Transcription factor ABF3 modulates salinity stress-enhanced jasmonate signaling in Arabidopsis

doi:10.1016/j.pld.2024.05.003

Abstract

Abstract: Salinity is a severe abiotic stress that affects plant growth and yield. Salinity stress activates jasmonate (JA) signaling in Arabidopsis thaliana, but the underlying molecular mechanism remains to be elucidated. In this study, we confirmed the activation of JA signaling under saline conditions and demonstrated the importance of the CORONATINE INSENSITIVE1 (COI1)-mediated JA signaling for this process. Phenotypic analyses reflected the negative regulation of JASMONATE ZIM-DOMAIN (JAZ) repressors during salinity stress-enhanced JA signaling. Mechanistic analyses revealed that JAZ proteins physically interact with ABSCISIC ACID-RESPONSIVE ELEMENT BINDING FACTOR1 (ABF1), AREB1/ABF2, ABF3, and AREB2/ABF4, which belong to the basic leucine zipper (bZIP) transcription factor family and respond to salinity stress. Analyses on the ABF3 overexpression plants and ABF mutants indicated the positive role of ABF3 in regulating JA signaling under saline condition. Furthermore, ABF3 overexpression partially recovered the JA-related phenotypes of JAZ1-Δ3A plants. Moreover, ABF3 was observed to indirectly activate ALLENE OXIDE SYNTHASE (AOS) transcription, but this activation was inhibited by JAZ1. In addition, ABF3 competitively bind to JAZ1, thereby decreasing the interaction between JAZ1 and MYC2, which is the master transcription factor controlling JA signaling. Collectively, our findings have clarified the regulatory effects of ABF3 on JA signaling and provide new insights into how JA signaling is enhanced following an exposure to salinity stress.

Key words: Salinity stress, Jasmonate, JAZ1, ABF3, Arabidopsis

Qi Zhang, Jiancan Du, Xiao Han, Yanru Hu. Transcription factor ABF3 modulates salinity stress-enhanced jasmonate signaling in Arabidopsis[J]. Plant Diversity, 2024, 46(06): 791-803.

References

Campos, M.L., Yoshida, Y., Major, I.T., et al., 2016. Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nat. Commun. 7, 12570.
Chen, Q., Sun, J.Q., Zhai, Q.Z., et al., 2011. The basic helix-loop-helix transcription factor MYC2 directly represses PLETHORA expression during jasmonate-mediated modulation of the root stem cell niche in Arabidopsis. Plant Cell 2, 3335-3352.
Chen, X.D., Zhang, X.M. Jia, A.Q., et al. 2016. Jasmonate mediates salt-induced nicotine biosynthesis in tobacco (Nicotiana tabacum L.). Plant Divers. 38, 118-123.
Chen, Y.M., Wang, Y., Huang, J.G, et al., 2017. Salt and methyl jasmonate aggravate growth inhibition and senescence in Arabidopsis seedlings via the JA signaling pathway. Plant Sci. 261, 1-9.
Chico, J.M., Fernandez-Barbero, G., Chini, A., et al., 2014. Repression of jasmonate-dependent defenses by shade involves differential regulation of protein stability of MYC transcription factors and their JAZ repressors in Arabidopsis. Plant Cell 26, 1967-1980.
Chini, A., Fonseca, S., Fernandez, G., et al., 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448, 666-671.
Choi, H.I., Hong, J.H., Ha, J.O., et al., 2000. ABFs, a family of ABA-responsive element binding factors. J. Biol. Chem. 275, 1723-1730.
Collin, A., Daszkowska-Golec, A., Szarejko, I., 2021. Updates on the role of ABSCISIC ACID INSENSITIVE 5 (ABI5) and ABSCISIC ACID-RESPONSIVE ELEMENT BINDING FACTORs (ABFs) in ABA signaling in different developmental stages in plants. Cells 1, 1996.
Dabravolski, S.A. and Isayenkov, S.V., 2023. The role of anthocyanins in plant tolerance to drought and salt stresses. Plants-basel 12, 2558.
Dar, T.A., Uddin, M., Khan, M.M.A., et al., 2015. Jasmonates counter plant stress: a Review. Environ. Exp. Bot. 115, 49-57.
Dong, W., Wang, M.C., Xu, F., et al., 2013. Wheat oxophytodienoate reductase gene TaOPR1 confers salinity tolerance via enhancement of abscisic acid signaling and reactive oxygen species scavenging. Plant Physiol. 161, 1217-1228.
Du, J.C., Zhu, X., He, K.R., et al., 2023. CONSTANS interacts with and antagonizes ABF transcription factors during salt stress under long-day conditions. Plant Physiol. 193, 1675-1694.
Ellis, C., Turner, J., 2002. A conditionally fertile coi1 allele indicates cross-talk between plant hormone signalling pathways in Arabidopsis thaliana seeds and young seedlings. Planta 215, 549-556.
Fernandez-Calvo, P., Chini, A., Fernandez-Barbero, G., et al., 2011. The Arabidopsis bHLH transcription factors MYC3 and MYC4 are targets of JAZ repressors and act additively with MYC2 in the activation of jasmonate responses. Plant Cell 23, 701-715.
Finkelstein, R., Gampala, S.S.L., Lynch, T.J., et al., 2005. Redundant and distinct functions of the ABA response loci ABA-INSENSITIVE(ABI)5 and ABRE-BINDING FACTOR (ABF)3. Plant Mol. Biol. 59, 253-267.
Furihata, T., Maruyama, K., Fujita, Y., et al., 2006. Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc. Natl. Acad. Sci. U. S. A. 103, 1988-1993.
Han, X., Kui, M.Y., He, K.H., et al., 2023a. Jasmonate-regulated root growth inhibition and root hair elongation. J. Exp. Bot. 74, 1176-1185.
Han, X., Kui, M.Y., Xu, T.T., et al., 2023b. CO interacts with JAZ repressors and bHLH subgroup IIId factors to negatively regulate jasmonate signaling in Arabidopsis seedlings. Plant Cell 35, 852-873.
Han, X., Zhang, M.H., Yang, M.L., et al., 2020. Arabidopsis JAZ proteins interact with and suppress RHD6 transcription factor to regulate jasmonate-stimulated root hair development. Plant Cell 32, 1049-1062.
He, K.R., Du, J.C., Han, X., et al., 2023. PHOSPHATE STARVATION RESPONSE1 (PHR1) interacts with JASMONATE ZIM-DOMAIN (JAZ) and MYC2 to modulate phosphate deficiency-induced jasmonate signaling in Arabidopsis. Plant Cell 35, 2132-2156.
Hossain, M.A., Cho, J.I., Han, M., et al., 2010. The ABRE-binding bZIP transcription factor OsABF2 is a positive regulator of abiotic stress and ABA signaling in rice. J. Plant Physiol. 167, 1512-1520.
Howe, G.A., Major, I.T., Koo, A.J., 2018. Modularity in jasmonate signaling for multistress resilience. Annu. Rev. Plant Biol. 69, 387-415.
Hu, S., Yu, K.M., Yan, J.B., et al., 2023. Jasmonate perception: ligand-receptor interaction, regulation, and evolution. Mol. Plant 16, 23-42.
Hu, Y.R., Jiang, L.Q., Wang, F., et al., 2013. Jasmonate regulates the inducer of CBF EXPRESSION-C-REPEAT BINDING FACTOR/DRE BINDING FACTOR1 cascade and freezing tolerance in Arabidopsis. Plant Cell 25, 2907-2924.
Hu, Y.R., Jiang, Y.J., Han, X., et al., 2017. Jasmonate regulates leaf senescence and tolerance to cold stress: crosstalk with other phytohormones. J. Exp. Bot. 68, 1361-1369.
Huang, H., Chen, S., Wang, T., et al., 2022. Jasmonate action and crosstalk in flower development and fertility. J. Exp. Bot. 74, 1186-1197.
Huang, H., Wang, C.L., Tian, H.X., et al., 2014. Amino acid substitutions of GLY98, LEU245 and GLU543 in COI1 distinctively affect jasmonate-regulated male fertility in Arabidopsis. Sci. China Life Sci. 57, 145-154.
Jayakannan, M., Bose, J., Babourina, O., et al., 2015. The NPR1-dependent salicylic acid signaling pathway is pivotal for enhanced salt and oxidative stress tolerance in Arabidopsis. J. Exp. Bot. 66, 1865-1875.
Jiang, Y.J., Liang, G., Yang, S.Z., et al., 2014. Arabidopsis WRKY57 functions as a node of convergence for jasmonic acid- and auxin-mediated signaling in jasmonic acid-induced leaf senescence. Plant Cell 26, 230-245.
Kang, J.Y., Choi, H.I., Im, M.Y., et al., 2002. Arabidopsis basic leucine zipper proteins that mediate stress-responsive abscisic acid signaling. Plant Cell 14, 343-357.
Kazan, K., Manners, J.M., 2013. MYC2: the master in action. Mol. Plant 6, 686-703.
Kim J., Lee, W.J., Vu, T.T., et al., 2017. High accumulation of anthocyanins via the ectopic expression of AtDFR confers significant salt stress tolerance in Brassica napus L. Plant Cell Rep. 36, 1215-1224.
Kim, S., Kang, J.Y., Cho, D.I., et al., 2004. ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J. 40, 75-87.
Kim, S.Y., 2005. The role of ABF family bZIP class transcription factors in stress response. Physiol. Plantarum 126, 519-527.
Kramell, R., Atzorn, R., Schneider, O., et al., 1995. Occurrence and identification of jasmonic acid and its amino acid conjugates induced by osmotic stress in barley leaf tissue. J. Plant Growth Regul. 14, 29-36.
Li, H.Q., He, K.R., Zhang, Z.Q., et al., 2023. Molecular mechanism of phosphorous signaling inducing anthocyanin accumulation in Arabidopsis. Plant Physiol. Biochem. 196, 121-129.
Li, X., Li C.J., Shi L., et al., 2024. Jasmonate signaling pathway confers salt tolerance through a NUCLEAR FACTOR-Y trimeric transcription factor complex in Arabidopsis. Cell Rep. 43, 113825.
Liu, J., Shu, D.F., Tan, Z.L., et al., 2022. The Arabidopsis IDD14 transcription factor interacts with bZIP-type ABFs/AREBs and cooperatively regulates ABA-mediated drought tolerance. New Phytol. 236, 929-942.
Lorenzo, O., Chico, J.M., Sanchez-Serrano, J.J., et al., 2004. JASMONATE-INSENSITIVE1 encodes a MYC transcription factor essential to discriminate between different jasmonate-regulated defense responses in Arabidopsis. Plant Cell 16, 1938-1950.
Mao, Y.B., Liu, Y.Q., Chen, D.Y., et al., 2017. Jasmonate response decay and defense metabolite accumulation contributes to age-regulated dynamics of plant insect resistance. Nat. Commun. 8, 13925.
Munns, R., Tester, M., 2008. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol. 71, 403-433.
Osakabe, Y., Yamaguchi-Shinozaki, K., Shinozaki, K., et al., 2013. ABA control of plant macroelement membrane transport systems in response to water deficit and high salinity. New Phytol. 202, 35-49.
Pan, J.J., Hu, Y.R., Wang, H.P., et al., 2020. Molecular mechanism underlying the synergetic effect of jasmonate on abscisic acid signaling during seed germination in Arabidopsis. Plant Cell 32, 3846-3865.
Pan, J.J., Wang, H.P., You, Q.G., et al., 2022. Jasmonate-regulated seed germination and crosstalk with other phytohormones. J. Exp. Bot. 74, 1162-1175.
Pedranzani, H., Racagni, G., Alemano, S., et al., 2003. Salt tolerant tomato plants show increased levels of jasmonic acid. Plant Growth Regul. 41, 149-158.
Peng, J.Y., Li, Z.H., Wen, X., et al., 2014. Salt-induced stabilization of EIN3/EIL1 confers salinity tolerance by deterring ROS accumulation in Arabidopsis. PLoS Genet. 10.
Qi, T.C., Song, S.S., Ren, Q.C., 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. Plant Cell 23, 1795-1814.
Schweizer, F., Fernandez-Calvo, P., Zander, M., et al., 2013. Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, and MYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell 25, 3117-3132.
Shan, X.Y., Zhang, Y.S., Peng, W., et al., 2009. Molecular mechanism for jasmonate-induction of anthocyanin accumulation in Arabidopsis. J. Exp. Bot. 60, 3849-3860.
Sheen, J., 2001. Signal transduction in maize and Arabidopsis mesophyll protoplasts. Plant Physiol. 127, 1466-1475.
Song, J., Sun, P.P., Kong, W.A., et al., 2022. SnRK2.4-mediated phosphorylation of ABF2 regulates ARGININE DECARBOXYLASE expression and putrescine accumulation under drought stress. New Phytol. 238, 216-236.
Song, S.S., Qi, T.C., Huang, H., et al., 2011. The Jasmonate-ZIM domain proteins interact with the R2R3-MYB transcription factors MYB21 and MYB24 to affect Jasmonate-regulated stamen development in Arabidopsis. Plant Cell 23, 1000-1013.
Staswick, P.E., Tiryaki, I., 2004. The oxylipin signal jasmonic acid is activated by an enzyme that conjugates it to isoleucine in Arabidopsis. Plant Cell 16, 2117-2127.
Stitz, M., Gase, K., Baldwin, I., 2011. Ectopic expression of AtJMT in Nicotiana attenuata: creating a metabolic sink has tissue specific consequences for the jasmonate metabolic network and silences downstream gene expression. Plant Physiol. 157, 341-354.
Thines, B., Katsir, L., Melotto, M., et al., 2007. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448, 661-665.
Toda, Y., Tanaka, M., Ogawa, D., et al., 2013. RICE SALT SENSITIVE3 forms a ternary complex with JAZ and class-C bHLH factors and regulates jasmonate-induced gene expression and root cell elongation. Plant Cell 25, 1709-1725.
Uno, Y., Furihata, T., Abe, H., et al., 2000. Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc. Natl. Acad. Sci. U. S. A. 97, 11632-11637.
Valenzuela, C.E., Acevedo-Acevedo, O., Miranda, G.S., et al., 2016. Salt stress response triggers activation of the jasmonate signaling pathway leading to inhibition of cell elongation in Arabidopsis primary root. J. Exp. Bot. 67, 4209-4220.
Wang, X.J., Guo, C., Peng, J., et al., 2018. ABRE-BINDING FACTORS play a role in the feedback regulation of ABA signaling by mediating rapid ABA induction of ABA co-receptor genes. New Phytol. 221, 341-355.
Wasternack, C., Song, S., 2017. Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. J. Exp. Bot. 68, 1303-1321.
Xiang, X.Y., Wu, S.G., Jin, Y.F., et al., 2022. Phytochrome B regulates jasmonic acid-mediated defense response against Botrytis cinerea in Arabidopsis. Plant Divers. 44, 109-115.
Xie, D.X, Feys, B.F., James, S., et al., 1998. COI1: an Arabidopsis gene required for jasmonate-regulated defense and fertility. Science 280, 1091-1094.
Xu, L.H., Liu, F.Q., Lechner, E., et al., 2002. The SCFCOI1 ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14, 1919-1935.
Yan, J.B., Li, H.O., Li, S.H., et al., 2013. The Arabidopsis F-box protein CORONATINE INSENSITIVE1 is stabilized by SCFCOI1 and degraded via the 26S proteasome pathway. Plant Cell 25, 486-498.
Yan, J.B., Zhang, C., Gu, M., et al., 2009. The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21, 2220-2236.
Yoon, J., Hamayun, M., Lee, S., et al., 2009. Methyl jasmonate alleviated salinity stress in soybean. J. Crop Sci. Biotech. 12, 63-68.
Yoshida, T., Fujita, Y., Maruyama, K., et al., 2015. Four Arabidopsis AREB/ABF transcription factors function predominantly in gene expression downstream of SnRK2 kinases in abscisic acid signalling in response to osmotic stress. Plant Cell Environ. 38, 35-49.
Yoshida, T., Fujita, Y., Sayama, H., et al., 2010. AREB1, AREB2, and ABF3 are master transcription factors that cooperatively regulate ABRE-dependent ABA signaling involved in drought stress tolerance and require ABA for full activation. Plant J. 61, 672-685.
Yu, Z.P., Duan, X.B., Luo, L., et al., 2020. How plant hormones mediate salt stress responses. Trends Plant Sci. 25, 1117-1130.
Zhao, C.Z., Zhang, H., Song, C.P., et al., 2020. Mechanisms of plant responses and adaptation to soil salinity. Innovation 1, 10017.
Zhao, Y., Dong, W., Zhang, N.B., et al., 2014. A wheat allene oxide cyclase gene enhances salinity tolerance via jasmonate signaling. Plant Physiol. 164, 1068-1076.
Zhou, H.P., Shi, H.F., Yang, Y.Q., et al., 2023. Insights into plant salt stress signaling and tolerance. J. Genet. Genomics. 51, 16-34.
Zhu, Z.Q., An, F.Y., Feng, Y., et al., 2011. Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 108, 12539-12544.

[1]	Shanni Cao, Xue Zhao, Zhuojin Li, Ranran Yu, Yuqi Li, Xinkai Zhou, Wenhao Yan, Dijun Chen, Chao He. Comprehensive integration of single-cell transcriptomic data illuminates the regulatory network architecture of plant cell fate specification [J]. Plant Diversity, 2024, 46(03): 372-385.
[2]	Yunrui Ji, Minghui Mou, Huimin Zhang, Ruling Wang, Songguo Wu, Yifen Jing, Haiyan Zhang, Lanxin Li, Zhifang Li, Ligang Chen. GhWRKY33 negatively regulates jasmonate-mediated plant defense to Verticillium dahliae [J]. Plant Diversity, 2023, 45(03): 337-346.
[3]	Junbin Cheng, Na Song, Jinsong Wu. A patatin-like protein synergistically regulated by jasmonate and ethylene signaling pathways plays a negative role in Nicotiana attenuata resistance to Alternaria alternata [J]. Plant Diversity, 2019, 41(01): 7-12.
[4]	Zhen Xu, Na Song, Lan Ma, Dunhuang Fang, Jinsong Wu. NaPDR1 and NaPDR1-like are essential for the resistance of Nicotiana attenuata against fungal pathogen Alternaria alternata [J]. Plant Diversity, 2018, 40(02): 68-73.
[5]	Xiaodong Chen, Xiaoming Zhang, Aiqun Jia, Gang Xu, Hong Hu, Xiangyang H. Jasmonate mediates saltinduced nicotine biosynthesis in tobacco (Nicotiana tabacum L.) [J]. Plant Diversity, 2016, 38(02): 146-152.
[6]	YANG Ying, ZHENG Hui , HE Feng, JI Jia-Xing, YU Long-Jiang. The Effects of Methyl Jasmonate on the Flavonoids Synthesis in Cell Suspension Culture of Glycyrrhiza inflata (Leguminosae) [J]. Plant Diversity, 2008, 30(05): 586-592.