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. 2020 Jul 7:11:852.
doi: 10.3389/fpls.2020.00852. eCollection 2020.

Phaeophyceaean (Brown Algal) Extracts Activate Plant Defense Systems in Arabidopsis thaliana Challenged With Phytophthora cinnamomi

Md Tohidul Islam  1   2 , Han Ming Gan  1 , Mark Ziemann  1 , Hashmath Inayath Hussain  3 , Tony Arioli  1   3 , David Cahill  1
Affiliations

Phaeophyceaean (Brown Algal) Extracts Activate Plant Defense Systems in Arabidopsis thaliana Challenged With Phytophthora cinnamomi

Md Tohidul Islam et al. Front Plant Sci. .

Abstract

Seaweed extracts are important sources of plant biostimulants that boost agricultural productivity to meet current world demand. The ability of seaweed extracts based on either of the Phaeophyceaean species Ascophyllum nodosum or Durvillaea potatorum to enhance plant growth or suppress plant disease have recently been shown. However, very limited information is available on the mechanisms of suppression of plant disease by such extracts. In addition, there is no information on the ability of a combination of extracts from A. nodosum and D. potatorum to suppress a plant pathogen or to induce plant defense. The present study has explored the transcriptome, using RNA-seq, of Arabidopsis thaliana following treatment with extracts from the two species, or a mixture of both, prior to inoculation with the root pathogen Phytophthora cinnamomi. Following inoculation, five time points (0-24 h post-inoculation) that represented early stages in the interaction of the pathogen with its host were assessed for each treatment and compared with their respective water controls. Wide scale transcriptome reprogramming occurred predominantly related to phytohormone biosynthesis and signaling, changes in metabolic processes and cell wall biosynthesis, there was a broad induction of proteolysis pathways, a respiratory burst and numerous defense-related responses were induced. The induction by each seaweed extract of defense-related genes coincident with the time of inoculation showed that the plants were primed for defense prior to infection. Each seaweed extract acted differently in inducing plant defense-related genes. However, major systemic acquired resistance (SAR)-related genes as well as salicylic acid-regulated marker genes (PR1, PR5, and NPR1) and auxin associated genes were found to be commonly up-regulated compared with the controls following treatment with each seaweed extract. Moreover, each seaweed extract suppressed P. cinnamomi growth within the roots of inoculated A. thaliana by the early induction of defense pathways and likely through ROS-based signaling pathways that were linked to production of ROS. Collectively, the RNA-seq transcriptome analysis revealed the induction by seaweed extracts of suites of genes that are associated with direct or indirect plant defense in addition to responses that require cellular energy to maintain plant growth during biotic stress.

Keywords: Arabidopsis thaliana; Ascophyllum nodosum; Durvillaea potatorum; Phytophthora cinnamomi; RNA-Seq; seaweed.

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Figures

FIGURE 1
FIGURE 1
Effect of seaweed extracts on P. cinnamomi infection in roots of A. thaliana. Plants were grown in a sand culture system with either seaweed extracts (AN, DP, and AN/DP) or water as a control for 6 days and then inoculated with P. cinnamomi on day 7. (A) Nested real time PCR quantification of P. cinnamomi DNA. Plant roots were harvested from 12 to 96 hpi. Data presented are from two experimental repeats each with three biological replicates. Error bars represent the standard error of means. *significant difference for amount of pathogen in different treatment compared to water control at P = 0.05 according to Duncan’s multiple range test. (B) Whole roots of A. thaliana infected with P. cinnamomi zoospores following treatment of roots with seaweed extracts (AN, DP, or AN/DP). Images were captured at 12 and 24 hpi. Scale bar = 20 μM. Each image is representative of three biological replicates.
FIGURE 2
FIGURE 2
Venn diagrams that show commonalities and differences among up-regulated DEGs at five time points following treatment of A. thaliana with (A) AN, (B) DP, (C) AN/DP, and (D) up-regulated DEGs (at at least one time point) for each of the three treatments.
FIGURE 3
FIGURE 3
Gene ontology (GO) enrichment analysis of differentially expressed genes (DEGs) from the AN treatment. The DEGs were categorized into panels (A) Molecular function, (B) Biological process, and (C) Cellular component.
FIGURE 4
FIGURE 4
Gene ontology (GO) enrichment analysis of differentially expressed genes (DEGs) from the DP treatment. The DEGs were categorized into panels (A) Molecular function, (B) Biological process, and (C) Cellular component.
FIGURE 5
FIGURE 5
Gene ontology (GO) enrichment analysis of differentially expressed genes (DEGs) from the AN/DP treatment. The DEGs were categorized into panel (A) Molecular function, (B) Biological process, and (C) Cellular component.
FIGURE 6
FIGURE 6
Validation of the differentially expressed genes by RT-qPCR for A. thaliana plants treated with AN extract. Samples were collected from the plants grown with the seaweed extract and harvested at 0, 3, 6, 12, and 24 h after P. cinnamomi inoculation. All data were normalized to the expression level of actin 2 (ACT2) and actin 8 (ACT8). The data represent the fold change at each time point in the infected samples vs. the control sample. Bars show the standard error of the mean from three biological replicates.
FIGURE 7
FIGURE 7
Validation of the differentially expressed genes by RT-qPCR for A. thaliana plants treated with the DP extract. Samples were collected from the plants grown with the seaweed extract and harvested at 0, 3, 6, 12, and 24 h after P. cinnamomi inoculation. All data were normalized to the expression level of actin 2 (ACT2) and actin 8 (ACT8). The data represent the fold change at each time point in the infected samples vs. the control sample. Bars show the standard error of the mean from three biological replicates.
FIGURE 8
FIGURE 8
Validations of the differentially expressed genes by RT-qPCR for A. thaliana plants treated with the AN/DP extract. Samples were collected from the plants grown with the seaweed extract and harvested at 0, 3, 6, 12, and 24 h after P. cinnamomi inoculation. All data were normalized to the expression level of actin 2 (ACT2) and actin 8 (ACT8). The data represent the fold change at each time point in the infected samples vs. the control sample. Bars show the standard error of the mean from three biological replicates.
FIGURE 9
FIGURE 9
Mapman overview of DEGs related to hormone, stress and metabolic responses in plants of A. thaliana following seaweed treatment and after inoculation with P. cinnamomi (at 3 and 12 hpi). The average fold change of genes are indicated by the color scale (red represents up-regulated genes and blue represents down-regulated genes).
FIGURE 10
FIGURE 10
Hydrogen peroxide detection in A. thaliana roots grown with seaweed extracts or water as the control and inoculated with P. cinnamomi or mock-inoculated with water. Hydrogen peroxide was detected using the 3,3 O-diaminobenzidine tetrachloride (DAB) stain, which resulted in a reddish-brown precipitate in the root tissue. (A) Control root grown with water and mock inoculated with water showing no H2O2 production. (B) Control root grown with water and inoculated with the pathogen showing no H2O2 production. (C) Infected root grown with seaweed extract AN and mock inoculated with water showing a low level of H2O2 production. (D) Infected root grown with seaweed extract AN and then inoculated with the pathogen showing H2O2 production. (E) Control root grown with seaweed extract DP and mock inoculated with water showing low level H2O2 production. (F) Infected root grown with seaweed extract DP and inoculated with the pathogen showing H2O2 production. (G) Control root grown with seaweed extract AN/DP and mock inoculated with water showing low level of H2O2 production. (H) Infected root grown with seaweed extract AN/DP and inoculated with the pathogen showing H2O2 production. Scale bar = 20 μM. Each image is representative of three biological replicates.
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