Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis

Niu, Yajie; Figueroa, Pablo; Browse, John

doi:10.1093/jxb/erq408

Characterization of JAZ-interacting bHLH transcription factors that regulate jasmonate responses in Arabidopsis

Journal Article · Mon Feb 14 00:00:00 EST 2011 · Journal of Experimental Botany

DOI:https://doi.org/10.1093/jxb/erq408· OSTI ID:1625369

Niu, Yajie ^[1]; Figueroa, Pablo ^[2]; Browse, John ^[2]

Washington State Univ., Pullman, WA (United States). Inst. of Biological Chemistry; DOE/OSTI
Washington State Univ., Pullman, WA (United States). Inst. of Biological Chemistry

The plant hormone jasmonate (JA) plays important roles in the regulation of plant defence and development. JASMONATE ZIM-DOMAIN (JAZ) proteins inhibit transcription factors that regulate early JA-responsive genes, and JA-induced degradation of JAZ proteins thus allows expression of these response genes. To date, MYC2 is the only transcription factor known to interact directly with JAZ proteins and regulate early JA responses, but the phenotype of myc2 mutants suggests that other transcription factors also activate JA responses. To identify JAZ1-interacting proteins, a yeast two-hybrid screen of an Arabidopsis cDNA library was performed. Two basic helix-loop-helix (bHLH) proteins, MYC3 and MYC4, were identified. MYC3 and MYC4 share high sequence similarity with MYC2, suggesting they may have similar biological functions. MYC3 and MYC4 interact not only with JAZ1 but also with other JAZ proteins (JAZ3 and JAZ9) in both yeast two-hybrid and pull-down assays. MYC2, MYC3, and MYC4 were all capable of inducing expression of JAZ::GUS reporter constructs following transfection of carrot protoplasts. Although myc3 and myc4 loss-of-function mutants showed no phenotype, transgenic plants overexpressing MYC3 and MYC4 had higher levels of anthocyanin compared to the wild-type plants. In addition, roots of MYC3 overexpression plants were hypersensitive to JA. Quantitative real-time RT-PCR expression analysis of nine JAresponsive genes revealed that eight of them were induced in MYC3 and MYC4 overexpression plants, except for a pathogen-responsive gene, PDF1.2. Similar to MYC2, MYC4 negatively regulates expression of PDF1.2. Together, these results suggest that MYC3 and MYC4 are JAZ-interacting transcription factors that regulate JA responses.

View Accepted Manuscript (DOE)

Research Organization:: Washington State Univ., Pullman, WA (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES). Chemical Sciences, Geosciences & Biosciences Division

Grant/Contract Number:: FG02-99ER20323

OSTI ID:: 1625369

Journal Information:: Journal of Experimental Botany, Journal Name: Journal of Experimental Botany Journal Issue: 6 Vol. 62; ISSN 0022-0957

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

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Plants Know Where It Hurts: Root and Shoot Jasmonic Acid Induction Elicit Differential Responses in Brassica oleracea Tytgat, Tom O. G.; Verhoeven, Koen J. F.; Jansen, Jeroen J. PLoS ONE, Vol. 8, Issue 6 https://doi.org/10.1371/journal.pone.0065502	journal	June 2013
bHLH003, bHLH013 and bHLH017 Are New Targets of JAZ Repressors Negatively Regulating JA Responses Fonseca, Sandra; Fernández-Calvo, Patricia; Fernández, Guillermo M. PLoS ONE, Vol. 9, Issue 1 https://doi.org/10.1371/journal.pone.0086182	journal	January 2014
The Positive Regulatory Roles of the TIFY10 Proteins in Plant Responses to Alkaline Stress Zhu, Dan; Li, Rongtian; Liu, Xin PLoS ONE, Vol. 9, Issue 11 https://doi.org/10.1371/journal.pone.0111984	journal	November 2014
Transcriptome and metabolome analysis reveal candidate genes and biochemicals involved in tea geometrid defense in Camellia sinensis Wang, Wei-Wei; Zheng, Chao; Hao, Wan-Jun PLOS ONE, Vol. 13, Issue 8 https://doi.org/10.1371/journal.pone.0201670	journal	August 2018
Correction: Jasmonate signalling pathway in strawberry: Genome-wide identification, molecular characterization and expression of JAZs and MYCs during fruit development and ripening Garrido-Bigotes, Adrián; Figueroa, Nicolás E.; Figueroa, Pablo M. PLOS ONE, Vol. 13, Issue 10 https://doi.org/10.1371/journal.pone.0206559	journal	October 2018
Bacterial Effector Activates Jasmonate Signaling by Directly Targeting JAZ Transcriptional Repressors Jiang, Shushu; Yao, Jian; Ma, Ka-Wai PLoS Pathogens, Vol. 9, Issue 10 https://doi.org/10.1371/journal.ppat.1003715	journal	October 2013
Plant begomoviruses subvert ubiquitination to suppress plant defenses against insect vectors Li, Ping; Liu, Chao; Deng, Wen-Hao PLOS Pathogens, Vol. 15, Issue 2 https://doi.org/10.1371/journal.ppat.1007607	journal	February 2019
A Regulatory Network for Coordinated Flower Maturation E., Farmer, Edward; Ina, Haupt,; M., Ellis, Christine The University of North Carolina at Chapel Hill University Libraries https://doi.org/10.17615/qc2e-g010	text	January 2012
The DELLA Proteins Interact with MYB21 and MYB24 to Regulate Filament Elongation in Arabidopsis Huang, Huang; Gong, Yilong; Liu, Bei https://doi.org/10.21203/rs.2.18302/v3	posted_content	January 2020
A Functional Genomic Perspective on Drought Signalling and its Crosstalk with Phytohormone-mediated Signalling Pathways in Plants Tiwari, Shalini; Lata, Charu; Chauhan, Puneet Singh Current Genomics, Vol. 18, Issue 6 https://doi.org/10.2174/1389202918666170605083319	journal	September 2017
Social Network: JAZ Protein Interactions Expand Our Knowledge of Jasmonate Signaling Wager, Amanda; Browse, John Frontiers in Plant Science, Vol. 3 https://doi.org/10.3389/fpls.2012.00041	journal	January 2012
Nuclear jasmonate and salicylate signaling and crosstalk in defense against pathogens Gimenez-Ibanez, Selena; Solano, Roberto Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00072	journal	January 2013
Onset of herbivore-induced resistance in systemic tissue primed for jasmonate-dependent defenses is activated by abscisic acid Vos, Irene A.; Verhage, Adriaan; Schuurink, Robert C. Frontiers in Plant Science, Vol. 4 https://doi.org/10.3389/fpls.2013.00539	journal	January 2013
Evolutionary tinkering of the expression of PDF1s suggests their joint effect on zinc tolerance and the response to pathogen attack Nguyen, Nga N. T.; Ranwez, Vincent; Vile, Denis Frontiers in Plant Science, Vol. 5 https://doi.org/10.3389/fpls.2014.00070	journal	March 2014
Impact of hormonal crosstalk on plant resistance and fitness under multi-attacker conditions Vos, Irene A.; Moritz, Liselotte; Pieterse, Corné M. J. Frontiers in Plant Science, Vol. 6 https://doi.org/10.3389/fpls.2015.00639	journal	August 2015
Identification of TIFY Family Genes and Analysis of Their Expression Profiles in Response to Phytohormone Treatments and Melampsora larici-populina Infection in Poplar Xia, Wenxiu; Yu, Hongyan; Cao, Pei Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00493	journal	April 2017
Arabidopsis MYB24 Regulates Jasmonate-Mediated Stamen Development Huang, Huang; Gao, Hua; Liu, Bei Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01525	journal	September 2017
Nucleolar GTP-Binding Protein 1-2 (NOG1-2) Interacts with Jasmonate-ZIMDomain Protein 9 (JAZ9) to Regulate Stomatal Aperture during Plant Immunity Lee, Seonghee; Rojas, Clemencia; Oh, Sunhee International Journal of Molecular Sciences, Vol. 19, Issue 7 https://doi.org/10.3390/ijms19071922	journal	June 2018
Sedoheptulose-1,7-Bisphosphatase is Involved in Methyl Jasmonate- and Dark-Induced Leaf Senescence in Tomato Plants Ding, Fei; Wang, Meiling; Zhang, Shuoxin International Journal of Molecular Sciences, Vol. 19, Issue 11 https://doi.org/10.3390/ijms19113673	journal	November 2018
Application of a JA-Ile Biosynthesis Inhibitor to Methyl Jasmonate-Treated Strawberry Fruit Induces Upregulation of Specific MBW Complex-Related Genes and Accumulation of Proanthocyanidins Delgado, Laura; Zúñiga, Paz; Figueroa, Nicolás Molecules, Vol. 23, Issue 6 https://doi.org/10.3390/molecules23061433	journal	June 2018
Circadian Network Interactions with Jasmonate Signaling and Defense Thines, Bryan; Parlan, Emily V.; Fulton, Elena C. Plants, Vol. 8, Issue 8 https://doi.org/10.3390/plants8080252	journal	July 2019
Jasmonate Biosynthesis, Perception and Function in Plant Development and Stress Responses Yan, Yuanxin; Borrego, Eli; Kolomiets, Michael V. Lipid Metabolism https://doi.org/10.5772/52675	book	January 2013
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Jasmonate responsive transcription factor WsMYC2 regulates the biosynthesis of triterpenoid withanolides and phytosterol via key pathway genes in Withania somnifera (L.) Dunal Sharma, Arti; Rather, Gulzar A.; Misra, Prashant Plant Molecular Biology, Vol. 100, Issue 4-5 https://doi.org/10.1007/s11103-019-00880-4	journal	May 2019
Rational design of a ligand-based antagonist of jasmonate perception Monte, Isabel; Hamberg, Mats; Chini, Andrea Nature Chemical Biology, Vol. 10, Issue 8 https://doi.org/10.1038/nchembio.1575	journal	July 2014
Arabidopsis ERF109 mediates cross-talk between jasmonic acid and auxin biosynthesis during lateral root formation Cai, Xiao-Teng; Xu, Ping; Zhao, Ping-Xia Nature Communications, Vol. 5, Issue 1 https://doi.org/10.1038/ncomms6833	journal	December 2014
Novel players fine-tune plant trade-offs Gimenez-Ibanez, Selena; Boter, Marta; Solano, Roberto Essays in Biochemistry, Vol. 58 https://doi.org/10.1042/bse0580083	journal	September 2015
Derepression of ethylene-stabilized transcription factors (EIN3/EIL1) mediates jasmonate and ethylene signaling synergy in Arabidopsis Zhu, Z.; An, F.; Feng, Y. Proceedings of the National Academy of Sciences, Vol. 108, Issue 30 https://doi.org/10.1073/pnas.1103959108	journal	July 2011
Arabidopsis JASMONATE-INDUCED OXYGENASES down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid Caarls, Lotte; Elberse, Joyce; Awwanah, Mo Proceedings of the National Academy of Sciences, Vol. 114, Issue 24 https://doi.org/10.1073/pnas.1701101114	journal	May 2017
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New perspective of the bHLH-MYB complex in jasmonate-regulated plant fertility in arabidopsis Chen, Xi; Huang, Huang; Qi, Tiancong Plant Signaling & Behavior, Vol. 11, Issue 2 https://doi.org/10.1080/15592324.2015.1135280	journal	August 2015
Transcriptome analysis identifies differentially expressed genes in maize leaf tissues in response to elevated atmospheric [CO ₂ ] Ge, Yuan; Guo, Baoqiang; Cai, Yaomin Journal of Plant Interactions, Vol. 13, Issue 1 https://doi.org/10.1080/17429145.2018.1483035	journal	January 2018
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The interplay between light and jasmonate signalling during defence and development Kazan, K.; Manners, J. M. Journal of Experimental Botany, Vol. 62, Issue 12 https://doi.org/10.1093/jxb/err142	journal	June 2011
Molecular basis for jasmonate and ethylene signal interactions in Arabidopsis Zhu, Z. Journal of Experimental Botany, Vol. 65, Issue 20 https://doi.org/10.1093/jxb/eru349	journal	August 2014
Characterization of a JAZ7 activation-tagged Arabidopsis mutant with increased susceptibility to the fungal pathogen Fusarium oxysporum Thatcher, Louise F.; Cevik, Volkan; Grant, Murray Journal of Experimental Botany, Vol. 67, Issue 8 https://doi.org/10.1093/jxb/erw040	journal	February 2016
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Jasmonate regulates leaf senescence and tolerance to cold stress: crosstalk with other phytohormones Hu, Yanru; Jiang, Yanjuan; Han, Xiao Journal of Experimental Botany, Vol. 68, Issue 6 https://doi.org/10.1093/jxb/erx004	journal	February 2017
Jasmonate signalling in the regulation of rubber biosynthesis in laticifer cells of rubber tree, Hevea brasiliensis Deng, Xiaomin; Guo, Dong; Yang, Shuguang Journal of Experimental Botany, Vol. 69, Issue 15 https://doi.org/10.1093/jxb/ery169	journal	May 2018
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The plant Mediator complex and its role in jasmonate signaling Zhai, Qingzhe; Li, Chuanyou Journal of Experimental Botany, Vol. 70, Issue 13 https://doi.org/10.1093/jxb/erz233	journal	May 2019
Involvement of OsJAZ8 in Jasmonate-Induced Resistance to Bacterial Blight in Rice Yamada, Shoko; Kano, Akihito; Tamaoki, Daisuke Plant and Cell Physiology, Vol. 53, Issue 12 https://doi.org/10.1093/pcp/pcs145	journal	October 2012
MYC5 is Involved in Jasmonate-Regulated Plant Growth, Leaf Senescence and Defense Responses Song, Susheng; Huang, Huang; Wang, Jiaojiao Plant and Cell Physiology, Vol. 58, Issue 10 https://doi.org/10.1093/pcp/pcx112	journal	August 2017
The JASMONATE ZIM-Domain Gene Family Mediates JA Signaling and Stress Response in Cotton Sun, Heng; Chen, Lin; Li, Jianying Plant and Cell Physiology, Vol. 58, Issue 12 https://doi.org/10.1093/pcp/pcx148	journal	October 2017
A Chimeric IDD4 Repressor Constitutively Induces Immunity in Arabidopsis via the Modulation of Salicylic Acid and Jasmonic Acid Homeostasis Vï¿½lz, Ronny; Kim, Soon-Kap; Mi, Jianing Plant and Cell Physiology, Vol. 60, Issue 7 https://doi.org/10.1093/pcp/pcz057	journal	April 2019
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Induction of jasmonate signalling regulators MaMYC2s and their physical interactions with MaICE1 in methyl jasmonate-induced chilling tolerance in banana fruit: Interaction between MaMYC2 and MaICE1 Zhao, Ming-Lei; Wang, Jun-Ning; Shan, Wei Plant, Cell & Environment, Vol. 36, Issue 1 https://doi.org/10.1111/j.1365-3040.2012.02551.x	journal	June 2012
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JAZ2 controls stomata dynamics during bacterial invasion Gimenez-Ibanez, Selena; Boter, Marta; Ortigosa, Andrés New Phytologist, Vol. 213, Issue 3 https://doi.org/10.1111/nph.14354	journal	December 2016
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Genome-wide analysis of long non-coding RNAs in Catalpa bungei and their potential function in floral transition using high-throughput sequencing Wang, Zhi; Zhu, Tianqing; Ma, Wenjun BMC Genetics, Vol. 19, Issue 1 https://doi.org/10.1186/s12863-018-0671-2	journal	September 2018
Comparative transcriptome analysis of the interaction between Actinidia chinensis var. chinensis and Pseudomonas syringae pv. actinidiae in absence and presence of acibenzolar-S-methyl Michelotti, Vania; Lamontanara, Antonella; Buriani, Giampaolo BMC Genomics, Vol. 19, Issue 1 https://doi.org/10.1186/s12864-018-4967-4	journal	August 2018
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A Maize Jasmonate Zim-Domain Protein, ZmJAZ14, Associates with the JA, ABA, and GA Signaling Pathways in Transgenic Arabidopsis Zhou, Xiaojin; Yan, Shengwei; Sun, Cheng PLOS ONE, Vol. 10, Issue 3 https://doi.org/10.1371/journal.pone.0121824	journal	March 2015
Transcription factors and molecular markers revealed asymmetric contributions between allotetraploid Upland cotton and its two diploid ancestors Jazayeri, Seyed Mehdi; Villamar-Torres, Ronald Oswaldo; Zambrano-Vega, Cristian Bragantia, Vol. 79, Issue 1 https://doi.org/10.1590/1678-4499.20190161	journal	March 2020
The DELLA Proteins Interact with MYB21 and MYB24 to Regulate Filament Elongation in Arabidopsis Huang, Huang; Gong, Yilong; Liu, Bei BMC Plant Biology https://doi.org/10.21203/rs.2.18302/v2	posted_content	February 2020
Critical analysis of protein signaling networks involved in the regulation of plant secondary metabolism: focus on anthocyanins Bulgakov, Victor P.; Avramenko, Tatiana V.; Tsitsiashvili, Gurami Sh. Critical Reviews in Biotechnology, Vol. 37, Issue 6 https://doi.org/10.3109/07388551.2016.1141391	journal	February 2016
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Genome-Wide Identification and Characterization of JAZ Protein Family in Two Petunia Progenitors Tian, Shaoze; Liu, Siyu; Wang, Yu Plants, Vol. 8, Issue 7 https://doi.org/10.3390/plants8070203	journal	July 2019
Characteristics and Expression Pattern of MYC Genes in Triticum aestivum, Oryza sativa, and Brachypodium distachyon Chen, Shoukun; Zhao, Hongyan; Luo, Tengli Plants, Vol. 8, Issue 8 https://doi.org/10.3390/plants8080274	journal	August 2019
Two bHLH-type transcription factors, JA-ASSOCIATED MYC2-LIKE2 and JAM3, are transcriptional repressors and affect male fertility Nakata, Masaru; Ohme-Takagi, Masaru Plant Signaling & Behavior, Vol. 8, Issue 12 https://doi.org/10.4161/psb.26473	journal	December 2013
Critical analysis of protein signaling networks involved in the regulation of plant secondary metabolism: focus on anthocyanins Bulgakov, Victor P.; Avramenko, Tatiana V.; Tsitsiashvili, Gurami Sh. Taylor & Francis https://doi.org/10.6084/m9.figshare.2798092	text	January 2016

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