E3 ubiquitin ligases SINA4 and SINA11 regulate anthocyanin biosynthesis by targeting the IAA29-ARF5-1-ERF3 module in apple.

Publisher: John Wiley & Sons Ltd Country of Publication: United States NLM ID: 9309004 Publication Model: Print-Electronic Cited Medium: Internet ISSN: 1365-3040 (Electronic) Linking ISSN: 01407791 NLM ISO Abbreviation: Plant Cell Environ Subsets: MEDLINE

Publication: Hoboken, NJ : John Wiley & Sons Ltd.
Original Publication: Oxford, UK : Blackwell Scientific Publications

Ubiquitin-Protein Ligases*/genetics ; Ubiquitin-Protein Ligases*/metabolism ; Malus*/genetics ; Malus*/metabolism; Anthocyanins ; Indoleacetic Acids/metabolism ; Ethylenes ; Gene Expression Regulation, Plant ; Plant Proteins/genetics ; Plant Proteins/metabolism

Auxin/indole-3-acetic acid (AUX/IAA) and auxin response factor (ARF) proteins are important components of the auxin signalling pathway, but their ubiquitination modification and the mechanism of auxin-mediated anthocyanin biosynthesis remain elusive. Here, the ARF MdARF5-1 was identified as a negative regulator of anthocyanin biosynthesis in apple, and it integrates auxin and ethylene signals by inhibiting the expression of the ethylene response factor MdERF3. The auxin repressor MdIAA29 decreased the inhibitory effect of MdARF5-1 on anthocyanin biosynthesis by attenuating the transcriptional inhibition of MdERF3 by MdARF5-1. In addition, the E3 ubiquitin ligases MdSINA4 and MdSINA11 played negative and positive regulatory roles in anthocyanin biosynthesis by targeting MdIAA29 and MdARF5-1 for ubiquitination degradation, respectively. MdSINA4 destabilized MdSINA11 to regulate anthocyanin accumulation in response to auxin signalling. In sum, our data revealed the crosstalk between auxin and ethylene signals mediated by the IAA29-ARF5-1-ERF3 module and provide new insights into the ubiquitination modification of the auxin signalling pathway.
(© 2023 John Wiley & Sons Ltd.)

Albert, N.W., Davies, K.M., Lewis, D.H., Zhang, H., Montefiori, M., Brendolise, C. et al. (2014) A conserved network of transcriptional activators and repressors regulates anthocyanin pigmentation in eudicots. The Plant Cell, 26, 962-980.
Allan, A.C., Hellens, R.P. & Laing, W.A. (2008) MYB transcription factors that colour our fruit. Trends in Plant Science, 13, 99-102.
An, J.P., Song, L.Q., Zhao, L.L., You, C.X., Wang, X.F. & Hao, Y.J. (2018) Cloning and functional characterization of an auxin response factor gene MdARF5 in apple. Scientia Agricultura Sinica, 51, 1345-1352.
An, J.P., Wang, X.F., Li, Y.Y., Song, L.Q., Zhao, L.L., You, C.X. et al. (2018) EIN3-LIKE1, MYB1, and ETHYLENE RESPONSE FACTOR3 act in a regulatory loop that synergistically modulates ethylene biosynthesis and anthocyanin accumulation. Plant Physiology, 178, 808-823.
An, J.P., Zhang, C.L., Li, H.L., Wang, G.L. & You, C.X. (2022) Apple SINA E3 ligase MdSINA3 negatively mediates JA-triggered leaf senescence by ubiquitinating and degrading the MdBBX37 protein. The Plant Journal, 111, 457-472.
An, J.P., Zhang, X.W., Li, H.L., Wang, D.R., You, C.X. & Han, Y. (2023) The E3 ubiquitin ligases SINA1 and SINA2 integrate with the protein kinase CIPK20 to regulate the stability of RGL2a, a positive regulator of anthocyanin biosynthesis. New Phytologist, 239, 1332-1352.
An, J.P., Zhang, X.W., Liu, Y.J., Wang, X.F., You, C.X. & Hao, Y.J. (2021) ABI5 regulates ABA-induced anthocyanin biosynthesis by modulating the MYB1-bHLH3 complex in apple. Journal of Experimental Botany, 72, 1460-1472.
An, X.H., Tian, Y., Chen, K.Q., Wang, X.F. & Hao, Y.J. (2012) The apple WD40 protein MdTTG1 interacts with bHLH but not MYB proteins to regulate anthocyanin accumulation. Journal of Plant Physiology, 169, 710-717.
Ban, Y., Honda, C., Hatsuyama, Y., Igarashi, M., Bessho, H. & Moriguchi, T. (2007) Isolation and functional analysis of a MYB transcription factor gene that is a key regulator for the development of red coloration in apple skin. Plant & Cell Physiology, 48, 958-970.
Chandler, J.W. (2016) Auxin response factors. Plant, Cell & Environment, 39, 1014-1028.
Chen, H., Ma, B., Zhou, Y., He, S.J., Tang, S.Y., Lu, X. et al. (2018) E3 ubiquitin ligase SOR1 regulates ethylene response in rice root by modulating stability of Aux/IAA protein. Proceedings of the National Academy of Sciences, 115, 4513-4518.
Clough, S.J. & Bent, A.F. (1998) Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. The Plant Journal, 16, 735-743.
Deshaies, R.J. & Joazeiro, C.A.P. (2009) RING domain E3 ubiquitin ligases. Annual Review of Biochemistry, 78, 399-434.
Dreher, K.A., Brown, J., Saw, R.E. & Callis, J. (2006) The Arabidopsis Aux/IAA protein family has diversified in degradation and auxin responsiveness. The Plant Cell, 18, 699-714.
Duplan, V. & Rivas, S. (2014) E3 ubiquitin-ligases and their target proteins during the regulation of plant innate immunity. Frontiers in Plant Science, 5, 42.
Espley, R.V., Hellens, R.P., Putterill, J., Stevenson, D.E., Kutty-Amma, S. & Allan, A.C. (2007) Red colouration in apple fruit is due to the activity of the MYB transcription factor, MdMYB10. The Plant Journal, 49, 414-427.
Fan, Z.Q., Chen, J.Y., Kuang, J.F., Lu, W.J. & Shan, W. (2017) The banana fruit SINA ubiquitin ligase MaSINA1 regulates the stability of MaICE1 to be negatively involved in cold stress response. Frontiers in Plant Science, 8, 995.
Freire-Rios, A., Tanaka, K., Crespo, I., Van der Wijk, E., Sizentsova, Y., Levitsky, V. et al. (2020) Architecture of DNA elements mediating ARF transcription factor binding and auxin-responsive gene expression in Arabidopsis. Proceedings of the National Academy of Sciences, 117, 24557-24566.
Gao, Z., Li, Q., Li, J., Chen, Y., Luo, M., Li, H. et al. (2018) Characterization of the ABA receptor VlPYL1 that regulates anthocyanin accumulation in grape berry skin. Frontiers in Plant Science, 9, 592.
Ghanashyam, C. & Jain, M. (2009) Role of auxin-responsive genes in biotic stress responses. Plant Signaling & Behavior, 4, 846-848.
Gonzalez, A., Zhao, M., Leavitt, J.M. & Lloyd, A.M. (2008) Regulation of the anthocyanin biosynthetic pathway by the TTG1/bHLH/Myb transcriptional complex in Arabidopsis seedlings. The Plant Journal, 53, 814-827.
Gray, W.M., Kepinski, S., Rouse, D., Leyser, O. & Estelle, M. (2001) Auxin regulates SCFTIR1-dependent degradation of AUX/IAA proteins. Nature, 414, 271-276.
He, H. & Yamamuro, C. (2022) Interplays between auxin and GA signaling coordinate early fruit development. Horticulture Research, 9, uhab078.
Hill, K. (2015) Post-translational modifications of hormone-responsive transcription factors: the next level of regulation. Journal of Experimental Botany, 66, 4933-4945.
Hu, J., Su, H., Cao, H., Wei, H., Fu, X., Jiang, X. et al. (2022) AUXIN RESPONSE FACTOR7 integrates gibberellin and auxin signaling via interactions between DELLA and AUX/IAA proteins to regulate cambial activity in poplar. The Plant Cell, 34, 2688-2707.
Jaakola, L. (2013) New insights into the regulation of anthocyanin biosynthesis in fruits. Trends in Plant Science, 18, 477-483.
Jia, H., Xie, Z., Wang, C., Shangguan, L., Qian, N., Cui, M. et al. (2017) Abscisic acid, sucrose, and auxin coordinately regulate berry ripening process of the Fujiminori grape. Functional & Integrative Genomics, 17, 441-457.
Ji, X.H., Wang, Y.T., Zhang, R., Wu, S.J., An, M.M., Li, M. et al. (2015) Effect of auxin, cytokinin and nitrogen on anthocyanin biosynthesis in callus cultures of red-fleshed apple (Malus sieversii f. niedzwetzkyana). Plant Cell, Tissue and Organ Culture (PCTOC), 120, 325-337.
Ji, X.L., Li, H.L., Qiao, Z.W., Zhang, J.C., Sun, W.J., You, C.X. et al. (2022) The BTB protein MdBT2 recruits auxin signaling components to regulate adventitious root formation in apple. Plant Physiology, 189, 1005-1020.
Khaksar, G. & Sirikantaramas, S. (2020) Auxin response factor 2A is part of the regulatory network mediating fruit ripening through auxin-ethylene crosstalk in durian. Frontiers in Plant Science, 11, 543747.
Landi, M., Tattini, M. & Gould, K.S. (2015) Multiple functional roles of anthocyanins in plant-environment interactions. Environmental and Experimental Botany, 119, 4-17.
Lavy, M. & Estelle, M. (2016) Mechanisms of auxin signaling. Development, 143(18), 3226-3229.
Li, H.L., Wang, X., Ji, X.L., Qiao, Z.W., You, C.X. & Hao, Y.J. (2020) Genome-wide identification of apple ubiquitin SINA E3 ligase and functional characterization of MdSINA2. Frontiers in Plant Science, 11, 1109.
Li, L., Yang, G., Ren, M., Wang, Z., Peng, Y. & Xu, R. (2021) Co-regulation of auxin and cytokinin in anthocyanin accumulation during natural development of purple wheat grains. Journal of Plant Growth Regulation, 40, 1881-1893.
Li, S.B., Xie, Z.Z., Hu, C.G. & Zhang, J.Z. (2016) A review of auxin response factors (ARFs) in plants. Frontiers in Plant Science, 7, 47.
Liscum, E. & Reed, J.W. (2002) Genetics of Aux/IAA and ARF action in plant growth and development. Plant Molecular Biology, 49, 387-400.
Liu, N. (2019) Effects of IAA and ABA on the immature peach fruit development process. Horticultural Plant Journal, 5, 145-154.
Liu, Z., Shi, M.Z. & Xie, D.Y. (2014) Regulation of anthocyanin biosynthesis in Arabidopsis thaliana red pap1-D cells metabolically programmed by auxins. Planta, 239, 765-781.
Mazzucotelli, E., Belloni, S., Marone, D., De Leonardis, A., Guerra, D., Di Fonzo, N. et al. (2006) The E3 ubiquitin ligase gene family in plants: regulation by degradation. Current Genomics, 7, 509-522.
Miao, M., Niu, X., Kud, J., Du, X., Avila, J., Devarenne, T.P. et al. (2016) The ubiquitin ligase SEVEN IN ABSENTIA (SINA) ubiquitinates a defense-related NAC transcription factor and is involved in defense signaling. New Phytologist, 211, 138-148.
Moon, J., Parry, G. & Estelle, M. (2004) The ubiquitin-proteasome pathway and plant development. The Plant Cell, 16, 3181-3195.
Morreale, F.E. & Walden, H. (2016) Types of ubiquitin ligases. Cell, 165, 248.
Muday, G.K., Rahman, A. & Binder, B.M. (2012) Auxin and ethylene: collaborators or competitors? Trends in Plant Science, 17, 181-195.
Naing, A.H. & Kim, C.K. (2021) Abiotic stress-induced anthocyanins in plants: their role in tolerance to abiotic stresses. Physiologia Plantarum, 172, 1711-1723.
Ning, Y., Jantasuriyarat, C., Zhao, Q., Zhang, H., Chen, S., Liu, J. et al. (2011) The SINA E3 ligase OsDIS1 negatively regulates drought response in rice. Plant Physiology, 157, 242-255.
Orosa-Puente, B., Leftley, N., Von Wangenheim, D., Banda, J., Srivastava, A.K., Hill, K. et al. (2018) Root branching toward water involves posttranslational modification of transcription factor ARF7. Science, 362, 1407-1410.
Owens, D.K., Alerding, A.B., Crosby, K.C., Bandara, A.B., Westwood, J.H. & Winkel, B.S.J. (2008) Functional analysis of a predicted flavonol synthase gene family in Arabidopsis. Plant Physiology, 147, 1046-1061.
Pérez-Henríquez, P. & Yang, Z. (2023) Extranuclear auxin signaling: a new insight into auxin's versatility. New Phytologist, 237, 1115-1121.
Pernisová, M., Klíma, P., Horák, J., Válková, M., Malbeck, J., Souček, P. et al. (2009) Cytokinins modulate auxin-induced organogenesis in plants via regulation of the auxin efflux. Proceedings of the National Academy of Sciences, 106, 3609-3614.
Piya, S., Shrestha, S.K., Binder, B., Stewart Jr., C.N. & Hewezi, T. (2014) Protein-protein interaction and gene co-expression maps of ARFs and Aux/IAAs in Arabidopsis. Frontiers in Plant Science, 5, 744.
Powers, S.K. & Strader, L.C. (2020) Regulation of auxin transcriptional responses. Developmental Dynamics, 249, 483-495.
Qi, T., Song, S., Ren, Q., Wu, D., Huang, H., Chen, Y. et al. (2011) The Jasmonate-ZIM-domain proteins interact with the WD-Repeat/bHLH/MYB complexes to regulate jasmonate-mediated anthocyanin accumulation and trichome initiation in Arabidopsis thaliana. The Plant Cell, 23, 1795-1814.
Raspor, M., Motyka, V., Kaleri, A.R., Ninković, S., Tubić, L., Cingel, A. et al. (2021) Integrating the roles for cytokinin and auxin in de novo shoot organogenesis: from hormone uptake to signaling outputs. International Journal of Molecular Sciences, 22, 8554.
Salmon, J., Ramos, J. & Callis, J. (2008) Degradation of the auxin response factor ARF1. The Plant Journal, 54, 118-128.
Santner, A. & Estelle, M. (2010) The ubiquitin-proteasome system regulates plant hormone signaling. The Plant Journal, 61, 1029-1040.
dos Santos Maraschin, F., Memelink, J. & Offringa, R. (2009) Auxin-induced, SCFTIR1-mediated poly-ubiquitination marks AUX/IAA proteins for degradation. The Plant Journal, 59, 100-109.
Santos-Buelga, C., Mateus, N. & De Freitas, V. (2014) Anthocyanins. Plant pigments and beyond. Journal of Agricultural and Food Chemistry, 62, 6879-6884.
Sauer, M., Robert, S. & Kleine-Vehn, J. (2013) Auxin: simply complicated. Journal of Experimental Botany, 64, 2565-2577.
Shu, K. & Yang, W. (2017) E3 ubiquitin ligases: ubiquitous actors in plant development and abiotic stress responses. Plant and Cell Physiology, 58, 1461-1476.
Song, X., Xiong, Y., Kong, X. & Huang, G. (2023) Roles of auxin response factors in rice development and stress responses. Plant, Cell & Environment, 46, 1075-1086.
Sun, L. & Chen, Z.J. (2004) The novel functions of ubiquitination in signaling. Current Opinion in Cell Biology, 16, 119-126.
Sun, T., Liu, Z. & Yang, Q. (2020) The role of ubiquitination and deubiquitination in cancer metabolism. Molecular Cancer, 19, 146.
Suzuki, M., Kao, C.Y., Cocciolone, S. & McCarty, D.R. (2001) Maize VP1 complements Arabidopsisabi3 and confers a novel ABA/auxin interaction in roots. The Plant Journal, 28, 409-418.
Takos, A.M., Jaffé, F.W., Jacob, S.R., Bogs, J., Robinson, S.P. & Walker, A.R. (2006) Light-induced expression of a MYB gene regulates anthocyanin biosynthesis in red apples. Plant Physiology, 142, 1216-1232.
Tanimoto, E. (2005) Regulation of root growth by plant hormones-roles for auxin and gibberellin. Critical Reviews in Plant Sciences, 24, 249-265.
Tan, S., Luschnig, C. & Friml, J. (2021) Pho-view of auxin: reversible protein phosphorylation in auxin biosynthesis, transport and signaling. Molecular Plant, 14, 151-165.
Tian, H., Lv, B., Ding, T., Bai, M. & Ding, Z. (2018) Auxin-BR interaction regulates plant growth and development. Frontiers in Plant Science, 8, 2256.
Tiwari, S.B., Wang, X.J., Hagen, G. & Guilfoyle, T.J. (2001) AUX/IAA proteins are active repressors, and their stability and activity are modulated by auxin. The Plant Cell, 13, 2809-2822.
Trenner, J., Poeschl, Y., Grau, J., Gogol-Döring, A., Quint, M. & Delker, C. (2017) Auxin-induced expression divergence between Arabidopsis species may originate within the TIR1/AFB-AUX/IAA-ARF module. Journal of Experimental Botany, 68, 539-552.
Trujillo, M. & Shirasu, K. (2010) Ubiquitination in plant immunity. Current Opinion in Plant Biology, 13, 402-408.
Wang, C.K., Han, P.L., Zhao, Y.W., Ji, X.L., Yu, J.Q., You, C.X. et al. (2020) Auxin regulates anthocyanin biosynthesis through the auxin repressor protein MdIAA26. Biochemical and Biophysical Research Communications, 533, 717-722.
Wang, C.K., Han, P.L., Zhao, Y.W., Yu, J.Q., You, C.X., Hu, D.G. et al. (2021) Genome-wide analysis of auxin response factor (ARF) genes and functional identification of MdARF2 reveals the involvement in the regulation of anthocyanin accumulation in apple. New Zealand Journal of Crop and Horticultural Science, 49, 78-91.
Wang, D., Pajerowska-Mukhtar, K., Culler, A.H. & Dong, X. (2007) Salicylic acid inhibits pathogen growth in plants through repression of the auxin signaling pathway. Current Biology, 17, 1784-1790.
Wang, L., Yang, S., Ni, J., Teng, Y. & Bai, S. (2023) Advances of anthocyanin synthesis regulated by plant growth regulators in fruit trees. Scientia Horticulturae, 307, 111476.
Wang, S., Li, L.X., Zhang, Z., Fang, Y., Li, D., Chen, X.S. et al. (2022) Ethylene precisely regulates anthocyanin synthesis in apple via a module comprising MdEIL1, MdMYB1, and MdMYB17. Horticulture Research, 9, uhac034.
Wang, Y., Wang, N., Xu, H., Jiang, S., Fang, H., Su, M. et al. (2018) Auxin regulates anthocyanin biosynthesis through the Aux/IAA-ARF signaling pathway in apple. Horticulture Research, 5, 59.
Weijers, D., Benkova, E., Jäger, K.E., Schlereth, A., Hamann, T., Kientz, M. et al. (2005) Developmental specificity of auxin response by pairs of ARF and Aux/IAA transcriptional regulators. The EMBO Journal, 24, 1874-1885.
Wen, R., Wang, S., Xiang, D., Venglat, P., Shi, X., Zang, Y. et al. (2014) UBC 13, an E2 enzyme for L ys63-linked ubiquitination, functions in root development by affecting auxin signaling and Aux/IAA protein stability. The Plant Journal, 80, 424-436.
Xie, Q., Guo, H.S., Dallman, G., Fang, S., Weissman, A.M. & Chua, N.H. (2002) SINAT5 promotes ubiquitin-related degradation of NAC1 to attenuate auxin signals. Nature, 419, 167-170.
Xie, X.B., Li, S., Zhang, R.F., Zhao, J., Chen, Y.C., Zhao, Q. et al. (2012) The bHLH transcription factor MdbHLH3 promotes anthocyanin accumulation and fruit colouration in response to low temperature in apples. Plant, Cell & Environment, 35, 1884-1897.
Xie, Y., Tan, H., Ma, Z. & Huang, J. (2016) DELLA proteins promote anthocyanin biosynthesis via sequestering MYBL2 and JAZ suppressors of the MYB/bHLH/WD40 complex in Arabidopsis thaliana. Molecular Plant, 9, 711-721.
Xu, F.Q. & Xue, H.W. (2019) The ubiquitin-proteasome system in plant responses to environments. Plant, Cell & Environment, 42, 2931-2944.
Xu, P., Zhao, P.X., Cai, X.T., Mao, J.L., Miao, Z.Q. & Xiang, C.B. (2020) Integration of jasmonic acid and ethylene into auxin signaling in root development. Frontiers in Plant Science, 11, 271.
Yang, M., Li, C., Cai, Z., Hu, Y., Nolan, T., Yu, F. et al. (2017) SINAT E3 ligases control the light-mediated stability of the brassinosteroid-activated transcription factor BES1 in Arabidopsis. Developmental Cell, 41, 47-58.e4.
Yao, G., Ming, M., Allan, A.C., Gu, C., Li, L., Wu, X. et al. (2017) Map-based cloning of the pear gene MYB114 identifies an interaction with other transcription factors to coordinately regulate fruit anthocyanin biosynthesis. The Plant Journal, 92, 437-451.
Yue, P., Lu, Q., Liu, Z., Lv, T., Li, X., Bu, H. et al. (2020) Auxin-activated MdARF5 induces the expression of ethylene biosynthetic genes to initiate apple fruit ripening. New Phytologist, 226, 1781-1795.
Yu, Z., Zhang, F., Friml, J. & Ding, Z. (2022) Auxin signaling: research advances over the past 30 years. Journal of Integrative Plant Biology, 64, 371-392.
Zemlyanskaya, E.V., Omelyanchuk, N.A., Ubogoeva, E.V. & Mironova, V.V. (2018) Deciphering auxin-ethylene crosstalk at a systems level. International Journal of Molecular Sciences, 19, 4060.
Zhang, C., Hao, Z., Ning, Y. & Wang, G.L. (2019) SINA E3 ubiquitin ligases: versatile moderators of plant growth and stress response. Molecular Plant, 12, 610-612.
Zhang, T., Li, W., Xie, R., Xu, L., Zhou, Y., Li, H. et al. (2020) CpARF2 and CpEIL1 interact to mediate auxin-ethylene interaction and regulate fruit ripening in papaya. The Plant Journal, 103, 1318-1337.
Zhang, X., Wang, B., Zhao, Y., Zhang, J. & Li, Z. (2019) Auxin and GA signaling play important roles in the maize response to phosphate deficiency. Plant Science, 283, 177-188.
Zhang, Y. (2003) Transcriptional regulation by histone ubiquitination and deubiquitination. Genes & Development, 17, 2733-2740.
Zhang, Y., Butelli, E. & Martin, C. (2014) Engineering anthocyanin biosynthesis in plants. Current Opinion in Plant Biology, 19, 81-90.
Zhao, Y., Xing, L., Wang, X., Hou, Y.J., Gao, J., Wang, P. et al. (2014) The ABA receptor PYL8 promotes lateral root growth by enhancing MYB77-dependent transcription of auxin-responsive genes. Science Signaling, 7, ra53.

ZR2022YQ24 Natural Science Foundation of Shandong Province; 2022KJ326 Development Plan of the Youth Innovation Team of the Higher Education Institutions in Shandong Province; E3559901 Wuhan Botanical Garden Scientific Research Support Project

Keywords: ARF; AUX/IAA; auxin; ubiquitination modification

EC 2.3.2.27 (Ubiquitin-Protein Ligases)
0 (Anthocyanins)
0 (Indoleacetic Acids)
91GW059KN7 (ethylene)
0 (Ethylenes)
0 (Plant Proteins)

Date Created: 20230902 Date Completed: 20231103 Latest Revision: 20231103

20231103

10.1111/pce.14709

37658649