acid signaling by inducing ARF-mediated ABI3 activation in Arabidopsis. Proc Natl Acad Sci US A 110:15485–15490. https://doi.org/10.1073/pnas.1304651110
Luo P, Di DW, Wu L, Yang JW, Lu YF, Shi WM (2022) MicroRNAs are involved in regulating plant development and stress response through fine-tuning of TIR1/AFB-dependent auxin signaling. Int J Mol Sci 23:510. https://doi.org/10.3390/ijms23010510
Ma YL, Cui JQ, Lu XJ, Zhang LJ, Chen ZJ, Fei RW, Sun XM (2017) Transcriptome analysis of two different developmental stages of Paeonia lactiflora seeds. Int J Genom 2017:8027626. https://doi.org/10.1155/2017/8027626
Marchler-Bauer A, Bo Y, Han LY, He JE, Lanczycki CJ, Lu SN et al (2017) CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res 45:D200–D203. https://doi.org/10.1093/nar/gkw1129
Matilla AJ (2020) Auxin: hormonal signal required for seed development and dormancy. Plants-Basel 9(6):705. https://doi.org/10.3390/plants9060705
Mei M, Ai W, Liu L, Xu X, Lu X (2022) Genome-wide identification of the auxin response factor (ARF) gene family in Magnolia sieboldii and functional analysis of MsARF5. Front Plant Sci 13:958816. https://doi.org/10.3389/fpls.2022.958816
Meng YJ, Shuai HW, Luo XF, Chen F, Zhou WG, Yang WY, Shu K (2017) Karrikins: regulators involved in phytohormone signaling networks during seed germination and seedling development. Front Plant Sci 7:2021. https://doi.org/10.3389/fpls.2016.02021
Nanao MH, Vinos-Poyo T, Brunoud G, Thevenon E, Mazzoleni M, Mast D et al (2014) Structural basis for oligomerization of auxin transcriptional regulators. Nature Commun 5:3617. https://doi.org/10.1038/ncomms4617
Okushima Y, Mitina I, Quach HL, Theologis A (2005a) Auxin response Factor 2 (ARF2): a pleiotropic developmental regulator. Plant J 43:29–46. https://doi.org/10.1111/j.1365-313X.2005.02426.x
Okushima Y, Overvoorde PJ, Arima K, Alonso JM, Chan A, Chang C, Ecker JR, Hughes B, Lui A, Nguyen D, Onodera C, Quach H, Smith A, Yu G, Theologis A (2005b) Functional genomic analysis of the Auxin Response Factor gene family members in Arabidopsis thaliana: unique and overlapping functions of ARF7 and ARF19. Plant Cell 17:444–463. https://doi.org/10.1105/tpc.104.028316
Pekker I, Alvarez JP, Eshed Y (2005) Auxin response factors mediate Arabidopsis organ asymmetry via modulation of KANADI activity. Plant Cell 17:2899–2910. https://doi.org/10.1105/tpc.105.034876
Ramaih S, Guedira M, Paulsen GM (2003) Relationship of indoleacetic acid and tryptophan to dormancy and preharvest sprouting of wheat. Funct Plant Biol 30:939–945. https://doi.org/10.1071/fp03113
Rena Z, Liu R, Gu W, Dong X (2017) The Solanum lycopersicum auxin response factor SlARF2 participates in regulating lateral root formation and flower organ senescence. Plant Sci 256:103–111. https://doi.org/10.1016/j.plantsci.2016.12.008
Roosjen M, Paque S, Weijers D (2018) Auxin response factors: output control in auxin biology. J Exp Bot 69:179–188. https://doi.org/10.1093/jxb/erx237
Rousselin P, Kraepiel Y, Maldiney R, Miginiac E, Caboche M (1992) Characterization of three hormone mutants of Nicotiana plumbaginifolia: evidence for a common ABA deficiency. Theor Applied Genetics 85:213–221. https://doi.org/10.1007/bf00222862
Sasnauskas G, Kauneckaite K, Siksnys V (2018) Structural basis of DNA target recognition by the B3 domain of Arabidopsis epigenome reader VAL1. Nucleic Acids Res 46:4316–4324. https://doi.org/10.1093/nar/gky256
Schmitz RJ, Grotewold E, Stam M (2022) Cis-regulatory sequences in plants: their importance, discovery, and future challenges. Plant Cell 34:718–741. https://doi.org/10.1093/plcell/koab281
Shen MM, Tang ZJ, da Silva JAT, Yu XN (2015) Induction and proliferation of axillary shoots from in vitro culture of Paeonia lactiflora Pall. mature zygotic embryos. N Z J Crop Hortic Sci 43:42–52. https://doi.org/10.1080/01140671.2014.944548
Shi X, He Y, Wang R, Wang Z, Liu Z, Gao C, Wang Y (2022) Tamarix hispida ThEIL1 improves salt tolerance by adjusting osmotic potential and increasing reactive oxygen species scavenging capability. Environ Exp Bot. https://doi.org/10.1016/j.envexpbot.2021.104707
Shu K, Liu XD, Xie Q, He ZH (2016) Two faces of one seed: hormonal regulation of dormancy and germination. Mol Plant 9:34–45. https://doi.org/10.1016/j.molp.2015.08.010
Shuai HW, Meng YJ, Luo XF, Chen F, Zhou WG, Dai YJ, Qi Y, Du JB, Yang F, Liu J, Yang WY, Shu K (2017) Exogenous auxin represses soybean seed germination through decreasing the gibberellin/abscisic acid (GA/ABA) ratio. Sci Rep 7:12620. https://doi.org/10.1038/s41598-017-13093-w
Simonini S, Mas PJ, Mas C, Ostergaard L, Hart DJ (2018) Auxin sensing is a property of an unstructured domain in the auxin response factor ETTIN of Arabidopsis thaliana. Sci Rep 8:13563. https://doi.org/10.1038/s41598-018-31634-9
Tiwari SB, Hagen G, Guilfoyle T (2003) The roles of auxin response factor domains in auxin-responsive transcription. Plant Cell 15:533–543. https://doi.org/10.1105/tpc.008417
Truskina J, Han J, Chrysanthou E, Galvan-Ampudia CS, Laine S, Brunoud G et al (2021) A network of transcriptional repressors modulates auxin responses. Nature 589:116–119. https://doi.org/10.1038/s41586-020-2940-2
Varaud E, Brioudes F, Szecsi J, Leroux J, Brown S, Perrot-Rechenmann C, Bendahmane M (2011) Auxin response factor8 regulates Arabidopsis petal growth by interacting with the bHLH transcription factor BIGPETALp. Plant Cell 23:973–983. https://doi.org/10.1105/tpc.110.081653
Wang S, Tiwari SB, Hagen G, Guilfoyle TJ (2005) AUXIN RESPONSE FACTOR7 restores the expression of auxin-responsive genes in mutant Arabidopsis leaf mesophyll protoplasts. Plant Cell 17:1979–1993. https://doi.org/10.1105/tpc.105.031096
Wang D, Pei K, Fu Y, Sun Z, Li S, Liu H, Tang K, Han B, Tao Y (2007) Genome-wide analysis of the auxin response factors (ARF) gene family in rice (Oryza sativa). Gene 394:13–24. https://doi.org/10.1016/j.gene.2007.01.006
Wang L, Hua DP, He JN, Duan Y, Chen ZZ, Hong XH, Gong ZZ (2011) Auxin response factor2 (ARF2) and its regulated homeodomain gene HB33 mediate abscisic acid response in Arabidopsis. PLoS Genet 7:e1002172. https://doi.org/10.1371/journal.pgen.1002172
Wang Z, Chen F, Li X, Cao H, Ding M, Zhang C, Zuo J, Xu C, Xu J, Deng X, Xiang Y, Soppe WJJ, Liu Y (2016) Arabidopsis seed germination speed is controlled by SNL histone deacetylase-binding factor-mediated regulation of AUX1. Nature Commun 7:13412. https://doi.org/10.1038/ncomms13412
Wang SX, Shi FY, Dong XX, Li YX, Zhang ZH, Li H (2019) Genome-wide identification and expression analysis of auxin response factor (ARF) gene family in strawberry (Fragaria vesca). J Integr Agric 18:1587–1603. https://doi.org/10.1016/s2095-3119(19)62556-6
Weitbrecht K, Müller K, Leubner-Metzger G (2011) First off the mark: early seed germination. J Exp Bot 62:3289–3309. https://doi.org/10.1093/jxb/err030
Whiteside ST, Goodbourn S (1993) Signal transduction and nuclear targeting: regulation of transcription factor activity by subcellular localisation. J Cell Sci 104(4):949–955. https://doi.org/10.1242/jcs.104.4.949
Wu B, Li YH, Wu JY, Chen QZ, Huang X, Chen YF, Huang XL (2011) Over-expression of mango (Mangifera indica L.) MiARF2 inhibits root and hypocotyl growth of Arabidopsis. Mol Biol Rep 38:3189–3194. https://doi.org/10.1007/s11033-010-9990-8
Xing HY, Pudake RN, Guo GG, Xing GF, Hu ZR, Zhang YR, Sun QX, Ni ZF (2011) Genome-wide identification and expression profiling of auxin response factor (ARF) gene family in maize. BMC Genom 12:178. https://doi.org/10.1186/1471-2164-12-178
Yang J, Tian L, Sun MX, Huang XY, Zhu J, Guan YF, Jia QS, Yang ZN (2013) AUXIN RESPONSE FACTOR17 is essential for pollen wall pattern formation in Arabidopsis. Plant Physiol 162:720–731. https://doi.org/10.1104/pp.113.214940
Yu ZP, Zhang F, Friml J, Ding ZJ (2022) Auxin signaling: research advances over the past 30 years. J Integr Plant Biol 64:371–392. https://doi.org/10.1111/jipb.13225
Yuan Y, Xu X, Gong Z, Tang Y, Wu M, Yan F, Zhang X, Zhang Q, Yang F, Hu X, Yang Q, Luo Y, Mei L, Zhang W, Jiang C-Z, Lu W, Li Z, Deng W (2019) Auxin response factor 6A regulates photosynthesis, sugar accumulation, and fruit development in tomato. Hortic Res 6:85. https://doi.org/10.1038/s41438-019-0167-x
Zhang K, Yao L, Zhang Y, Baskin JM, Baskin CC, Xiong Z, Tao J (2019) A review of the seed biology of Paeonia species (Paeoniaceae), with particular reference to dormancy and germination. Planta 249:291–303. https://doi.org/10.1007/s00425-018-3017-4
Zhang RL, Wang XB, Shi XH, Shao LM, Xu T, Xia YP, Li DQ, Zhang JP (2021) Chilling requirement validation and physiological and molecular responses of the bud endodormancy release in Paeonia lactiflora ‘Meiju.’ Int J Mol Sci 22:8382. https://doi.org/10.3390/ijms22168382
Zhao D, Tao J, Han C, Ge J (2012) An actin gene as the internal control for gene expression analysis in herbaceous peony (Paeonia lactiflora Pall.). Afr J Agric Res 7:2153–2159. https://doi.org/10.5897/AJAR11.1613
Zhao Y (2018) Essential roles of local auxin biosynthesis in plant development and in adaptation to environmental changes. Annu Rev Plant Biol 69:417–435
Acknowledgements
This work was supported by the National Natural Science Foundation of China (32071814 and 31470696).
Author information
Authors and Affiliations
Contributions
SD was responsible for the experimental design of the study, the operation of all experiments, data analysis, and manuscript writing. SG was responsible for the review and revision of manuscripts. RF was involved in PlARF cloning, bioinformatics analysis, subcellular localization plant transformation, and data analysis. XK and TS were involved in protein purification, EMSA, and data analysis. RX and WS were involved in plant transformation and data analysis. XS was responsible for project direction, financial support, and manuscript review and revision. All the authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interests regarding the publication of this article.
Additional information
Communicated by Dorothea Bartels.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Duan, S., Guan, S., Fei, R. et al. Unraveling the role of PlARF2 in regulating deed formancy in Paeonia lactiflora. Planta 259, 133 (2024). https://doi.org/10.1007/s00425-024-04411-4
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-024-04411-4