Comprehensive Understanding of the Interaction Among Stress Hormones Signalling Pathways by Gene Co-expression Network

Author(s): Maryam Mortezaeefar, Reza Fotovat*, Farid Shekari, Shahryar Sasani

Journal Name: Current Bioinformatics

Volume 14 , Issue 7 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Background: Plants respond to various stresses at the same time. Recent studies show that interactions of various phytohormones can play important roles in response to stresses.

Objective: Although many studies have been done about the effects of the individual hormones, little information exists about the crosstalk among the hormone signalling pathways in plants.

Methods: In this work, the weighted gene co-expression network analysis method was used to define modules containing genes with highly correlated expression patterns in response to abscisic acid, jasmonic acid, and salicylic acid in Arabidopsis.

Results: Results indicate that plant hormones cause major changes the expression profile and control diverse cell functions, including response to environmental stresses and external factors, cell cycle, and antioxidant activity. In addition, AtbHLH15 and HY5 transcription factors can participate in phytochrome pathways in response to the phytohormones. It is probable that some Type III WRKY transcription factors control the response to bacterium separately from the other stresses. The E2Fa/DPa transcription factor also regulates the cell cycle.

Conclusion: In general, many processes and pathways in plants may be regulated using a combination of abscisic acid, jasmonic acid, and salicylic acid.

Keywords: Abscisic acid, jasmonic acid, salicylic acid, E2Fa/DPa, HY5, light signalling.

Stingl N, Krischke M, Fekete A, Mueller MJ. Analysis of defense signals in Arabidopsis thaliana leaves by ultra-performance liquid chromatography/tandem mass spectrometry: jasmonates, salicylic acid, abscisic acid Plant Lipid Signaling Protocols. Springer 2013; pp. 103-13.
Okamoto M, Tsuboi Y, Goda H, et al. Multiple hormone treatment revealed novel cooperative relationships between abscisic acid and biotic stress hormones in cultured cells. Plant Biotechnol 2012; 29(1): 19-34.
Bosco R, Daeseleire E, Van Pamel E, Scariot V, Leus L. Development of an ultrahigh-performance liquid chromatography–electrospray ionization–tandem mass spectrometry method for the simultaneous determination of salicylic acid, jasmonic acid, and abscisic acid in rose leaves. J Agric Food Chem 2014; 62(27): 6278-84.
Delaney TP, Uknes S, Vernooij B, Friedrich L. A central role of salicylic acid in plant disease resistance. Science 1994; 266(5188): 1247.
Jiang CJ, Shimono M, Sugano S, et al. Abscisic acid interacts antagonistically with salicylic acid signaling pathway in rice-Magnaporthe grisea interaction. Mol Plant Microbe Interact 2010; 23(6): 791-8.
Creelman RA, Mullet JE. Jasmonic acid distribution and action in plants: regulation during development and response to biotic and abiotic stress. Proc Natl Acad Sci 1995; 92(10): 4114-9.
Lackman P, González-Guzmán M, Tilleman S, et al. Jasmonate signaling involves the abscisic acid receptor PYL4 to regulate metabolic reprogramming in Arabidopsis and tobacco. Proc Natl Acad Sci 2011; 108(14): 5891-6.
Anderson JP, Badruzsaufari E, Schenk PM, et al. Antagonistic interaction between abscisic acid and jasmonate-ethylene signaling pathways modulates defense gene expression and disease resistance in Arabidopsis. Plant Cell 2004; 16(12): 3460-79.
Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinformatics 2008; 9(1): 559.
Zhang B, Horvath S. A general framework for weighted gene co-expression network analysis. Stat Appl Genet Mol Biol 2005; 4(1): 17.
Smoot ME, Ono K, Ruscheinski J, Wang PL, Ideker T. Cytoscape 2.8: new features for data integration and network visualization. Bioinformatics 2011; 27(3): 431-2.
Du Z, Zhou X, Ling Y, Zhang Z, Su Z. agriGO: a GO analysis toolkit for the agricultural community. Nucleic Acids Res 2010; 38: 64-70.
Yi X, Du Z, Su Z. PlantGSEA: a gene set enrichment analysis toolkit for plant community. Nucleic Acids Res 2013; 41(1): 98-103.
Chen YA, Wen YC, Chang WC. AtPAN: an integrated system for reconstructing transcriptional regulatory networks in Arabidopsis thaliana. BMC Genomics 2012; 13(1): 85.
Duek PD, Fankhauser C. bHLH class transcription factors take centre stage in phytochrome signalling. Trends Plant Sci 2005; 10(2): 51-4.
Castillon A, Shen H, Huq E. Phytochrome interacting factors: central players in phytochrome-mediated light signaling networks. Trends Plant Sci 2007; 12(11): 514-21.
Sailsbery JK, Dean RA. Accurate discrimination of bHLH domains in plants, animals, and fungi using biologically meaningful sites. BMC Evol Biol 2012; 12(1): 154.
Yang T, Hao L, Yao S, et al. TabHLH1, a bHLH-type transcription factor gene in wheat, improves plant tolerance to Pi and N deprivation via regulation of nutrient transporter gene transcription and ROS homeostasis. Plant Physiol Biochem 2016; 104: 99-113.
Moon J, Zhu L, Shen H, Huq E. PIF1 directly and indirectly regulates chlorophyll biosynthesis to optimize the greening process in Arabidopsis. Proc Natl Acad Sci 2008; 105(27): 9433-8.
Seo JS, Joo J, Kim MJ, et al. OsbHLH148, a basic helix-loop-helix protein, interacts with OsJAZ proteins in a jasmonate signaling pathway leading to drought tolerance in rice. Plant J 2011; 65(6): 907-21.
Feng XM, Zhao Q, Zhao LL, et al. The cold-induced basic helix-loop-helix transcription factor gene MdCIbHLH1 encodes an ICE-like protein in apple. BMC Plant Biol 2012; 12(1): 22.
Goossens J, Swinnen G, Vanden-Bossche R, Pauwels L, Goossens A. Change of a conserved amino acid in the MYC2 and MYC3 transcription factors leads to release of JAZ repression and increased activity. New Phytol 2015; 206(4): 1229-37.
Pauwels L, Morreel K, De Witte E, et al. Mapping methyl jasmonate-mediated transcriptional reprogramming of metabolism and cell cycle progression in cultured Arabidopsis cells. Proc Natl Acad Sci 2008; 105(4): 1380-5.
Abe H, Urao T, Ito T, et al. Arabidopsis AtMYC2 (bHLH) and AtMYB2 (MYB) function as transcriptional activators in abscisic acid signaling. Plant Cell 2003; 15(1): 63-78.
Yadav V, Mallappa C, Gangappa SN, Bhatia S, Chattopadhyay S. A basic helix-loop-helix transcription factor in Arabidopsis, MYC2, acts as a repressor of blue light–mediated photomorphogenic growth. Plant Cell 2005; 17(7): 1953-66.
Toledo-Ortiz G, Johansson H, Lee KP, et al. The HY5-PIF regulatory module coordinates light and temperature control of photosynthetic gene transcription. PLoS Genet 2014; 10(6)e1004416
Casal JJ, Luccioni LG, Oliverio KA, Boccalandro HE. Light, phytochrome signalling and photomorphogenesis in Arabidopsis. Photochem Photobiol Sci 2003; 2(6): 625-36.
Carvalho RF, Campos ML, Azevedo RA. The role of phytochrome in stress tolerance. J Integr Plant Biol 2011; 53(12): 920-9.
Bu Q, Zhu L, Dennis MD, et al. Phosphorylation by CK2 enhances the rapid light-induced degradation of phytochrome interacting factor 1 in Arabidopsis. J Biol Chem 2011; 286(14): 12066-74.
Brock MT, Maloof JN, Weinig C. Genes underlying quantitative variation in ecologically important traits: PIF4 (phytochrome interacting factor 4) is associated with variation in internode length, flowering time, and fruit set in Arabidopsis thaliana. Mol Ecol 2010; 19(6): 1187-99.
de Lucas M, Davière JM, Rodríguez-Falcón M, et al. A molecular framework for light and gibberellin control of cell elongation. Nature 2008; 451(7177): 480-4.
Genoud T, Buchala AJ, Chua NH, Métraux JP. Phytochrome signalling modulates the SA‐perceptive pathway in Arabidopsis. Plant J 2002; 31(1): 87-95.
Chen F, Li B, Li G, et al. Arabidopsis phytochrome A directly targets numerous promoters for individualized modulation of genes in a wide range of pathways. Plant Cell 2014; 26(5): 1949-66.
Svyatyna K, Riemann M. Light-dependent regulation of the jasmonate pathway. Protoplasma 2012; 249(2): 137-45.
Staneloni RJ, Rodriguez-Batiller MJ, Casal JJ. Abscisic acid, high-light, and oxidative stress down-regulate a photosynthetic gene via a promoter motif not involved in phytochrome-mediated transcriptional regulation. Mol Plant 2008; 1(1): 75-83.
Schwechheimer C, Willige BC. Shedding light on gibberellic acid signalling. Curr Opin Plant Biol 2009; 12(1): 57-62.
Kidokoro S, Maruyama K, Nakashima K, et al. The phytochrome-interacting factor PIF7 negatively regulates DREB1 expression under circadian control in Arabidopsis. Plant Physiol 2009; 151(4): 2046-57.
Kim HJ, Kim YK, Park JY, Kim J. Light signalling mediated by phytochrome plays an important role in cold‐induced gene expression through the C‐repeat/dehydration responsive element (C/DRE) in Arabidopsis thaliana. Plant J 2002; 29(6): 693-704.
Zhang Y, Liu Z, Liu R, Hao H, Bi Y. Gibberellins negatively regulate low temperature-induced anthocyanin accumulation in a HY5/HYH-dependent manner. Plant Signal Behav 2011; 6(5): 632-4.
Catalá R, Medina J, Salinas J. Integration of low temperature and light signaling during cold acclimation response in Arabidopsis. Proc Natl Acad Sci 2011; 108(39): 16475-80.
Rushton PJ, Somssich IE, Ringler P, Shen QJ. WRKY transcription factors. Trends Plant Sci 2010; 15(5): 247-58.
Li J, Brader G, Palva ET. The WRKY70 transcription factor: a node of convergence for jasmonate-mediated and salicylate-mediated signals in plant defense. Plant Cell 2004; 16(2): 319-31.
Li J, Brader G, Kariola T, Tapio Palva E. WRKY70 modulates the selection of signaling pathways in plant defense. Plant J 2006; 46(3): 477-91.
Spoel SH, Koornneef A, Claessens SM, et al. NPR1 modulates cross-talk between salicylate-and jasmonate-dependent defense pathways through a novel function in the cytosol. Plant Cell 2003; 15(3): 760-70.
Wang D, Amornsiripanitch N, Dong X. A genomic approach to identify regulatory nodes in the transcriptional network of systemic acquired resistance in plants. PLoS Pathog 2006; 2(11)e123
Kim KC, Lai Z, Fan B, Chen Z. Arabidopsis WRKY38 and WRKY62 transcription factors interact with histone deacetylase 19 in basal defense. Plant Cell 2008; 20(9): 2357-71.
Pieterse CM, Van Loon L. NPR1: the spider in the web of induced resistance signaling pathways. Curr Opin Plant Biol 2004; 7(4): 456-64.
Fu ZQ, Yan S, Saleh A, et al. NPR3 and NPR4 are receptors for the immune signal salicylic acid in plants. Nature 2012; 486(7402): 228-32.
Moreau M, Tian M, Klessig DF. Salicylic acid binds NPR3 and NPR4 to regulate NPR1-dependent defense responses. Cell Res 2012; 22(12): 1631-3.
Ding Y, Dommel M, Mou Z. Abscisic acid promotes proteasome‐mediated degradation of the transcription coactivator NPR1 in Arabidopsis thaliana. Plant J 2016.
Shi Z, Maximova S, Liu Y, Verica J, Guiltinan MJ. The salicylic acid receptor NPR3 is a negative regulator of the transcriptional defense response during early flower development in Arabidopsis. Mol Plant 2013; 6(3): 802-16.
Zhang J, Liu B, Li M, et al. The bHLH transcription factor bHLH104 interacts with IAA-LEUCINE RESISTANT3 and modulates iron homeostasis in Arabidopsis. Plant Cell 2015; 27(3): 787-805.
Long TA, Tsukagoshi H, Busch W, et al. The bHLH transcription factor POPEYE regulates response to iron deficiency in Arabidopsis roots. Plant Cell 2010; 22(7): 2219-36.
Rodríguez-Celma J, Pan IC, Li W, et al. The transcriptional response of Arabidopsis leaves to Fe deficiency. Front Plant Sci 2013; 4: 276.
Montgomery BL, Oh S, Karakkat B. Molecular basis and fitness implications of the interplay between light and the regulation of iron homeostasis in photosynthetic organisms. Environ Exp Bot 2015; 114: 48-56.
Salomé PA, Oliva M, Weigel D, Krämer U. Circadian clock adjustment to plant iron status depends on chloroplast and phytochrome function. EMBO J 2013; 32(4): 511-23.
Li H, Wang L, Yang ZM. Co-expression analysis reveals a group of genes potentially involved in regulation of plant response to iron-deficiency. Gene 2015; 554(1): 16-24.
Aznar A, Chen NW, Rigault M, et al. Scavenging iron: a novel mechanism of plant immunity activation by microbial siderophores. Plant Physiol 2014; 164(4): 2167-83.
Cakmak I, Kirkby EA. Role of magnesium in carbon partitioning and alleviating photooxidative damage. Physiol Plant 2008; 133(4): 692-704.
Hermans C, Chen J, Coppens F, Inzé D, Verbruggen N. Low magnesium status in plants enhances tolerance to cadmium exposure. New Phytol 2011; 192(2): 428-36.
De Veylder L, Beeckman T, Beemster GT, et al. Control of proliferation, endoreduplication and differentiation by the Arabidopsis E2Fa–DPa transcription factor. EMBO J 2002; 21(6): 1360-8.
Vlieghe K, Vuylsteke M, Florquin K, et al. Microarray analysis of E2Fa-DPa-overexpressing plants uncovers a cross-talking genetic network between DNA replication and nitrogen assimilation. J Cell Sci 2003; 116(20): 4249-59.
Ganguly A, Dixit R. Mechanisms for regulation of plant kinesins. Curr Opin Plant Biol 2013; 16(6): 704-9.
Reddy A, Safadi F, Narasimhulu SB, Golovkin M, Hu X. A novel plant calmodulin-binding protein with a kinesin heavy chain motor domain. J Biol Chem 1996; 271(12): 7052-60.
Vinogradova MV, Malanina GG, Waitzman JS, Rice SE, Fletterick RJ. Plant kinesin-like calmodulin binding protein employs its regulatory domain for dimerization. PLoS One 2013; 8(6)e66669
Nishihama R, Soyano T, Ishikawa M, et al. Expansion of the cell plate in plant cytokinesis requires a kinesin-like protein/MAPKKK complex. Cell 2002; 109(1): 87-99.
Zhang Y, Turner JG. Wound-Induced Endogenous Jasmonates Stunt Plant Growth by Inhibiting Mitosis. PLoS One 2008; 3(11)e3699
Abe M, Shibaoka H, Yamane H, Takahashi N. Cell cycle-dependent disruption of microtubules by methyl jasmonate in tobacco BY-2 cells. Protoplasma 1990; 156(1): 1-8.
Noir S, Bömer M, Takahashi N, et al. Jasmonate controls leaf growth by repressing cell proliferation and the onset of endoreduplication while maintaining a potential stand-by mode. Plant Physiol 2013; 161(4): 1930-51.
Świa̧tek A, Lenjou M, Van Bockstaele D, Inzé D, Van Onckelen H. Differential effect of jasmonic acid and abscisic acid on cell cycle progression in tobacco BY-2 cells. Plant Physiol 2002; 128(1): 201-11.
Takatsuka H, Umeda M. Hormonal control of cell division and elongation along differentiation trajectories in roots. J Exp Bot 2014; 65(10): 2633-43.
Vanacker H, Lu H, Rate DN, Greenberg JT. A role for salicylic acid and NPR1 in regulating cell growth in Arabidopsis. Plant J 2001; 28(2): 209-16.
Peres A, Churchman ML, Hariharan S, et al. Novel plant-specific cyclin-dependent kinase inhibitors induced by biotic and abiotic stresses. J Biol Chem 2007; 282(35): 25588-96.
Chini A, Fonseca S, Fernandez G, et al. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 2007; 448(7154): 666-71.
Kazan K, Manners JM. JAZ repressors and the orchestration of phytohormone crosstalk. Trends Plant Sci 2012; 17(1): 22-31.
Pauwels L, Goossens A. The JAZ proteins: a crucial interface in the jasmonate signaling cascade. Plant Cell 2011; 23(9): 3089-100.
Qi T, Huang H, Wu D, et al. Arabidopsis DELLA and JAZ proteins bind the WD-repeat/bHLH/MYB complex to modulate gibberellin and jasmonate signaling synergy. Plant Cell 2014; 26(3): 1118-33.
Apel K, Hirt H. Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 2004; 55: 373-99.
Waszczak C, Akter S, Jacques S, et al. Oxidative post-translational modifications of cysteine residues in plant signal transduction. J Exp Bot 2015; 66(10): 2923-34.

Rights & PermissionsPrintExport Cite as

Article Details

Year: 2019
Published on: 17 September, 2019
Page: [602 - 613]
Pages: 12
DOI: 10.2174/1574893614666190226160742
Price: $65

Article Metrics

PDF: 38
PRC: 1