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Proline-mediated modulation on DNA repair pathway in rice seedlings under chromium stress by integrating gene chip and co-expression network analysis

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Abstract

Chromium (Cr) stress can cause oxidative burst to plants. Application of exogenous proline (Pro) is one of the most effective approaches to improve the tolerance of plants to Cr stress. In this study, we integrated the data of gene chip with co-expression network analysis to identify the key pathways involved in the DNA repair processes in rice seedlings under Cr(VI) stress. Based on KEGG pathway analysis, 158 genes identified are activated in five different types of DNA repair pathways, namely base excision repair (BER, 20 genes), mismatch repair (MMR, 30 genes), nonhomologous end joining (NHEJ, 8 genes), nucleotide excision repair (NER, 56 genes) and homologous recombination (HR, 44 genes). Co-expression network analysis showed that genes activated in DNA repair pathways were categorized into six different modules, wherein Module 1 (45.36%), Module 2 (27.84%) and Module 3 (19.59%) carried more weight than others. Integrating the data of gene chip and co-expression network analysis indicated that coordinated actions of HR and NER pathways are mainly associated with DNA repair processes in Cr(VI)-treated rice seedlings supplied with exogenous Pro. OsCSB, OsXPG, OsBRIP1, OsRAD51C, OsRAD51A2, OsRPA, OsTOPBP1C, OsTOP3, and OsXRCC3 activated in the HR pathway had a stronger impact on repairing DNA damage induced by Cr(VI) stress in rice seedlings supplied with exogenous Pro, while OsXPB1, OsTTDA2, OsTFIIH1, OsXPC, OsRAD23, OsDSS1, and OsRPA located at the NER pathway showed more contribution to repairing DNA damage than others.

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References

  • Al-Huqail AA, Ali HM, Kushwaha BK, AL-Huqail AA, Singh VP, Siddiqui MH (2020) Ascorbic acid is essential for inducing chromium (VI) toxicity tolerance in tomato roots. J Biotechnol 322:66–73

    Article  CAS  Google Scholar 

  • Ao M, Chen X, Deng T, Sun S, Tang Y, Morel JL, Qiu R, Wang S (2022) Chromium biogeochemical behaviour in soil-plant systems and remediation strategies: A critical review. J Hazard Mater 424:127233

    Article  CAS  Google Scholar 

  • Cadet J, Davies KJA (2017) Oxidative DNA damage & repair: An introduction. Free Radical Bio Med 107:2–12

    Article  CAS  Google Scholar 

  • Chidambaram A, Sundaramoorthy P, Murugan A, Sankar Ganesh K, Baskaran L (2009) Chromium induced cytotoxicity in blackgram (Vigna mungo L.). J Environ Health Sci 6:17–22

    CAS  Google Scholar 

  • Choudhary A, Kumar A, Kaur N (2020) ROS and oxidative burst: Roots in plant development. Plant Diversity 42:33–43

    Article  Google Scholar 

  • Ding G, Jin Z, Han Y, Sun P, Li G, Li W (2019) Mitigation of chromium toxicity in Arabidopsis thaliana by sulfur supplementation. Ecotox Environ Safe 182:109379

    Article  CAS  Google Scholar 

  • Fan WJ, Feng YX, Li YH, Lin YJ, Yu XZ (2020) Unraveling genes promoting ROS metabolism in subcellular organelles of Oryza sativa in response to trivalent and hexavalent chromium. Sci Total Environ 744:140951

    Article  CAS  Google Scholar 

  • Feng YX, Yu XZ, Mo CH, Lu CJ (2019) Regulation network of sucrose metabolism in response to trivalent and hexavalent chromium in Oryza sativa. J Agric Food Chem 67:9738–9748

    Article  CAS  Google Scholar 

  • Ferrando B, Furlanetto ALDM, Gredilla R, Havelund JF, Hebelstrup KH, Moller LM, Stevnsner T (2018) DNA repair in plant mitochondria- a complete base excision repair pathway in potato tuber mitochondria. Physiol Plantarum 166:494–512

    Article  Google Scholar 

  • Garg N, Manchanda G (2009) ROS generation in plants: Boon or bane? Plant Biosyst 143:81–96

    Article  Google Scholar 

  • Gupta D, Heinen CD (2019) The mismatch repair-dependent DNA damage response: Mechanisms and implications. DNA Repair 78:60–69

    Article  CAS  Google Scholar 

  • Kapoor D, Singh S, Kumar V, Romero R, Prasad R, Singh J (2019) Antioxidant enzymes regulation in plants in reference to reactive oxygen species (ROS) and reactive nitrogen species (RNS). Plant Gene 19:100182

    Article  CAS  Google Scholar 

  • Krejci L, Altmannova V, Spirek M, Zhao X (2012) Homologous recombination and its regulation. Nucleic Acids Res 40:5795–5818

    Article  CAS  Google Scholar 

  • Li CZ, Yang L, Lin YJ, Zhang H, Yu XZ (2020) Assimilation of exogenous cyanide cross talk in Oryza sativa L. to the key nodes in nitrogen metabolism. Ecotoxicology 29:1552–1564

    Article  CAS  Google Scholar 

  • Lin YJ, Yu XZ, Zhang Q (2019) Transcriptome analysis of Oryza sativa in responses to different concentrations of thiocyanate. Environ Sci Pollut Res 26:11696–11709

    Article  CAS  Google Scholar 

  • Mao Z, Bozzella M, Seluanov A, Gorbunova V (2008) Comparison of nonhomologous end joining and homologous recombination in human cells. DNA Repair 7:1765–1771

    Article  CAS  Google Scholar 

  • Nie G, Zhong M, Cai J, Yang X, Zhpu J, Appiah C, Tang M, Wang X, Feng G, Huang L, Zhang X (2021) Transcriptome characterization of candidate genes related to chromium uptake, transport and accumulation in Miscanthus sinensis. Ecotox Environ Safe 221:112445

    Article  CAS  Google Scholar 

  • Pourrut B, Jean S, Silvestre J, Pinelli E (2011) Lead-induced DNA damage in Vicia faba root cells: Potential involvement of oxidative stress. Muta Res 726:123–128

    Article  CAS  Google Scholar 

  • Rastgoo L, Alemzadeh A (2011) Biochemical responses of Gouan (Aeluropus littoralis) to heavy metals stress. Aust J Crop Sci 5:375–383

    CAS  Google Scholar 

  • Shahid M, Shamshad S, Rafiq M, Khalid S, Bibi I, Niazi NK, Dumat C, Rashid MI (2017) Chromium speciation, bioavailability, uptake, toxicity and detoxification in soil-plant system: A review. Chemosphere 178:513–533

    Article  CAS  Google Scholar 

  • Sharma A, Kapoor D, Wang J, Shahzad B, Kumar V, Bali AS, Jasrotia S, Zheng B, Yuan H, Yan D (2020) Chromium bioaccumulation and its impacts on plants: An overview. Plants 9:100

    Article  CAS  Google Scholar 

  • Singh HP, Mahajan P, Kaur S, Batish DR, Kohli RK (2013) Chromium toxicity and tolerance in plants. Environ Chem Lett 11:229–254

    Article  CAS  Google Scholar 

  • Szabados L, Savouré A (2010) Proline: a multifunctional amino acid. Trends Plant Sci 15:89–97

    Article  CAS  Google Scholar 

  • Tripathi BN, Singh V, Ezaki B, Sharma V, Gaur JP (2013) Mechanism of Cu- and Cd-induced proline hyperaccumulation in triticum aestivum (wheat). J Plant Growth Regul 32:799–808

    Article  CAS  Google Scholar 

  • Tuteja N, Singh MB, Misra MK, Bhalla PL, Tuteja R (2001) Molecular mechanisms of DNA damage and repair: progress in plants. Crit Rev Biochem Mol 36:337–397

    Article  CAS  Google Scholar 

  • Wakeel A, Xu M, Gan Y (2020) Chromium-induced reactive oxygen species accumulation by altering the enzymatic antioxidant system and sssociated sytotoxic, genotoxic, ultrastructural, and photosynthetic changes in plants. Int J Mol Sci 21:728

    Article  CAS  Google Scholar 

  • Wu Z, McGrouther K, Chen D, Wu W, Wang H (2013) Subcellular distribution of metals within Brassica chinensis L. in response to elevated lead and chromium stress. J Agri. Food Chem 61:4715–4722

    Article  CAS  Google Scholar 

  • Yang F, Lian M, Ma H, Feng L, Shen X, Chen J, Gang J (2022) Identification of key genes associated with papillary thyroid microcarcinoma characteristics by integrating transcriptome sequencing and weighted gene co-expression network analysis. Gene 811:146086

    Article  CAS  Google Scholar 

  • Yang L, Feng YX, Lin YJ, Yu XZ (2021) Comparative effects of sodium hydrosulfide and proline on functional repair in rice chloroplast through the D1 protein and thioredoxin system under simulated thiocyanate pollution. Chemosphere 284:131389

    Article  CAS  Google Scholar 

  • Yu XZ, Feng YX, Liang YP (2018a) Kinetics of phyto-accumulation of hexavalent and trivalent chromium in rice seedlings. Int Biodeter Biodegr 128:72–77

    Article  CAS  Google Scholar 

  • Yu XZ, Lin YJ, Zhang Q (2019) Metallothioneins enhance chromium detoxification through scavenging ROS and stimulating metal chelation in Oryza sativa. Chemosphere 220:300–313

    Article  CAS  Google Scholar 

  • Yu XZ, Lin YJ, Fan WJ, Lu MR (2017) The role of exogenous proline in amelioration of lipid peroxidation in rice seedlings exposed to Cr(VI). Int Biodeter Biodegr 123:106–112

    Article  CAS  Google Scholar 

  • Yu XZ, Fan WJ, Lin YJ, Zhang FF, Gupta DK (2018b) Differential expression of the PAL gene family in rice seedlings exposed to chromium by microarray analysis. Ecotoxicology. 27:325–335

    Article  CAS  Google Scholar 

  • Zhang Q, Feng YX, Lin YJ, Yu XZ (2021) Indigenous proline is a two-dimensional safety-relief value in balancing specific amino acids in rice under hexavalent chromium stress. J Agri Food Chem 69:11185–11195

    Article  CAS  Google Scholar 

  • Zhang Q, Feng YX, Lin YJ, Yu XZ (2022) Mathematical quantification of interactive complexity of transcription factors involved in proline-mediated regulative strategies in Oryza sativa under chromium stress. Plant Physiol Biochem 182:36–44

    Article  CAS  Google Scholar 

  • Zhang Y, Xu S, Yang S, Chen Y (2015) Salicylic acid alleviates cadmium-induced inhibition of growth and photosynthesis through upregulating antioxidant defense system in two melon cultivars (Cucumis melo L.). Protoplasma 252:911–924

    Article  CAS  Google Scholar 

  • Zhao Y, Yu H, Zhou J, Smith SM, Li J (2020) Malate circulation: linking chloroplast metabolism to mitochondrial ROS. Trends Plant Sci 25:446–454

    Article  Google Scholar 

Download references

Acknowledgements

This work was financially supported by the Natural Science Foundation of Guangxi (No. 2018GXNSFDA281024).

Author contributions

Writing-original draft preparation, Data analysis and Visualization Y-JL; Writing-reviewing and Editing, and Visualization Y-XF; Data analysis and Visualization QZ; Conceptualization, Supervision, Writing-reviewing and Editing, and Funding acquisition, X-ZY. All of the authors contributed to the final review of the manuscript.

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Correspondence to Xiao-Zhang Yu.

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Lin, YJ., Feng, YX., Zhang, Q. et al. Proline-mediated modulation on DNA repair pathway in rice seedlings under chromium stress by integrating gene chip and co-expression network analysis. Ecotoxicology 31, 1266–1275 (2022). https://doi.org/10.1007/s10646-022-02586-8

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