Enhancing phosphorus uptake efficiency through QTL-based selection for root system architecture in maize

Riliang Gu; Fanjun Chen; Lizhi Long; Hongguang Cai; Zhigang Liu; Jiabo Yang; Lifeng Wang; Huiyong Li; Junhui Li; Wenxin Liu; Guohua Mi; Fusuo Zhang; Lixing Yuan

doi:10.1016/j.jgg.2016.11.002

Volume 43 Issue 11

Nov. 2016

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Article Navigation > Journal of Genetics and Genomics > 2016 > 43(11): 663-672

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Enhancing phosphorus uptake efficiency through QTL-based selection for root system architecture in maize

doi: 10.1016/j.jgg.2016.11.002

a
Key Lab of Plant-Soil Interaction, MOE, Center for Resources, Environment and Food Security, College Resources and Environmental Sciences, China Agricultural University, Beijing 100193, China
b
College of Agronomy and Biotechnology, China Agricultural University, Beijing 100193, China
c
Institute of Agricultural Resource and Environment, Jilin Academy of Agricultural Sciences, Changchun 130033, China
d
Cereal Crops Research Institute, Henan Academy of Agricultural Sciences, Zhengzhou 450002, China

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Corresponding author: E-mail address: yuanlixing@cau.edu.cn (Lixing Yuan)
Received Date: 2016-05-19
Accepted Date: 2016-11-06
Rev Recd Date: 2016-09-09

Available Online: 2016-11-09

Publish Date: 2016-11-20

Abstract

Abstract

Root system architecture (RSA) plays an important role in phosphorus (P) acquisition, but enhancing P use efficiency (PUE) in maize via genetic manipulation of RSA has not yet been reported. Here, using a maize recombinant inbred line (RIL) population, we investigated the genetic relationships between PUE and RSA, and developed P-efficient lines by selection of quantitative trait loci (QTLs) that coincide for both traits. In low-P (LP) fields, P uptake efficiency (PupE) was more closely correlated with PUE (r = 0.48–0.54), and RSA in hydroponics was significantly related to PupE (r = 0.25–0.30) but not to P utilization efficiency (PutE). QTL analysis detected a chromosome region where two QTLs for PUE, three for PupE and three for RSA were assigned into two QTL clusters, Cl-bin3.04a and Cl-bin3.04b. These QTLs had favorable effects from alleles derived from the large-rooted and high-PupE parent. Marker-assisted selection (MAS) identified nine advanced backcross-derived lines carrying Cl-bin3.04a or Cl-bin3.04b that displayed mean increases of 22%–26% in PUE in LP fields. Furthermore, a line L224 pyramiding Cl-bin3.04a and Cl-bin3.04b showed enhanced PupE, relying mainly on changes in root morphology, rather than root physiology, under both hydroponic and field conditions. These results highlight the physiological and genetic contributions of RSA to maize PupE, and provide a successful study case of developing P-efficient crops through QTL-based selection.
- Maize,
- Quantitative trait loci,
- Phosphorus,
- Root system architecture,
- Marker-assisted selection

These authors contributed equally to this work.

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References(66)

References

[1]	Ai, P.H., Sun, S.B., Zhao, J.N. et al. Two rice phosphate transporters, OsPht1;2 and OsPht1;6, have different functions and kinetic properties in uptake and translocation Plant J., 57 (2009),pp. 798-809
[2]	Azevedo, G.C., Cheavegatti-Gianotto, A., Negri, B.F. et al. BMC Plant Biol., 15 (2015),pp. 172-188
[3]	Bremner, J.M.
[4]	Cai, H., Chen, F., Mi, G. et al. Theor. Appl. Genet., 125 (2012),pp. 1313-1324
[5]	Cakmak, I. Plant nutrition research: priorities to meet human needs for food in sustainable ways Plant Soil, 247 (2002),pp. 3-24
[6]	Calderon-Vazquez, C., Ibarra-Laclette, E., Caballero-Perez, J. et al. J. Exp. Bot., 59 (2008),pp. 2479-2497
[7]	Chen, J., Xu, L., Cai, Y. et al. Plant Soil, 313 (2008),pp. 251-266
[8]	Chen, J., Xu, L., Cai, Y. et al. Euphytica, 167 (2009),pp. 245-252
[9]	Chen, J., Cai, Y., Xu, L. et al. Front. Agric. China, 5 (2011),pp. 152-161
[10]	Chin, J.H., Lu, X., Haefele, S.M. et al. Theor. Appl. Genet., 120 (2010),pp. 1073-1086
[11]	Cordell, D., Drangert, J.O., White, S. The story of phosphorus: global food security and food for thought Glob. Environ. Change, 19 (2009),pp. 292-305
[12]	Corrales, I., Amenos, M., Poschenrieder, C. et al. Phosphorus efficiency and root exudates in two contrasting tropical maize varieties J. Plant Nutr., 30 (2007),pp. 887-900
[13]	Dodds, W.K., Bouska, W.W., Eitzmann, J.L. et al. Eutrophication of U.S. freshwaters: analysis of potential economic damages Environ. Sci. Technol., 43 (2009),pp. 12-19
[14]	Gamuyao, R., Chin, J.H., Pariasca-Tanaka, J. et al. The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency Nature, 488 (2012),pp. 535-539
[15]	Gaume, A., Machler, F., De Leon, C. et al. Plant Soil, 228 (2001),pp. 253-264
[16]	Gu, R., Duan, F., An, Xia, Zhang, F. et al. Plant Cell Physiol., 54 (2013),pp. 1515-1524
[17]	Hermans, C., Hammond, J.P., White, P.J. et al. How do plants respond to nutrient shortage by biomass allocation? Trends Plant Sci., 11 (2006),pp. 610-617
[18]	Hochholdinger, F., Zimmermann, R. Conserved and diverse mechanisms in root development Curr. Opin. Plant Biol., 11 (2008),pp. 70-74
[19]	Hufnagel, B., De Sousa, S.M., Assis, L. et al. Plant Physiol., 166 (2014),pp. 659-677
[20]	Lambers, H., Raven, J.A., Shaver, G.R. et al. Plant nutrient-acquisition strategies change with soil age Trends Ecol. Evol., 23 (2008),pp. 95-103
[21]	Li, M., Guo, X., Zhang, M. et al. Plant Sci., 178 (2010),pp. 454-462
[22]	Liu, Y., Mi, G.H., Chen, F.J. et al. Plant Sci., 167 (2004),pp. 217-223
[23]	Liu, J., Li, J., Chen, F. et al. Plant Soil, 305 (2008),pp. 253-265
[24]	Liu, J., Chen, F., Olokhnuud, C. et al. J. Plant Nutr. Soil Sci., 172 (2009),pp. 230-236
[25]	Liu, J., Cai, H., Chu, Q. et al. Genetic analysis of vertical root pulling resistance (VRPR) in maize using two genetic populations Mol. Breed., 28 (2011),pp. 463-474
[26]	Liu, H., White, P., Li, C.J. Biomass partitioning and rhizosphere responses of maize and faba bean to phosphorus deficiency Crop Pasture Sci., 67 (2016),pp. 847-856
[27]	Lynch, J. The role of nutrient-efficient crops in modern agriculture J. Crop Prod., 1 (1998),pp. 241-264
[28]	Lynch, J.P., Brown, K.M. Topsoil foraging an architectural adaptation of plants to low phosphorus availability Plant Soil, 237 (2001),pp. 225-237
[29]	Ma, Q., Rengel, Z., Rose, T. The effectiveness of deep placement of fertilisers is determined by crop species and edaphic conditions in mediterranean-type environments: a review Aust. J. Soil Res., 47 (2009),pp. 19-32
[30]	Manske, G.G.B., Ortiz-Monasterio, J.I., Van Ginkel, M. et al. Eur. J. Agron., 14 (2001),pp. 261-274
[31]	Marschner, H.
[32]	Mendes, F.F., Guimaraes, L.J.M., Souza, J.C. et al. Genetic architecture of phosphorus use efficiency in tropical maize cultivated in a low-P soil Crop Sci., 54 (2014),pp. 1530-1538
[33]	Miao, J., Sun, J.H., Liu, D.C. et al. Characterization of the promoter of phosphate transporter TaPHT1.2 differentially expressed in wheat varieties J. Genet. Genomics, 36 (2009),pp. 455-466
[34]	Miguel, M.A., Postma, J.A., Lynch, J.P. Phene synergism between root hair length and basal root growth angle for phosphorus acquisition Plant Physiol., 167 (2015),pp. 1430-1439
[35]	Mitsukawa, N., Okumura, S., Shirano, Y. et al. Proc. Natl. Acad. Sci. U.S.A., 94 (1997),pp. 7098-7102
[36]	Moll, R.H., Kamprath, E.J., Jackson, W.A. Analysis and interpretation of factors which contribute to efficiency of nitrogen-utilization Agron. J., 74 (1982),pp. 562-564
[37]	Murphy, J., Riley, J.P. A modified single solution method for the determination of phosphate in natural waters Anal. Chim. Acta, 27 (1962),pp. 31-36
[38]	Nagy, R., Vasconcelos, M.J.V., Zhao, S. et al. Plant Biol., 8 (2006),pp. 186-197
[39]	Nyquist, W.E. Estimation of heritability and prediction of selection response in plant-populations Crit. Rev. Plant Sci., 10 (1991),pp. 235-322
[40]	Olsen, S.R., Cole, C.V., Watanabe, F.S. et al. Estimation of available phosphorus in soils by extraction with sodium bicarbonate U.S. Dept. Agric. Circ. 939 (1954),pp. 1-19
[41]	Parentoni, S.N., De Souza Junior, C.L. Phosphorus acquisition and internal utilization efficiency in tropical maize genotypes Pesqui. Agropecu. Bras., 43 (2008),pp. 893-901
[42]	Parentoni, S.N., , De Carvalho Alves, V.M., Gama, E.E.G. et al. Maydica, 55 (2010),pp. 1-15
[43]	Pariasca-Tanaka, J., Chin, J.H., Drame, K.N. et al. Theor. Appl. Genet., 127 (2014),pp. 1387-1398
[44]	Postma, J.A., Dathe, A., Lynch, J.P. The optimal lateral root branching density for maize depends on nitrogen and phosphorus availability Plant Physiol., 166 (2014),pp. 590-602
[45]	Qin, L., Guo, Y.X., Chen, L.Y. et al. PLoS One, 7 (2012),p. e47726
[46]	Raghothama, K. Phosphate acquisition Annu. Rev. Plant Physiol. Plant Mol. Biol., 50 (1999),pp. 665-693
[47]	Rose, T.J., Impa, S.M., Rose, M.T. et al. Enhancing phosphorus and zinc acquisition efficiency in rice: a critical review of root traits and their potential utility in rice breeding Ann. Bot., 112 (2013),pp. 331-345
[48]	Shen, H., Chen, J.H., Wang, Z.Y. et al. J. Exp. Bot., 57 (2006),pp. 1353-1362
[49]	Shen, J., Yuan, L., Zhang, J. et al. Phosphorus dynamics: from soil to plant Plant Physiol., 156 (2011),pp. 997-1005
[50]	Shenoy, V.V., Kalagudi, G.M. Enhancing plant phosphorus use efficiency for sustainable cropping Biotechnol. Adv., 23 (2005),pp. 501-513
[51]	Shin, H., Shin, H., Dewbre, G.R. et al. Plant J., 39 (2004),pp. 629-642
[52]	De Sousa, S.M., Clark, R.T., Mendes, F.F. et al. A role for root morphology and related candidate genes in P acquisition efficiency in maize Funct. Plant Biol., 39 (2012),pp. 925-935
[53]	Usuda, H., Shimogawara, K. Phosphate deficiency in maize.I. leaf phosphate status, growth, photosynthesis and carbon partitioning Plant Cell Physiol., 32 (1991),pp. 497-504
[54]	Vance, C.P., Uhde-Stone, C., Allan, D.L. Phosphorus acquisition and use: critical adaptations by plants for securing a nonrenewable resource New Phytol., 157 (2003),pp. 423-447
[55]	Veneklaas, E.J., Lambers, H., Bragg, J. et al. Opportunities for improving phosphorus-use efficiency in crop plants New Phytol., 195 (2012),pp. 306-320
[56]	Walkley, A. A critical examination of a rapid method for determining organic carbon in soils: effect of variations in digestion conditions and of inorganic soil constituents Soil Sci., 63 (1947),pp. 251-264
[57]	Wang, L.D., Liao, H., Yan, X.L. et al. Genetic variability for root hair traits as related to phosphorus status in soybean Plant Soil, 261 (2004),pp. 77-84
[58]	Wang, X., Shen, J., Liao, H. Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops? Plant Sci., 179 (2010),pp. 302-306
[59]	Wang, X., Yan, X., Liao, H. Genetic improvement for phosphorus efficiency in soybean: a radical approach Ann. Bot., 106 (2010),pp. 215-222
[60]	Wang, S., Basten, C., Zeng, Z.
[61]	White, P.J., George, T.S., Gregory, P.J. et al. Matching roots to their environment Ann. Bot., 112 (2013),pp. 207-222
[62]	Wissuwa, M. How do plants achieve tolerance to phosphorus deficiency? Small causes with big effects Plant Physiol., 133 (2003),pp. 1947-1958
[63]	Wissuwa, M. Combining a modelling with a genetic approach in establishing associations between genetic and physiological effects in relation to phosphorus uptake Plant Soil, 269 (2005),pp. 57-68
[64]	Zhang, H., Uddin, M.S., Zou, C. et al. Meta-analysis and candidate gene mining of low-phosphorus tolerance in maize J. Integr. Plant Biol., 56 (2014),pp. 262-270
[65]	Zhao, J., Fu, J.B., Liao, H. et al. Characterization of root architecture in an applied core collection for phosphorus efficiency of soybean germplasm Chin. Sci. Bull., 49 (2004),pp. 1611-1620
[66]	Zhu, J.M., Lynch, J.P. Funct. Plant Biol., 31 (2004),pp. 949-958

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Periodical cited type(48)

1.	Sun, H., Liang, H., Shao, C. et al. Effect of Phosphate-Deficiency Stress on the Biological Characteristics and Transcriptomics of Panax ginseng. Horticulturae, 2024, 10(5): 506. doi:10.3390/horticulturae10050506
2.	Shin, N.-H., Cho, L.-H. Phosphate depletion: research status and challenges in agriculture \| [식물에서 인의 역할과 인산염 고갈 위기 대응 방안]. Journal of Plant Biotechnology, 2024, 51(1): 129-142. doi:10.5010/JPB.2024.51.014.129
3.	Schuster, A., Santana, A.S., Uberti, A. et al. Genetic diversity, relationships among traits and selection of tropical maize inbred lines for low-P tolerance based on root and shoot traits at seedling stage. Frontiers in Plant Science, 2024, 15: 1429901. doi:10.3389/fpls.2024.1429901
4.	Zeffa, D.M., Júnior, L.P., de Assis, R. et al. Multi-locus genome-wide association study for phosphorus use efficiency in a tropical maize germplasm. Frontiers in Plant Science, 2024, 15: 1366173. doi:10.3389/fpls.2024.1366173
5.	Vera-García, S.-L., Rodríguez-Casasola, F.-N., Barrera-Cortés, J. et al. Enhancing Phosphorus and Nitrogen Uptake in Maize Crops with Food Industry Biosolids and Azotobacter nigricans. Plants, 2023, 12(17): 3052. doi:10.3390/plants12173052
6.	Liu, Z., Li, P., Ren, W. et al. Hybrid performance evaluation and genome-wide association analysis of root system architecture in a maize association population. Theoretical and Applied Genetics, 2023, 136(9): 194. doi:10.1007/s00122-023-04442-7
7.	Li, X., Zhang, X., Zhao, Q. et al. Genetic improvement of legume roots for adaption to acid soils. Crop Journal, 2023, 11(4): 1022-1033. doi:10.1016/j.cj.2023.04.002
8.	He, K., Zhao, Z., Ren, W. et al. Mining genes regulating root system architecture in maize based on data integration analysis. Theoretical and Applied Genetics, 2023, 136(6): 127. doi:10.1007/s00122-023-04376-0
9.	Liang, L., An, T., Liu, S. et al. Assessing phosphorus efficiency and tolerance in maize genotypes with contrasting root systems at the early growth stage using the semi-hydroponic phenotyping system. Journal of Plant Nutrition and Soil Science, 2023, 186(3): 286-297. doi:10.1002/jpln.202200196
10.	Prathap, V., Kumar, S., Tyagi, A. Comparative proteome analysis of phosphorus-responsive genotypes reveals the proteins differentially expressed under phosphorous starvation stress in rice. International Journal of Biological Macromolecules, 2023, 234: 123760. doi:10.1016/j.ijbiomac.2023.123760
11.	Yi, H., Hu, S., Zhang, Y. et al. Proper Delay of Phosphorus Application Promotes Wheat Growth and Nutrient Uptake under Low Phosphorus Condition. Agriculture (Switzerland), 2023, 13(4): 884. doi:10.3390/agriculture13040884
12.	Zhao, Q., Ma, N., Li, R. et al. Seed Protein Genetics Linked with Nitrogen and Phosphorus Translocation Efficiency in Soybean. Agronomy, 2023, 13(2): 598. doi:10.3390/agronomy13020598
13.	Jin, Y., Wang, Y., Liu, J. et al. Genome-wide linkage mapping of root system architecture-related traits in common wheat (Triticum aestivum L.). Frontiers in Plant Science, 2023, 14: 1274392. doi:10.3389/fpls.2023.1274392
14.	Barbieri, P.A., Echeverría, H.E., Sainz Rozas, H.R. et al. Row spacing and phosphorus use efficiency in no-tillage maize. Journal of Plant Nutrition, 2023, 46(15): 3726-3736. doi:10.1080/01904167.2023.2211601
15.	Upadhyay, P., Gupta, M., Sra, S.K. et al. Genome wide association studies for acid phosphatase activity at varying phosphorous levels in Brassica juncea L. Frontiers in Plant Science, 2022, 13: 1056028. doi:10.3389/fpls.2022.1056028
16.	Giovannini, L., Sbrana, C., Giovannetti, M. et al. Diverse mycorrhizal maize inbred lines differentially modulate mycelial traits and the expression of plant and fungal phosphate transporters. Scientific Reports, 2022, 12(1): 21279. doi:10.1038/s41598-022-25834-7
17.	Kumar, K., Yadava, P., Gupta, M. et al. Narrowing down molecular targets for improving phosphorus-use efficiency in maize (Zea mays L.). Molecular Biology Reports, 2022, 49(12): 12091-12107. doi:10.1007/s11033-022-07679-5
18.	Liang, L., Liu, B., Huang, D. et al. Arbuscular Mycorrhizal Fungi Alleviate Low Phosphorus Stress in Maize Genotypes with Contrasting Root Systems. Plants, 2022, 11(22): 3105. doi:10.3390/plants11223105
19.	Ojeda-Rivera, J.O., Alejo-Jacuinde, G., Nájera-González, H.-R. et al. Prospects of genetics and breeding for low-phosphate tolerance: an integrated approach from soil to cell. Theoretical and Applied Genetics, 2022, 135(11): 4125-4150. doi:10.1007/s00122-022-04095-y
20.	Chien, P.-S., Chao, Y.-T., Chou, C.-H. et al. Phosphate transporter PHT1;1 is a key determinant of phosphorus acquisition in Arabidopsis natural accessions. Plant Physiology, 2022, 190(1): 682-697. doi:10.1093/plphys/kiac250
21.	Zhu, S., Luo, L., Zhang, X. et al. Study on the Relationship of Root Morphology and Phosphorus Absorption Efficiency With Phosphorus Uptake Capacity in 235 Peanut (Arachis hypogaea L.) Germplasms. Frontiers in Environmental Science, 2022, 10: 855815. doi:10.3389/fenvs.2022.855815
22.	Yang, M., Wang, C., Hassan, M.A. et al. QTL mapping of root traits in wheat under different phosphorus levels using hydroponic culture. BMC Genomics, 2021, 22(1): 174. doi:10.1186/s12864-021-07425-4
23.	Uddin, M.S., Azam, M.G., Billah, M. et al. High-throughput root network system analysis for low phosphorus tolerance in maize at seedling stage. Agronomy, 2021, 11(11): 2230. doi:10.3390/agronomy11112230
24.	Li, D., Wang, H., Wang, M. et al. Genetic dissection of phosphorus use efficiency in a maize association population under two p levels in the field. International Journal of Molecular Sciences, 2021, 22(17): 9311. doi:10.3390/ijms22179311
25.	Liu, D.. Root developmental responses to phosphorus nutrition. Journal of Integrative Plant Biology, 2021, 63(6): 1065-1090. doi:10.1111/jipb.13090
26.	Long, L., Kristensen, R.K., Guo, J. et al. Assessing the variation in traits for manganese deficiency tolerance among maize genotypes. Environmental and Experimental Botany, 2021, 183: 104344. doi:10.1016/j.envexpbot.2020.104344
27.	Li, D., Chen, Z., Wang, M. et al. Dissecting the phenotypic response of maize to low phosphorus soils by field screening of a large diversity panel. Euphytica, 2021, 217(1): 12. doi:10.1007/s10681-020-02727-2
28.	Dormatey, R., Sun, C., Ali, K. et al. Gene pyramiding for sustainable crop improvement against biotic and abiotic stresses. Agronomy, 2020, 10(9): 1255. doi:10.3390/agronomy10091255
29.	Zhang, T., He, X., Deng, Y. et al. Swine manure valorization for phosphorus and nitrogen recovery by catalytic–thermal hydrolysis and struvite crystallization. Science of the Total Environment, 2020, 729: 138999. doi:10.1016/j.scitotenv.2020.138999
30.	Li, C.. Breeding crops by design for future agriculture. Journal of Zhejiang University: Science B, 2020, 21(6): 423-425. doi:10.1631/jzus.B2010001
31.	Zhang, T., He, X., Deng, Y. et al. Phosphorus recovered from digestate by hydrothermal processes with struvite crystallization and its potential as a fertilizer. Science of the Total Environment, 2020, 698: 134240. doi:10.1016/j.scitotenv.2019.134240
32.	Shen, J., Wang, L., Jiao, X. et al. Innovations of phosphorus sustainability: Implications for the whole chain. Frontiers of Agricultural Science and Engineering, 2019, 6(4): 321-331. doi:10.15302/J-FASE-2019283
33.	Li, D., Wang, M., Kuang, X. et al. Genetic study and molecular breeding for high phosphorus use efficiency in maize. Frontiers of Agricultural Science and Engineering, 2019, 6(4): 366-379. doi:10.15302/J-FASE-2019278
34.	Ludewig, U., Yuan, L., Neumann, G. Improving the efficiency and effectiveness of global phosphorus use: Focus on root and rhizosphere levels in the agronomic system. Frontiers of Agricultural Science and Engineering, 2019, 6(4): 357-365. doi:10.15302/J-FASE-2019275
35.	Fu, Y., Zhong, X., Pan, J. et al. QTLs identification for nitrogen and phosphorus uptake-related traits using ultra-high density SNP linkage. Plant Science, 2019, 288: 110209. doi:10.1016/j.plantsci.2019.110209
36.	Wang, H., Wei, J., Li, P. et al. Integrating GWAS and gene expression analysis identifies candidate genes for root morphology traits in Maize at the seedling stage. Genes, 2019, 10(10): 773. doi:10.3390/genes10100773
37.	Yang, Y., Tong, Y., Li, X. et al. Genetic analysis and fine mapping of phosphorus efficiency locus 1 (PE1) in soybean. Theoretical and Applied Genetics, 2019, 132(10): 2847-2858. doi:10.1007/s00122-019-03392-3
38.	Long, L., Ma, X., Ye, L. et al. Root plasticity and Pi recycling within plants contribute to low-P tolerance in Tibetan wild barley. BMC Plant Biology, 2019, 19(1): 341. doi:10.1186/s12870-019-1949-x
39.	Wang, J., Kuang, L., Wang, X. et al. Temporal genetic patterns of root growth in Brassica napus L. revealed by a low-cost, high-efficiency hydroponic system. Theoretical and Applied Genetics, 2019, 132(8): 2309-2323. doi:10.1007/s00122-019-03356-7
40.	Wang, W., Ding, G.-D., White, P.J. et al. Mapping and cloning of quantitative trait loci for phosphorus efficiency in crops: opportunities and challenges. Plant and Soil, 2019, 439(1-2): 91-112. doi:10.1007/s11104-018-3706-6
41.	Dun, X., Shi, J., Liu, H. et al. Genetic dissection of root morphological traits as related to potassium use efficiency in rapeseed under two contrasting potassium levels by hydroponics. Science China Life Sciences, 2019, 62(6): 746-757. doi:10.1007/s11427-018-9503-x
42.	Schegoscheski Gerhardt, I.F., do Amaral Junior, A.T., Ferreira Pena, G. et al. Genetic effects on the efficiency and responsiveness to phosphorus use in popcorn as estimated by diallel analysis. PLoS ONE, 2019, 14(5): e0216980. doi:10.1371/journal.pone.0216980
43.	Li, P., Pan, T., Wang, H. et al. Natural variation of ZmHKT1 affects root morphology in maize at the seedling stage. Planta, 2019, 249(3): 879-889. doi:10.1007/s00425-018-3043-2
44.	Xu, C., Zhang, H., Sun, J. et al. Genome-wide association study dissects yield components associated with low-phosphorus stress tolerance in maize. Theoretical and Applied Genetics, 2018, 131(8): 1699-1714. doi:10.1007/s00122-018-3108-4
45.	Guo, J., Chen, G., Zhang, X. et al. Quantitative trait locus analysis of adventitious and lateral root morphology of barley grown at low and high P. Functional Plant Biology, 2018, 45(9): 957-967. doi:10.1071/FP17271
46.	Liu, Z., Liu, X., Craft, E.J. et al. Physiological and genetic analysis for maize root characters and yield in response to low phosphorus stress. Breeding Science, 2018, 68(2): 268-277. doi:10.1270/jsbbs.17083
47.	Wang, J., Dun, X., Shi, J. et al. Genetic dissection of root morphological traits related to nitrogen use efficiency in brassica napus L. Under two contrasting nitrogen conditions. Frontiers in Plant Science, 2017, 8: 1709. doi:10.3389/fpls.2017.01709
48.	Liu, Z., Gao, K., Shan, S. et al. Comparative analysis of root traits and the associated QTLs for maize seedlings grown in paper roll, hydroponics and vermiculite culture system. Frontiers in Plant Science, 2017, 8: 436. doi:10.3389/fpls.2017.00436