Abstract
The jasmonate ZIM-domain (JAZ) proteins are repressors that function in the regulation of plant growth, development, and response to stimulation of different signals in the JA signaling pathway. Erigeron breviscapus is characteristic of sporophyte self-incompatibility (SSI). However, whether JA signaling is involved in regulation of development processes in E. breviscapus is unclear. In this study, the JAZ homolog EbJAZ1 was isolated and characterized from E. breviscapus. EbJAZ1 was localized to the nucleus, and expressed in roots, stems, leaves and flowers. Ectopic expression of EbJAZ1 in Arabidopsis resulted in shorter filament and silique length, and lower seed fertility. In addition, MeJA-induced root growth inhibition was compromised in transgenic plants. Further qRT-PCR analysis indicated that expression patterns of marker genes for VSP1, VSP2, JAZ1, JAZ5, JAZ8, JAZ10, MYC2, and bHLH17 were downregulated in transgenic plants compared to wild-type, suggesting that EbJAZ regulates the development of flower organs, seed fertility, and primary root growth through the JA signaling pathway. Thus, our results indicate that EbJAZ1 is one of the important regulators possibly involved in SSI and other developmental processes in Erigeron breviscapus.
Similar content being viewed by others
References
Boter M, Golz JF, GiménezIbañez S, Fernandez-Barbero G, Franco-Zorrilla JM, Solano R (2015) FILAMENTOUS FLOWER is a direct target of JAZ3 and modulates responses to jasmonate. Plant Cell 27(11):3160
Chen RB., Liu JH, Xiao Y, Zhang F, Chen, JF, Ji Q, Tan HX, Huang X, Feng H, Hao BK, Chen WS, Zhang L (2015) Deep sequencing reveals the effect of MeJA on scutellarin biosynthesis in Erigeron breviscapus. PLoS One. 10(12)
Cheng H, Song SS, Xiao LT, Soo HM, Cheng ZW, Xie DX, Peng JR (2009) Gibberellin acts through jasmonate to control the expression of MYB21, MYB24, and MYB57 to promote stamen filament growth in Arabidopsis. PLoS Genet. 5(3)
Chinese Pharmacopoeia Commission. Pharmacopoeia of the People’s Republic of China (2010) China medical science and technology press part 1, 138, 379, 848
Debora G, Chételat A, Acosta IF, Goossens J, Pauwels L, Goossens A, Dreos R, Alfonso E, Farmer EE (2015) Multilayered organization of jasmonate signalling in the regulation of root growth. PLoS Genet 11(6):e1005300
Dombrecht B, Xue GP, Sprague SJ, Kirkegaard JA, Ross JJ, Reid JB, Fitt GP, Sewelam N, Schenk PM, Manners JM, Kazan K (2007) MYC2 differentially modulates diverse Jasmonate-dependent functions in Arabidopsis. Plant Cell 19(7):2225–2245
Fernandezcalvo P, Chini A, Fernandezbarbero G, Chico JM, Gimenezibanez S, Geerinck J, Eeckhout D, Schweiizer F, Godoy M, Francozorrilla JM, Pauwels L, Witters E, Puga ML, PazAres J, Goossens A, Reymond P, DeJaeger G, Solano R (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(2):701–715
Gu ZY, Li W, Doughty J, Meng D, Yang Q, Yuan H, Li Y, Chen QJ, Yu J, Liu CS, Li TZ (2019) A gamma-thionin protein from apple, MdD1, is required for defence against S-RNase-induced inhibition of pollen tube prior to self/non-self- recognition. Plant Biotechnol J 17(11):2184–2198
Hou XL, Lee LYC, Xia KF, Yan YY, Yu H (2010) DELLAs modulate jasmonate signaling via competitive binding to JAZs. Dev cell 19:884–894
Howe GA, Yoshida Y (2019) Evolutionary origin of JAZ proteins and jasmonate signaling. Mol Plant 12(2):153–155
Hu FX, Zhong JJ (2008) Jasmonic acid mediates gene transcription of ginsenoside biosynthesis in cell cultures of Panax notoginseng treated with chemically synthesized 2-hydroxyethyl jasmonate. Process Biochem 43(1):113–118
Hu YR, Dong QY, Yu DQ (2012) Arabidopsis WRKY46 coordinates with WRKY70 and WRKY53 in basal resistance against pathogen Pseudomonas syringae. Plant Sci 185–186:288–297
Hu YR, Jiang LQ, Wang F, Yu DQ (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 YR, Jiang YJ, Han X, Wang HP, Pan JJ, Yu DQ (2017) Jasmonate regulates leaf senescence and tolerance to cold stress: crosstalk with other phytohormones. J Exp Bot 68(6):1361–1369
Huang H, Wang C, Tian H et al (2014a) Amino acid substitutions of GLY98, LEU245 and GLU543 in COI1 distinctively affect jasmonate-regulated male fertility in Arabidopsis[J]. Science China Life Sciences 57(1):145–154
Huang ZJ, He SA, Lei B (2014) Clinical analysis of acute cerebral infarction by Dengzhanhua injection and Xiongqin injection combined with Xuesaitong treatment. Journal of Chinese medicinal materials. 37(6)
Liu HC, Wu W, Hou K, Chen JW, Zhao Z (2016) Deep sequencing reveals transcriptome re-programming of Polygonum multiflorum thunb. roots to the elicitation with methyl jasmonate. Mol Genet Genomics. 291(1):337–348
Liu SH, Zhang PY, Li CC, Xia GM (2019) The moss jasmonate ZIM-domain protein PnJAZ1 confers salinity tolerance via crosstalk with the abscisic acid signalling pathway. Plant sci 280(2019):1–11
Lin LL, Liu AJ, Liu JG, Yu XH, Qin LP, Su DF (2007) Protective effects of scutellarin and breviscapine on brain and heart ischemia in rats. J Cardiovasc PharmJ 50(3):327–332
Liu YM, He W, Lin AH, Zeng FD (2008) Neuroprotective effects of breviscapine against apoptosis induced by transient focal cerebral ischaemia in rats. J Pharm Pharmacol 60(3):349–355
Ma Y, Li HG, Guan SX (2015) Enhancement of the oral bioavailability of breviscapine by nanoemulsions drug delivery system. Drug Dev Ind Pharm 41(2):177–182
Mandaokar A, Thines B, Shin B, Lange BM, Choi G, Koo YJ, Yoo YJ, Choi YD, Choi G, Browse J (2006) Transcriptional regulators of stamen development in Arabidopsis identified by transcriptional profiling. Plant J 46(6):984–1008
Pan JJ, Hu YR, Wang HP, Guo Q, Chen YN, Howe GA, Yu DQ (2020) Molecular mechanism underlying the synergetic effect of jasmonate on abscisic acid signaling during seed germination in Arabidopsis. Plant Cell 32(12):3846–3865
Pei TL, Ma PD, Ding K, Liu SJ, Jia YY, Ru M, Dong J, Liang ZS (2018) SmJAZ8 acts as a core repressor regulating JA-induced biosynthesis of salvianolic acids and tanshinones in Salvia miltiorrhiza hairy roots. J Exp Bot 69(7):1663–1678
Qi TC, Song SS, Ren QC, Wu DW, Huang H, Chen Y, Fan M, Peng W, Ren CM, Xie DX (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(5):1795–1814
Qi TC, Huang H, Song SS, Xie DX (2015) Regulation of Jasmonate-mediated stamen development and seed production by a bHLH-MYB complex in Arabidopsis. Plant Cell 27(6):1620
Shan XY, Wang JX, Chua LL, Jiang D, Peng W, Xie D (2015) The role of Arabidopsis rubisco activase in jasmonate-induced leaf senescence. Plant Physiol 155:751–764
Sheard LB, Tan X, Mao HB, Withers J, Nissan GB, Hinds TR, Kobayashi Y, Hsu FF, Sharon M, Browse J, He SY, Rizo J, Howe GA, Zheng N (2010) Jasmonate perception by inositol-phosphate-potentiated COI1-JAZ co-receptor. Nature 468(7322):400–405
Shi DQ, Tang C, Wang RZ, Gu C, Wu X, Hu S, Jiao J, Zhang SL (2017) Transcriptome and phytohormone analysis reveals a comprehensive phytohormone and pathogen defence response in pear self-/cross-pollination. Plant Cell Rep 36(11):1785–1799
Song SS, Q TC, Huang H, Ren QC, Wu DW, Chang CQ, Peng W, Liu YL, Peng JW, Xie DX, (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
Thines B, Katsir L, Melotto M, Niu YJ, Mandaokar A, Liu GH, Nomura K, He SY, Howe GA, Browse J (2007) JAZ repressor proteins are targets of the SCF(COI1) complex during jasmonate signaling. Nature 448(7154):661–665
Wang JJ, Wu DW, Wang YP, Xie DX (2019) Jasmonate action in plant defense against insects. J Exp Bot 70(13):3391–3400
Withers J, Yao J, Mecey C, Howe GA, Melotto M, He SY (2012) Transcription factor-dependent nuclear localization of a transcriptional repressor in jasmonate hormone signaling. Proc Natl Acad Sci U S A 109(49):20148–20153
Xie Y, Tan HJ, Ma ZX, Huang JR (2016) DELLA proteins promote anthocyanin biosynthesis via sequestering MYBL2 and JAZ suppressors of the MYB/bHLH/WD40 complex in Arabidopsis thaliana. Mol Plant 9(5):711–721
Yan JB, Zhang C, Gu M, Bai ZY, Zhang WG, Qi TC, Cheng ZW, Peng W, Luo HB, Nan FJ, Wang Z, Xie DX (2009) The Arabidopsis CORONATINE INSENSITIVE1 protein is a jasmonate receptor. Plant Cell 21:2220–2236
Zhai QZ, Zhang X, Wu FM, Feng HL, Deng L, Xu L, Zhang M, Wang QM, Li CY (2015) Transcriptional mechanism of jasmonate receptor COI1-mediated delay of flowering time in Arabidopsis. Plant Cell 27:2814–2828
Zhang W, Wei X, Meng HL, Ma CH, Jiang NH, Zhang G, Yang SC (2015) Transcriptomic comparison of the self-pollinated and cross-pollinated flowers of Erigeron breviscapus to analyze candidate self-incompatibility-associated genes. BMC Plant Biol 15(1):248–248
Zhang GF, Zhao F, Chen LQ, Pan Y, Sun LJ, Bao N, Zhang T, Cui CX, Qiu ZZ, Zhang YJ, Yang L (2019) Jasmonate-mediated wound signalling promotes plant regeneration. Nat Plants 5(5):491–497
Zhu Y, Wagner D (2019) Plant inflorescence architecture: the formation, activity, and fate of axillary meristems. Csh Perspect Biol 12(1):a034652
Funding
This work was supported by the National Natural Sciences Foundation of China (Nos. 81760692, 81960684), the Major Science and Technique Programs in Yunnan province (No. 2017ZF002), and the special fund project for basic research of local universities in Yunnan Province (No. 2018FH001-011).
Author information
Authors and Affiliations
Contributions
YRH and SCY conceived and designed the research; MC and MY conducted the experiments; WZ, SMH, and YCL analyzed the data and created the figures; GHZ, BH, and FW performed the statistical analysis; MC and WF wrote the manuscript. All authors read and approved the manuscript.
Corresponding authors
Ethics declarations
Conflict of Interest
The authors declare no competing interests.
Additional information
Key message
• EbJAZ1 is one of the important regulators involved in developmental processes in Erigeron breviscapus.
• The ectopic expression of EbJAZ1 can regulate the development of flower organs, seed fertility, and primary root growth through the JA signaling pathway.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Chen, M., Zhang, W., Yan, M. et al. Ectopic Expression of Erigeron breviscapus JAZ1 Affects JA-Induced Development Processes in Transgenic Arabidopsis. Plant Mol Biol Rep 40, 530–538 (2022). https://doi.org/10.1007/s11105-021-01289-4
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11105-021-01289-4