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. 2024 Apr 9;13(8):1062.
doi: 10.3390/plants13081062.

Carotenoid Accumulation in the Rhododendron chrysanthum Is Mediated by Abscisic Acid Production Driven by UV-B Stress

Fushuai Gong  1 , Xiangru Zhou  1 , Wang Yu  1 , Hongwei Xu  1 , Xiaofu Zhou  1
Affiliations

Carotenoid Accumulation in the Rhododendron chrysanthum Is Mediated by Abscisic Acid Production Driven by UV-B Stress

Fushuai Gong et al. Plants (Basel). .

Abstract

Rhododendron chrysanthum (R. chrysanthum) development is hampered by UV-B sunlight because it damages the photosynthetic system and encourages the buildup of carotenoids. Nevertheless, it is still unclear how R. chrysanthum repairs the photosynthetic system to encourage the formation of carotenoid pigments. The carotenoid and abscisic acid (ABA) concentrations of the R. chrysanthum were ascertained in this investigation. Following UV-B stress, the level of carotenoids was markedly increased, and there was a strong correlation between carotenoids and ABA. The modifications of R. chrysanthum's OJIP transient curves were examined in order to verify the regulatory effect of ABA on carotenoid accumulation. It was discovered that external application of ABA lessened the degree of damage on the donor side and lessened the damage caused by UV-B stress on R. chrysanthum. Additionally, integrated metabolomics and transcriptomics were used to examine the changes in differentially expressed genes (DEGs) and differential metabolites (DMs) in R. chrysanthum in order to have a better understanding of the role that ABA plays in carotenoid accumulation. The findings indicated that the majority of DEGs were connected to carotenoid accumulation and ABA signaling sensing. To sum up, we proposed a method for R. chrysanthum carotenoid accumulation. UV-B stress activates ABA production, which then interacts with transcription factors to limit photosynthesis and accumulate carotenoids, such as MYB-enhanced carotenoid biosynthesis. This study showed that R. chrysanthum's damage from UV-B exposure was lessened by carotenoid accumulation, and it also offered helpful suggestions for raising the carotenoid content of plants.

Keywords: ABA; Rhododendron chrysanthum; UV-B; carotenoids; metabolomics; transcriptomics.

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Conflict of interest statement

The authors have no relevant financial or non-financial interests to disclose.

Figures

Figure 1
Figure 1
Changes in fluorescence parameters of the R. chrysanthum under UV-B stress. (a) Comparison of real-time fluorescence images of R. chrysanthum in control (M) and UV-B stress-treated group (N). (b–e) The bar graphs represent the maximum quantum yield of PSII (Fv/Fm), the actual quantum yield of PSII (Y(II)), the maximum fluorescence after photoacclimatization (Fm’), and the maximum photoconversion potential of PSII (Fv’/Fo’) in two groups of R. chrysanthum, the control group (M), and the UV-B stress-treated group (N), respectively. (f,g) The line graphs show the electron transport rate (ETR, μmol e−1 s−1 m−2) and NPQ as a function of PAR for the R. chrysanthum control (M) and UV-B stress-treated group (N), respectively. Values are means ± SD (n = 3). Different letters indicate significant difference at p < 0.05 among treatments.
Figure 1
Figure 1
Changes in fluorescence parameters of the R. chrysanthum under UV-B stress. (a) Comparison of real-time fluorescence images of R. chrysanthum in control (M) and UV-B stress-treated group (N). (b–e) The bar graphs represent the maximum quantum yield of PSII (Fv/Fm), the actual quantum yield of PSII (Y(II)), the maximum fluorescence after photoacclimatization (Fm’), and the maximum photoconversion potential of PSII (Fv’/Fo’) in two groups of R. chrysanthum, the control group (M), and the UV-B stress-treated group (N), respectively. (f,g) The line graphs show the electron transport rate (ETR, μmol e−1 s−1 m−2) and NPQ as a function of PAR for the R. chrysanthum control (M) and UV-B stress-treated group (N), respectively. Values are means ± SD (n = 3). Different letters indicate significant difference at p < 0.05 among treatments.
Figure 2
Figure 2
ABA is correlated with changes in R. chrysanthum’s carotenoid concentration following UV-B stress. (a) Variations in control (M) and UV-B stress-treated group (N) levels of Chl a, Chl b, and Chl a/Chl b. (b) Carotenoid content variations in control (M) and UV-B stress-treated group (N). (c) Changes in ABA abundance in Control (M) and UV-B stress-treated group (N). (d) Correlation study examining the relationship between variations in control (M) and UV-B stress-treated group (N). ABA abundance and carotenoid content. Green and purple star denote negative and positive correlations, respectively, and the size of the star reflects the correlation’s magnitude. Values are means ± SD (n = 3). Different letters (a, b) indicate significant difference at p < 0.05 among treatments. Significant difference (* p < 0.05).
Figure 3
Figure 3
R. chrysanthum rapid fluorescence curves following UV-B stress and exogenous ABA application. (a) Shows the rapid fluorescence curves for the OP section. (b,c) Denotes the fast light curves of the OP section after normalization using WO-P = (Ft − Fo)/(Fm − Fo) and the OJ section after normalization with WO-J = (Ft − Fo)/(FJ − Fo), respectively. (d) WK = (FK − Fo)/(FJ − Fo), which represents the ratio of the variable fluorescence FK to the amplitude FJ − Fo. (e) Standardized fluorescence differences between the control(M), UV-B stress-treated(N), and exogenous ABA-treated (Q) OJs. (f,g,h) Stands for ϕEo, Sm, and ETo/RC variation, respectively. Values are means ± SD (n = 3). Different letters (a, b) indicate a significant difference at p < 0.05 among treatments.
Figure 3
Figure 3
R. chrysanthum rapid fluorescence curves following UV-B stress and exogenous ABA application. (a) Shows the rapid fluorescence curves for the OP section. (b,c) Denotes the fast light curves of the OP section after normalization using WO-P = (Ft − Fo)/(Fm − Fo) and the OJ section after normalization with WO-J = (Ft − Fo)/(FJ − Fo), respectively. (d) WK = (FK − Fo)/(FJ − Fo), which represents the ratio of the variable fluorescence FK to the amplitude FJ − Fo. (e) Standardized fluorescence differences between the control(M), UV-B stress-treated(N), and exogenous ABA-treated (Q) OJs. (f,g,h) Stands for ϕEo, Sm, and ETo/RC variation, respectively. Values are means ± SD (n = 3). Different letters (a, b) indicate a significant difference at p < 0.05 among treatments.
Figure 4
Figure 4
JIP parameters for control (M), UV-B stress treatment (N), and exogenous ABA treatment (Q) of R. chrysanthum were determined from the chlorophyll fluorescence OJIP transient curves. (a) Radargram showing how the values fluctuated in control (M), UV-B stress treatment (N), and exogenous ABA treatment (Q). (b–d) Indicate the variations in the PSII-related metrics PI ABS, DIo/RC, and Fv/Fm, respectively. Values are means ± SD (n = 3). Different letters (a, b, c) indicate significant difference at p < 0.05 among treatments.
Figure 4
Figure 4
JIP parameters for control (M), UV-B stress treatment (N), and exogenous ABA treatment (Q) of R. chrysanthum were determined from the chlorophyll fluorescence OJIP transient curves. (a) Radargram showing how the values fluctuated in control (M), UV-B stress treatment (N), and exogenous ABA treatment (Q). (b–d) Indicate the variations in the PSII-related metrics PI ABS, DIo/RC, and Fv/Fm, respectively. Values are means ± SD (n = 3). Different letters (a, b, c) indicate significant difference at p < 0.05 among treatments.
Figure 5
Figure 5
Enrichment pathways and occupancy of different metabolites in R. chrysanthums after UV-B stress and exogenous ABA treatment. (a) Distribution of distinct differential metabolites by percentage and primary and secondary classification. The circle near the center represents the primary classification of the metabolite and the outer circle represents the secondary classification of the metabolite. The lighter color highlights the terpenes. (b) Metabolite enrichment for each difference between the control (M) and UV-B stress-treated group (N) and between the UV-B stress-treated (N) and exogenous ABA-treated group (Q); larger circles indicate more metabolites enriched in the pathway, and redder colors indicate smaller and more significant p-values. (c) Heatmap of differential metabolite combinations in the p < 0.05 metabolic pathway: the right heatmap is calculated as a p-value, light blue indicates p ≥ 0.05, and pink indicates p < 0.05 with significant difference. The left heatmap is calculated as log2FC. Darker color indicates greater change in metabolite abundance, lighter color indicates lesser change in metabolite abundance.
Figure 6
Figure 6
Following exogenous ABA treatment and UV- B stress, R. chrysanthum exhibits enrichment of important genes and transcription factor screening. (a) Annotation of key genes to Venn diagrams in KEGG, GO, and TF. (b) Selecting key genes for KEGG enrichment analysis through screening. Significantly enriched pathways (p < 0.01) are indicated by the three red-highlighted pathways. (c) The top five genes’ transcription factor families, ranked numerically, are analyzed for expression patterns. Redder colors indicate higher expression, while greener colors indicate lower expression.
Figure 7
Figure 7
DEGs and DMs change following exogenous ABA therapy and UV-B stress in the R. chrysanthum carotenoid pathway. (a) ABA production, signal transduction pathways, and the biosynthesis of carotenoids. DEGs involved in the carotenoid biosynthesis pathway: crtZ, beta-carotene 3-hydroxylase; LUT5, beta-ring hydroxylase; ZEP, zeaxanthin epoxidase; NCED, 9-cis-epoxycarotenoid dioxygenase; ABA2, xanthoxin dehydrogenase; AAO3, abscisic-aldehyde oxidase; PYR/PYL, pyrabactin resistance–like; PP2C, protein phosphatase 2C; SnRK2, sucrose non–fermenting–1–related protein kinase 2; ABF, ABA-responsive element–binding factors; AOG, abscisate beta-glucosyltransferase; MAPK, mitogen–activated protein kinase; TPI, triosephosphate isomerase; gapN, glyceraldehyde-3-phosphate dehydrogenase; gpmI, 2,3-bisphosphoglycerate-independent phosphoglycerate mutase; PGAM, 2,3-bisphosphoglycerate-dependent phosphoglycerate mutase; ENO, enolase; PDHA, pyruvate dehydrogenase E1 component subunit alpha; PDHB, pyruvate dehydrogenase E1 component subunit beta; DLAT, pyruvate dehydrogenase E2 component (dihydrolipoyllysine-residue acetyltransferase); HMGCS, hydroxymethylglutaryl-CoA synthase; HMGCR, hydroxymethylglutaryl-CoA reductase; MVK, mevalonate kinase; MVD, diphosphomevalonate decarboxylase; GGPS, geranylgeranyl diphosphate synthase, type II; FDPS, farnesyl diphosphate synthase; dxr, 1-deoxy-D-xylulose-5-phosphate reductoisomerase; ispD, 2-C-methyl-D-erythritol 4-phosphate cytidylyltransferase; ispF, 2-C-methyl-D-erythritol 2,4-cyclodiphosphate synthase; gcpE, (E)-4-hydroxy-3-methylbut-2-enyl-diphosphate synthase; PDS, 15-cis-phytoene desaturase and ZDS, zeta-carotene desaturase. DMs involved in the carotenoid biosynthesis pathway: C06082, Abscisate; C15970, Abscisic acid glucose ester; C00111, Glycerone phosphate and C00416, Phosphatidate. (b) An overview of photosynthetic processes and circadian rhythms in plants. DEGs involved in photosynthesis and circadian pathways in plants: PIF3, phytochrome-interacting factor 3; CSNK2A, casein kinase II subunit alpha; LHCA2, light-harvesting complex I chlorophyll a/b binding protein 2; LHCA3, light-harvesting complex I chlorophyll a/b binding protein 3; LHCA5, light-harvesting complex I chlorophyll a/b binding protein 5; PsbP, photosystem II oxygen-evolving enhancer protein 2; PetH, ferredoxin--NADP+ reductase and petJ, cytochrome c6. Where heat maps depict changes in genes and metabolites. On the metabolite heat map, a significant down-regulation is indicated by a green hue, while significant up-regulation is indicated by a bluer color. Considerable down-regulation is shown by the gene heatmap’s more purple color, while considerable up-regulation is indicated by its more brown color.
Figure 7
Figure 7
DEGs and DMs change following exogenous ABA therapy and UV-B stress in the R. chrysanthum carotenoid pathway. (a) ABA production, signal transduction pathways, and the biosynthesis of carotenoids. DEGs involved in the carotenoid biosynthesis pathway: crtZ, beta-carotene 3-hydroxylase; LUT5, beta-ring hydroxylase; ZEP, zeaxanthin epoxidase; NCED, 9-cis-epoxycarotenoid dioxygenase; ABA2, xanthoxin dehydrogenase; AAO3, abscisic-aldehyde oxidase; PYR/PYL, pyrabactin resistance–like; PP2C, protein phosphatase 2C; SnRK2, sucrose non–fermenting–1–related protein kinase 2; ABF, ABA-responsive element–binding factors; AOG, abscisate beta-glucosyltransferase; MAPK, mitogen–activated protein kinase; TPI, triosephosphate isomerase; gapN, glyceraldehyde-3-phosphate dehydrogenase; gpmI, 2,3-bisphosphoglycerate-independent phosphoglycerate mutase; PGAM, 2,3-bisphosphoglycerate-dependent phosphoglycerate mutase; ENO, enolase; PDHA, pyruvate dehydrogenase E1 component subunit alpha; PDHB, pyruvate dehydrogenase E1 component subunit beta; DLAT, pyruvate dehydrogenase E2 component (dihydrolipoyllysine-residue acetyltransferase); HMGCS, hydroxymethylglutaryl-CoA synthase; HMGCR, hydroxymethylglutaryl-CoA reductase; MVK, mevalonate kinase; MVD, diphosphomevalonate decarboxylase; GGPS, geranylgeranyl diphosphate synthase, type II; FDPS, farnesyl diphosphate synthase; dxr, 1-deoxy-D-xylulose-5-phosphate reductoisomerase; ispD, 2-C-methyl-D-erythritol 4-phosphate cytidylyltransferase; ispF, 2-C-methyl-D-erythritol 2,4-cyclodiphosphate synthase; gcpE, (E)-4-hydroxy-3-methylbut-2-enyl-diphosphate synthase; PDS, 15-cis-phytoene desaturase and ZDS, zeta-carotene desaturase. DMs involved in the carotenoid biosynthesis pathway: C06082, Abscisate; C15970, Abscisic acid glucose ester; C00111, Glycerone phosphate and C00416, Phosphatidate. (b) An overview of photosynthetic processes and circadian rhythms in plants. DEGs involved in photosynthesis and circadian pathways in plants: PIF3, phytochrome-interacting factor 3; CSNK2A, casein kinase II subunit alpha; LHCA2, light-harvesting complex I chlorophyll a/b binding protein 2; LHCA3, light-harvesting complex I chlorophyll a/b binding protein 3; LHCA5, light-harvesting complex I chlorophyll a/b binding protein 5; PsbP, photosystem II oxygen-evolving enhancer protein 2; PetH, ferredoxin--NADP+ reductase and petJ, cytochrome c6. Where heat maps depict changes in genes and metabolites. On the metabolite heat map, a significant down-regulation is indicated by a green hue, while significant up-regulation is indicated by a bluer color. Considerable down-regulation is shown by the gene heatmap’s more purple color, while considerable up-regulation is indicated by its more brown color.
Figure 8
Figure 8
Important genes and terpenoids in R. chrysanthum following UV-B stress and exogenous ABA injection during UV-B stress. (a,b) Nine-quadrant plots of the DEGs and DMs following external application of ABA under UV-B stress and UV-B stress, respectively, where the log2FC of DMs is represented by the horizontal coordinates, and the log2FC of DEGs is represented by the vertical coordinates. Quadrants 1 and 9 are characterized by a positive correlation between the horizontal and vertical coordinates; quadrants 3 and 7 are characterized by a negative correlation between the horizontal and vertical coordinates; quadrant 5 is characterized by no correlation between the horizontal and vertical coordinates; quadrants 2 and 8 are characterized by a significant change in the horizontal coordinates without a significant change in the vertical coordinates; quadrants 4 and 6 are characterized by a significant change in the vertical coordinates without a significant change in the horizontal coordinates. (c,d) Number of DMs and DEGs in each quadrant for the control group (M) versus the UV-B stress-treated group (N) and the UV-B stress-treated group (N) versus the exogenous ABA-treated group (Q). (e,f) Chord plots of DEGs and key terpene correlations in quadrants 3 and 7, respectively. A stronger positive correlation is shown by a redder color, and a stronger negative correlation is indicated by a bluer tint.
Figure 8
Figure 8
Important genes and terpenoids in R. chrysanthum following UV-B stress and exogenous ABA injection during UV-B stress. (a,b) Nine-quadrant plots of the DEGs and DMs following external application of ABA under UV-B stress and UV-B stress, respectively, where the log2FC of DMs is represented by the horizontal coordinates, and the log2FC of DEGs is represented by the vertical coordinates. Quadrants 1 and 9 are characterized by a positive correlation between the horizontal and vertical coordinates; quadrants 3 and 7 are characterized by a negative correlation between the horizontal and vertical coordinates; quadrant 5 is characterized by no correlation between the horizontal and vertical coordinates; quadrants 2 and 8 are characterized by a significant change in the horizontal coordinates without a significant change in the vertical coordinates; quadrants 4 and 6 are characterized by a significant change in the vertical coordinates without a significant change in the horizontal coordinates. (c,d) Number of DMs and DEGs in each quadrant for the control group (M) versus the UV-B stress-treated group (N) and the UV-B stress-treated group (N) versus the exogenous ABA-treated group (Q). (e,f) Chord plots of DEGs and key terpene correlations in quadrants 3 and 7, respectively. A stronger positive correlation is shown by a redder color, and a stronger negative correlation is indicated by a bluer tint.
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