logo

SCIENCE CHINA Technological Sciences, Volume 62 , Issue 9 : 1616-1627(2019) https://doi.org/10.1007/s11431-018-9426-3

Application of phosphate-containing materials affects bioavailability of rare earth elements and bacterial community in soils

More info
  • ReceivedSep 30, 2018
  • AcceptedDec 28, 2018
  • PublishedFeb 21, 2019

Abstract

The exploitation and smelting of rare earths can cause serious pollution to the farmland around the mining area. The rare earth elements (REEs) are absorbed by crops and enter the human body through the food chain, which threatens people’s health. The effects of four phosphorus-containing materials-calcium superphosphate (SSP), phosphate rock (PR), calcium magnesium phosphate (CMP) and bone charcoal (BC) on rice growth and bacterial community structure in REE mining area of Xinfeng County were studied by pot experiment. The soil solution was collected during rice transplanting and harvest periods respectively, the rice and soil samples were collected and sequenced. The concentrations of water-soluble REEs were measured by inductively coupled plasma mass spectrometry (ICP-MS), and bacteria in soil was deeply sequenced by the Illumina Miseq sequencing platform. PR, CMP and BC promoted the growth of rice, improved the biomass of rice roots, shoots and grains, and significantly reduced absorption and accumulation of REEs in rice roots, shoots and grains. SSP treatment reduced the pH value of soil, significantly improved the concentration of REE solution in soil and improved biomass of rice roots, shoots and grains, and significantly improved the concentration of REEs in grain. The effects of phosphorus-containing materials on the absorption and accumulation of 15 REEs in rice roots, shoots and grains were very different, and significantly influenced the soil bacterial community. SSP reduced richness and diversity of bacteria. CMP improved the diversity of soil bacteria, but reduced their richness. PR and BC treatment improved the richness and diversity of soil bacteria, and significantly increased the abundance of Bacillus. The results showed that adding PR, CMP and BC to soil in the REE mining area of Xinfeng can improve food security and eco-environmental quality, and hence, are potential restorative materials; SSP is not recommended for use in acidic soils.


Funded by

the National Natural Science Foundation of China(Grant,Nos.,41561096,&,41867062)

Shangrao Science and Technology Project of China(Grant,No.,18C019)

and Jiangxi Science and Technology Project of China(Grant,No.,20142BAB203026)


Acknowledgment

This work was supported by the National Natural Science Foundation of China (Grant Nos. 41561096 & 41867062), Shangrao Science and Technology Project of China (Grant No. 18C019), and Jiangxi Science and Technology Project of China (Grant No. 20142BAB203026).


Supplement

Supporting information

The supporting information is available online at tech.scichina.com and link.springer.com. The supporting materials are published as submitted, without typesetting or editing. The responsibility for scientific accuracy and content remains entirely with the authors.


References

[1] Wang L, Liang T. Accumulation and fractionation of rare earth elements in atmospheric particulates around a mine tailing in Baotou, China. Atmos Environ, 2014, 88: 23-29 CrossRef ADS Google Scholar

[2] Wiche O, Kummer N A, Heilmeier H. Interspecific root interactions between white lupin and barley enhance the uptake of rare earth elements (REEs) and nutrients in shoots of barley. Plant Soil, 2016, 402: 235-245 CrossRef Google Scholar

[3] Wang L, Liang T, Kleinman P J A, et al. An experimental study on using rare earth elements to trace phosphorous losses from nonpoint sources. Chemosphere, 2011, 85: 1075-1079 CrossRef PubMed ADS Google Scholar

[4] Liao S G. Study on the development strategy of Jiangxi rare earth industry. Dissertation of Masteral Degree. Nanchang: Nanchang University, 2011. Google Scholar

[5] Jin S L, Hu Z J, Qiu Q P, et al. Effects of phosphate amendments on the concentrations of rare earth elements in soil solution (in Chinese). Chin J Ecol, 2018, 37: 1693–1701. Google Scholar

[6] Jin S L, Huang Y Z, Hu Y, et al. Effects of bone char, phosphate rock and modifying agent on leaching of rare earth elements in soil (in Chinese). Acta Sci Circumst, 2016, 36: 3818–3825. Google Scholar

[7] Khan A M, Bakar N K A, Bakar A F A, et al. Chemical speciation and bioavailability of rare earth elements (REEs) in the ecosystem: A review. Environ Sci Pollut Res, 2017, 24: 22764-22789 CrossRef PubMed Google Scholar

[8] Suja S, Fernandes L L, Rao V P. Distribution and fractionation of rare earth elements and Yttrium in suspended and bottom sediments of the Kali estuary, western India. Environ Earth Sci, 2017, 76: 174 CrossRef Google Scholar

[9] Liang T, Li K, Wang L. State of rare earth elements in different environmental components in mining areas of China. Environ Monit Assess, 2014, 186: 1499-1513 CrossRef PubMed Google Scholar

[10] Jin S L, Huang Y Z, Hu Y, et al. Rare earth elements content and health risk assessment of soil and crops in typical rare earth mine area in Jiangxi Province. Acta Sci Circumst, 2014, 34: 3084–3093. Google Scholar

[11] Zhu W F, Xu S Q, Shao P P, et al. Investigation on intake allowance of rare earth: A study on bio-effect of rare earth in South Jiangxi. Chin Environ Sci, 1997, 17: 63–66. Google Scholar

[12] Li X, Chen Z, Chen Z, et al. A human health risk assessment of rare earth elements in soil and vegetables from a mining area in Fujian Province, Southeast China. Chemosphere, 2013, 93: 1240-1246 CrossRef PubMed ADS Google Scholar

[13] Marzec-Wróblewska U, Kamiński P, Łakota P, et al. Determination of rare earth elements in human sperm and association with semen quality. Arch Environ Contam Toxicol, 2015, 69: 191-201 CrossRef PubMed Google Scholar

[14] Rim K T, Koo K H, Park J S. Toxicological evaluations of rare earths and their health impacts to workers: A literature review. Saf Health Work, 2013, 4: 12-26 CrossRef PubMed Google Scholar

[15] Liu H, Wang J, Yang Z, et al. Serum proteomic analysis based on iTRAQ in miners exposed to soil containing rare earth elements. Biol Trace Elem Res, 2015, 167: 200-208 CrossRef PubMed Google Scholar

[16] Zhang H, Feng J, Zhu W, et al. Chronic toxicity of rare-earth elements on human beings: Implications of blood biochemical indices in ree-high regions, South Jiangxi. Biol Trace Elem Res, 2000, 73: 1-18 CrossRef Google Scholar

[17] Zhong W H, Cai Z C. Long-term effects of inorganic fertilizers on microbial biomass and community functional diversity in a paddy soil derived from quaternary red clay. Appl Soil Ecol, 2007, 36: 84-91 CrossRef Google Scholar

[18] Beauregard M S, Hamel C, Atul-Nayyar C, et al. Long-term phosphorus fertilization impacts soil fungal and bacterial diversity but not AM fungal community in alfalfa. Microb Ecol, 2010, 59: 379-389 CrossRef PubMed Google Scholar

[19] Yi B, Zhang Q, Gu C, et al. Effects of different fertilization regimes on nitrogen and phosphorus losses by surface runoff and bacterial community in a vegetable soil. J Soils Sediment, 2018, 18: 3186-3196 CrossRef Google Scholar

[20] Teufel A G, Li W, Kiss A J, et al. Impact of nitrogen and phosphorus on phytoplankton production and bacterial community structure in two stratified Antarctic lakes: A bioassay approach. Polar Biol, 2017, 40: 1007-1022 CrossRef Google Scholar

[21] Tan H, Barret M, Mooij M J, et al. Long-term phosphorus fertilisation increased the diversity of the total bacterial community and the phoD phosphorus mineraliser group in pasture soils. Biol Fertil Soils, 2013, 49: 661-672 CrossRef Google Scholar

[22] Lagos L M, Acuña J J, Maruyama F, et al. Effect of phosphorus addition on total and alkaline phosphomonoesterase-harboring bacterial populations in ryegrass rhizosphere microsites. Biol Fertil Soils, 2016, 52: 1007-1019 CrossRef Google Scholar

[23] Liu M, Liu J, Chen X, et al. Shifts in bacterial and fungal diversity in a paddy soil faced with phosphorus surplus. Biol Fertil Soils, 2018, 54: 259-267 CrossRef Google Scholar

[24] Hamel C, Hanson K, Selles F, et al. Seasonal and long-term resource-related variations in soil microbial communities in wheat-based rotations of the Canadian prairie. Soil Biol Biochem, 2006, 38: 2104-2116 CrossRef Google Scholar

[25] Huang J, Hu B, Qi K, et al. Effects of phosphorus addition on soil microbial biomass and community composition in a subalpine spruce plantation. Eur J Soil Biol, 2016, 72: 35-41 CrossRef Google Scholar

[26] Shi Y, Lalande R, Ziadi N, et al. An assessment of the soil microbial status after 17 years of tillage and mineral P fertilization management. Appl Soil Ecol, 2012, 62: 14-23 CrossRef Google Scholar

[27] Jiang Z W, Weng B Q, Huang Y F, et al. Effects of lanthanum on soil microorganism (in Chinese). J Chin Rare Earth, 2008, 26: 498–502. Google Scholar

[28] Zhou J, Xia B, Treves D S, et al. Spatial and resource factors influencing high microbial diversity in soil. Appl Environ Microbiol, 2002, 68: 326-334 CrossRef Google Scholar

[29] Pol A, Barends T R M, Dietl A, et al. Rare earth metals are essential for methanotrophic life in volcanic mudpots. Environ Microbiol, 2014, 16: 255-264 CrossRef PubMed Google Scholar

[30] Keltjens J T, Pol A, Reimann J, et al. PQQ-dependent methanol dehydrogenases: Rare-earth elements make a difference. Appl Microbiol Biotechnol, 2014, 98: 6163-6183 CrossRef PubMed Google Scholar

[31] Wang Y S, Hou X L, Cai L P, et al. Impacts of rare earth mining on soil bacterial community composition and biodiversity (in Chinese). J Environ Sci-China, 2017, 37: 3089–3095. Google Scholar

[32] Wang J H. Study on characteristic of soil microb exogenous rare earths accumulation area Baosteel Tailings Dam. Dissertation of Masteral Degree. Hohhot: Inner Mongolia Normal University, 2011. Google Scholar

[33] Ding S M, Liang T, Yan J C, et al. Fractionations of rare earth elements in plants and their conceptive model. Sci China Ser C, 2007, 50: 47-55 CrossRef PubMed Google Scholar

[34] Jones R T, Robeson M S, Lauber C L, et al. A comprehensive survey of soil acidobacterial diversity using pyrosequencing and clone library analyses. ISME J, 2009, 3: 442-453 CrossRef PubMed Google Scholar

[35] Fierer N, Lauber C L, Ramirez K S, et al. Comparative metagenomic, phylogenetic and physiological analyses of soil microbial communities across nitrogen gradients. ISME J, 2012, 6: 1007-1017 CrossRef PubMed Google Scholar

[36] Bulgarelli D, Schlaeppi K, Spaepen S, et al. Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol, 2013, 64: 807-838 CrossRef PubMed Google Scholar

[37] Ward N L, Challacombe J F, Janssen P H, et al. Three genomes from the phylum Acidobacteria provide insight into the lifestyles of these microorganisms in soils. Appl Environ Microbiol, 2009, 75: 2046-2056 CrossRef PubMed Google Scholar

[38] Chhabra S, Brazil D, Morrissey J, et al. Fertilization management affects the alkaline phosphatase bacterial community in barley rhizosphere soil. Biol Fertil Soils, 2013, 49: 31-39 CrossRef Google Scholar

[39] Lauber C L, Hamady M, Knight R, et al. Pyrosequencing-based assessment of soil pH as a predictor of soil bacterial community structure at the continental scale. Appl Environ Microbiol, 2009, 75: 5111-5120 CrossRef PubMed Google Scholar

[40] Tarasov A L, Osipov G A, Borzenkov I A. Desulfovibrios from marine biofoulings at the South Vietnam coastal area and description of Desulfovibrio hontreensis sp. nov.. Microbiology, 2015, 84: 654-664 CrossRef Google Scholar

[41] Geelhoed J S, Henstra A M, Stams A J M. Carboxydotrophic growth of Geobacter sulfurreducens. Appl Microbiol Biotechnol, 2016, 100: 997-1007 CrossRef PubMed Google Scholar

[42] Tanasupawat S, Takehana T, Yoshida S, et al. Ideonella sakaiensis sp. nov., isolated from a microbial consortium that degrades poly(ethylene terephthalate). Int J Systatic Evolary MicroBiol, 2016, 19: 2813-2818 CrossRef PubMed Google Scholar

[43] Berini F, Verce M, Ausec L, et al. Isolation and characterization of a heterologously expressed bacterial laccase from the anaerobe Geobacter metallireducens. Appl Microbiol Biotechnol, 2018, 102: 2425-2439 CrossRef PubMed Google Scholar

[44] Kulichevskaya I S, Suzina N E, Liesack W, et al. Bryobacter aggregatus gen. nov., sp. nov., a peat-inhabiting, aerobic chemo-organotroph from subdivision 3 of the Acidobacteria. Int J Syst Evol Micr, 2010, 60: 301-306 CrossRef PubMed Google Scholar

[45] Chao Y, Liu W, Chen Y, et al. Structure, variation, and co-occurrence of soil microbial communities in abandoned sites of a rare earth elements mine. Environ Sci Technol, 2016, 50: 11481-11490 CrossRef PubMed ADS Google Scholar

[46] Nacke H, Thürmer A, Wollherr A, et al. Pyrosequencing-based assessment of bacterial community structure along different management types in German forest and grassland soils. PLoS ONE, 2011, 6: e17000 CrossRef PubMed ADS Google Scholar

[47] Leff J W, Jones S E, Prober S M, et al. Consistent responses of soil microbial communities to elevated nutrient inputs in grasslands across the globe. Proc Natl Acad Sci USA, 2015, 112: 10967-10972 CrossRef PubMed ADS Google Scholar

[48] Ahn J H, Song J, Kim B Y, et al. Characterization of the bacterial and archaeal communities in rice field soils subjected to long-term fertilization practices. J Microbiol, 2012, 50: 754-765 CrossRef PubMed Google Scholar

[49] Pereg L, de-Bashan L E, Bashan Y. Assessment of affinity and specificity of Azospirillum for plants. Plant Soil, 2016, 399: 389-414 CrossRef Google Scholar

[50] Fukami J, Cerezini P, Hungria M. Azospirillum: Benefits that go far beyond biological nitrogen fixation. AMB Expr, 2018, 8: 1-12 CrossRef PubMed Google Scholar

[51] Mignardi S, Corami A, Ferrini V. Evaluation of the effectiveness of phosphate treatment for the remediation of mine waste soils contaminated with Cd, Cu, Pb, and Zn. Chemosphere, 2012, 86: 354-360 CrossRef PubMed ADS Google Scholar

[52] Cleveland C C, Townsend A R, Schmidt S K. Phosphorus limitation of microbial processes in moist tropical forests: Evidence from short-term laboratory incubations and field studies. Ecosystems, 2002, 5: 0680-0691 CrossRef Google Scholar

[53] Zhu F, Lu X, Liu L, et al. Phosphate addition enhanced soil inorganic nutrients to a large extent in three tropical forests. Sci Rep, 2015, 5: 7923 CrossRef PubMed ADS Google Scholar

[54] Lehmann J, Rillig M C, Thies J, et al. Biochar effects on soil biota—A review. Soil Biol Biochem, 2011, 43: 1812-1836 CrossRef Google Scholar

[55] McCormack S A, Ostle N, Bardgett R D, et al. Biochar in bioenergy cropping systems: Impacts on soil faunal communities and linked ecosystem processes. GCB Bioenergy, 2013, 5: 81-95 CrossRef Google Scholar

[56] Gul S, Whalen J K, Thomas B W, et al. Physico-chemical properties and microbial responses in biochar-amended soils: Mechanisms and future directions. Agric Ecosyst Environ, 2015, 206: 46-59 CrossRef Google Scholar

[57] Steinbeiss S, Gleixner G, Antonietti M. Effect of biochar amendment on soil carbon balance and soil microbial activity. Soil Biol Biochem, 2009, 41: 1301-1310 CrossRef Google Scholar

[58] Ameloot N, De Neve S, Jegajeevagan K, et al. Short-term CO2 and N2O emissions and microbial properties of biochar amended sandy loam soils. Soil Biol Biochem, 2013, 57: 401-410 CrossRef Google Scholar

[59] Gomez J D, Denef K, Stewart C E, et al. Biochar addition rate influences soil microbial abundance and activity in temperate soils. Eur J Soil Sci, 2014, 65: 28-39 CrossRef Google Scholar

[60] Canbolat M Y, Bilen S, Çakmakçı R, et al. Effect of plant growth-promoting bacteria and soil compaction on barley seedling growth, nutrient uptake, soil properties and rhizosphere microflora. Biol Fertil Soils, 2006, 42: 350-357 CrossRef Google Scholar

[61] Graber E R, Meller Harel Y, Kolton M, et al. Biochar impact on development and productivity of pepper and tomato grown in fertigated soilless media. Plant Soil, 2010, 337: 481-496 CrossRef Google Scholar

[62] Kolton M, Meller Harel Y, Pasternak Z, et al. Impact of biochar application to soil on the root-associated bacterial community structure of fully developed greenhouse pepper plants. Appl Environ Microbiol, 2011, 77: 4924-4930 CrossRef PubMed Google Scholar

[63] Chen Y P, Rekha P D, Arun A B, et al. Phosphate solubilizing bacteria from subtropical soil and their tricalcium phosphate solubilizing abilities. Appl Soil Ecol, 2006, 34: 33-41 CrossRef Google Scholar

[64] Zaidi A, Khan M, Ahemad M, et al. Plant growth promotion by phosphate solubilizing bacteria. Acta Microbiol Imm H, 2009, 56: 263-284 CrossRef Google Scholar

[65] Linu M S, Stephen J, Jisha M S. Phosphate solubilizing Gluconacetobacter sp., Burkholderia sp. and their potential interaction with cowpea (Vigna unguiculata (L.) Walp.). Int J Agric Res, 2009, 4: 79-87 CrossRef Google Scholar

[66] Oteino N, Lally R D, Kiwanuka S, et al. Plant growth promotion induced by phosphate solubilizing endophytic Pseudomonas isolates. Front Microbiol, 2015, 6: 745 CrossRef Google Scholar

  • Figure 1

    (Color online) Effects of different phosphorus-containing materials on biomass of rice. Data is average (n=3), and different lowercase letters in the same part of rice show significant difference among different treatments (P<0.05).

  • Figure 2

    (Color online) The effects of different phosphorus-containing materials on the alpha diversity of soil community. The different letters indicate the significant difference among treatments of different phosphorus-containing materials, P<0.05.

  • Figure 3

    (Color online) Heat map of the top 30 genera in soil.

  • Figure 4

    (Color online) Canonical correspondence analysis (CCA) on soil bacterial communities with the environmental variables and CCA-based variation partitioning analysis (VPA) of bacterial communities explained by environmental factors.

  • Table 1   Effects of phosphorus-containing materials on the concentration of REEs in different parts of rice

    Parts

    Material

    Y

    La

    Ce

    Pr

    Nd

    Sm

    Eu

    Gd

    Tb

    Dy

    Ho

    Er

    Tm

    Yb

    Lu

    ∑REE

    Grain

    SSP

    46.36b

    74.55b

    107.57b

    83.03b

    92.75b

    73.51b

    73.70b

    53.19a

    51.44b

    51.19a

    41.80b

    54.51b

    42.73b

    48.98b

    38.24b

    933.59b

    CK

    28.08a

    72.83ab

    95.24ab

    66.50a

    79.32ab

    57.22a

    56.63a

    40.20a

    34.00a

    40.40a

    25.65a

    36.21a

    26.39a

    31.99a

    21.30a

    712.04ab

    PR

    19.76a

    49.82a

    78.02a

    60.16a

    68.34a

    52.10a

    50.60a

    33.68a

    30.97a

    33.72a

    21.87a

    31.73a

    23.24a

    27.70a

    18.49a

    600.27a

    CMP

    17.84a

    38.33a

    71.84a

    59.08a

    65.62a

    51.85a

    49.41a

    36.86a

    31.94a

    35.74a

    22.82a

    32.04a

    23.64a

    28.15a

    19.05a

    584.26a

    BC

    17.28a

    49.62a

    74.37a

    58.44a

    64.52a

    51.95a

    49.47a

    36.48a

    30.66a

    34.10a

    21.42a

    30.82a

    22.82a

    26.85a

    18.15a

    587.02a

    Shoot

    SSP

    0.62a

    1.41a

    1.14a

    0.32a

    0.99a

    0.23a

    0.10a

    0.22a

    0.06a

    0.15a

    0.05a

    0.10a

    0.04a

    0.08a

    0.03a

    5.53a

    CK

    1.04a

    3.18ab

    2.48a

    0.57ab

    1.95ab

    0.39a

    0.15ab

    0.31a

    0.07a

    0.22a

    0.06a

    0.13a

    0.04a

    0.11a

    0.03a

    10.73ab

    PR

    1.01a

    2.66b

    2.16a

    0.55b

    1.90b

    0.38a

    0.15b

    0.29a

    0.07a

    0.21a

    0.06a

    0.13a

    0.04a

    0.11a

    0.03a

    9.76b

    CMP

    0.53a

    1.31a

    1.11a

    0.31a

    0.96a

    0.23a

    0.09a

    0.18a

    0.06a

    0.14a

    0.05a

    0.09a

    0.04a

    0.08a

    0.03a

    5.19a

    BC

    0.53a

    1.32a

    1.16a

    0.32a

    0.99a

    0.24a

    0.11a

    0.20a

    0.06a

    0.15a

    0.05a

    0.09a

    0.04a

    0.08a

    0.03a

    5.34a

    Root

    SSP

    30.63a

    70.98b

    46.09b

    6.00a

    39.35b

    0.53a

    4.09b

    4.78a

    1.87b

    0.08a

    2.19b

    6.15b

    0.87b

    5.26b

    0.79b

    219.67b

    CK

    42.67a

    150.87d

    114.82d

    18.84b

    96.91d

    13.82b

    5.55c

    17.09b

    2.68c

    0.14a

    2.79b

    7.49b

    1.04b

    6.02b

    0.87b

    481.62c

    PR

    44.12a

    112.86c

    82.09c

    7.63a

    75.77c

    9.13b

    5.09c

    15.55b

    2.47c

    0.1a

    2.73b

    7.56b

    1.04b

    6.22b

    0.88b

    373.26c

    CMP

    0.65a

    22.66a

    14.236a

    2.64a

    11.44a

    2.48a

    3.00a

    1.04a

    0.81a

    0.04a

    0.92a

    2.60a

    0.40a

    2.41a

    0.37a

    65.70a

    BC

    6.79a

    30.04b

    19.40b

    2.12a

    18.52b

    2.40a

    3.25b

    7.89a

    1.09b

    0.04a

    1.30b

    3.71b

    0.55b

    3.31b

    0.50b

    100.91b

    Data are average (n=3), and different lowercase letters in the same part of rice show significant difference among different treatments (P<0.05).

  • Table 2   Effect of phosphorus-containing materials on the concentration of REEs (g L) in soil solution

    Time

    Material

    Y

    La

    Ce

    Pr

    Nd

    Sm

    Eu

    Gd

    Tb

    Dy

    Ho

    Er

    Tm

    Yb

    Lu

    ∑REE

    Transplantingperiod

    SSP

    210.14c

    343.32c

    211.96c

    32.92b

    156.42b

    26.73b

    5.56b

    35.55c

    3.60c

    22.28c

    4.29c

    13.89c

    1.40c

    8.82c

    1.21c

    1078.16c

    CK

    116.47b

    199.80b

    173.46b

    30.50b

    128.45b

    23.45b

    4.38b

    23.87b

    2.71b

    16.52b

    2.78b

    8.85b

    0.97b

    6.73b

    0.85b

    739.87b

    PR

    14.04a

    8.57a

    6.75a

    2.02a

    12.47a

    2.70a

    0.65a

    2.40a

    0.27a

    1.74a

    0.36a

    1.32a

    0.16a

    1.30a

    0.18a

    54.99a

    CMP

    0.90a

    0.89a

    0.93a

    0.19a

    1.00a

    0.26a

    0.08a

    0.22a

    0.02a

    0.18a

    0.03a

    0.13a

    0.02a

    0.17a

    0.03a

    5.11a

    BC

    14.08a

    12.22a

    10.31a

    2.71a

    16.71a

    3.18a

    0.66a

    3.13a

    0.31a

    2.02a

    0.40a

    1.51a

    0.18a

    1.38a

    0.21a

    69.10a

    Maturing period

    SSP

    42.90b

    37.48b

    17.25c

    3.84a

    20.21a

    3.70a

    0.89b

    5.62b

    0.60b

    4.18b

    0.88b

    3.06b

    0.34b

    2.42b

    10.24a

    153.67b

    CK

    131.17c

    205.75c

    138.07d

    27.03a

    111.38b

    19.90b

    4.01c

    23.71c

    2.66c

    16.24c

    2.77c

    8.63c

    0.90c

    6.13c

    0.75a

    699.18c

    PR

    7.23a

    5.74a

    3.35b

    0.90b

    5.08a

    1.26a

    0.45a

    0.99a

    0.10a

    0.69a

    0.14a

    0.55a

    0.07a

    0.50a

    0.07a

    27.20a

    CMP

    0.58a

    0.14a

    0.10a

    0.03a

    0.19a

    0.06a

    0.02a

    0.05a

    0.01a

    0.07a

    0.01a

    0.06a

    0.01a

    0.08a

    0.01a

    1.49a

    BC

    1.32a

    0.56a

    0.41a

    0.11a

    0.62a

    0.19a

    0.07a

    0.16a

    0.02a

    0.13a

    0.03a

    0.12a

    0.02a

    0.16a

    0.02b

    3.99a

    Data are average (n=3), and different lowercase letters in the same part of rice show significant difference among different treatments (P<0.05).

Copyright 2020  CHINA SCIENCE PUBLISHING & MEDIA LTD.  中国科技出版传媒股份有限公司  版权所有

京ICP备14028887号-23       京公网安备11010102003388号