The implications of planting mode on cadmium uptake and remobilization in rice: Field experiments across growth stages

Highlights

•Direct seeding (DS) method led to more distributed Cd in aerial parts of rice.

•The Cd content was significantly higher in brown rice with planting mode of DS.

•Using DS lessened the Fe plaque covering the root surface in all growth stages.

•Transplantation mode should be considered as a priority in Cd-contaminated areas.

Abstract

Global rice production practices have gradually changed from a reliance on transplanting to direct seeding. Yet how this shift may alter cadmium (Cd) accumulation in rice is poorly known. Here we conducted field experiments with two rice genotypes cultivars that were planted using three methods: via direct seeding (DS), seedling throwing (ST), and manual transplanting (MT). Rice samples were collected during four growth stages. The formation and distribution of iron plaque were analyzed using DCB (dithionite-citrate-bicarbonate) extractions and observed under micro-XRF (micro X-ray fluorescence). The results revealed that, in each growth stage, DS rice was more apt to harbor Cd distributed in the plant’s aerial parts, and the Cd concentration of brown rice from DS was 21.8%–43.3% significantly higher than those from ST and MT at maturity stage (p<0.05). During the vegetative stages, the Cd uptake percentage was higher in DS than MT rice, and those plants arising from the DS method were capable of absorbing more Cd earlier in their growth and development. Conversely, using DS decreased the amount of iron plaque covering the root surface in every growth stage, especially in the critical period of Cd accumulation, such that the roots’ middle areas were distinguished by a near-complete absence of iron plaque, thus weakening its role as an effective barrier to Cd uptake from soil. Collectively, this study demonstrated that implementing the DS mode of planting will increase Cd’s distribution in the aboveground parts of rice, and heightening the risk of Cd contamination in grain.

Graphical abstract

Keywords

Cadmium / Genotypes / Growth stages / Micro X-ray fluorescence / Planting mode

References

[1] Amaral D C, Lopes G, Guilherme L R, Seyfferth A L (2017). A new approach to sampling intact Fe plaque reveals Si-induced changes in Fe mineral composition and shoot As in rice. Environmental Science & Technology, 51(1): 38–45

[2] Cao Z Z, Qin M L, Lin X Y, Zhu Z W, Chen M X (2018). Sulfur supply reduces cadmium uptake and translocation in rice grains (Oryza sativa L.) by enhancing iron plaque formation, cadmium chelation and vacuolar sequestration. Environmental Pollution, 238: 76–84

[3] Chauhan B S, Awan T H, Abugho S B, Evengelista G, Sudhir-Yadav (2015). Effect of crop establishment methods and weed control treatments on weed management, and rice yield. Field Crops Research, 172: 72–84

[4] Chen D, Guo H, Li R, Li L, Pan G, Chang A, Joseph S (2016). Low uptake affinity cultivars with biochar to tackle Cd-tainted rice–A field study over four rice seasons in Hunan, China. Science of the Total Environment, 541: 1489–1498

[5] Chen S, Cai S G, Chen X, Zhang G P (2009). Genotypic differences in growth and physiological responses to transplanting and direct seeding cultivation in rice. Rice Science, 16(2): 143–150

[6] Chen S, Ge Q, Chu G, Xu C, Yan J, Zhang X, Wang D (2017). Seasonal differences in the rice grain yield and nitrogen use efficiency response to seedling establishment methods in the Middle and Lower reaches of the Yangtze River in China. Field Crops Research, 205: 157–169

[7] Cheng H, Wang M, Wong M H Z, Ye (2014). Does radial oxygen loss and iron plaque formation on roots alter Cd and Pb uptake and distribution in rice plant tissues? Plant and Soil, 375(1–2): 137–148

[8] Dahlin A S, Eriksson J, Campbell C D, Oborn I (2016). Soil amendment affects Cd uptake by wheat: Are we underestimating the risks from chloride inputs? Science of the Total Environment, 554–555: 349–357

[9] Deng X, Chen Y, Yang Y, Lu L, Yuan X, Zeng H, Zeng Q (2020a). Cadmium accumulation in rice (Oryza sativa L.) alleviated by basal alkaline fertilizers followed by topdressing of manganese fertilizer. Environmental Pollution, 262: 114289

[10] Deng X, Yang Y, Zeng H, Chen Y, Zeng Q (2020b). Variations in iron plaque, root morphology and metal bioavailability response to seedling establishment methods and their impacts on Cd and Pb accumulation and translocation in rice (Oryza sativa L.). Journal of Hazardous Materials, 384: 121343

[11] Devkota K P, Sudhir-Yadav C M, Khanda S J, Beebout B K, Mohapatra G R, Singleton R, Puskur (2020). Assessing alternative crop establishment methods with a sustainability lens in rice production systems of Eastern India. Journal of Cleaner Production, 244: 118835

[12] Dingkuhn M, Schnier H, de Datta S, Dorffling K, Javellana C (1991). Relationships between ripening-phase productivity and crop duration, canopy photosynthesis and senescence in transplanted and direct-seeded lowland rice. Field Crops Research, 26(3–4): 327–345

[13] Dong M F, Feng R W, Wang R G, Sun Y, Ding Y Z, Xu Y M, Fan Z L, Guo J K (2016). Inoculation of Fe/Mn-oxidizing bacteria enhances Fe/Mn plaque formation and reduces Cd and As accumulation in rice plant tissues. Plant and Soil, 404(1–2): 75–83

[14] Honma T, Ohba H, Kaneko-Kadokura A, Makino T, Nakamura K, Katou H (2016). Optimal soil Eh, pH, and water management for simultaneously minimizing arsenic and cadmium concentrations in rice grains. Environmental Science & Technology, 50(8): 4178–4185

[15] Huang H, Chen H P, Kopittke P M, Kretzschmar R, Zhao F J, Wang P, (2021). The voltaic effect as a novel mechanism controlling the remobilization of cadmium in paddy soils during drainage. Environmental Science & Technology,55(3): 1750–1758

[16] Huang G, Ding C, Hu Z, Cui C, Zhang T, Wang X (2018). Topdressing iron fertilizer coupled with pre-immobilization in acidic paddy fields reduced cadmium uptake by rice (Oryza sativa L.). Science of the Total Environment, 636: 1040–1047

[17] Kashiwagi T, Shindoh K, Hirotsu N, Ishimaru K (2009). Evidence for separate translocation pathways in determining cadmium accumulation in grain and aerial plant parts in rice. BMC Plant Biology, 9(1): 8–17

[18] 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

[19] Liu F, Liu X, Ding C, Wu L (2015). The dynamic simulation of rice growth parameters under cadmium stress with the assimilation of multi-period spectral indices and crop model. Field Crops Research, 183: 225–234

[20] Liu H, Hussain S, Zheng M, Peng S, Huang J, Cui K, Nie L (2015). Dry direct-seeded rice as an alternative to transplanted-flooded rice in Central China. Agronomy for Sustainable Development, 35(1): 285–294

[21] Liu J, Leng X, Wang M, Zhu Z, Dai Q (2011). Iron plaque formation on roots of different rice cultivars and the relation with lead uptake. Ecotoxicology and Environmental Safety, 74(5): 1304–1309

[22] Naklang K, Shu F, Nathabut K (1996). Growth of rice cultivars by direct seeding and transplanting under upland and lowland conditions. Field Crops Research, 48(2): 115–123

[23] Rodda M S, Li G, Reid R J (2011). The timing of grain Cd accumulation in rice plants: the relative importance of remobilisation within the plant and root Cd uptake post-flowering. Plant and Soil, 347(1–2): 105–114

[24] Shen Y T, Song Y F (2017). Effects of organic ligands on Pb absorption and speciation changes in Arabidopsis as determined by micro X-ray fluorescence and X-ray absorption near-edge structure analysis. Journal of Synchrotron Radiation, 24(2): 463–468

[25] Tao Y, Chen Q, Peng S, Wang W, Nie L (2016). Lower global warming potential and higher yield of wet direct-seeded rice in Central China. Agronomy for Sustainable Development, 36(2): 24–32

[26] Wang M, Chen W, Peng C (2016). Risk assessment of Cd polluted paddy soils in the industrial and township areas in Hunan, Southern China. Chemosphere, 144: 346–351

[27] Wang X, Yao H, Wong M H, Ye Z (2013). Dynamic changes in radial oxygen loss and iron plaque formation and their effects on Cd and As accumulation in rice (Oryza sativa L.). Environmental Geochemistry and Health, 35(6): 779–788

[28] Williams P N, Lei M, Sun G, Huang Q, Lu Y, Deacon C, Meharg A A, Zhu Y G (2009). Occurrence and partitioning of cadmium, arsenic and lead in mine impacted paddy rice: Hunan, China. Environmental Science & Technology, 43(3): 637–642

[29] Yan Y F, Choi D H, Kim D S, Lee B W (2010). Absorption, translocation, and remobilization of cadmium supplied at different growth stages of rice. Journal of Crop Science and Biotechnology, 13(2): 113–119

[30] Yang W T, Zhou H, Gu J F, Zeng Q R, Liao B H (2017). Influence of rapeseed cake on iron plaque formation and Cd uptake by rice (Oryza sativa L.) seedlings exposed to excess Cd. Bulletin of Environmental Contamination and Toxicology, 99(5): 601-606

[31] Zhang C, Ge Y, Yao H, Chen X, Hu M (2012). Iron oxidation-reduction and its impacts on cadmium bioavailability in paddy soils: A review. Frontiers of Environmental Science & Engineering, 6(4): 509–517

[32] Zhang X, Zhang F, Mao D (1998). Effect of iron plaque outside roots on nutrient uptake by rice (Oryza sativa L.). Zinc uptake by Fe-deficient rice. Plant and Soil, 202(1): 33–39

[33] Zhang Y, Liu H, Guo Z, Zhang C, Sheng J, Chen L, Luo Y, Zheng J (2018). Direct-seeded rice increases nitrogen runoff losses in southeastern China. Agriculture, Ecosystems & Environment, 251: 149–157

[34] Zhong S, Shi J, Xu J (2010). Influence of iron plaque on accumulation of lead by yellow flag (Iris pseudacorus L.) grown in artificial Pb-contaminated soil. Journal of Soils and Sediments, 10(5): 964–970

[35] Zhou H, Zhu W, Yang W T, Gu J F, Gao Z X, Chen L W, Du W Q, Zhang P, Peng P Q, Liao B H (2018). Cadmium uptake, accumulation, and remobilization in iron plaque and rice tissues at different growth stages. Ecotoxicology and Environmental Safety, 152: 91–97

Acknowledgements

This research was supported by grants from the National Natural Science Foundation of China (Nos. 42077142 and 41701366), and the Changsha Plan Project of Science and Technology (kq1801025).

Electronic Supplementary Material

Supplementary material is available in the online version of this article at https://doi.org/10.1007/s11783-021-1431-5 and is accessible for authorized users.

RIGHTS & PERMISSIONS

2021 Higher Education Press