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. 2023 Dec 14:14:1284529.
doi: 10.3389/fpls.2023.1284529. eCollection 2023.

Simulated galactic cosmic ray exposure activates dose-dependent DNA repair response and down regulates glucosinolate pathways in arabidopsis seedlings

Anirudha R Dixit #  1 , Alexander D Meyers #  2 , Brian Richardson #  3 , Jeffrey T Richards  1 , Stephanie E Richards  4 , Srujana Neelam  2 , Howard G Levine  5 , Mark J Cameron  3 , Ye Zhang  5
Affiliations

Simulated galactic cosmic ray exposure activates dose-dependent DNA repair response and down regulates glucosinolate pathways in arabidopsis seedlings

Anirudha R Dixit et al. Front Plant Sci. .

Abstract

Outside the protection of Earth's magnetic field, organisms are constantly exposed to space radiation consisting of energetic protons and other heavier charged particles. With the goal of crewed Mars exploration, the production of fresh food during long duration space missions is critical for meeting astronauts' nutritional and psychological needs. However, the biological effects of space radiation on plants have not been sufficiently investigated and characterized. To that end, 10-day-old Arabidopsis seedlings were exposed to simulated Galactic Cosmic Rays (GCR) and assessed for transcriptomic changes. The simulated GCR irradiation was carried out in the NASA Space Radiation Laboratory (NSRL) at Brookhaven National Lab (BNL). The exposures were conducted acutely for two dose points at 40 cGy or 80 cGy, with sequential delivery of proton, helium, oxygen, silicon, and iron ions. Control and irradiated seedlings were then harvested and preserved in RNAlater at 3 hrs post irradiation. Total RNA was isolated for transcriptomic analyses using RNAseq. The data revealed that the transcriptomic responses were dose-dependent, with significant upregulation of DNA repair pathways and downregulation of glucosinolate biosynthetic pathways. Glucosinolates are important for plant pathogen defense and for the taste of a plant, which are both relevant to growing plants for spaceflight. These findings fill in knowledge gaps of how plants respond to radiation in beyond-Earth environments.

Keywords: Arabidopsis; DNA damage response; galactic cosmic ray; glucosinolate pathway; space radiation; transcriptomic analysis.

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Conflict of interest statement

AD and JR were employed by the company AETOS Systems Inc. under NASA LASSO II contract. SR was employed by the company Bionetics Corp. under NASA LASSO contract. The remaining authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. The funders had no role in the design of the study; in the collection, analyses, or interpretation of data; in the writing of the manuscript, or in the decision to publish the results.

Figures

Figure 1
Figure 1
Venn diagrams showing distribution of differentially expressed genes between 40 cGy vs. Control and 80 cGy vs. Control comparisons evaluated using p ≤ 0.01 (A–C) and (FDR ≤ 0.1 criterion (D–F). Volcano plots represent differentially expressed genes at a significance cutoff set to p ≤ 0.01 for 40 cGy (G) and 80 cGy (H) compared to the control (0 cGy).
Figure 2
Figure 2
Comparison of log-fold change values (LFC) for DEGs (FDR ≤ 0.1) common to 40 cGy vs. Control and 80 cGy vs. Control comparisons.
Figure 3
Figure 3
Boxplots showing dose-dependent changes in gene expression among 0, 40 and 80 cGy of simulated GCR exposure. Kruskal-Wallis p-value at the top represents overall statistical significance comparing all three treatments. Horizontal bars spanning 0 and 40 cGy; 0 and 80 cGy compared each of the treatment and the numbers represent statistical significance for each of the comparisons.
Figure 4
Figure 4
Gene interaction networks from genes of interest (FDR ≤ 0.1) identified by STRING. Color coded nodes show DNA repair (red), glucosinolate biosynthesis pathways (green), and genes involved in responses to stimuli (purple) in plants exposed to (A) 40 cGy and (B) 80 cGy. Network edges indicate co-occurrence, co-expression, and evidence from experiments and databases. Network edge width indicates the confidence or strength level from 0.17 to 2.56 (40 cGy) and 0.28 to 2.85 (80 cGy).
Figure 5
Figure 5
Genes and their expression changes in glucosinolate biosynthesis and sulfate assimilation pathways.
Figure 6
Figure 6
Gene interaction networks from genes of interest (p ≤ 0.01) identified by STRING. Network edges indicate co-occurrence, co-expression, and evidence from experiments and databases. Network edge width indicates the confidence and strength level higher than 0.4. Color coded nodes show glucosinolate biosynthesis and cellular response to sulfur starvation (red), glucosinolate biosynthesis from methionine (light blue), sulfate assimilate (green), and sulfur metabolism and methionine metabolic process (dark green) in both (A) 40 cGy and (B) 80 cGy treatments. Dose dependent responses include more hormone related responses in the 40 cGy treatment (yellow, pink, and orange). In contrast, the 80 cGy treatment has more enriched gene clusters in DNA repair (pink), cell cycle (yellow), and circadian clock (purple) pathways. Genes related to DNA repair and cell cycle are highlighted in a circle in the 40 cGy treatment, and genes responding to hypoxia and light are highlighted in circles in the 80 cGy treatment.
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