Abstract
Main conclusion
Co-expression and regulatory networks yield important insights into the growth–defense tradeoffs mechanism under jasmonic acid (JA) signals in Arabidopsis.
Abstract
Elevated defense is commonly associated with growth inhibition. However, a comprehensive atlas of the genes associated with the plant growth–defense tradeoffs under JA signaling is lacking. To gain an insight into the dynamic architecture of growth–defense tradeoffs, a coexpression network analysis was employed on publicly available high-resolution transcriptomes of Arabidopsis treated with coronatine (COR), a mimic of jasmonoyl-l-isoleucine. The genes involved in JA-mediated growth–defense tradeoffs were systematically revealed. Promoter enrichment analysis revealed the core regulatory module in which the genes underwent rapid activation, sustained upregulation after COR treatment, and mediated the growth–defense tradeoffs. Several transcription factors (TFs), including RAP2.6L, MYB44, WRKY40, and WRKY18, were identified as instantly activated components associated with pathogen and insect resistance. JA might rapidly activate RAV1 and KAN1 to repress brassinosteroid (BR) response genes, upregulate KAN1, the C2H2 TF families ZF2, ZF3, ZAT6, and STZ/ZAT10 to repress the biosynthesis, transport, and signaling of auxin to arrest growth. Independent datasets and preserved analyses validated the reproducibility of the results. Our study provided a comprehensive snapshot of genes that respond to JA signals and provided valuable resources for functional studies on the genetic modification of breeding population that exhibit robust growth and defense simultaneously.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
Abbreviations
- BR:
-
Brassinosteroid
- COR:
-
Coronatine
- JA:
-
Jasmonic acid
- TF:
-
Transcription factor
References
Attaran E, Major IT, Cruz JA et al (2014) Temporal dynamics of growth and photosynthesis suppression in response to jasmonate signaling. Plant Physiol 165:1302–1314. https://doi.org/10.1104/pp.114.239004
Bergelson J, Purrington CB (1996) Surveying patterns in the cost of resistance in plants. Am Nat 148:536–558. https://doi.org/10.1086/285938
Caarls L, Elberse J, Awwanah M et al (2017) Arabidopsis jasmonate-induced oxygenases down-regulate plant immunity by hydroxylation and inactivation of the hormone jasmonic acid. Proc Natl Acad Sci USA 114:6388–6393. https://doi.org/10.1073/pnas.1701101114
Campos ML, Yoshida Y, Major IT et al (2016) Rewiring of jasmonate and phytochrome B signaling uncouples plant growth-defense tradeoffs. Nat Commun 7:12570. https://doi.org/10.1038/ncomms12570
Causier B, Ashworth M, Guo W, Davies B (2011) The TOPLESS interactome: a framework for gene repression in Arabidopsis. Plant Physiol 158:423–438. https://doi.org/10.1104/pp.111.186999
Chang L-W, Nagarajan R, Magee JA et al (2006) A systematic model to predict transcriptional regulatory mechanisms based on overrepresentation of transcription factor binding profiles. Genome Res 16:405–413. https://doi.org/10.1101/gr.4303406
Cheng M-C, Liao P-M, Kuo W-W, Lin T-P (2013) The Arabidopsis ethylene-response-Factor1 regulates abiotic-stress-responsive gene expression by binding to different cis-acting elements in response to different stress signals. Plant Physiol 162:1566–1582. https://doi.org/10.1104/pp.113.221911
Ciftci-Yilmaz S, Morsy MR, Song L et al (2007) The ear-motif of the C2H2 zinc-finger protein ZAT7 plays a key role in the defense response of Arabidopsis to salinity stress. J Biol Chem 282:9260–9268. https://doi.org/10.1074/jbc.M611093200
Davletova S, Schlauch K, Coutu J, Mittler R (2005) The zinc-finger protein ZAT12 plays a central role in reactive oxygen and abiotic stress signaling in Arabidopsis. Plant Physiol 139:847–856. https://doi.org/10.1104/pp.105.068254
Dubois M, Van den Broeck L, Inzé D (2018) The pivotal role of ethylene in plant growth. Trends Plant Sci 23:311–323. https://doi.org/10.1016/j.tplants.2018.01.003
Fan M, Bai M-Y, Kim J-G et al (2014) The bHLH transcription factor HBI1 mediates the trade-off between growth and pathogen-associated molecular pattern-triggered immunity in Arabidopsis. Plant Cell 26:828–841. https://doi.org/10.1105/tpc.113.121111
Goossens J, Fernández-Calvo P, Schweizer F, Goossens A (2016) Jasmonates: signal transduction components and their roles in environmental stress responses. Plant Mol Biol 91:673–689. https://doi.org/10.1007/s11103-016-0480-9
Grant CE, Bailey TL, Noble WS (2011) FIMO: scanning for occurrences of a given motif. Bioinformatics 27:1017–1018. https://doi.org/10.1093/bioinformatics/btr064
Guo Q, Major IT, Howe GA (2018) Resolution of growth–defense conflict: mechanistic insights from jasmonate signaling. Curr Opin Plant Biol 44:72–81. https://doi.org/10.1016/j.pbi.2018.02.009
He X-J, Mu R-L, Cao W-H et al (2005) AtNAC2, a transcription factor downstream of ethylene and auxin signaling pathways, is involved in salt stress response and lateral root development. Plant J 44:903–916. https://doi.org/10.1111/j.1365-313X.2005.02575.x
Hickman R, Verk MCV, Dijken AJHV et al (2017) Architecture and dynamics of the jasmonic acid gene regulatory network. Plant Cell 29:2086–2105. https://doi.org/10.1105/tpc.16.00958
Horan K, Jang C, Bailey-Serres J et al (2008) Annotating genes of known and unknown function by large-scale coexpression analysis. Plant Physiol 147:41–57. https://doi.org/10.1104/pp.108.117366
Hsu PY, Harmer SL (2014) Wheels within wheels: the plant circadian system. Trends Plant Sci 19:240–249. https://doi.org/10.1016/j.tplants.2013.11.007
Hu YX, Wang YH, Liu XF, Li JY (2004) Arabidopsis RAV1 is down-regulated by brassinosteroid and may act as a negative regulator during plant development. Cell Res 14:8–15. https://doi.org/10.1038/sj.cr.7290197
Hu P, Zhou W, Cheng Z et al (2013) JAV1 controls jasmonate-regulated plant defense. Mol Cell 50:504–515. https://doi.org/10.1016/j.molcel.2013.04.027
Huang T, Harrar Y, Lin C et al (2014) Arabidopsis KANADI1 acts as a transcriptional repressor by interacting with a specific cis-element and regulates auxin biosynthesis, transport, and signaling in opposition to HD-ZIPIII factors. Plant Cell 26:246–262. https://doi.org/10.1105/tpc.113.111526
Huot B, Yao J, Montgomery BL, He SY (2014) Growth–defense tradeoffs in plants: a balancing act to optimize fitness. Mol Plant 7:1267–1287. https://doi.org/10.1093/mp/ssu049
Jiang Y, Yu D (2016) The WRKY57 transcription factor affects the expression of jasmonate ZIM-domain genes transcriptionally to compromise Botrytis cinerea resistance. Plant Physiol 171:2771–2782. https://doi.org/10.1104/pp.16.00747
Jiang Y, Liang G, Yang S, Yu D (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. https://doi.org/10.1105/tpc.113.117838
Jin J, He K, Tang X et al (2015) An Arabidopsis transcriptional regulatory map reveals distinct functional and evolutionary features of novel transcription factors. Mol Biol Evol 32:1767–1773. https://doi.org/10.1093/molbev/msv058
Jin J, Tian F, Yang D-C et al (2016) PlantTFDB 4.0: toward a central hub for transcription factors and regulatory interactions in plants. Nucleic Acids Res 45:D1040–D1045
Kim D, Langmead B, Salzberg SL (2015) HISAT: a fast spliced aligner with low memory requirements. Nat Methods 12:357–360. https://doi.org/10.1038/nmeth.3317
Kodaira K-S, Qin F, Tran L-SP et al (2011) Arabidopsis Cys2/His2 zinc-finger proteins AZF1 and AZF2 negatively regulate abscisic acid-repressive and auxin-Inducible genes under abiotic stress conditions. Plant Physiol 157:742–756. https://doi.org/10.1104/pp.111.182683
Krech K, Ruf S, Masduki FF et al (2012) The plastid genome-encoded ycf4 protein functions as a nonessential assembly factor for photosystem I in higher plants. Plant Physiol 159:579–591. https://doi.org/10.1104/pp.112.196642
Krishnaswamy S, Verma S, Rahman MH, Kav NNV (2011) Functional characterization of four APETALA2-family genes (RAP2.6, RAP2.6L, DREB19 and DREB26) in Arabidopsis. Plant Mol Biol 75:107–127. https://doi.org/10.1007/s11103-010-9711-7
Kudo M, Kidokoro S, Yoshida T et al (2019) A gene-stacking approach to overcome the trade-off between drought stress tolerance and growth in Arabidopsis. Plant J 97:240–256. https://doi.org/10.1111/tpj.14110
Langfelder P, Horvath S (2008) WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 9:559. https://doi.org/10.1186/1471-2105-9-559
Langfelder P, Luo R, Oldham MC, Horvath S (2011) Is my network module preserved and reproducible? PLoS Comput Biol 7:e1001057. https://doi.org/10.1371/journal.pcbi.1001057
Li Y, Chu Z, Luo J et al (2018) The C2H2 zinc-finger protein SlZF3 regulates AsA synthesis and salt tolerance by interacting with CSN5B. Plant Biotechnol J 16:1201–1213. https://doi.org/10.1111/pbi.12863
Liao Y, Smyth GK, Shi W (2014) FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30:923–930. https://doi.org/10.1093/bioinformatics/btt656
Liu X-M, Nguyen XC, Kim KE et al (2013) Phosphorylation of the zinc finger transcriptional regulator ZAT6 by MPK6 regulates Arabidopsis seed germination under salt and osmotic stress. Biochem Biophys Res Commun 430:1054–1059. https://doi.org/10.1016/j.bbrc.2012.12.039
Mao J-L, Miao Z-Q, Wang Z et al (2016) Arabidopsis ERF1 mediates cross-talk between ethylene and auxin biosynthesis during primary root elongation by regulating ASA1 expression. PLoS Genet 12:e1005760. https://doi.org/10.1371/journal.pgen.1005760
McGrath KC, Dombrecht B, Manners JM et al (2005) Repressor- and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol 139:949–959. https://doi.org/10.1104/pp.105.068544
Merelo P, Xie Y, Brand L et al (2013) Genome-wide identification of KANADI1 target genes. PLoS ONE 8:e77341. https://doi.org/10.1371/journal.pone.0077341
Meyer K, Köster T, Nolte C et al (2017) Adaptation of iCLIP to plants determines the binding landscape of the clock-regulated RNA-binding protein AtGRP7. Genome Biol 18:204. https://doi.org/10.1186/s13059-017-1332-x
Mravec J, Skůpa P, Bailly A et al (2009) Subcellular homeostasis of phytohormone auxin is mediated by the ER-localized PIN5 transporter. Nature 459:1136–1140. https://doi.org/10.1038/nature08066
Naseem M, Kaltdorf M, Dandekar T (2015) The nexus between growth and defence signaling: auxin and cytokinin modulate plant immune response pathways. J Exp Bot 66:4885–4896. https://doi.org/10.1093/jxb/erv297
Nelson R, Wiesner-Hanks T, Wisser R, Balint-Kurti P (2017) Navigating complexity to breed disease-resistant crops. Nat Rev Genet 19:21–33. https://doi.org/10.1038/nrg.2017.82
Nusinow DA, Helfer A, Hamilton EE et al (2011) The ELF4–ELF3–LUX complex links the circadian clock to diurnal control of hypocotyl growth. Nature 475:398–402. https://doi.org/10.1038/nature10182
Pandey SP, Roccaro M, Schön M et al (2010) Transcriptional reprogramming regulated by WRKY18 and WRKY40 facilitates powdery mildew infection of Arabidopsis. Plant J 64:912–923. https://doi.org/10.1111/j.1365-313X.2010.04387.x
Paponov IA, Paponov M, Teale W et al (2008) Comprehensive transcriptome analysis of auxin responses in Arabidopsis. Mol Plant 1:321–337. https://doi.org/10.1093/mp/ssm021
Pinon V, Prasad K, Grigg SP et al (2013) Local auxin biosynthesis regulation by PLETHORA transcription factors controls phyllotaxis in Arabidopsis. Proc Natl Acad Sci USA 110:1107–1112. https://doi.org/10.1073/pnas.1213497110
Ritchie ME, Phipson B, Wu D et al (2015) Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res 43:e47–e47. https://doi.org/10.1093/nar/gkv007
Sakamoto H, Araki T, Meshi T, Iwabuchi M (2000) Expression of a subset of the Arabidopsis Cys2/His2-type zinc-finger protein gene family under water stress. Gene 248:23–32. https://doi.org/10.1016/S0378-1119(00)00133-5
Sakamoto H, Maruyama K, Sakuma Y et al (2004) Arabidopsis Cys2/His2-type zinc-finger proteins function as transcription repressors under drought, cold, and high-salinity stress conditions. Plant Physiol 136:2734–2746. https://doi.org/10.1104/pp.104.046599
Schult K, Meierhoff K, Paradies S et al (2007) The nuclear-encoded factor HCF173 is involved in the initiation of translation of the psbA mRNA in Arabidopsis thaliana. Plant Cell 19:1329–1346. https://doi.org/10.1105/tpc.106.042895
Shi H, Wang X, Ye T et al (2014) The cysteine2/histidine2-type transcription factor ZINC FINGER OF ARABIDOPSIS THALIANA6 modulates biotic and abiotic stress responses by activating salicylic acid-related genes and C-repeat-binding factor genes in Arabidopsis. Plant Physiol 165:1367–1379. https://doi.org/10.1104/pp.114.242404
Strange RN, Scott PR (2005) Plant disease: a threat to global food security. Annu Rev Phytopathol 43:83–116. https://doi.org/10.1146/annurev.phyto.43.113004.133839
Thines B, Katsir L, Melotto M et al (2007) JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signaling. Nature 448:661–665. https://doi.org/10.1038/nature05960
van Dam S, Võsa U, van der Graaf A et al (2018) Gene co-expression analysis for functional classification and gene-disease predictions. Brief Bioinform 19:575–592. https://doi.org/10.1093/bib/bbw139
Vandepoele K, Quimbaya M, Casneuf T et al (2009) Unraveling transcriptional control in Arabidopsis using cis-regulatory elements and coexpression networks. Plant Physiol 150:535–546. https://doi.org/10.1104/pp.109.136028
Windram O, Madhou P, McHattie S et al (2012) Arabidopsis defense against Botrytis cinerea: chronology and regulation deciphered by high-resolution temporal transcriptomic analysis. Plant Cell 24:3530–3557. https://doi.org/10.1105/tpc.112.102046
Xie Y, Mao Y, Lai D et al (2012) H2 enhances Arabidopsis salt tolerance by manipulating ZAT10/12-mediated antioxidant defence and controlling sodium exclusion. PLoS ONE 7:e49800. https://doi.org/10.1371/journal.pone.0049800
Xie Y, Straub D, Eguen T et al (2015) Meta-analysis of Arabidopsis KANADI1 direct target genes identifies a basic growth-promoting module acting upstream of hormonal signaling pathways. Plant Physiol 169:1240–1253. https://doi.org/10.1104/pp.15.00764
Yang L, Teixeira PJPL, Biswas S et al (2017) Pseudomonas syringae Type III effector HopBB1 promotes host transcriptional repressor degradation to regulate phytohormone responses and virulence. Cell Host Microbe 21:156–168. https://doi.org/10.1016/j.chom.2017.01.003
Yin M, Wang Y, Zhang L et al (2017) The Arabidopsis Cys2/His2 zinc finger transcription factor ZAT18 is a positive regulator of plant tolerance to drought stress. J Exp Bot 68:2991–3005. https://doi.org/10.1093/jxb/erx157
Acknowledgements
This paper was dedicated to The 100th Anniversary of Nankai University and The 100th Birthday Anniversary of Professor Ruyu Chen.
Funding
This work was supported in part by the National Key Research & Development Program of China (No. 2017YFD0200900 and No. 2017YFD0200903), the National Natural Science Foundation of China (No. 31872007 and No. 31571991), the Tianjin Natural Science Foundation (No. 18JCZDJC33500), the International Science & Technology Cooperation Program of China (No. 2014DFR41030) and The Fundamental Research Funds for the Central Universities, Nankai University (No 63191743 and No 63191323).
Author information
Authors and Affiliations
Contributions
ZF and NZ conceived the original research plan; NZ analyzed the data, performed statistical analyses, data visualization, and wrote the manuscript; BZ performed RT-qPCR experiments. BZ, DY, XG, QW, BY, SZ, and HW authored or reviewed drafts of the paper. All authors read and approved the final manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no competing interests.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Zhang, N., Zhao, B., Fan, Z. et al. Systematic identification of genes associated with plant growth–defense tradeoffs under JA signaling in Arabidopsis. Planta 251, 43 (2020). https://doi.org/10.1007/s00425-019-03335-8
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s00425-019-03335-8