24-Epibrassinolide Facilitates Adventitious Root Formation by Coordinating Cell-Wall Polyamine Oxidase- and Plasma Membrane Respiratory Burst Oxidase Homologue-Derived Reactive Oxygen Species in Capsicum annuum L.
<p>EBL promotes AR formation in the hypocotyls of pepper explants. (<b>A</b>–<b>C</b>) Effects of EBL on AR formation of pepper. Pepper explants with primary root excision were treated with EBL at different concentrations (0–5000 nM) for 10 days, followed by photographing (<b>A</b>), counting of AR number (<b>B</b>), and determination of AR average length (<b>C</b>). (<b>D</b>–<b>F</b>) Effects of BRz on AR formation of pepper. Pepper explants were treated with BRz at concentrations of 1.5 and 5.0 μM for 10 days. Each treatment has 15 pepper explants. Different lowercase letters indicate that the values were significantly different among different treatments (<span class="html-italic">p</span> < 0.05).</p> "> Figure 2
<p>Kinetics of changes in H<sub>2</sub>O<sub>2</sub> and O<sub>2</sub><sup>•−</sup> contents during AR formation in EBL- or BRz-treated pepper explants. (<b>A</b>,<b>B</b>) Contents of H<sub>2</sub>O<sub>2</sub> (<b>A</b>) and O<sub>2</sub><sup>•−</sup> (<b>B</b>) in the AR zone of pepper hypocotyls after different durations of EBL or BRz treatments. (<b>C</b>,<b>D</b>) Histochemical staining of H<sub>2</sub>O<sub>2</sub> (<b>C</b>) and O<sub>2</sub><sup>•−</sup> (<b>D</b>) in the AR zone after different durations of EBL or BRz treatments. Once primary roots were cut, pepper explants were treated with water (Control), EBL (50 nM), or BRz (5 μM), and used for AR formation. Hypocotyl samples were harvested at indicated hours (h) after treatment. One asterisk (*) and two asterisks (**) in (<b>A</b>,<b>B</b>) indicate that the mean values of three replicates were significantly different between control and treatment at each time point at <span class="html-italic">p</span> < 0.05 and <span class="html-italic">p</span> < 0.01, respectively. FW, fresh weight. The scale bar in (<b>C</b>,<b>D</b>) is 5 mm.</p> "> Figure 3
<p>Involvement of ROS in EBL-promoted AR formation in pepper explants. (<b>A</b>) Effects of KI and DMTU on EBL-induced AR formation. Once primary roots were cut, pepper explants were used for AR formation in water without (Control) or with EBL (50 nM), EBL + KI (0.5 mM), or EBL + DMTU (2 mM) for 10 days, followed by photographing phenotype and counting AR number. KI and DMTU were used as ROS scavengers. KI, potassium iodide; DMTU, <span class="html-italic">N</span>,<span class="html-italic">N</span>’-Dimethylthiourea. (<b>B</b>,<b>C</b>) Contents of H<sub>2</sub>O<sub>2</sub> (<b>B</b>) and O<sub>2</sub><sup>•−</sup> (<b>C</b>) in the AR zone of pepper explants treated with EBL, EBL + KI, or EBL + DMTU for 6, 24, 48, and 120 h. (<b>D</b>) Effects of CAT on EBL-induced AR formation. AR formation in pepper explants treated with EBL (50 nM) or EBL + CAT (200 unit/mg) for 10 days, followed by photographing phenotype and counting AR number. Each treatment has 15 pepper explants. Different lowercase letters indicated that the values were significantly different among different treatments (<span class="html-italic">p</span> < 0.05).</p> "> Figure 4
<p>Involvement of PAO-dependent H<sub>2</sub>O<sub>2</sub> and NADPH oxidase-dependent O<sub>2</sub><sup>•−</sup> in EBL-promoted AR formation in pepper explants: (<b>A</b>) Effects of AG, MDL72527, 2-HEH, and DPI on EBL-induced AR formation. Once primary roots were cut, pepper explants were used for AR formation in water with EBL (50 nM), EBL + AG (100 μM), EBL + MDL72527 (MDL, 100 μM), EBL + 2-HEH (100 μM), or EBL + DPI (10 μM) for 10 days, followed by photographing phenotype and counting AR number. DPI and AG were inhibitors of copper amine oxidase and NADPH oxidase, respectively; MDL and 2-HEH were PAO inhibitors. AG, aminoguanidine; 2-HEH, 2-hydroxyethylhydrazine; DPI, diphenyleneiodonium. (<b>B</b>) Effects of EBL on the activities of cell-wall PAO (CW-PAO) during AR formation. (<b>C</b>,<b>D</b>) Effects of MDL72527 and 2-HEH on EBL-induced CW-PAO activity (<b>C</b>) and H<sub>2</sub>O<sub>2</sub> content (<b>D</b>) at 24 h of AR formation. (<b>E</b>) Effects of EBL on the activities of plasma membrane NADPH oxidase (PM-NADPH oxidase) during AR formation. (<b>F</b>,<b>G</b>) Effects of DPI on EBL-induced PM-NADPH oxidase activity (<b>F</b>) and O<sub>2</sub><sup>•−</sup> content (<b>G</b>) at 72 h of AR formation. (<b>H</b>) Expression of <span class="html-italic">CaLBD</span>, <span class="html-italic">CaCYCLIN</span>, and <span class="html-italic">CaCDK</span> genes in response to EBL, EBL + MDL, and EBL + DPI treatments at 72 h of AR formation. The expression level for each gene in the mock plants at 0 dpe was normalized to 1.0. The accession numbers for these genes are listed in <a href="#app1-antioxidants-12-01451" class="html-app">Table S4</a>. Each treatment contains three biological replicates, and each replicate has 15 explants. Different lowercase letters in (<b>A</b>,<b>C</b>,<b>D</b>,<b>F</b>–<b>H</b>) indicate that the mean values of three replicates are significantly different among different treatments (<span class="html-italic">p</span> < 0.05). Two asterisks (**) in (<b>B</b>,<b>E</b>) indicate significant differences between control and EBL treatment at <span class="html-italic">p</span> < 0.01.</p> "> Figure 5
<p>Phylogenetic analysis of CaPAO family and EBL-induced expression of <span class="html-italic">CaPAO</span>s during AR formation in pepper explants: (<b>A</b>) Neighbor-joining phylogenetic tree of the CaPAO, AtPAO, and SlPAO proteins. The accession numbers for these proteins are listed in <a href="#app1-antioxidants-12-01451" class="html-app">Table S1</a>. (<b>B</b>) The secretory signal peptide in the N-terminal of CaPAO1 and SlPAO1 proteins. The green dashed square indicates the secretory signal peptide. Invariant residues are shaded in blue boxes, with residues that are conserved colored red, and variable residues shown in black. (<b>C</b>) Expression levels of <span class="html-italic">CaPAO</span> genes in the base of pepper hypocotyls before AR formation. The expression level of each <span class="html-italic">CaPAO</span> gene was normalized to <span class="html-italic">CaUBI3</span> expression. (<b>D</b>) Effects of EBL and BRz on the expression of <span class="html-italic">CaPAO</span> genes during AR formation. The expression level at 0 h was normalized to 1.0. Each treatment contains three biological replicates, and each replicate has 15 explants. Different lowercase letters in (<b>C</b>) indicate that the mean values of three replicates are significantly different among different genes (<span class="html-italic">p</span> < 0.05). Two asterisks (**) in (<b>D</b>) indicate significant differences between control and EBL or BRz treatment at <span class="html-italic">p</span> < 0.01.</p> "> Figure 6
<p>Phylogenetic analysis of CaRBOH family and EBL-induced expression of <span class="html-italic">CaRBOH</span>s during AR formation in pepper explants. (<b>A</b>) Neighbor-joining phylogenetic tree of CaRBOH, AtRBOH, and SlRBOH proteins. The accession numbers of these proteins are listed in <a href="#app1-antioxidants-12-01451" class="html-app">Supplementary Table S1</a>. (<b>B</b>) Expression levels of <span class="html-italic">CaRBOH</span> genes in the base of pepper hypocotyls before AR formation. The expression level of each gene was normalized to <span class="html-italic">CaUBI3</span> expression. (<b>C</b>) Effects of EBL and BRz on the expression of <span class="html-italic">CaRBOH</span> genes during AR formation in pepper hypocotyls. The expression level for each gene at 0 h was normalized to 1.0. Each treatment contains three biological replicates, and each replicate has 15 explants. Different lowercase letters in (<b>B</b>) indicate that the mean values of three replicates are significantly different among different genes (<span class="html-italic">p</span> < 0.05). One asterisk (*) and two asterisks (**) in (<b>C</b>) indicate significant differences between control and EBL or BRz treatment at <span class="html-italic">p</span> < 0.05 and <span class="html-italic">p</span> < 0.01, respectively.</p> "> Figure 7
<p>Capability of CaPAO1, CaRBOH2, CaRBOH5, and CaRBOH6 in ROS production based on transient expression analysis. (<b>A</b>,<b>B</b>) Relative expression level of <span class="html-italic">CaPAO1</span> (<b>A</b>) and detection of endogenous H<sub>2</sub>O<sub>2</sub> by DAB staining (<b>B</b>) in pepper leaves expressing <span class="html-italic">CaPAO1</span>. (<b>C</b>,<b>D</b>) Relative expression levels of <span class="html-italic">CaRBOH2</span>, <span class="html-italic">CaRBOH5</span>, and <span class="html-italic">CaRBOH6</span> (<b>C</b>) and detection of endogenous O<sub>2</sub><sup>•−</sup> by NBT staining (<b>D</b>) in pepper leaves expressing <span class="html-italic">CaRBOH2</span>, <span class="html-italic">CaRBOH5</span>, and <span class="html-italic">CaRBOH6</span>. Control indicates the leaves without infiltration, and EV indicates infiltration of leaves with <span class="html-italic">Agrobacterium</span> carrying the empty vector. Each treatment has 15 pepper explants. In (<b>B</b>,<b>D</b>), the results show similar trends, and a representative result is shown. Different lowercase letters in (<b>A</b>,<b>C</b>) indicate that the mean values of three replicates were significantly different among different treatments (<span class="html-italic">p</span> < 0.05).</p> "> Figure 8
<p>Silencing of <span class="html-italic">CaPAO1</span> and <span class="html-italic">CaRBOH</span>s decreases AR formation in pepper. (<b>A</b>) Expression levels of <span class="html-italic">CaPAO1</span> and <span class="html-italic">CaRBOH</span>s in the epicotyls of control and VIGS plants. (<b>B</b>) H<sub>2</sub>O<sub>2</sub> contents in the AR zone of <span class="html-italic">CaPAO1</span>-silenced explants at 24 h of AR formation. (<b>C</b>) O<sub>2</sub><sup>•−</sup> contents in the AR zone of control and <span class="html-italic">CaRBOH</span>-silenced explants at 72 h of AR formation. (<b>D</b>) AR formation in the control and VIGS explants treated with or without EBL. Each treatment has 15 pepper explants. Different lowercase letters indicate that the mean values of ten replicates are significantly different among different treatments (<span class="html-italic">p</span> < 0.05).</p> "> Figure 9
<p>Schematic model for EBL-induced AR formation by coordinating ROS generation in pepper. EBL induces CaPAO1-derived H<sub>2</sub>O<sub>2</sub> generation and CaRBOH2/5/6-derived O<sub>2</sub><sup>•−</sup> generation in apoplasts. O<sub>2</sub><sup>•−</sup> and H<sub>2</sub>O<sub>2</sub> trigger signaling transduction to regulate the expression of <span class="html-italic">CaLBD</span>, <span class="html-italic">CaCYC</span>, and <span class="html-italic">CaCDK</span> genes, and further stimulate AR formation. PAs, polyamines. Put, putrescine. PM, plasma membrane.</p> ">
Abstract
:1. Introduction
2. Materials and Methods
2.1. Pepper Seedling Growth and Treatment
2.2. Measurement and Histochemical Analysis of H2O2 and O2•−
2.3. Determination of Cytoplasmic and Cell-Wall PAO Enzymatic Activities
2.4. Assay of Plasma Membrane (PM) NADPH Oxidase Activity
2.5. Genome-Wide Identification of CaPAO and CaRBOH Genes in Pepper
2.6. qRT-PCR Analysis
2.7. Transient Expression of CaPAO1 and CaRBOHs in Pepper Leaves
2.8. Virus-Induced Gene Silencing (VIGS) of CaPAO1 and CaRBOHs in Pepper
2.9. Statistical Analysis
3. Results
3.1. EBL Promoted AR Formation in Pepper
3.2. ROS was Involved in EBL-Promoted AR Formation
3.3. CW-PAO and PM-NADPH Oxidase Were Involved in EBL-Induced ROS Generation during AR Formation
3.4. Identification of EBL-Targeted CaPAO during Pepper AR Formation
3.5. Identification of EBL-Targeted CaRBOHs during Pepper AR Formation
3.6. Capacities of CaPAO1 and CaRBOHs in ROS Production in Pepper Leaves
3.7. Identification of the Capabilities of CaPAO1 and CaRBOHs in EBL-Induced AR Formation in Pepper
4. Discussion
4.1. BRs Promoted AR Formation in a Dose-Dependent Manner
4.2. BRs Promoted AR Formation through Apoplastic CaPAO1- and CaRBOHs-Derived ROS
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
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Wen, Z.; Chen, Z.; Liu, X.; Sun, J.; Zhang, F.; Zhang, M.; Dong, C. 24-Epibrassinolide Facilitates Adventitious Root Formation by Coordinating Cell-Wall Polyamine Oxidase- and Plasma Membrane Respiratory Burst Oxidase Homologue-Derived Reactive Oxygen Species in Capsicum annuum L. Antioxidants 2023, 12, 1451. https://doi.org/10.3390/antiox12071451
Wen Z, Chen Z, Liu X, Sun J, Zhang F, Zhang M, Dong C. 24-Epibrassinolide Facilitates Adventitious Root Formation by Coordinating Cell-Wall Polyamine Oxidase- and Plasma Membrane Respiratory Burst Oxidase Homologue-Derived Reactive Oxygen Species in Capsicum annuum L. Antioxidants. 2023; 12(7):1451. https://doi.org/10.3390/antiox12071451
Chicago/Turabian StyleWen, Zhengyang, Zhifeng Chen, Xinyan Liu, Jingbo Sun, Feng Zhang, Mengxia Zhang, and Chunjuan Dong. 2023. "24-Epibrassinolide Facilitates Adventitious Root Formation by Coordinating Cell-Wall Polyamine Oxidase- and Plasma Membrane Respiratory Burst Oxidase Homologue-Derived Reactive Oxygen Species in Capsicum annuum L." Antioxidants 12, no. 7: 1451. https://doi.org/10.3390/antiox12071451