Phenomic and metabolomic responses of roots to cadmium reveal contrasting resistance strategies in two rice cultivars (Oryza sativa L.)
Chong Liu, Mo-ming Lan, Er-kai He, Ai-jun Yao, Guo-bao Wang, Ye-tao Tang, Rong-liang Qiu
Phenomic and metabolomic responses of roots to cadmium reveal contrasting resistance strategies in two rice cultivars (Oryza sativa L.)
• We compared the phenomic and exudate metabolomic responses of roots of two rice cultivars to Cd.
• JY841 suffered serious root membrane damage and up-regulated phenylethanoid glycosides.
• TY816 up-regulated lipids and fatty acids to actively cope with oxidative stress.
• Reprogramming of root architecture and exudates contributed to contrasting Cd uptake.
To cope with heavy metal stress, plant root systems undergo root structure modification and release of multifarious metabolites. Elucidation of the resistance strategies to heavy metals mediated by the root system is crucial to comprehend the resistance mechanisms of plants. Here two rice varieties with contrasting grain cadmium (Cd) accumulation traits were selected and the responses of their root systems to Cd stress were evaluated by morphological and metabolomics analysis. The phenomic and metabolomic responses of the root system varied between the two cultivars under Cd stress. The low-Cd accumulation rice cultivar (TY816) had a more highly developed root system that coped with Cd stress (10 μM) by maintaining high root activity, while the root cells of the high-Cd accumulation cultivar (JY841) lost viability due to excessive Cd accumulation. TY816 upregulated lipids and fatty acids to reduce Cd uptake, whereas JY841 upregulated phenylethanoid glycosides to cope with Cd-induced oxidative stress. The combination of metabolomics and phenomics revealed that rice roots employ multiple strategies to increase their tolerance of Cd-induced oxidative stress. Differing capacities to shape the root system architecture and reprogram root exudate metabolites may contribute to the contrasting Cd accumulation abilities between JY841 and TY816.
Root morphology / Exudates / Cadmium / Rhizosphere / Metabolite
[1] |
Boursiac, Y., Léran, S., Corratgé-Faillie, C., Gojon, A., Krouk, G., Lacombe, B., 2013. ABA transport and transporters. Trends in Plant Science 18, 325–333
CrossRef
Pubmed
Google scholar
|
[2] |
Canarini, A., Kaiser, C., Merchant, A., Richter, A., Wanek, W., 2019. Root exudation of primary metabolites: mechanisms and their roles in plant responses to environmental stimuli. Frontiers in Plant Science 10, 1–19
CrossRef
Google scholar
|
[3] |
Chen, Y.T., Wang, Y., Yeh, K.C., 2017. Role of root exudates in metal acquisition and tolerance. Current Opinion in Plant Biology 39, 66–72
CrossRef
Pubmed
Google scholar
|
[4] |
Chi, Y., Li, F., Tam, N.F.y., Liu, C., Ouyang, Y., Qi, X., Li, W.C., Ye, Z., 2018. Variations in grain cadmium and arsenic concentrations and screening for stable low-accumulating rice cultivars from multi-environment trials. Science of the Total Environment 643, 1314–1324
CrossRef
Pubmed
Google scholar
|
[5] |
Debiane, D., Calonne, M., Fontaine, J., Laruelle, F., Grandmougin-Ferjani, A., Lounès-Hadj Sahraoui, A., 2012. Benzo[a]pyrene induced lipid changes in the monoxenic arbuscular mycorrhizal chicory roots. Journal of Hazardous Materials 209-210, 18–26
CrossRef
Pubmed
Google scholar
|
[6] |
Ding, Y., Feng, R., Wang, R., Guo, J., Zheng, X., 2014. A dual effect of Se on Cd toxicity: evidence from plant growth, root morphology and responses of the antioxidative systems of paddy rice. Plant and Soil 375, 289–301
CrossRef
Google scholar
|
[7] |
Duan, C., Fang, L., Yang, C., Chen, W., Cui, Y., Li, S., 2018. Reveal the response of enzyme activities to heavy metals through in situ zymography. Ecotoxicology and Environmental Safety 156, 106–115
CrossRef
Pubmed
Google scholar
|
[8] |
Fu, H., Yu, H., Li, T., Zhang, X., 2018. Influence of cadmium stress on root exudates of high cadmium accumulating rice line (Oryza sativa L.). Ecotoxicology and Environmental Safety 150, 168–175
CrossRef
Pubmed
Google scholar
|
[9] |
Harris, N.S., Taylor, G.J., 2013. Cadmium uptake and partitioning in durum wheat during grain filling. BMC Plant Biology 13, 103
CrossRef
Pubmed
Google scholar
|
[10] |
Hu, Y., Cheng, H., Tao, S., 2016. The challenges and solutions for cadmium-contaminated rice in China: a critical review. Environment International 92-93, 515–532
CrossRef
Pubmed
Google scholar
|
[11] |
Huang, B., Xin, J., Dai, H., Liu, A., Zhou, W., Yi, Y., Liao, K., 2015. Root morphological responses of three hot pepper cultivars to Cd exposure and their correlations with Cd accumulation. Environmental Science and Pollution Research International 22, 1151–1159
CrossRef
Pubmed
Google scholar
|
[12] |
Huang, L., Li, W.C., Tam, N.F.Y., Ye, Z., 2019. Effects of root morphology and anatomy on cadmium uptake and translocation in rice (Oryza sativa L.). Journal of Environmental Sciences (China) 75, 296–306
CrossRef
Pubmed
Google scholar
|
[13] |
Keunen, E., Peshev, D., Vangronsveld, J., Van Den Ende, W., Cuypers, A., 2013. Plant sugars are crucial players in the oxidative challenge during abiotic stress: extending the traditional concept. Plant, Cell & Environment 36, 1242–1255
CrossRef
Pubmed
Google scholar
|
[14] |
Khan, J., Yang, Y., Fu, Q., Shao, W., Wang, J., Shen, L., Huai, Y., Malangisha, G. K., Ali, A., Mahmoud, A., 2020. Screening of watermelon varieties for lead tolerance at the seedling stage HortScience 55, 858–869
CrossRef
Pubmed
Google scholar
|
[15] |
Kuzyakov, Y., Razavi, B.S., 2019. Rhizosphere size and shape: Temporal dynamics and spatial stationarity. Soil Biology & Biochemistry 135, 343–360
CrossRef
Google scholar
|
[16] |
Li, H., Luo, N., Li, Y.W., Cai, Q.Y., Li, H.Y., Mo, C.H., Wong, M.H., 2017. Cadmium in rice: Transport mechanisms, influencing factors, and minimizing measures. Environmental Pollution 224, 622–630
CrossRef
Pubmed
Google scholar
|
[17] |
Li, J., Lu, H., Liu, J., Hong, H., Yan, C., 2015. The influence of flavonoid amendment on the absorption of cadmium in Avicennia marina roots. Ecotoxicology and Environmental Safety 120, 1–6
CrossRef
Pubmed
Google scholar
|
[18] |
Li, T., Yang, X., Lu, L., Islam, E., He, Z., 2009. Effects of zinc and cadmium interactions on root morphology and metal translocation in a hyperaccumulating species under hydroponic conditions. Journal of Hazardous Materials 169, 734–741
CrossRef
Pubmed
Google scholar
|
[19] |
Liang, X., Strawn, D.G., Chen, J., Marshall, J., 2017. Variation in cadmium accumulation in spring wheat cultivars: uptake and redistribution to grain. Plant and Soil 421, 219–231
CrossRef
Google scholar
|
[20] |
Lin, Q., Chen, Y.X., Chen, H.M., Yu, Y.L., Luo, Y.M., Wong, M.H., 2003. Chemical behavior of Cd in rice rhizosphere. Chemosphere 50, 755–761
CrossRef
Pubmed
Google scholar
|
[21] |
Liu, J., Qian, M., Cai, G., Zhu, Q., Wong, M.H., 2007. Variations between rice cultivars in root secretion of organic acids and the relationship with plant cadmium uptake. Environmental Geochemistry and Health 29, 189–195
CrossRef
Pubmed
Google scholar
|
[22] |
Lu, Z., Zhang, Z., Su, Y., Liu, C., Shi, G., 2013. Cultivar variation in morphological response of peanut roots to cadmium stress and its relation to cadmium accumulation. Ecotoxicology and Environmental Safety 91, 147–155
CrossRef
Pubmed
Google scholar
|
[23] |
Lynch, J.P., 2019. Root phenotypes for improved nutrient capture: an underexploited opportunity for global agriculture. New Phytologist 223, 548–564
CrossRef
Pubmed
Google scholar
|
[24] |
Neumann, G., Martinoia, E., 2002. Cluster roots--an underground adaptation for survival in extreme environments. Trends in Plant Science 7, 162–167
CrossRef
Pubmed
Google scholar
|
[25] |
Nouairi, I., Ghnaya, T., Ben Youssef, N., Zarrouk, M., Habib Ghorbel, M., 2006. Changes in content and fatty acid profiles of total lipids of two halophytes: Sesuvium portulacastrum and Mesembryanthemum crystallinum under cadmium stress. Journal of Plant Physiology 163, 1198–1202
CrossRef
Pubmed
Google scholar
|
[26] |
Pan, J., Zhu, M., Chen, H., 2001. Aluminum-induced cell death in root-tip cells of barley. Environmental and Experimental Botany 46, 71–79
CrossRef
Pubmed
Google scholar
|
[27] |
Pétriacq, P., Williams, A., Cotton, A., McFarlane, A.E., Rolfe, S.A., Ton, J., 2017. Metabolite profiling of non-sterile rhizosphere soil. Plant Journal 92, 147–162
CrossRef
Pubmed
Google scholar
|
[28] |
Rajkumar, M., Ae, N., Prasad, M.N.V., Freitas, H., 2010. Potential of siderophore-producing bacteria for improving heavy metal phytoextraction. Trends in Biotechnology 28, 142–149
CrossRef
Pubmed
Google scholar
|
[29] |
Redjala, T., Zelko, I., Sterckeman, T., Leguv, V., Lux, A., 2011. Relationship between root structure and root cadmium uptake in maize. Environmental and Experimental Botany 71, 241–248
CrossRef
Google scholar
|
[30] |
Sun, X., Li, Z., Wu, L., Christie, P., Luo, Y., Fornara, D.A., 2019. Root-induced soil acidification and cadmium mobilization in the rhizosphere of Sedum plumbizincicola: evidence from a high-resolution imaging study. Plant and Soil 436, 267–282
CrossRef
Google scholar
|
[31] |
Tao, Q., Hou, D., Yang, X., Li, T., 2016. Oxalate secretion from the root apex of Sedum alfredii contributes to hyperaccumulation of Cd. Plant and Soil 398, 139–152
CrossRef
Google scholar
|
[32] |
Tao, Q., Zhao, J., Li, J., Liu, Y., Luo, J., Yuan, S., Li, B., Li, Q., Xu, Q., Yu, X., Huang, H., Li, T., Wang, C., 2020. Unique root exudate tartaric acid enhanced cadmium mobilization and uptake in Cd-hyperaccumulator Sedum alfredii. Journal of Hazardous Materials 383, 121177
CrossRef
Pubmed
Google scholar
|
[33] |
Ueno, D., Yamaji, N., Kono, I., Huang, C.F., Ando, T., Yano, M., Ma, J.F., 2010. Gene limiting cadmium accumulation in rice. Proceedings of the National Academy of Sciences of the United States of America 107, 16500–16505
CrossRef
Pubmed
Google scholar
|
[34] |
Upchurch, R.G., 2008. Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnology Letters 30, 967–977
CrossRef
Pubmed
Google scholar
|
[35] |
Uraguchi, S., Fujiwara, T., 2013. Rice breaks ground for cadmium-free cereals. Current Opinion in Plant Biology 16, 328–334
CrossRef
Pubmed
Google scholar
|
[36] |
Walker, T.S., Bais, H.P., Grotewold, E., Vivanco, J.M., 2003. Root exudation and rhizosphere biology. Plant Physiology 132, 44–51
CrossRef
Pubmed
Google scholar
|
[37] |
Wang, X., Tam, N.F.Y., He, H., Ye, Z., 2015. The role of root anatomy, organic acids and iron plaque on mercury accumulation in rice. Plant and Soil 394, 301–313
CrossRef
Google scholar
|
[38] |
Wen, Z., Li, H., Shen, Q., Tang, X., Xiong, C., Li, H., Pang, J., Ryan, M.H., Lambers, H., Shen, J., 2019. Tradeoffs among root morphology, exudation and mycorrhizal symbioses for phosphorus-acquisition strategies of 16 crop species. New Phytologist 223, 882–895
CrossRef
Pubmed
Google scholar
|
[39] |
Widodo., Broadley, M.R., Rose, T., Frei, M., Pariasca-Tanaka, J., Yoshihashi, T., Thomson, M., Hammond, J.P., Aprile, A., Close, T.J., Ismail, A.M., Wissuwa, M., 2010. Response to zinc deficiency of two rice lines with contrasting tolerance is determined by root growth maintenance and organic acid exudation rates, and not by zinc-transporter activity. New Phytologist 186, 400–414.
|
[40] |
Xia, J., Sinelnikov, I.V., Han, B., Wishart, D.S., 2015. MetaboAnalyst 3.0--making metabolomics more meaningful. Nucleic Acids Research 43, W251-7
CrossRef
Pubmed
Google scholar
|
[41] |
Xin, J., Huang, B., Dai, H., Mu, Y., 2017. Characterization of root morphology and root-derived low molecular weight organic acids in two sweet potato cultivars exposed to cadmium. Archives of Agronomy and Soil Science 63, 723–734
CrossRef
Google scholar
|
[42] |
Yoshida, S., Forno, D., Cock, J., Gomez, K., 1976. Laboratory manual for physiological studies of rice. Manila, Philippines.
|
[43] |
Zemanová, V., Pavlík, M., Kyjaková, P., Pavlíková, D., 2015. Fatty acid profiles of ecotypes of hyperaccumulator Noccaea caerulescens growing under cadmium stress. Journal of Plant Physiology 180, 27–34
CrossRef
Pubmed
Google scholar
|
[44] |
Zhang, H., Lu, L., Zhao, X., Zhao, S., Gu, X., Du, W., Wei, H., Ji, R., Zhao, L., 2019. Metabolomics reveals the “invisible” responses of spinach plants exposed to CeO2 nanoparticles. Environmental Science & Technology 53, 6007–6017
CrossRef
Pubmed
Google scholar
|
[45] |
Zhao, F.J., Ma, Y., Zhu, Y.G., Tang, Z., McGrath, S.P., 2015. Soil contamination in China: current status and mitigation strategies. Environmental Science & Technology 49, 750–759
CrossRef
Pubmed
Google scholar
|
[46] |
Zhao, J.Y., Ye, Z.H., Zhong, H., 2018. Rice root exudates affect microbial methylmercury production in paddy soils. Environmental Pollution 242, 1921–1929
CrossRef
Pubmed
Google scholar
|
[47] |
Zhao, L., Huang, Y., Hu, J., Zhou, H., Adeleye, A.S., Keller, A.A., 2016. 1H NMR and GC-MS based metabolomics reveal defense and detoxification mechanism of cucumber plant under nano-Cu stress. Environmental Science & Technology 50, 2000–2010
CrossRef
Pubmed
Google scholar
|
[48] |
Zhu, X.F., Zheng, C., Hu, Y.T., Jiang, T., Liu, Y., Dong, N.Y., Yang, J.L., Zheng, S.J., 2011. Cadmium-induced oxalate secretion from root apex is associated with cadmium exclusion and resistance in Lycopersicon esulentum. Plant, Cell & Environment 34, 1055–1064
CrossRef
Pubmed
Google scholar
|
/
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