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. 2024 Oct 17;24(1):973.
doi: 10.1186/s12870-024-05691-4.

Physiological, biochemical, and transcriptomic alterations in Castor (Ricinus communis L.) under polyethylene glycol-induced oxidative stress

Yong Zhao #  1 , Pei Lei #  2 , Huibo Zhao  3 , Rui Luo  3 , Guorui Li  3 , Jianjun Di  3 , Li Wen  1 , Zhibiao He  4 , Deyun Tan  5 , Fanjuan Meng  6 , Fenglan Huang  7   8   9   10   11
Affiliations

Physiological, biochemical, and transcriptomic alterations in Castor (Ricinus communis L.) under polyethylene glycol-induced oxidative stress

Yong Zhao et al. BMC Plant Biol. .

Abstract

Background: Castor is an important industrial raw material. Drought-induced oxidative stress leads to slow growth and decreased yields in castor. However, the mechanisms of drought-induced oxidative stress in castor remain unclear. Therefore, in this study, physiological, biochemical, and RNA-seq analyses were conducted on the roots of castor plants under PEG-6000 stress for 3 d and 7 d followed by 4 d of hydration.

Results: The photosynthetic rate of castor leaves was inhibited under PEG-6000 stress for 3 and 7 d. Biochemical analysis of castor roots stressed for 3 d and 7 d, and rehydrated for 4 d revealed that the activities of APX and CAT were highest after only 3 d of stress, whereas the activities of POD, GR, and SOD peaked after 7 d of stress. RNA-seq analysis revealed 2926, 1507, and 111 differentially expressed genes (DEGs) in the roots of castor plants under PEG-6000 stress for 3 d and 7 d and after 4 d of rehydration, respectively. GO analysis of the DEGs indicated significant enrichment in antioxidant activity. Furthermore, KEGG enrichment analysis of the DEGs revealed significantly enriched metabolic pathways, including glutathione metabolism, fatty acid metabolism, and plant hormone signal transduction. WGCNA identified the core genes PP2C39 and GA2ox4 in the navajowhite1 module, which was upregulated under PEG-6000 stress. On the basis of these results, we propose a model for the response to drought-induced oxidative stress in castor.

Conclusions: This study provides valuable antioxidant gene resources, deepening our understanding of antioxidant regulation and paving the way for further molecular breeding of castor plants.

Keywords: Castor; PEG stress; RNA-seq.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1
Fig. 1
Determination of biochemical indices in castor roots under PEG-6000 stress. Different letters above the bars indicate statistically significant differences between different days at P < 0.05 according to Duncan’s multiple range test
Fig. 2
Fig. 2
GO and KEGG pathway analyses of the DEGs. GO:0050896, response to stimulus; GO:0006796, single-organism process; GO:0023052, signaling; GO:0065007, biological regulation; GO:0040007, growth; GO:0002376, immune system process; GO:0051704, multiorganism process; GO:0003824, catalytic activity; GO:0015103, transporter activity; GO:0004871, signal transducer activity; GO:0098772, molecular function regulator; GO:0060089, molecular transducer activity; GO:0016209, antioxidant activity; GO:0005488, binding; GO:0044425, membrane part; GO:0016020, membrane; GO:0030054, cell junction; GO:0005576, extracellular region; GO:0044420, extracellular matrix component; GO:0044699, single-organism process; GO:0008152, metabolic process; GO:0007610, behavior; GO:0005215, transporter activity; GO:0009055, electron carrier activity; GO:0000988, transcription factor activity, protein binding; GO:0005623, cell; GO:0099512, supramolecular fiber; GO:0071840, cellular component organization or biogenesis; GO:0022414, reproductive process; GO:0000003, reproduction; GO:0001071, nucleic acid binding transcription factor activity; GO:0044422, organelle part; GO:0044464, cell part. ko00360, phenylalanine metabolism; ko00450, selenocompound metabolism; ko00480, glutathione metabolism; ko00500, starch and sucrose metabolism; ko00511, other glycan degradation; ko00520, amino sugar and nucleotide sugar metabolism; ko00531, glycosaminoglycan degradation; ko00906, carotenoid biosynthesis; ko00940, phenylpropanoid biosynthesis; ko01100, metabolic pathways; ko01110, biosynthesis of secondary metabolites; ko01212, fatty acid metabolism; ko03008, ribosome biogenesis in eukaryotes; ko04075, plant hormone signal transduction; ko04141, protein processing in the endoplasmic reticulum; ko00196, photosynthesis - antenna proteins; ko00195, photosynthesis; ko00260, glycine, serine and threonine metabolism; ko01200, carbon metabolism; ko00051, fructose and mannose metabolism; ko01120, microbial metabolism in diverse environments; ko01230, biosynthesis of amino acids; ko00630, glyoxylate and dicarboxylate metabolism; ko01130, biosynthesis of antibiotics; ko00460, cyanoamino acid metabolism; ko00052, galactose metabolism; ko00280, valine, leucine and isoleucine degradation; ko00040, pentose and glucuronate interconversions
Fig. 3
Fig. 3
WGCNA of DEGs in castor roots. A: Grouping of differential gene expression modules. B: DEGs enriched in each module. C: Matrix showing the module–trait relationships (MTRs) of different modules under control conditions and PEG stress. Positive correlation is represented in red, negative correlation in green, and no correlation in white. D: Expression pattern of the navajowhite1 module. The heatmap was plotted using the log10(FPKM) values
Fig. 4
Fig. 4
Coexpressed DEGs in the navajowhite1 module are involved in metabolic pathways. I: biosynthesis of amino acids (ko01230); II: alanine, aspartate, and glutamate metabolism (ko00250); III: biosynthesis of unsaturated fatty acids (ko01040); IV: glutathione metabolism (ko00480); V: spliceosome (ko03040). Relative expression levels are shown by a color gradient from low (blue) to high (red). LEUD3 (ncbi_8267727), aconitase/3-isopropyl malate dehydratase protein; LEU32 (ncbi_8283093), 3-isopropyl malate dehydrogenase 2; ACO1 (ncbi_8267700), aconitate hydratase 1; IDHC (ncbi_8258744), isocitrate dehydrogenase; AATC (ncbi_8268349), aspartate aminotransferase; P5CS (ncbi_8287478), delta-1-pyrroline-5-carboxylate synthase; ENO1 (ncbi_8264565), enolase 1; KPYC (ncbi_8274900), pyruvate kinase; PFKA5 (ncbi_8267060), phosphofructokinase; ALF (ncbi_8288389), fructose-bisphosphate aldolase; TKTC2 (ncbi_8270608), transketolase; KPRS1 (ncbi_8266684), ribose-phosphate pyrophosphokinase 1; HIS7 (ncbi_8280924), imidazole glycerol-phosphate dehydratase; SAT3 (ncbi_8266938), serine acetyltransferase 1; METC (ncbi_8273083), chloroplast cystathionine beta lyase family protein; GGT2 (ncbi_8273496), glutamate-glyoxylate aminotransferase 2; ALAT2 (ncbi_8276551), alanine aminotransferase 2-like; GAD1 (ncbi_ 8286428), glutamate decarboxylase 4; SSDH (ncbi_8279668), succinate-semialdehyde dehydrogenase, mitochondrial; SDR1 (ncbi_8261843), short-chain dehydrogenase/reductase family protein; STAD (ncbi_8263458), stearoyl-acyl-carrier protein desaturase; FAD6C (ncbi_8276565), omega-6 fatty acid desaturase; SDR1 (ncbi_8261843), short-chain dehydrogenase; THIK2 (ncbi_8265629), peroxisomal 3-keto-acyl-CoA thiolase; PSA (ncbi_8287399), puromycin-sensitive aminopeptidase; GSTX6 (ncbi_8262580), glutathione S-transferase X6; IDHC (ncbi_8258744), isocitrate dehydrogenase; GPX2 (ncbi_8264294), glutathione peroxidase; RIR2 (ncbi_8271445), ribonucleoside-diphosphate reductase small chain family protein; RIR1 (ncbi_8283227), ribonucleoside-diphosphate reductase large subunit-like; RH56 (ncbi_8259463), ATP-dependent RNA helicase 56; RH30 (ncbi_8280293), ATP-dependent RNA helicase 30; RSE1 (ncbi_8258409), pre-mRNA-splicing factor; U2AFA (ncbi_8267025), splicing factor U2af small subunit ; THO4D (ncbi_8272182), THO complex subunit 4D
Fig. 5
Fig. 5
Coexpression network analysis of genes in the navajowhite1 module. The larger the circle is and the deeper the red color is, the more genes that gene interacts with
Fig. 6
Fig. 6
qRT‒PCR analysis of DEGs in castor roots. The gene IDs (8261021, 8283829, 8274172, 8264294, 8276521, 8266789, 8261301, and 8288116) were all obtained from the NCBI database of the castor genome. 3d: Comparison of gene expression in the roots of castor plants between the treatment group (subjected to stress for 3 d in 15% PEG-containing Hoagland’s nutrient solution) and the control group (cultivated in Hoagland’s nutrient solution for 3 d). 7d: Comparison of gene expression in the roots of castor plants between the treatment group (subjected to stress for 7 d in 15% PEG Hoagland’s nutrient solution) and the control group (cultivated in Hoagland’s nutrient solution for 7 d). 11d: Comparison of gene expression in the roots of castor plants between the rewatered treatment group (after 4 d of rewatering) and the control group (cultivated in Hoagland’s nutrient solution for 11 d)
Fig. 7
Fig. 7
Expression patterns of abscisic acid (ABA), ethylene, and gibberellin (GA) signal-related DEGs in castor bean under PEG-6000 stress. CK 3d, CK 7d, and CK 11d: castor plants grown in Hoagland’s solution without PEG for 3, 7, and 11 d. T 3d, T 7d, and T 11d: castor plants stressed with 15% PEG in Hoagland’s solution for 3 d and 7 d and rehydrated for 4 d. The gene IDs were obtained from the NCBI castor genome database
Fig. 8
Fig. 8
Response of castor to oxidative stress under drought stress. The solid arrows represent positive regulation, whereas the lines with blunted ends represent negative regulation. The dashed lines represent a negatively regulated mechanism that might exist in castor, but this warrants further investigation
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