Analysis of the Transcriptome of Potentilla sericea Under Cadmium Stress Conditions

Jianhui Wu, Weifang Fan, Pengfei Gao, Qingjie Yang, Jing Zhang, Ling Wang

Abstract


Cadmium (Cd) stress significantly affects plant growth and development. Potentilla sericea is typically grown in gardens or as ground cover. In this study, the Cd response of P. sericea was analyzed based on physiological examinations and transcriptome analyses that uncovered the gene expression changes in P. sericea roots induced by a 7-day treatment with 90 µmol/L Cd2+. A total of 53,225 unigenes were identified, including 11,684 differentially expressed genes (DEGs; 8,083 upregulated and 3,601 downregulated). Additionally, 44 gene ontology terms and 127 Kyoto Encyclopedia of Genes and Genomes pathways were significantly enriched among these DEGs. Genes related to glutathione metabolism, plant hormone signal transduction, peroxisome processes, sulfur metabolism, and flavonoid biosynthesis pathways were confirmed as relevant to the Cd response of P. sericea. The molecular biology-related data described here may be useful for the future breeding of transgenic P. sericea plants with increased resistance to heavy metal stresses.

Keywords


glutathione metabolism; sulfur metabolism

Full Text:

PDF XML (JATS)

References


Adrian, R., Schmutz, D., & Brunold, C. (1990). Regulation of glutathione synthesis by cadmium in Pisum sativum L. Plant Physiology, 93(4), 1579–1584. https://doi.org/10.1104/pp.93.4.1579

Altschul, S. F., Madden, T. L., Schaffer, A. A., Zhang, J., Zhang, Z., Miller, W., & Lipman, D. J. (1997). Gapped blast and psi-blast: A new generation of protein detabase search programs. Nucleic Acids Research, 25(17), 3389–3402. https://doi.org/10.1093/nar/25.17.3389

Anjum, N. A., Umar, S., Ahmad, A., Iqbal, M., & Khan, N. A. (2008). Sulphur protects mustard (Brassica campestris L.) from cadmium toxicity by improving leaf ascorbate and glutathione. Plant Growth Regulation, 54(3), 271–279. https://doi.org/10.1007/s10725-007-9251-6

Apweiler, R., Bairoch, A., Wu, C. H., Barker, W. C., Boeckmann, B., Ferro, S., Gasteiger, E., Huang, H., Lopez, R., Magrane, M., Martin, M. J., Natale, D. A., O’Donovan, C., Redaschi, N., & Yeh, L. S. L. (2004). UniProt: The Universal Protein knowledgebase. Nucleic Acids Research, 32, 115–119. https://doi.org/10.1093/nar/gkh131

Bagheri, R., Ahmad, J., Bashir, H., Iqbal, M., & Qureshi, M. I. (2017). Changes in rubisco, cysteine-rich proteins and antioxidant system of spinach (Spinacia oleracea L.) due to sulphur deficiency, cadmium stress and their combination. Protoplasma, 254(2), 1031–1043. https://doi.org/10.1007/s00709-016-1012-9

Baszyński, T., Wajda, L., Król, M., Wolińska, D., Krupa, Z., & Tukendorf, A. (1980). Photosynthetic activities of cadmium treated tomato plants. Physiologia Plantarum, 48(3), 365–370. https://doi.org/10.1111/j.1399-3054.1980.tb03269.x

Bolger, A. M., Lohse, M., & Usadel, B. (2014). Trimmomatic: A flexible trimmer for Illumina sequence data. Bioinformatics, 30(15), 2114–2120. https://doi.org/10.1093/bioinformatics/btu170

Clemens, S. (2001). Molecular mechanisms of plant metal tolerance and homeostasis. Planta, 212(4), 475–486. https://doi.org/10.1007/s004250000458

Clemens, S., Aarts, M. G. M., Thomine, S., & Verbruggen, N. (2013). Plant science: The key to preventing slow cadmium poisoning. Trends in Plant Science, 18(2), 92–99. https://doi.org/10.1016/j.tplants.2012.08.003

Cosio, C., DeSantis, L., Beat, F., Diallo, S., & Keller, C. (2005). Distribution of cadmium in leaves of Thlaspi caerulescens. Journal of Experimental Botany, 412(56), 765–775. https://doi.org/10.1093/jxb/eri062

Dias, M. C., Monteiro, C., Moutinho-Pereira, J., Correia, C., Gonçalves, B., & Santos, C. (2013). Cadmium toxicity affects photosynthesis and plant growth at different levels. Acta Physiologiae Plantarum, 35(4), 1281–1289. https://doi.org/10.1007/s11738-012-1167-8

Drążkiewicz, M., Skórzyńska-Polit, E., & Krupa, Z. (2003). Response of the ascorbate– glutathione cycle to excess copper in Arabidopsis thaliana (L.). Plant Science, 164(2), 195–202. https://doi.org/10.1016/s0168-9452(02)00383-7

Ferretti, M., Ghisi, R., Merlo, L., Vecchia, F. D., & Passera, C. (1994). Effect of cadmium on photosynthesis and enzymes of photosynthetic sulphate and nitrate assimilation pathways in maize (Zea mays). Photosynthetica, 29(1), 49–54.

Gallego, S. M., Pena, L. B., Barcia, R. A., Azpilicueta, C. E., Iannone, M. F., Rosales, E. P., Zawoznik, M. S., Groppa, M. D., & Benavides, M. P. (2012). Unravelling cadmium toxicity and tolerance in plants: Insight into regulatory mechanisms. Environmental and Experimental Botany, 83, 33–46. https://doi.org/10.1016/j.envexpbot.2012.04.006

Gao, J. (2013). Hyperaccumulation of Sedum alfredii transcriptomics analysis and ZIP family gene function research. Zhejiang University.

Gill, S. S., Anjum, N. A., Hasanuzzaman, M., Gill, R., Trivedi, D. K., Ahmad, I., & Tuteja, N. (2013). Glutathione and glutathione reductase: A boon in disguise for plant abiotic stress defense operations. Plant Physiology and Biochemistry, 70, 204–212. https://doi.org/10.1016/j.plaphy.2013.05.032

Gill, S. S., & Tuteja, N. (2011). Cadmium stress tolerance in crop plants. Plant Signaling & Behavior, 6(2), 215–222. https://doi.org/10.4161/psb.6.2.14880

Ha, S. B., Smith, A. P., Howden, R., Dietrich, W. M., Bugg, S., O’Connell, M. J., Goldsburgh, P. B., & Cobbett, C. S. (1999). Phytochelatin synthase genes from Arabidopsis thaliana and the yeast Schizosaccharomyces pombe. The Plant Cell, 11(6), 1153–1163. https://doi.org/10.2307/3870806

Hall, J. L. (2002). Cellular mechanisms for heavy metal detoxification and tolerance. Journal of Experimental Botany, 53(366), 1–11. https://doi.org/10.1093/jexbot/53.366.1

Hossain, M. A., Piyatida, P., da Silva, J. A. T., & Fujita, M. (2012). Molecular mechanism of heavy metal toxicity and tolerance in plants: Central role of glutathione in detoxification of reactive oxygen species and methylglyoxal and in heavy metal chelation. Journal of Botany, 2012, Article 872875. https://doi.org/10.1155/2012/872875

Izbiańska, K., Arasimowicz-Jelonek, M., & Deckert, J. (2014). Phenylpropanoid pathway metabolites promotes tolerance response of lupine roots to lead stress. Ecotoxicology Environmental Safety, 110, 61–67. https://doi.org/10.1016/j.ecoenv.2014.08.014

Jin, W., Lu, M., & Wang, R. (1998). The effect of Cr(III) to the ultrastructure of Platymonas subcordiformis. Journal of Liaoning Normal University (Natural Science Edition), 21(4), 319–322.

Kanehisa, M., Goto, S., Kawashima, S., Okuno, Y., & Hattori, M. (2004). The KEGG resource for deciphering the genome. Nucleic Acids Research, 32(Suppl.), 277–280. https://doi.org/10.1093/nar/gkh063

Kim, D. Y., Bovet, L., Maeshima, M., Martinoia, E., & Lee, Y. (2007). The ABC transporter ATPDR8 is a cadmium extrusion pump conferring heavy metal resistance. Plant Journal, 50(2), 207–218. https://doi.org/10.1111/j.1365-313x.2007.03044.x

Langmead, B., & Salzberg, S. L. (2012). Fast gapped-read alignment with Bowtie 2. Nature Methods, 9(4), 357–359. https://doi.org/10.1038/nmeth.1923

Lee, S., Moon, J. S., Ko, T. S., Petros, D., Goldsbrough, B. P., & Korban, S. S. (2003). Overexpression of Arabidopsis phytochelatin synthase paradoxically leads to hypersensitivity to cadmium stress. Plant Physiology, 131(2), 656–663. https://doi.org/10.1104/pp.014118

Li, W., Jaroszewski, L., & Godzik, A. (2002). Tolerating some redundancy significantly speeds up clustering, of large protein databases. Bioinformatics, 18(1), 77–82. https://doi.org/10.1093/bioinformatics/18.1.77

Lin, Y. F., & Aarts, M. G. M. (2012). The molecular mechanism of zinc and cadmium stress response in plants. Cellular and Molecular Life Sciences, 69(19), 3187–3206. https://doi.org/10.1007/s00018-012-1089-z

Mobin, M., & Khan, N. A. (2007). Photosynthetic activity, pigment composition and antioxidative response of two mustard (Brassica juncea) cultivars differing in photosynthetic capacity subjected to cadmium stress. Journal of Plant Physiology, 164(5), 601–610. https://doi.org/10.1016/j.jplph.2006.03.003

Mohanpuria, P., Rana, N. K., & Yadav, S. K. (2008). Transient RNAi based gene silencing of glutathione synthetase reduces glutathione content in Camellia sinensis (L.) O. Kuntze somatic embryos. Biologia Plantarum, 52(2), 381–384. https://doi.org/10.1007/s10535- 008-0080-x

Ni, T. H., & Wei, Y. Z. (2003). Subcellular distribution of cadmium in mining ecotype Sedum alfredii. Acta Botanica Sinica, 45(8), 925–928.

Nocito, F. F., Lancilli, C., Crema, B., Fourcroy, P., Davidian, J. C., & Sacchi, G. A. (2006). Heavy metal stress and sulfate uptake in maize roots. Plant Physiology, 141(3), 1138–1148. https://doi.org/10.1104/pp.105.076240

Pence, N. S., Larsen, P. B., Ebbs, S. D., Letham, D. L. D., Lasat, M. M., Garvin, D. F., Eide, D., & Kochian, L. V. (2000). The molecular physiology of heavy metal transport in the Zn/Cd hyperaccumulator Thlaspi caerulescens. Proceedings of the National Academy of Sciences of the United States of America, 97(9), 4956–4960. https://doi.org/10.1073/pnas.97.9.4956

Rani, A., Kumar, A., Lal, A., & Pant, M. (2014). Cellular mechanisms of cadmium-induced toxicity: A review. International Journal of Environmental Health Research, 24(4), 378–399. https://doi.org/fs2b

Rao, A. S. V. C., & Reddy, A. R. (2008). Glutathione reductase: A putative redox regulatory system in plant cells. In N. A. Khan, S. Singh, & S. Umar (Eds.), Sulfur assimilation and abiotic stress in plants (pp. 111–147). Springer. https://doi.org/10.1007/978-3-540- 76326-0_6

Rausch, T., & Wachter, A. (2005). Sulfur metabolism: A versatile platform for launching defence operations. Trends in Plant Science, 10(10), 503–509. https://doi.org/10.1016/j.tplants.2005.08.006

Sasaki, A., Yamaji, N., Yokosho, K., & Ma, J. F. (2012). Nramp5 is a major transporter responsible for manganese and cadmium uptake in rice. Plant Cell, 24(5), 2155–2167. https://doi.org/10.1105/tpc.112.096925

Satoh-Nagasawa, N., Mori, M., Nakazawa, N., Kawamoto, T., Nagato, Y., Sakurai, K., Takahashi, H., Watanabe, A., & Akagi, H. (2011). Mutations in rice (Oryza sativa) heavy metal ATPase 2 (OsHMA2) restrict the translocation of zinc and cadmium. Plant and Cell Physiology, 53(1), 213–224. https://doi.org/10.1093/pcp/pcr166

Sheng, Y., Yan, X., Huang, Y., Han, Y., Zhang, C., Ren, Y., Fan, T., Xiao, F., Liu, Y., & Cao, S. (2018). The WRKY transcription factor, WRKY13, activates PDR8 expression to positively regulate cadmium tolerance in Arabidopsis. Plant, Cell & Environment, 42(3), 891–903. https://doi.org/10.1111/pce.13457

Sheoran, I. S., Aggarwal, N., & Singh, R. (1990). Effects of cadmium and nickel on in vivo carbon dioxide exchange rate of pigeon pea (Cajanus cajan L.). Plant and Soil, 129(2), 243–249. https://doi.org/10.1007/bf00032419

Spadaro, D., Yun, B. W., Spoel, S. H., Chu, C., Wang, Y. Q., & Loake, G. J. (2010). The redox switch: Dynamic regulation of protein function by cysteine modifications. Physiologia Plantarum, 138(4), 360–371. https://doi.org/10.1111/j.1399-3054.2009.01307.x

Sun, Y. M., Liu, L. J., Feng, M. Y., Wang, J. H., Cang, J., Li, S., & Wang, X. T. (2015). Research progress of sugar metabolism of plants under cold stress. Journal of Northeast Agricultural University, 46(07), 95–102. https://doi.org/fs2h

Takahashi, R., Ishimaru, Y., Shimo, H., Ogo, Y., Senoura, T., Nishizwa, N. K., & Nakanishi, H. (2012). The OsHMA2 transporter is involved in root-to-shoot translocation of Zn and Cd in rice. Plant, Cell & Environment, 35(11), 1948–1957. https://doi.org/10.1111/j.1365-3040.2012.02527.x

Tatusov, R. L., Galperin, M. Y., Natale, D. A., & Koonin, E. V. (2000). The COG database: A tool for genome-scale analysis of protein functions and evolution. Nucleic Acids Research, 28(1), 33–36. https://doi.org/10.1093/nar/28.1.33

Vogt, T. (2010). Phenylpropanoid biosynthesis. Molecular Plant, 3(1), 2–20. https://doi.org/10.1093/mp/ssp106

Vollenweider, P., Cosio, C., Günthardt-Goerg, M. S., & Keller, C. (2006). Localization and effects of cadmium in leaves of a cadmium-tolerant willow (Salix viminalis L.): Part II microlocalization and cellular effects of cadmium. Environmental and Experimental Botany, 58(1–3), 25–40. https://doi.org/10.1016/j.envexpbot.2005.06.012

Wang, J. C. (2016). Mechanism research on cadmium-stress response of Brassica based on transcriptomics [Unpublished doctoral dissertation]. Southwest University.

Wixon, J., & Kell, D. (2000). The Kyoto Encyclopedia of Genes and Genomes – KEGG. Yeast, 17(1), 48–55. https://doi.org/bkb7gc

Wong, C. K. E., & Cobbett, C. S. (2009). HMA P-type ATPases are the major mechanism for root-to-shoot Cd translocation in Arabidopsis thaliana. New Phytologist, 181(1), 71–78. https://doi.org/10.1111/j.1469-8137.2008.02638.x

Wu, J. H., Liu, J. X., Zhang, J., Hao, H. J., & Zhao, Q. Y. (2016). The response of ultrastructure and physiological characteristics of Potentilla sericea leaves to cadmium stress. Acta Agrestia Sinica, 24(6), 1278–1282.

Yeh, C. M., Chien, P. S., & Huang, H. J. (2006). Distinct signalling pathways for induction of MAP kinase activities by cadmium and copper in rice roots. Journal of Experimental Botany, 58(3), 659–671. https://doi.org/10.1093/jxb/erl240

Zhang, J., Zhao, X., Wang, X., & Lu, W. (2015). Effects of heavy metal cadmium (Cd) stress on growth and physiological property of Oenanthe javanica. Acta Physiologica Sinica, 51(11), 1969–1974. https://doi.org/10.13592/j.cnki.ppj.2015.0457

Zhang, Z., Wang, H., Wang, X., & Bi, Y. (2011). Nitric oxide enhances aluminum tolerance by affecting cell wall polysaccharides in rice roots. Plant Cell Reports, 30(9), Article 1701. https://doi.org/10.1007/s00299-011-1078-y




DOI: https://doi.org/10.5586/asbp.8943

Journal ISSN:
  • 2083-9480 (online)
  • 0001-6977 (print; ceased since 2016)
This is an Open Access journal, which distributes its content under the terms of the Creative Commons Attribution License, which permits redistribution, commercial and non-commercial, provided that the content is properly cited.
The journal is a member of the Committee on Publication Ethics (COPE) and aims to follow the COPE’s principles.
The journal publisher is a member of the Open Access Scholarly Publishers Association.
The journal content is indexed in Similarity Check, the Crossref initiative to prevent scholarly and professional plagiarism.
Publisher
Polish Botanical Society