5.9
CiteScore
5.9
Impact Factor
Volume 43 Issue 11
Nov.  2016
Turn off MathJax
Article Contents

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

doi: 10.1016/j.jgg.2016.11.002
More Information
  • 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
  • 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.
  • These authors contributed equally to this work.
  • loading
  • [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
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (72) PDF downloads (1) Cited by ()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return