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. 2022 Jan 16;17(1):2024738. doi: 10.1080/15592324.2021.2024738

A DEK domain-containing protein GhDEK2D mediated Gossypium hirsutum enhanced resistance to Verticillium dahliae

Jinglong Zhou a,b,*, Lihong Zhao b,*, Yajie Wu b,c, Xiaojian Zhang b,c, Sheng Cheng a, Feng Wei b,c, Yalin Zhang b, Heqin Zhu b,c, Yi Zhou a,✉, Zili Feng b,✉, Hongjie Feng b,c,✉
PMCID: PMC9176258  PMID: 35034577

ABSTRACT

DEK is associated with DNA replication and break repair, mRNA splicing, and transcriptional regulation, which had been studied in humans and mammals. The function of DEK in plants was poorly understood. In this study, GhDEK2D was identified in Gossypium hirsutum by genome-wide and post-translational modifications. GhDEK2D had been phosphorylated, acetylated and ubiquitylated under Verticillium dahliae (Vd) challenge. The GhDEK2D-silenced cotton decreased resistance against Vd. In GhDEK2D-silenced cotton plants, the reactive oxygen species was activated, the callose, xylogen, hypersensitive reaction (HR) and expression levels of defense-related genes were reduced. Homozygous overexpressing-GhDEK2D transgenic Arabidopsis lines were more resistant to Verticillium wilt (Vw). We propose that GhDEK2D was a potential molecular target for improving resistance to Vw in cotton.

KEYWORDS: Verticillium dahliae (Vd), Dek domain containing protein, cotton resistance

1. Introduction

Cotton is one of the most important economic,1 textile fiber, and oilseed crop.2 G. hirsutum is characterized by high yield and quality fiber, and becomes the most cultivated species in the world cotton production.3 However, cotton production was affected by abiotic and biotic stresses in many regions of the world, among them, Vw is a destructive biotic stresses, which caused by the soil-borne fungus Vd.4,5 For the past few years, in the wake of climatic change, long-term mono-cropping and frequent introduction of a fine variety led to break out Vw in cotton.6 The fungus can form dormant structures called microsclerotia that can survive in the soil for years without a host and infect subsequent crops, so that Vw is difficult to control in cotton.

Post-translational modifications (PTMs) play a role in every aspect of cell biology by regulating many cellular processes.7 Phosphorylation, acetylation, and ubiquitination are important PTMs. They are necessary for functional signal transduction and metabolism, and are involved in chromatin conformation regulation, transcription, and cell metabolism.8 PTMs also affects cell localization, stability, interaction, and enzyme activity.9 Activity of proteins Phosphorylation, one of the most extensive modifications of proteins, is a reversible process catalyzed by a kinase that transfers a phosphorylating group in ATP to the hydroxyl group of a specific serine, threonine or tyrosine residue in the target protein.10,11 Phosphorylation is a key process that regulates plant growth, development and stress response.12 Reversible phosphorylation of serine, threonine, and tyrosine residues performs many important functions, such as altering protein conformation and activation states, protein stability and degradation, subcellular localization, and interaction with protein substrates.13 Mining resistance genes has become the major way to sustain cotton industry. Protein post-translational modifications is major defense mechanism for regulating plant immune.14 A growing body of PTMs profiling has provide convenience to excavate new resources.

DEK was originally cloned from acute myeloid leukemia and is a bona fide oncoprotein associated with many different tumor types, as well as with stem cell and progenitor cell quality.15–17 DEK was found in all multicellular organisms.18 Chromatin structure plays an important role in various processes.19 DEK proteins are involved in the control of various chromatin related processes.20 The function of DEK has been widely studied in mammals, and it takes part in DNA replication and repair, mRNA splicing, transcription regulation, cell lifetime, division and differentiation.21–24 In Arabidopsis, there are four DEK proteins, and named DEK1, DEK2, DEK3 and DEK4. DEK has been reported to be present in the nucleolus. DEK3 affects nucleosome occupancy and chromatin accessibility, and adjusts the expression levels of its target genes.25 The correct expression of DEK3 can regulate the response of plants to stress conditions such as high salt and heat shock. Arabidopsis DEK3 and DEK4 prevent early flowering by activating transcription of key flowering inhibitors.26 Silencing DEK2 or DEK4 in tomatoes accumulates more ROS during pathogen infection and alters the expression of PR1b, PR2, LaPA and PIN2. The results showed that DEK is involved in the regulation of defense response to pathogens.27

In this study, there were six DEKs, which were highly conservative proteins in G. hirsutum. GhDEK2D had been phosphorylated, acetylated and ubiquitylated after Vd inoculation. The GhDEK2D-silenced cottons decreased resistance against Vd. In contrast, overexpressing-GhDEK2D enhanced Arabidopsis resistance to Vd. In GhDEK2D-silenced cotton plants, ROS, callose, xylogen, expression levels of defense-related genes and HR genes were reduced. These all indicate that GhDEK2D involves in defense response’ regulation to pathogen in G. hirsutum.

2. Materials and methods

2.1. Fungal strain, plant lines, and culture conditions

In this study, a virulent, defoliating Vd Vd080 was used to infect plants,28 and its cultural method referenced Zhou et al.5

A G. hirsutum cultivar Zhongzhimian NO. 2 is resistance to Vd. They were grown in a conditioned greenhouse with a 16 h/8 h photoperiod at 22°C to 28°C. A. thaliana (Columbia) was grown in a conditioned greenhouse with a 16 h/8 h photoperiod at 22°C. The culture method of Nicotiana benthamiana is the same as that of Zhongzhimian NO. 2.

2.2. Sequence retrieval and identification of DEK genes

Twenty Arabidopsis DEK protein sequences were used as queries to conduct a homologous blast search against G. hirsutum, G. raimondii, G. arboretum, G. barbadense (https://cottonfgd.org/sequenceserver/),29–32 G. darwinii (https://phytozome-next.jgi.doe.gov/info/Gdarwinii_v1_1),33 G. tomentosum (https://phytozome-next.jgi.doe.gov/info/Gtomentosum_v1_1),34 G. mustelinum (https://phytozome-next.jgi.doe.gov/info/Gmustelinum_v1_1),33 Populus trichocarpa (https://phytozome-next.jgi.doe.gov/info/Ptrichocarpa_v4_1),35 Zea mays (https://phytozome-next.jgi.doe.gov/info/ZmaysB84_v1_2),36 Manihot esculenta (https://phytozome-next.jgi.doe.gov/info/Mesculenta_v8_1),37 Solanum lycopersicum (https://phytozome-next.jgi.doe.gov/info/Slycopersicum_ITAG4_0),38 S. tuberosum (https://phytozome-next.jgi.doe.gov/info/Stuberosum_v6_1)39 and Linum usitatissimum (https://phytozome-next.jgi.doe.gov/info/Lusitatissimum_v1_0)40 protein databases. The molecular weights (kDa) andisoelectric points (pI) of DEK proteins (G. hirsutum, G. raimondii, G. arboretum and G. barbadense) were surveyed from Cotton Functional Genomics Database.41

2.3. Phylogenetic, gene structure, conserved domain analysis and chromosomal mapping

A total of 4 Arabidopsis DEK protein sequences were downloaded from TAIR (https://www.arabidopsis.org/). Multiple sequence alignments of all identified DEK from cotton, P. trichocarpa, Z. mays, S. lycopersicum, S. tuberosum, L. usitatissimum and Arabidopsis were performed in ClustalX 2.0. After conducting a model test, a maximum likelihood (ML) phylogenic tree was constructed with the best substitution model using MEGA X software.42

TBtools was extracted to draw the gene structure of DEK based on the whole-genome sequence and annotation datas.43 Conserved motifs of DEK proteins were identified using the Multiple Em for Motif Elicitation Version 5.4.1 (https://meme-suite.org/meme/tools/meme) with the default parameters.44 The conserved domains of DEK proteins were identified by Batch Web CD-Search Tool (https://www.ncbi.nlm.nih.gov/Structure/bwrpsb/bwrpsb.cgi).45,46 The figures of gene structure, conserved motifs and domains were drew by TBtools software.47

Chromosomal position information about cotton DEKs was obtained from the CottonFGD webpage. GhDEK, GrDEK, GaDEK and GbDEK genes synteny and collinearity were determined and analyzed by the MCScanX software.48 And the distribution of DEK genes were draw used TBtools.

2.4. Transcriptome analysis of GhDEK in tissues of cotton and responded to Vd

The expression patterns of GhDEKs were exhibited in tissues, TM-1 transcriptome data from (Accession codes, SRA: PRJNA490626, https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA490626).49 The Zhongzhimian NO. 2 plants treated with Vd at 12 and 24 hpi, quantitative reverse transcription PCR (RT-qPCR) was used to determine GhDEKs expression levels.

2.5. Virus-induced gene silencing (VIGS) of GhDEK2D in cotton

VIGS were performed to inhibit expression of GhDEK2D, the experimentation as Feng et al.50

2.6. Arabidopsis thaliana transformation

In order to express GhDEK2D in A. thaliana, the primers OE-GhDEK2D-F and OE-GhDEK2D-R (Table S2) were used to clone the GhDEK2D. The GhDEK2D was inserted into the pCAMBIA3300-eGFP vector containing a glufosinate (Basta) resistance gene for overexpression studies. T0 – T3 transgenic seeds were sprayed with 0.01% Basta and PCR to select positive transformants. The high GhDEK2D expression T4 lines were used to study.

2.7. Plant disease resistance assay

Plants (A. tumefaciens and cotton) disease resistance assay as Zhou et al.5

2.8. Visualization and quantification of H2O2, lignification and callose staining

To visualize the accumulation of H2O2, cotton leaves were collected 48 h after Vd080 inoculation and incubated in DAB solution (1 mg/mL, pH 7.5) for 8 h. leaves were decolorized in 95% ethanol until the green color was completely removed in boiling water bath. ROS accumulation of leaves in 70% glycerol was observed under a microscope.

Cotton lignification was examined with phloroglucinol staining. The experimental procedure referenced Zhou et al.5 Thickness measurement were manipulated using ImageJ software.

Cotton callose deposition was visualized by aniline blue staining. The experimental procedure referenced Zhou et al.5 Thickness measurement were manipulated using ImageJ software.

2.9. Expression of defense-related genes by RT-qPCR

Cotton leaves were excised 0, 3, 6, 9, 12, 24, and 48 h post inoculation for RT-qPCR. The RNA was extracted by RNAprep Pure Plant Kit (TIANGEN, Beijing, China). The cDNA was synthesized by TransScript® All‐in‐One first‐strand cDNA Synthesis Super Mix for qPCR reverse transcription kit (TransGen, Beijing, China). qPCR was execute by TransStart® Tip Green qPCR Super Mix kit (TransGen, Beijing, China). The specific primers of cotton defense-related genes were listed in Table S4. Technical replicates of three independent biological samples were performed.

2.10. Subcellular localization

The A. tumefaciens strain GV3101 containing pCAMBIA3300-GhDEK2D-eGFP vector was used for subcellular localization. The experimentation as Feng et al.50 DAPI was used to mark cell nucleus.

3. Results

3.1. Identification and phylogenetic analysis of DEK genes family in cotton

To identify putative DEK family genes in cotton, 4 Arabidopsis DEK protein sequences were used as queries, and then conducted a homologous blast search against G. hirsutum (CRI), G. raimondii (JGI), G. arboretum (CRI) and G. barbadense (CRI) protein databases (https://cottonfgd.org/sequenceserver/). The potential DEK sequences were further inspected whether containing the conserved DEK motif by the InterProScan databases (https://www.ebi.ac.uk/interpro/search/sequence/). We obtained 6, 2, 3, and 7 DEKs in G. hirsutum, G. raimondii, G. arboretum and G. barbadense, respectively. The lengths of DEK proteins ranged from 360 to 642 amino acids, the molecular weight (MW) ranged from 41.333 kDa to 73.261 kDa, and the isoelectric point (IP) ranged from 4.571 to 8.033 (Table S1).

To further explore the evolutionary relationship of DEKs, 6 GhDEKs, 2 GrDEKs, 3 GaDEKs, 7 GbDEK, 6 GdDEK, 6 GtDEK, 5 GmDEK from cotton, 3 PtDEK from P. trichocarpa, 4 ZmDEK from Z. mays, 4 MeDEK from M. esculenta, 2 SlDEK from S. lycopersicum, 4 StDEK from S. tuberosum, 4 LuDEK from L. usitatissimum and 4 AtDEKs from Arabidopsis were used for constructing a phylogenetic tree by MEGA X software using the maximum likelihood (ML) method (Figure 1). The DEK family can be divided into four groups (I to IV), Group I only contained AtDEKs, Group II only contained 2 ZmDEKs, Group III contained 20 DEKs of 11 species, Group IV contained 30 DEKs of 12 species. The results suggested DEKs were highly conservative in respective species. The DEKs ID and names were listed in Table S2.

Figure 1.

Figure 1.

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Phylogenetic analysis of DEK in cotton and Arabidopsis.

A phylogenetic tree of DEK proteins from G. arboreum, G. raimondii, G. hirsutum, G. barbadense, G. darwinii, G. tomentosum, G. mustelinum, Populus trichocarpa, Zea mays, Manihot esculenta, Solanum lycopersicum, S. tuberosum, Linum usitatissimum and A. thaliana. The full-length amino acid sequences of the DEK proteins were aligned using ClustalX in MEGA X. The unrooted tree was generated by the maximum likelihood (ML) method (n = 1000 bootstraps). Clades are distinguished by different-colored line.

3.2. Chromosomal location and gene synteny analysis of DEK genes in Gossypium

The chromosomal locations of genes were investigated by the complete Gossypium genome sequence. A total of six GhDEK genes were distributed throughout the Gh_A04, Gh_A07, Gh_A12, Gh_D05, Gh_D07, and Gh_D12 subgenome. Three GaDEKs were distributed throughout the Ga_Chr05, Ga_Chr07, and Ga_Chr12 subgenome. Two GrDEKs were distributed throughout the Gr_Chr08 and Gr_Chr09 subgenome. Seven GbDEKs were distributed throughout the Gb_A04, Gb_A07, Gb_A12, Gb_D01, Gb_D05, Gb_D07 and Gb_D12 subgenome (Figure 2).

Figure 2.

Figure 2.

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The synteny relationship of DEK genes in G. arboreum, G. raimondii, G. hirsutum and G. barbadense.

MCScanX was used to identify genome collinearity and tandem repeats under default parameters, and TBtools was used to show collinearity. The different-colored lines represents paralogous gene pairs.

Syntenic analysis were performed to studies the relationships of DEK genes among the G. hirsutum, G. raimondii, G. arboretum, and G. barbadense (Figure 2). Among the DEK genes, six GhDEKs were the orthologous genes of the two GrDEKs, five GbDEKs and three GaDEKs, respectively. Five GbDEKs were the orthologous genes of the two GrDEKs and three GaDEKs, respectively. Two GrDEKs were the orthologous genes of the three GaDEKs. Some DEKs had not only one orthologous gene, such as GrDEK1 had four genes (GhDEK1A, GhDEK1D, GhDEK2A and GhDEK2D) in G. hirsutum, three genes (GbDEK1A, GbDEK2A and GbDEK2D) in G. barbadense, and two genes (GaDEK2 and GaDEK1) in G. arboretum. GrDEK4 had two genes (GhDEK4A and GhDEK4D) in G. hirsutum, two genes (GbDEK3D, and GbDEK4D) in G. barbadense. More orthologous genes were displayed in Table S5. In addition, there were two paralogous gene pairs (GhDEK1A/2A/1D/2D and GhDEK4A/4D) in G. hirsutum, one paralogous gene pair (GaDEK1/2) in G. arboretum, two paralogous gene pairs (GhDEK1A/2A/1D/2D and GhDEK3D/4A/4D) in G. barbadense, and zero paralogous gene pair in G. raimondii genome (Table S3). Furthermore, all cotton DEKs were classified into WGD or segmental duplications (Table S3). In the expansion of the DEK gene family, WGD or segmental duplication might play a crucial role.

3.3. Gene structure, conserved motifs and domain of DEKs

To better reveal the evolutionary relationships of the DEK gene family, a separate unrooted phylogenetic tree was constructed with DEK DNA sequences (Figure 3a). The comparative analysis of intron–exon structure showed that GhDEK gene length varied significantly. DEK genes had a highly rich distribution of introns in the regions, except GbDEK3D possessed 12 exons, other DEK genes possessed 11 exons (Figure 3b). In addition, closely related genes had more similar arrangements of gene structure. There were 15 conserved motifs (motif 1 to 15) in DEKs were identified by MEME software. The group I DEK proteins had fourteen motifs (except motif 14), the group II DEK (GbDEK3D) protein had nine motifs (motif 1, 2, 3, 4, 5, 10, 11, 12 and 13), and the group III DEK proteins contained all motifs (Figure 3c), indicating that they are highly conserved among DEKs. We also identified domains in the DEKs using Batch Web CD-Search Tool, so as to gene structure, closely related proteins had more similar arrangements of motifs and domains (Figure 3d).

Figure 3.

Figure 3.

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Homologous relationship, Structural, motif and domain analysis of DEKs in G. arboreum, G. raimondii, G. hirsutum and G. barbadense.

(a) Phylogenetic tree of DEK genes. The ML phylogenetic tree was constructed by using MEGA X with 1000 replicates. (b) Exon-intron organization analyses of DEK genes. Yellow boxes mean Untranslated Regions (UTR), Exons and introns are distinguished in green boxes and in black lines, respectively. (c) Conserved motifs of DEK proteins. Fifteen conserved motifs were identified through a MEME analysis, represented by different color boxes, and protein length was estimated via the scale at the bottom. (d) The conserved domains of DEK proteins.

3.4. Prediction of cis-acting elements in the promoters of GhDEKs

The 2.0 kb upstream promoter regions of GhDEKs were obtained and analyzed to predict the possible biological functions. Response to various stresses were our main focus, for instance salicylic acid, abscisic acid, defense, auxin, methyl jasmonate (MeJA), drought, etc., (Table 1). The abundance of cis-acting showed that GhDEK genes might perform different biological functions.

Table 1.

Prediction of cis-acting regulatory elements about various responses of GhDEK genes

  SA JA ABA Auxin Defense and stress Drought
GhDEK1A 0 2 2 2 1 0
GhDEK1D 0 2 2 2 1 0
GhDEK2A 1 4 0 0 0 2
GhDEK2D 0 6 4 0 0 0
GhDEK4A 1 2 2 0 2 1
GhDEK4D 2 2 3 0 2 0
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3.5. Expression patterns of GhDEKs in tissues of cotton

To explore the functions of the GhDEKs, the expression patterns of the six GhDEKs were analyzed in leaf, bract, filament, pental, anther, root, torus, stem, and sepal. GhDEK4A and GhDEK4D were higher than other genes in all tissues. All the genes expression were the highest in root (Figure 4a). Vd is a soil-borne fungus, which infests cotton roots, the abundance of DEKs in roots portend that DEKs might play an important role in against soil-borne fungus.

Figure 4.

Figure 4.

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Expression pattern analysis of GhDEK genes in tissues and under stress.

(a) The expression patterns of GhDEK genes in tissues (leaf, bract, filament, pental, anther, root, torus, stem and sepal.) were exhibited from the TM-1 transcriptome data. (b) The expression of GhDEKs under Vd080 were exhibited through RT-qPCR.

3.6. Expression patterns and post-translational modifications of GhDEKs under V. dahliae challenge

In the Vw-resistant cotton (Zhongzhimian NO. 2) plants treated with Vd080, at 12 hpi and 24 hpi, GhDEKs expression had no significant change compared with 0 hpi (Figure 4b). Under Vd challenge, only GhDEK2D had been phosphorylated, acetylated and ubiquitylated. A day after inoculation, GhDEK2D was phosphorylated, deubiquitylated in cotton resistant cultivar. GhDEK2D acetylation was activated in susceptible cultivar one and two days after inoculation. The mass spectrometry results showed that phosphorylation sites were Thr327 and Ser329, acetylation and ubiquitylation sites were Lys273 (Fig. S1). The results suggested that the GhDEK2D was important in response to Vd infection.

3.7. GhDEK2D silencing reduced the resistance of cotton to Vd

To verify the function of GhDEK2D resistance to Vd in cotton, the transcript activity of GhDEK2D was restrained by VIGS. When Zhongzhimian NO. 2 seedlings had grown for 10 days, we infiltrated cotyledons with TRV::00, TRV::GhDEK2D or TRV::PDS (a visible gene marker). When the albino phenotype appeared in TRV::GhPDS infected newly true leaves (Figure 5a). After 1 week of treatment with Vd080 by root dipping method. Compared with the TRV::00 plants, the morbidity of silencing plants was higher, such as wilted leaves and dark vascular bundles (Figure 5b,c). The disease index (Figure 5e) and disease levels (Figure 5f) were consistent with the plant phenotype. The results showed that the GhDEK2D silencing could attenuate plant resistance to Vd infection.

Figure 5.

Figure 5.

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Knock-down of GhDEK2D attenuates plant resistance to V. dahliae.

(a) Albino phenotype of GhPDS appeared 10 days after injection. (b) Disease phenotype of cotton plants post-infection with Vd080. Seedlings were inoculated with Vd a week after VIGS and photographed 30 days later. (c) Compared with the control plants, the silencing cottons were higher dark vascular bundles. The successful knock-down of the GhDEK2D transcript was confirmed by the qPCR analysis (d). The disease index (e) and disease levels analysis (f) of the plant were calculated. The data represent the mean ± SD, n = 3 (biological replicates) (*p < .05; **p < .01, t test).

3.8. GhDEK2D promotes plant defensive reaction

In order to explore the mechanism of GhDEK2D resistance to Vd infection, the cotton xylem was observed. A noticeable increase in the thickness of xylem in the control plants was observed (Figure 6a). The thickness of xylem were 52.99 μm and 115.09 μm in TRV::GhDEK2D and TRV::00, respectively (Figure 6b). A decreased density of callose depositions (number per mm2) was visualized in the leaves of silencing plants by staining with aniline blue (Figure 6c,d). The ROS changed in the control group was stronger (Figure 6e). Thesa results suggested that GhDEK2D silencing could reduce physical defense.

Figure 6.

Figure 6.

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GhDEK2D promotes plant defensive reaction.

The phenotype (a) and thickness (b) of xylem in the cotton plants were observed. Scale bar, 100 μm. (c, d) Callose deposition in leaves of TRV::00 and TRV:GhDEK2D cottons. Leaves were collected for aniline blue staining. Microscopy images were shown (c) and the number of callose deposits was recorded (d). Scale bar, 2 mm. (e) The ROS changed in the control group was stronger. The data represent the mean ± SD, n = 3 (biological replicates) (*p < .05; **p < .01, t test).

The expressions of cotton defense-related genes were tested by RT-qPCR in root. NOA is a gene related to nitricoxide synthesis pathway, NOA1 expression of TRV::00 plants were significantly higher than TRV::GhDEK2D at 3, 9, 12, 24 and 48 hpi (Figure 7a) HIN1 and HSR203J are HR marker gene. HIN1 expression of TRV::GhDEK2D were inhibited all the time (Figure 7b). HSR203J expression of TRV::GhDEK2D were inhibited at 3, 6, 12, 24 and 48 hpi (Figure 7c). PAL, PPO and POD play important roles in plant immunology. In our study, PAL expression of TRV::00 plants were significantly higher than TRV::GhDEK2D all the time (Figure 7d); PPO expression of TRV::00 plants were significantly higher than TRV::GhDEK2D at 3, 24 and 48 hpi (Figure 7e). At 6, 12, 24 and 48 hpi, POD expression was significant increase in TRV::00 plants, but it also had a quick low afterward (Figure 7f). The results suggested that the expressions of defense-related genes were broke in silenced cotton plants.

Figure 7.

Figure 7.

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Expression analysis of defense-related genes in roots of GhDEK2D-silenced and control cotton plants.

The expression levels of GhNOA1 (a), GhHIN1 (b), GhHSR203J (c), GhPAL (d), GhPPO (e) and GhPOD (f) defense-related genes under Vd080 inoculation in 3, 6, 9, 12, 24, and 48 hpi. The data represent the mean ± SD, n = 3 (biological replicates and technical replicates) (*p < .05; **p < .01, t test).

3.9. Overexpression of GhDEK2D enhances Arabidopsis resistance to Vd

In order to analyze the subcellular localization of GhDEK2D, by heterologous expression in tobacco leaves, we observed GhDEK2D was located on the cell nucleus of tobacco cells (Figure 8a). The resistance of overexpression of GhDEK2D transgenic plants to Vd was assessed with an in vitro technique. GhDEK2D-overexpressing Arabidopsis were more resistant to Vw than the WT plants (Figure 8b,c). These results indicated that GhDEK2D overexpression enhances Arabidopsis resistance to Vd.

Figure 8.

Figure 8.

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Enhanced disease resistance of Arabidopsis plants overexpressing GhDEK2D.

(a) The GhDEK2D was transiently expressed in tobacco leaves, GFP and DAPI staining were observed using confocal microscopy. GhDEK2D was located on cell nucleus of tobacco cells. DAPI is a cell nucleus-specific fluorescent probe. Scale bar, 50 μm. Symptoms of wild-type (WT), OE-GhDEK2D plants in nutrient soil at three weeks (b) after inoculation with Vd. The disease index (c) and disease levels (d) of WT and transgenic plants. Error bars indicate the SD of three biological replicates. The data represent the mean ± SD, n = 3 (biological replicates) (*p < .05; **p < .01, t test).

4. Disscussion

Chromatin plays a major role in the regulation of DNA-dependent processes. DEK as an architectural chromatin protein, which is associated with DNA, chromatin, and histone binding as well as DNA-folding activities.51 in Arabidopsis thaliana, there are four DEK genes, they are named DEK1, DEK2, DEK3, and DEK4, respectively.52 In G. hirsutum, six DEK proteins were named GhDEK1A, GhDEK1D, GhDEK2A, GhDEK2D, GhDEK4A, and GhDEK4D. The 60 DEK proteins were used for constructing a phylogenetic tree from 14 species. The same species proteins were clustered together, such as: SlDEKs, AtDEKs, LuDEKs, and so on (Figure 1). In cottons, gene structure, conserved motifs and domain of DEKs were semblable (Figure 3). The results suggested DEKs were conserved at the evolution.

Post-translationally can regulate a lot of plant receptors and critical signaling nodes, so that plant can rapidly and appropriately respond to biotic stresses. Protein is phosphorylated on serine, threonine, and tyrosine residues, which is a reversible reaction.53 Phosphorylation is major defense mechanism for controlling plant immune.14 The phosphorylation of WRKY33 upregulates camalexin biosynthesis in Arabidopsis upon pathogen infection.54 MPK3 and MPK6 phosphorylated ERF72 and improved its transactivation activity, resulting in increased camalexin concentration and increased resistance to Botrytis cinerea.55 The DEK (human chromatin protein) is phosphorylated by the protein kinase CK2.56 Acetylation of DEK affects the sub-nuclear localization and the ability to bind DNA.57 Fbxw7 acts as a tumor suppressor targeting multiple transcriptional activators and may target DEK for degradation to influence murine intestinal homeostasis and cancer by DEK ubiquitination.58 The intricate network of phosphorylation, acetylation, and ubiquitination mediated plant immunity had been reported. However, phosphorylation, acetylation, and ubiquitination of DEK hasn’t been studied. In this study, GhDEK2D had been phosphorylated, acetylated, and ubiquitylated under Vd challenge. As a positive regulator disease-resistant protein, GhDEK2D activated immunity by phosphorylated in cotton-resistant cultivar, and it was influenced by ubiquitylated in cotton-susceptible cultivar. GhDEK2D acetylation was activated in susceptible cultivar one and two days after inoculation, however, the function of DEK acetylation was unclear. The network of GhDEK2D phosphorylation, acetylation, and ubiquitination still needs further research.

In GhDEK2D-silenced cotton plants, the disease index was increscent (Figure 5), and the accumulation of ROS and callose in leaves, and xylogen in stems were reduced (Figure 6). ROS is an early events responses and a signal that activates downstream biochemical reaction.59 Deposition of callose at the cell wall is used in response to stress.60 Xylogen is a physical mechanism of plant stress resistance.61 Nitric oxide associated factor (NOA) is related to nitricoxide synthesis pathway, and indirectly regulates nitric oxide (NO) accumulation and response to stress.62,63 HIN1 and HSR203J are another specific marker gene for HR cell death.64,65 In the current study, the expression of GhNOA1, GhHIN1, and GhHSR203J were inhibited in silenced cotton plants (Figure 7a,b,c). PAL, POD and PPO as defense enzymes to involve in the formation of barriers against pathogens,66–68 the expression of disease-resistant genes in GhDEK2D silenced cottons were significantly decreased after Vd inoculation (Figure 7d,e,f). These changes lead to Vd was more likely to infect silenced cotton.

In Arabidopsis, DEK plays a central role in balancing the response between growth and arrest.69 Arabidopsis DEK3 and DEK4 facilitate the transcription of key flowering repressors by interacting with chromatin, and prevent precocious flowering. Tomato DEK involves in defense response regulation to Botrytis cinerea and Pseudomonas syringae.27 Overexpression of GhDEK2D enhances Arabidopsis resistance to Vd. However, the molecular mechanism of GhDEK2D against pathogen, which we need do in the future.

Supplementary Material

Supplemental Material
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Funding Statement

This work was supported by the Natural Science Foundation of Henan Province (No. 212300410418), the Central Public-interest Scientific Institution Basal Research Fund (No. 1610162021031), Key Technologies R&D Program of Henan Province (No. 192102110167) and the Agricultural Science and Technology Innovation Program of Chinese Academy of Agricultural Sciences.

Disclosure statement

No potential conflict of interest was reported by the author(s).

Contribution

Jinglong Zhou: Conceptualization, Methodology, Investigation, Validation, Writing – Original Draft, Writing - Review & Editing; Heqin Zhu: Conceptualization and supervision; Hongjie Feng: Conceptualization and supervision, funding acquisition; Yi Zhou: Conceptualization; Lihong Zhao: Methodology, Investigation; Sheng Cheng: Investigation; Yajie Wu: Data curation; Xiaojian Zhang: Data curation; Zili Feng: Formal analysis and Writing - original draft; Feng Wei: Conceptualization and supervision; Yalin Zhang: Writing - review & editing.

Supplementary material

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References

  • 1.Ai XT, Liang YJ, Wang JD, Zheng JY, Gong ZL, Guo JP, Li X, Qu Y.. Genetic diversity and structure of elite cotton germplasm (Gossypium hirsutum L.) using genome-wide SNP data. Genetica. 2017;145:409–13. doi: 10.1007/s10709-017-9976-8. [DOI] [PubMed] [Google Scholar]
  • 2.Zhang XY, Wang LM, Xu XY, Cai CP, Guo WZ.. Genome-wide identification of mitogen-activated protein kinase gene family in Gossypium raimondii and the function of their corresponding orthologs in tetraploid cultivated cotton. Bmc Plant Biol. 2014;14:14. doi: 10.1186/1471-2229-14-14. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 3.Zhang JF, Sanogo S, Flynn R, Baral JB, Bajaj S, Hughs SE, Percy RG . Germplasm evaluation and transfer of Verticillium wilt resistance from Pima (Gossypium barbadense) to Upland cotton (G. hirsutum). Euphytica. 2012; 187:147–160. doi: 10.1007/s10681-011-0549-0. [DOI] [Google Scholar]
  • 4.Fradin EF, Thomma BPHJ. Physiology and molecular aspects of Verticillium wilt diseases caused by V-dahliae and V-albo-atrum. Mol Plant Pathol. 2006;7:71–86. doi: 10.1111/j.1364-3703.2006.00323.x. [DOI] [PubMed] [Google Scholar]
  • 5.Zhou JL, Feng ZL, Liu SC, Wei F, Shi YQ, Zhao LH, Huang W, Zhou Y, Feng H, Zhu H . CGTase, a novel antimicrobial protein from Bacillus cereus YUPP-10, suppresses Verticillium dahliae and mediates plant defence responses. Mol Plant Pathol. 2021;22:130–144. doi: 10.1111/mpp.13014. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 6.Guo XH, Cai CP, Yuan DD, Zhang RS, Xi JL, Guo WZ. Development and identification of Verticillium wilt-resistant upland cotton accessions by pyramiding QTL related to resistance. J Integr Agr. 2016;15:512–520. doi: 10.1016/S2095-3119(15)61083-8. [DOI] [Google Scholar]
  • 7.Yakubu RR, Weiss LM, de Monerri NCS. Post-translational modifications as key regulators of apicomplexan biology: insights from proteome-wide studies. Mol Microbiol. 2018;107:1–23. doi: 10.1111/mmi.13867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 8.Hong G, Su X, Xu K, Liu B, Wang G, Li J, Wang R, Zhu M, Li G. Salt stress downregulates 2-hydroxybutyrylation in Arabidopsis siliques. J Proteomics. 2022;250:104383. doi: 10.1016/j.jprot.2021.104383. [DOI] [PubMed] [Google Scholar]
  • 9.Rao RSP, Thelen JJ, Miernyk JA. Is Lys-N-epsilon-acetylation the next big thing in post-translational modifications? Trends Plant Sci. 2014;19:550–553. doi: 10.1016/j.tplants.2014.05.001. [DOI] [PubMed] [Google Scholar]
  • 10.Zulawski M, Braginets R, Schulze WX. PhosPhAt goes kinases-searchable protein kinase target information in the plant phosphorylation site database PhosPhAt. Nucleic Acids Res. 2013;41:D1176–D84. doi: 10.1093/nar/gks1081. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 11.Sathyanarayanan PV, Poovaiah BW. Decoding Ca2+ signals in plants. CRC Crit Rev Plant Sci. 2004;23:1–11. doi: 10.1080/07352680490273310. [DOI] [PubMed] [Google Scholar]
  • 12.Yin XJ, Wang X, Komatsu S. Phosphoproteomics: protein phosphorylation in regulation of seed germination and plant growth. Curr Protein Pept Sc. 2018;19:401–412. doi: 10.2174/1389203718666170209151048. [DOI] [PubMed] [Google Scholar]
  • 13.Bredow M, Bender KW, Dingee AJ, Holmes DR, Thomson A, Ciren D, Tanney CAS, Dunning KE, Trujillo M, Huber SC, Monaghan J . Phosphorylation-dependent subfunctionalization of the calcium-dependent protein kinase CPK28. P Natl Acad Sci USA . 2021; 19:118. . doi: 10.1073/pnas.2024272118. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 14.Park CJ, Caddell DF, Ronald PC. Protein phosphorylation in plant immunity: insights into the regulation of pattern recognition receptor-mediated signaling. Front Plant Sci. 2012;3. doi: 10.3389/fpls.2012.00003. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 15.Von Lindern M, Fornerod M, van Baal S, Jaegle M, de Wit T, Buijs A, Grosveld G . The translocation (6;9), associated with a specific subtype of acute myeloid leukemia, results in the fusion of two genes, dek and can, and the expression of a chimeric, leukemia-specific dek-can mRNA. Mol Cell Biol. 1992;12:1687–1697. doi: 10.1128/mcb.12.4.1687-1697.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 16.Wise-Draper TM, Mintz-Cole RA, Morris TA, Simpson DS, Wikenheiser-Brokamp KA, Currier MA, Cripe TP, Grosveld GC, Wells SI. Overexpression of the cellular DEK protein promotes epithelial transformation in vitro and in vivo. Cancer Res. 2009;69:1792–1799. doi: 10.1158/0008-5472.CAN-08-2304. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 17.Riveiro-Falkenbach E, Soengas MS. Control of tumorigenesis and chemoresistance by the DEK oncogene. Clin Cancer Res. 2010;16:2932–2938. doi: 10.1158/1078-0432.CCR-09-2330. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 18.Waldmann T, Scholten I, Kappes F, Hu HG, Knippers R. The DEK protein–an abundant and ubiquitous constituent of mammalian chromatin. Gene. 2004;343:1–9. doi: 10.1016/j.gene.2004.08.029. [DOI] [PubMed] [Google Scholar]
  • 19.van Zanten M, Tessadori F, Peeters AJ, Fransz P. Shedding light on large-scale chromatin reorganization in Arabidopsis thaliana. Mol Plant. 2012;5:583–590. doi: 10.1093/mp/sss030. [DOI] [PubMed] [Google Scholar]
  • 20.Privette Vinnedge LM, Kappes F, Nassar N, Wells SI. Stacking the DEK: from chromatin topology to cancer stem cells. Cell Cycle. 2013;12:51–66. doi: 10.4161/cc.23121. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 21.Kavanaugh GM, Wise-Draper TM, Morreale RJ, Morrison MA, Gole B, Schwemberger S, Tichy ED, Lu L, Babcock GF, Wells JM, et al. The human DEK oncogene regulates DNA damage response signaling and repair. Nucleic Acids Res. 2011;39:7465–7476. doi: 10.1093/nar/gkr454. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 22.Alexiadis V, Waldmann T, Andersen J, Mann M, Knippers R, Gruss C. The protein encoded by the proto-oncogene DEK changes the topology of chromatin and reduces the efficiency of DNA replication in a chromatin-specific manner. Genes Dev. 2000;14:1308–1312. doi: 10.1101/gad.14.11.1308. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 23.Yang Y, Wu MY, Geng YQ, Liu XQ, Yang Y, Chen XM, Ding Y, He J, Wang Y, Xie L, et al. Roles of DEK in the endometrium of mice in early pregnancy. Gene. 2018;642:261–267. doi: 10.1016/j.gene.2017.11.011. [DOI] [PubMed] [Google Scholar]
  • 24.Smith EA, Gole B, Willis NA, Soria R, Starnes LM, Krumpelbeck EF, Jegga AG, Ali AM, Guo H, Meetei AR, Andreassen PR, Kappes F, Privette Vinnedge LM, Daniel JA, Scully R, Wiesmüller L, Wells SI . DEK is required for homologous recombination repair of DNA breaks. Sci Rep-Uk. 2017;7: 44662. doi: 10.1038/srep44662. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 25.Waidmann S, Kusenda B, Mayerhofer J, Mechtler K, Jonak C. A DEK domain-containing protein modulates chromatin structure and function in Arabidopsis. Plant Cell. 2014;26:4328–4344. doi: 10.1105/tpc.114.129254. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 26.Zong W, Zhao B, Xi Y, Bordiya Y, Mun H, Cerda NA, Kim D-H, Sung S. DEK domain-containing proteins control flowering time in Arabidopsis. New Phytol. 2021;231:182–192. doi: 10.1111/nph.17366. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 27.Zhang H, Yan M, Deng R, Song F, Jiang M. The silencing of DEK reduced disease resistance against Botrytis cinerea and Pseudomonas syringae pv. tomato DC3000 based on virus-induced gene silencing analysis in tomato. Gene. 2020;727:144245. doi: 10.1016/j.gene.2019.144245. [DOI] [PubMed] [Google Scholar]
  • 28.Li ZF, Liu YJ, Feng ZL, Feng HJ, Klosterman SJ, Zhou FF, Zhao LH, Shi YQ, Zhu QH . VdCYC8, encoding CYC8 glucose repression mediator protein, is required for microsclerotia formation and full virulence in Verticillium dahliae. Plos One. 2015;10:e0144020. doi: 10.1371/journal.pone.0144020. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 29.Li FG, Fan GY, Lu CR, Xiao GH, Zou CS, Kohel RJ, Ma Z, Shang H, Ma X, Wu J, et al. Genome sequence of cultivated Upland cotton (Gossypium hirsutum TM-1) provides insights into genome evolution. Nat Biotechnol. 2015;33:524–U242. doi: 10.1038/nbt.3208. [DOI] [PubMed] [Google Scholar]
  • 30.Paterson AH, Wendel JF, Gundlach H, Guo H, Jenkins J, Jin DC, Llewellyn D, Showmaker KC, Shu S, Udall J, et al. Repeated polyploidization of Gossypium genomes and the evolution of spinnable cotton fibres. Nature. 2012;492:423-+. doi: 10.1038/nature11798. [DOI] [PubMed] [Google Scholar]
  • 31.Li FG, Fan GY, Wang KB, Sun FM, Yuan YL, Song GL, Li Q, Ma ZY, Lu CR, Zou CS, Chen WB, Liang XM, Shang HH, Liu WQ, Shi CC, Xiao GH, Gou CY, Ye WW, Zhang XY, Wei HL, Li ZF, et al. Genome sequence of the cultivated cotton Gossypium arboreum. Nat Genet. 2014;46:567–572. doi: 10.1038/ng.2987. [DOI] [PubMed] [Google Scholar]
  • 32.Yuan DJ, Tang ZH, Wang MJ, Gao WH, Tu LL, Jin X, Chen LL, He YH, Zhang L, Zhu LF, Li Y, Liang QQ, Lin ZX, Yang XY, Liu N, Jin SX, Lei Y, Ding YH, Li GL, Ruan XA, Ruan YJ, et al. The genome sequence of Sea-Island cotton (Gossypium barbadense) provides insights into the allopolyploidization and development of superior spinnable fibres. Scientific reports. 2015;5:1–16 . doi: 10.1038/srep17662. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 33.Chen ZJ, Sreedasyam A, Ando A, Song QX, De Santiago LM, Hulse-Kemp AM, Ding M, Ye W, Kirkbride RC, Jenkins J, et al. Genomic diversifications of five Gossypium allopolyploid species and their impact on cotton improvement. Nat Genet. 2020;52:525-+. doi: 10.1038/s41588-020-0614-5. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 34.Shen C, Wang NA, Zhu D, Wang PC, Wang MJ, Wen TW, Le Y, Wu M, Yao T, Zhang X, et al. Gossypium tomentosum genome and interspecific ultra-dense genetic maps reveal genomic structures, recombination landscape and flowering depression in cotton. Genomics. 2021;113:1999–2009. doi: 10.1016/j.ygeno.2021.04.036. [DOI] [PubMed] [Google Scholar]
  • 35.Tuskan GA, Difazio S, Jansson S, Bohlmann J, Grigoriev I, Hellsten U, Putnam N, Ralph S, Rombauts S, Salamov A, Schein J, Sterck L, Aerts A, Bhalerao RR, Bhalerao RP, Blaudez D, Boerjan W, Brun A, Brunner A, Busov V, Campbell M, et al. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray). Vol. . Science. 2006;313: 1596–1604 . doi: 10.1126/science.1128691. [DOI] [PubMed] [Google Scholar]
  • 36.Bornowski N, Michel KJ, Hamilton JP, Ou S, Seetharam AS, Jenkins J, Grimwood J, Plott C, Shu S, Talag J, et al. Genomic variation within the maize stiff-stalk heterotic germplasm pool. The Plant Genome. 2021;14:e20114. doi: 10.1002/tpg2.20114. [DOI] [PubMed] [Google Scholar]
  • 37.Alaba OA, Bredeson JV, Egesi CN, Esuma W, Ezenwaka L, Ferguson ME, Ha CM, Hall M, Herselman L, Ikpan A, Kafiriti E, Kanju E, Kapinga F, Karugu A, Kawuki R, Kimata B, Kimurto R, Kulakow P, Kulembeka H, Kusolwa P, Lyons JB, et al. High-resolution linkage map and chromosome-scale genome assembly for cassava (Manihot esculenta Crantz) from 10 populations. G3-Genes Genom Genet. 2015;5:133–144. doi: 10.1534/g3.114.015008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 38.Hosmani PS, Flores-Gonzalez M, van de Geest H, Maumus F, Bakker LV, Schijlen E, Jan Cordewener JH, Sanchez-Perez G, Peters S, Fei Z, Giovannoni JJ, Mueller LA, Saha S . An improved de novo assembly and annotation of the tomato reference genome using single-molecule sequencing, Hi-C proximity ligation and optical maps. bioRxiv. 2019:767764. 10.1101/767764 [DOI]
  • 39.Pham GM, Hamilton JP, Wood JC, Burke JT, Zhao HN, Vaillancourt B, Ou S, Jiang J, Buell CR. Construction of a chromosome-scale long-read reference genome assembly for potato. Gigascience. 2020;9. doi: 10.1093/gigascience/giaa100. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 40.Wang ZW, Hobson N, Galindo L, Zhu SL, Shi DH, McDill J, Yang L, Hawkins S, Neutelings G, Datla R, et al. The genome of flax (Linum usitatissimum) assembled de novo from short shotgun sequence reads. Plant J. 2012;72:461–473. doi: 10.1111/j.1365-313X.2012.05093.x. [DOI] [PubMed] [Google Scholar]
  • 41.Zhu T, Liang CZ, Meng ZG, Sun GQ, Meng ZH, Guo SD, Zhang R . CottonFGD: an integrated functional genomics database for cotton. Bmc Plant Biol. 2017;17(1):17. doi: 10.1186/s12870-017-0972-z. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 42.Kumar S, Stecher G, Li M, Knyaz C, Tamura KMEGAX. Molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol. 2018;35:1547–1549. doi: 10.1093/molbev/msy096. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 43.Hu B, Jin J, Guo A-Y, Zhang H, Luo J, Gao GJB. GSDS 2.0: an upgraded gene feature visualization server. Bioinformatics (Oxford, England). 2015;31:1296–1297. doi: 10.1093/bioinformatics/btu817. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 44.Bailey TL, Williams N, Misleh C, Li WW. MEME: discovering and analyzing DNA and protein sequence motifs. Nucleic Acids Res. 2006;34:W369–W73. doi: 10.1093/nar/gkl198. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 45.Marchler-Bauer A, Bo Y, Han LY, He JE, Lanczycki CJ, Lu SN, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, et al. CDD/SPARCLE: functional classification of proteins via subfamily domain architectures. Nucleic Acids Res. 2017;45:D200–D3. doi: 10.1093/nar/gkw1129. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 46.Lu SN, Wang JY, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Marchler GH, Song JS, et al. CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res. 2020;48:D265–D8. doi: 10.1093/nar/gkz991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 47.Chen CJ, Chen H, Zhang Y, Thomas HR, Frank MH, He YH, Xia R. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020;13:1194–1202. doi: 10.1016/j.molp.2020.06.009. [DOI] [PubMed] [Google Scholar]
  • 48.Wang YP, Tang HB, DeBarry JD, Tan X, Li JP, Wang XY, Lee T, Jin HZ, Marler B, Guo H, Kissinger JC, Paterson AH . MCScanX: a toolkit for detection and evolutionary analysis of gene synteny and collinearity. Nucleic Acids Res . 2012;40:e49. doi: 10.1093/nar/gkr1293. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 49.Hu Y, Chen JD, Fang L, Zhang ZY, Ma W, Niu YC, Ju L, Deng J, Zhao T, Lian J, et al. Gossypium barbadense and Gossypium hirsutum genomes provide insights into the origin and evolution of allotetraploid cotton. Nat Genet. 2019;51:739-+. doi: 10.1038/s41588-019-0371-5. [DOI] [PubMed] [Google Scholar]
  • 50.Feng HJ, Li C, Zhou JL, Yuan Y, Feng ZL, Shi YQ, Zhao L, Zhang Y, Wei F, Zhu H, et al. A cotton WAKL protein interacted with a DnaJ protein and was involved in defense against Verticillium dahliae. Int J Biol Macromol. 2021;167:633–643. doi: 10.1016/j.ijbiomac.2020.11.191. [DOI] [PubMed] [Google Scholar]
  • 51.Sawatsubashi S, Murata T, Lim J, Fujiki R, Ito S, Suzuki E, Tanabe M, Zhao Y, Kimura S, Fujiyama S, et al. A histone chaperone, DEK, transcriptionally coactivates a nuclear receptor. Gene Dev. 2010;24:159. 2012; 26:2118. doi: 10.1101/gad.1857410. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 52.Pendle AF, Clark GP, Boon R, Lewandowska D, Lam YW, Andersen J, Mann M, Lamond AI, Brown JWS, Shaw PJ, et al. Proteomic analysis of the Arabidopsis nucleolus suggests novel nucleolar functions. Mol Biol Cell. 2005;16:260–269. doi: 10.1091/mbc.e04-09-0791. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 53.He ZQ, Huang TT, Ao K, Yan XF, Huang Y. Sumoylation, phosphorylation, and acetylation fine-tune the turnover of plant immunity components mediated by ubiquitination. Front Plant Sci. 2017;8:8. doi: 10.3389/fpls.2017.00008. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 54.Zhou JG, Wang XY, He YX, Sang T, Wang PC, Dai SJ, Zhang S, Meng X. Differential phosphorylation of the transcription factor WRKY33 by the protein kinases CPK5/CPK6 and MPK3/MPK6 cooperatively regulates camalexin biosynthesis in Arabidopsis. Plant Cell. 2020;32:2621–2638. doi: 10.1105/tpc.19.00971. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 55.Li Y, Liu K, Tong G, Xi C, Liu J, Zhao H, Wang Y, Ren D, Han S . MPK3/MPK6-mediated phosphorylation of ERF72 positively regulates resistance to Botrytis cinerea through directly and indirectly activating the transcription of camalexin biosynthesis enzymes. J Exp Bot. 2021;73:413–428. doi: 10.1093/jxb/erab415. [DOI] [PubMed] [Google Scholar]
  • 56.Kappes F, Damoc C, Knippers R, Przybylski M, Pinna LA, Gruss C. Phosphorylation by protein kinase CK2 changes the DNA binding properties of the human chromatin protein DEK. Mol Cell Biol. 2004;24:6011–6020. doi: 10.1128/MCB.24.13.6011-6020.2004. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 57.Cleary J, Sitwala KV, Khodadoust MS, Kwok RPS, Mor-Vaknin N, Cebrat M, Cole PA, Markovitz DM . p300/CBP-associated factor drives DEK into interchromatin granule clusters. J Biol Chem. 2005;280:31760–31767. doi: 10.1074/jbc.M500884200. [DOI] [PubMed] [Google Scholar]
  • 58.Babaei-Jadidi R, Li NN, Saadeddin A, Spencer-Dene B, Jandke A, Muhammad B, Ibrahim EE, Muraleedharan R, Abuzinadah M, Davis H, et al. FBXW7 influences murine intestinal homeostasis and cancer, targeting Notch, Jun, and DEK for degradation. J Exp Med. 2011;208:295–312. doi: 10.1084/jem.20100830. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 59.Wang S, Wu X, Liu CH, Shan JY, Guo HS. Verticillium dahliae chromatin remodeling facilitates the DNA damage repair in response to plant ROS stress. Plos Pathog. 2020;16:e1008481. doi: 10.1371/journal.ppat.1008481. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 60.Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J. Callose deposition: a multifaceted plant defense response. Mol Plant Microbe Interact. 2011;24:183–193. doi: 10.1094/MPMI-07-10-0149. [DOI] [PubMed] [Google Scholar]
  • 61.Barros J, Serk H, Granlund I, Pesquet E. The cell biology of lignification in higher plants. Ann Bot. 2015;115:1053–1074. doi: 10.1093/aob/mcv046. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 62.Mwaba I, Rey MEC. Nitric oxide associated protein 1 is associated with chloroplast perturbation and disease symptoms in Nicotiana benthamiana infected with South African cassava mosaic virus. Virus Res. 2017;238:75–83. doi: 10.1016/j.virusres.2017.05.022. [DOI] [PubMed] [Google Scholar]
  • 63.Durner J, Wendehenne D, Klessig DF. Defense gene induction in tobacco by nitric oxide, cyclic GMP, and cyclic ADP-ribose. P Natl Acad Sci USA. 1998;95:10328–10333. doi: 10.1073/pnas.95.17.10328. [DOI] [PMC free article] [PubMed] [Google Scholar]
  • 64.Pontier D, Tronchet M, Rogowsky P, Lam E, Roby D. Activation of hsr203, a plant gene expressed during incompatible plant-pathogen interactions, is correlated with programmed cell death. Mol Plant Microbe Interact. 1998;11:544–554. doi: 10.1094/MPMI.1998.11.6.544. [DOI] [PubMed] [Google Scholar]
  • 65.Takahashi Y, Berberich T, Yamashita K, Uehara Y, Miyazaki A, Kusano T. Identification of tobacco HIN1 and two closely related genes as spermine-responsive genes and their differential expression during the Tobacco mosaic virus-induced hypersensitive response and during leaf- and flower-senescence. Plant Mol Biol. 2004;54:613–622. doi: 10.1023/B:PLAN.0000038276.95539.39. [DOI] [PubMed] [Google Scholar]
  • 66.Appel HM. Phenolics in ecological interactions: the importance of oxidation. J Chem Ecol. 1993;19:1521–1552. doi: 10.1007/BF00984895. [DOI] [PubMed] [Google Scholar]
  • 67.Mandal S, Mitra A. Reinforcement of cell wall in roots of Lycopersicon esculentum through induction of phenolic compounds and lignin by elicitors. Physiol Mol Plant Pathol. 2007;71:201–209. doi: 10.1016/j.pmpp.2008.02.003. [DOI] [Google Scholar]
  • 68.Palmer CV, McGinty ES, Cummings DJ, Smith SM, Bartels E, Mydlarz LD. Patterns of coral ecological immunology: variation in the responses of Caribbean corals to elevated temperature and a pathogen elicitor. J Exp Biol. 2011;214:4240–4249. doi: 10.1242/jeb.061267. [DOI] [PubMed] [Google Scholar]
  • 69.Brestovitsky A, Ezer D, Waidmann S, Maslen SL, Balcerowicz M, Cortijo S, Charoensawan V, Martinho C, Rhodes D, Jonak C, Wigge PA . DEK influences the trade-off between growth and arrest via H2A. Z-nucleosomes in Arabidopsis. bioRxiv 2019:829226.

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