Abstract
Coronatine (COR) is a phytotoxin produced by Pseudomonas syringae and is a functional analogue of the bioactive hormone JA-Ile, which is widely involved in plant defence responses. In this study, we explored the effects of exogenous applications of COR on tobacco plants under polyethylene glycol-induced drought stress. Compared with control (CK), COR-treated tobacco plants exhibited higher leaf relative water content and better photosynthetic performance under drought exposure. Ultrastructural examination revealed that drought led to stomatal closure and disorganization of granum stacking in the chloroplasts (with obvious accumulation of plastoglobuli), and mitochondria in the CK samples presented injured cristae. In the leaf tissue of the COR-treated plants, regularly stacked granum thylakoids, few plastoglobuli and intact mitochondrial membranes and cristae were observed. Totals of 1803 and 6207 differentially expressed genes (DEGs) were identified between the samples from the COR-treated and CK plants under well-watered and drought conditions. Functional annotation analysis revealed that these DEGs were involved mainly in plant hormone signal transduction, cellular carbohydrate metabolic processes and photosynthesis processes. Six hundred forty transcription factor genes were also identified among the DEGs. This study provides a global view of COR-induced drought stress tolerance in tobacco from both physiological and transcriptional aspects.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ai L, Li ZH, Xie ZX, Tian XL, Eneji AE, Duan LS (2008) Coronatine alleviates polyethylene glycol-induced water stress in two rice (Oryza sativa L.) cultivars. J Agron Crop Sci 194:360–368
Arias-Baldrich C, de la Osa C, Bosch N, Ruiz-Ballesta I, Monreal JA, Garcia-Maurino S (2017) Enzymatic activity, gene expression and posttranslational modifications of photosynthetic and non-photosynthetic phosphoenolpyruvate carboxylase in ammonium-stressed sorghum plants. J Plant Physiol 214:39–47
Bolger AM, Lohse M, Usadel B (2014) Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30:2114–2120
Breithaupt C, Kurzbauer R, Lilie H, Schaller A, Strassner J, Huber R, Macheroux P, Clausen T (2006) Crystal structure of 12-oxophytodienoate reductase 3 from tomato: self-inhibition by dimerization. Proc Natl Acad Sci USA 103:14337–14342
Chaves MM, Maroco JP, Pereira JS (2003) Understanding plant responses to drought-from genes to the whole plant. Funct Plant Biol 30:239–264
Chaves MM, Flexas J, Pinheiro C (2009) Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Ann Bot 103:551–560
Cui Y, Chen C-L, Cui M, Zhou W-J, Wu H-L, Ling H-Q (2018) Four IVa bHLH transcription factors are novel interactors of FIT and mediate JA inhibition of iron uptake in Arabidopsis. Mol Plant 11:1166–1183
Dobakova M, Tichy M, Komenda J (2007) Role of the PsbI protein in photosystem II assembly and repair in the cyanobacterium Synechocystis sp. PCC 6803. Plant Physiol 145:1681–1691
Figueroa P, Browse J (2015) Male sterility in Arabidopsis induced by overexpression of a MYC5-SRDX chimeric repressor. Plant J 81:849–860
Flexas J, Medrano H (2002) Drought-inhibition of photosynthesis in C-3 plants: stomatal and non-stomatal limitations revisited. Ann Bot 89:183–189
Gimenez-Ibanez S, Boter M, Ortigosa A, Garcia-Casado G, Chini A, Lewsey MG, Ecker JR, Ntoukakis V, Solano R (2016) JAZ2 controls stomata dynamics during bacterial invasion. New Phytol 213:1378–1392
Goossens J, Mertens J, Goossens A (2017) Role and functioning of bHLH transcription factors in jasmonate signalling. J Exp Bot 68:1333–1347
Hao L, Wang Y, Zhang J, Xie Y, Zhang M, Duan L, Li Z (2013) Coronatine enhances drought tolerance via improving antioxidative capacity to maintaining higher photosynthetic performance in soybean. Plant Sci 210:1–9
Jensen PE, Haldrup A, Zhang SP, Scheller HV (2004) The PSI-O subunit of plant photosystem I is involved in balancing the excitation pressure between the two photosystems. J Biol Chem 279:24212–24217
Jiang W, Fu F-L, Zhang S-Z, Wu L, Li W-C (2010) Cloning and characterization of functional trehalose-6-phosphate synthase gene in maize. J Plant Biol 53:134–141
Kanehisa M, Araki M, Goto S, Hattori M, Hirakawa M, Itoh M, Katayama T, Kawashima S, Okuda S, Tokimatsu T, Yamanishi Y (2008) KEGG for linking genomes to life and the environment. Nucleic Acids Res 36:480–484
Katsir L, Schilmiller AL, Staswick PE, He SY, Howe GA (2008) COI1 is a critical component of a receptor for jasmonate and the bacterial virulence factor coronatine. Proc Natl Acad Sci USA 105:7100–7105
Kou X, Mao C, Wu M, Han L, Liu C, Jiang B, Xue Z (2017) Divergent functions of SNAC4-9 and possible mechanisms for tomato adaptation to abiotic stresses. J Hortic Sci Biotechnol 92:11–24
Lee KH, Kim Y-S, Park C-M, Kim H-J (2008) Proteomic identification of differentially expressed proteins in Arabidopsis mutant ntm1-D with disturbed cell division. Mol Cells 25:70–77
Li X, Shen X, Li J, Eneji AE, Li Z, Tian X, Duan L (2010) Coronatine alleviates water deficiency stress on winter wheat seedlings. J Integr Plant Biol 52:616–625
Littleson MM, Russell CJ, Frye EC, Ling KB, Jamieson C, Watson AJB (2016) Synthetic approaches to coronafacic acid, coronamic acid, and coronatine. Synth Stuttg 48:3429–3448
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Arch Biochem Biophys 444:139–158
Mao XZ, Cai T, Olyarchuk JG, Wei LP (2005) Automated genome annotation and pathway identification using the KEGG Orthology (KO) as a controlled vocabulary. Bioinformatics 21:3787–3793
Mattana M, Biazzi E, Consonni R, Locatelli F, Vannini C, Provera S, Coraggio I (2005) Overexpression of Osmyb4 enhances compatible solute accumulation and increases stress tolerance of Arabidopsis thaliana. Physiol Plant 125:212–223
Mirkovic T, Ostroumov EE, Anna JM, van Grondelle R, Govindjee SGD (2017) Light absorption and energy transfer in the antenna complexes of photosynthetic organisms. Chem Rev 117:249–293
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Methods 5:621–628
Munne-Bosch S, Jubany-Mari T, Alegre L (2003) Enhanced photo- and antioxidative protection, and hydrogen peroxide accumulation in drought-stressed Cistus clusii and Cistus albidus plants. Tree Physiol 23:1–12
Park M-R, Yun K-Y, Mohanty B, Herath V, Xu F, Wijaya E, Bajic VB, Yun S-J, De Los Reyes BG (2010) Supra-optimal expression of the cold-regulated OsMyb4 transcription factor in transgenic rice changes the complexity of transcriptional network with major effects on stress tolerance and panicle development. Plant Cell Environ 33:2209–2230
Pertea M, Kim D, Pertea GM, Leek JT, Salzberg SL (2016) Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown. Nat Protoc 11:1650–1667
Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? J Exp Bot 62:869–882
Rivero RM, Kojima M, Gepstein A, Sakakibara H, Mittler R, Gepstein S, Blumwald E (2007) Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc Natl Acad Sci USA 104:19631–19636
Royo J, Vancanneyt G, Perez AG, Sanz C, Stormann K, Rosahl S, SanchezSerrano JJ (1996) Characterization of three potato lipoxygenases with distinct enzymatic activities and different organ-specific and wound-regulated expression patterns. J Biol Chem 271:21012–21019
Seo JS, Joo J, Kim MJ, Kim YK, Nahm BH, Song SI, Cheong JJ, Lee JS, Kim JK, Do Choi Y (2011) OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J 65:907–921
Shang X-y, Liu H-b, Zhang X-q, Lin J, Duan W-j, Yang T-z (2010) Growth and physiological characteristics of roots in different flue-cured tobacco varieties under drought stress. Xibei Zhiwu Xuebao 30:357–361
Shen X, Zhao K, Liu L, Zhang K, Yuan H, Liao X, Wang Q, Guo X, Li F, Li T (2014) A role for PacMYBA in ABA-regulated anthocyanin biosynthesis in red-colored sweet Cherry cv. Hong Deng (Prunus avium L.). Plant Cell Physiol 55:862–880
Wang B, Li Z, Eneji AE, Tian X, Zhai Z, Li J, Duan L (2008) Effects of coronatine on growth, gas exchange traits, chlorophyll content, antioxidant enzymes and lipid peroxidation in maize (Zea mays L.) seedlings under simulated drought stress. Plant Prod Sci 11:283–290
Wang Z, Rashotte AM, Moss AG, Dane F (2014) Two NAC transcription factors from Citrullus colocynthis, CcNAC1, CcNAC2 implicated in multiple stress responses. Acta Physiol Plantarum 36:621–634
Wang Y, Wang Q, Liu M, Bo C, Wang X, Ma Q, Cheng B, Cai R (2017) Overexpression of a maize MYB48 gene confers drought tolerance in transgenic arabidopsis plants. J Plant Biol 60:612–621
Wasternack C (2017) The Trojan horse coronatine: the COI1-JAZ2-MYC2,3,4-ANAC019,055,072 module in stomata dynamics upon bacterial infection. New Phytol 213:972–975
Wasternack C, Song S (2017) Jasmonates: biosynthesis, metabolism, and signaling by proteins activating and repressing transcription. J Exp Bot 68:1303–1321
Wu Q, Wu J, Sun H, Zhang D, Yu D (2011) Sequence and expression divergence of the AOC gene family in soybean: insights into functional diversity for stress responses. Biotechnol Lett 33:1351–1359
Wu H, Wu X, Li Z, Duan L, Zhang M (2012) Physiological evaluation of drought stress tolerance and recovery in cauliflower (Brassica oleracea L.) seedlings treated with methyl jasmonate and coronatine. J Plant Growth Regul 31:113–123
Xie Z, Duan L, Li Z, Wang X, Liu X (2015) Dose-dependent effects of coronatine on cotton seedling growth under salt stress. J Plant Growth Regul 34:651–664
Young MD, Wakefield MJ, Smyth GK, Oshlack A (2010) Gene ontology analysis for RNA-seq: accounting for selection bias. Genome Biol. https://doi.org/10.1186/gb-2010-11-2-r14
Zhang XN, Li X, Liu JH (2014) Identification of conserved and novel cold-responsive microRNAs in trifoliate orange (Poncirus trifoliata (L.) Raf.) using high-throughput sequencing. Plant Mol Biol Rep 32:328–341
Zhou Y, Zhang M, Li J, Li Z, Tian X, Duan L (2015) Phytotoxin coronatine enhances heat tolerance via maintaining photosynthetic performance in wheat based on electrophoresis and TOF-MS analysis. Sci Rep 5:13870
Zou C, Li Y, Huang W, Zhao G, Pu G, Su J, Coyne MS, Chen Y, Wang L, He X, Jin Y (2018) Rotation and manure amendment increase soil macro-aggregates and associated carbon and nitrogen stocks in flue-cured tobacco production. Geoderma 325:49–58
Acknowledgements
The authors gratefully acknowledge the funding received from The National Key Research and Development Program of China (2017YFD0201300).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflicts of interest.
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.
344_2020_10074_MOESM6_ESM.tif
Supplementary file 6. Fig. S1 Pearson’s correlation of the expression level among tobacco leaf samples (R2). The number “1” in the box represents a high degree of correlation (TIF 1530 kb)
344_2020_10074_MOESM7_ESM.tif
Supplementary file 7. Fig. S2 Volcano plot illustrating the number of DEGs. DEGs distribution in COR vs CK (a) and COR_PT vs CK_PT (b). The X-axis represents the fold change on a log2 scale, and the Y-axis represents the negative log10-transformed P-values (P < 0.05) between the samples (TIF 316 kb)
344_2020_10074_MOESM8_ESM.tif
Supplementary file 8. Fig. S3 GO classification of significantly differentially expressed genes. GO classification of DEGs in COR vs CK (a), COR_PT vs CK_PT comparisons (b). The X-axis represents functional classification, Y-axis represents number of genes (TIF 3309 kb)
344_2020_10074_MOESM9_ESM.tif
Supplementary file 9. Fig. S4 Verification of expression patterns of selected differentially expressed genes by qRT-PCR. The fold changes in gene expression were transformed to log2 scale. The X-axis represents RNA-seq data, Y-axis represents qRT-PCR data (TIF 166 kb)
Rights and permissions
About this article
Cite this article
Xu, J., Zhou, Y., Xu, Z. et al. Physiological and Transcriptome Profiling Analyses Reveal Important Roles of Coronatine in Improving Drought Tolerance of Tobacco. J Plant Growth Regul 39, 1346–1358 (2020). https://doi.org/10.1007/s00344-020-10074-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00344-020-10074-8