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Journal of Integrative Agriculture  2013, Vol. 12 Issue (6): 1098-1111    DOI: 10.1016/S2095-3119(13)60329-9
Soil & Fertilization · Irrigation · Agro-Ecology & Environment Advanced Online Publication | Current Issue | Archive | Adv Search |
Genetic Improvement of Root Growth Contributes to Efficient Phosphorus Acquisition in maize (Zea mays L.)
 ZHANG Yi-kai, CHEN Fan-jun, CHEN Xiao-chao, LONG Li-zhi, GAO Kun, YUAN Li-xing, ZHANG Fu-suo, MI Guo-hua
Key Laboratory of Plant-Soil Interactions, Ministry of Education/Center for Resources, Environment and Food Security, College of Resources and Environmental Science, China Agricultural University, Beijing 100193, P.R.China
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摘要  Maize plants adapt to low phosphorus (P) stress by increasing root growth. It is of importance to know the extent to which genetic improvement of root growth can enhance P acquisiton. In the present study, the contribution of root growth improvement to efficient P acquisition was evaluated in two soils using T149 and T222, a pair of near isogenic maize testcrosses which were derived from a backcross BC4F3 population. T149 and T222 showed no difference in shoot biomass and leaf area under normal growth conditions, but differed greatly in root growth. T149 had longer lateral roots and a larger root surface area compared to T222. In calcareous soil, when P was insufficient, i.e., when P was either supplied as KH2PO4 at a concentration of 50 mg P kg-1 soil, or in the form of Phy-P, Ca3-P or Ca10-P, a 43% increase in root length in T149 compared to T222 resulted in an increase in P uptake by 53%, and shoot biomass by 48%. In acid soil, however, when P supply was insufficient, i.e., when P was supplied as KH2PO4 at a concentration of 100 mg P kg-1 soil, or in the form of Phy-P, Fe-P or Al-P, a 32% increase in root length in T149 compared to T222 resulted in an increase in P uptake by only 12%, and shoot biomass by 7%. No significant differences in the exudation of organic acids and APase activity were found between the two genotypes. It is concluded that genetic improvement of root growth can efficiently increase P acquisition in calcareous soils. In acid soils, however, improvements in the physiological traits of roots, in addition to their size, seem to be required for efficient P acquisition.

Abstract  Maize plants adapt to low phosphorus (P) stress by increasing root growth. It is of importance to know the extent to which genetic improvement of root growth can enhance P acquisiton. In the present study, the contribution of root growth improvement to efficient P acquisition was evaluated in two soils using T149 and T222, a pair of near isogenic maize testcrosses which were derived from a backcross BC4F3 population. T149 and T222 showed no difference in shoot biomass and leaf area under normal growth conditions, but differed greatly in root growth. T149 had longer lateral roots and a larger root surface area compared to T222. In calcareous soil, when P was insufficient, i.e., when P was either supplied as KH2PO4 at a concentration of 50 mg P kg-1 soil, or in the form of Phy-P, Ca3-P or Ca10-P, a 43% increase in root length in T149 compared to T222 resulted in an increase in P uptake by 53%, and shoot biomass by 48%. In acid soil, however, when P supply was insufficient, i.e., when P was supplied as KH2PO4 at a concentration of 100 mg P kg-1 soil, or in the form of Phy-P, Fe-P or Al-P, a 32% increase in root length in T149 compared to T222 resulted in an increase in P uptake by only 12%, and shoot biomass by 7%. No significant differences in the exudation of organic acids and APase activity were found between the two genotypes. It is concluded that genetic improvement of root growth can efficiently increase P acquisition in calcareous soils. In acid soils, however, improvements in the physiological traits of roots, in addition to their size, seem to be required for efficient P acquisition.
Keywords:  P efficiency       roots       low phosphorus       calcareous soil       acid soil       maize  
Received: 30 July 2012   Accepted:
Fund: 

This work was supported by the National Natural Science Foundation of China (31121062 and 31071852), EU Seventh Framework Programme of European Union (NUECROPS, 222645), and the Special Fund for the Agricultural Profession of China (201103003).

Corresponding Authors:  Correspondence MI Guo-hua, Tel: +86-10-62734454, Fax: +86-10-62731016, E-mail: miguohua@cau.edu.cn     E-mail:  miguohua@cau.edu.cn
About author:  ZHANG Yi-kai, Mobile: 13732279586, E-mail: yikaizhang168@163.com

Cite this article: 

ZHANG Yi-kai, CHEN Fan-jun, CHEN Xiao-chao, LONG Li-zhi, GAO Kun, YUAN Li-xing, ZHANG Fu-suo, MI Guo-hua. 2013. Genetic Improvement of Root Growth Contributes to Efficient Phosphorus Acquisition in maize (Zea mays L.). Journal of Integrative Agriculture, 12(6): 1098-1111.

[1]Anderson G, Williams E G, Moir J O. 1974. A comparison ofthe sorption of inorganic orthophosphate and inositolhexaphosphate by six acid soils. European Journal ofSoil Science, 25, 51-62

[2]Ao J H, Fu J B, Tian J, Yan X L, Liao H. 2010. Geneticvariability for root morph-architecture traits and rootgrowth dynamics as related to phosphorus efficiencyin soybean. Functional Plant Biology, 37, 304-312

[3]Bayuelo-Jimenez J S, Gallardo-Valdez M, Perez-Decelis VA, Magdaleno-Armas L, Ochoa I, Lynch J P. 2011.Genotypic variation for root traits of maize (Zea maysL.) from the Purhepecha Plateau under contrastingphosphorus availability. Field Crops Research, 121,350-362

[4]Betencourt E, Duputel M, Colomb B, Desclaux D, HinsingerP. 2011. Intercropping promotes the ability of durumwheat and chickpea to increase rhizosphere phosphorusavailability in a low P soil. Soil Biology andBiochemistry, 46, 181-190

[5]Bloom A J, Meyerhoff P A, Taylor A R, Rost T L. 2002. Rootdevelopment and absorption of ammonium and nitratefrom the rhizosphere. Journal of Plant GrowthRegulation, 21, 416-431

[6]Calderon-Vazquez C, Alatorre-Cobos F, Simpson-Williamson J, Herrera-Estrella L. 2009. Maize underphosphate limitation. In: Handbook of Maize: ItsBiology. Springer Online, New York. pp. 381-404

[7]Clark R B. 1983. Plant genotype differences in the uptake,translocation, accumulation, and use of mineralelements required for plant growth. Plant and Soil, 72,175-196

[8]Cordell D, Drangert J O, White S. 2009. The story ofphosphorus: global food security and food for thought.Global Environmental Change, 19, 292-305

[9]Corrales I, Amenós M, Poschenrieder C, Barceló J. 2007.Phosphorus efficiency and root exudates in twocontrasting tropical maize varieties. Journal of PlantNutrition, 30, 887-900

[10]Devau N, Hinsinger P, le Cadre E, Gérard F. 2011. Rootinducedprocesses controlling phosphate availabilityin soils with contrasted P-fertilized treatments. Plantand Soil, 348, 1-16

[11]Duff S M G, Sarath G, Plaxton W C. 1994. The role of acidphosphatases in plant phosphorus metabolism.Physiologia Plantarum, 90, 791-800

[12]Gahoonia T S, Nielsen N E, Joshi P A, Jahoor A. 2001. Aroot hairless barley mutant for elucidating genetic ofroot hairs and phosphorus uptake. Plant and Soil, 235,211-219

[13]Gaume A, Machler F, de Leon C, Narro L, Frossard E. 2001.Low-P tolerance by maize (Zea mays L.) genotypes:Significance of root growth, and organic acids and acidphosphatase root exudation. Plant and Soil, 228, 253-264

[14]Gewin V. 2010. An underground revolution. Nature, 466,29.Hajabbasi M A, Schumacher T E. 1994. Phosphorus effectson root growth and development in two maizegenotypes. Plant and Soil, 158, 39-46

[15]Hao L F, Zhang J L, Christie P, Li X L. 2008. Response oftwo maize inbred lines with contrasting phosphorusefficiency and root morphology to mycorrhizalcolonization at different soil phosphorus supply levels.Journal of Plant Nutrition, 31, 1059-1073

[16]Hayes J E, Richardson A E, Simpson R J. 1999. Phytase andacid phosphatase activities in extracts from roots oftemperate pasture grass and legume seedlings.Australian Journal of Plant Physiology, 26, 801-809

[17]Haynes R J. 1982. Effects of liming on phosphate availabilityin acid soils. a critical review. Plant and Soil, 68, 289-308

[18]Hermans C, Hammond J P, White P J, Verbruggen N. 2006.How do plants respond to nutrient shortage by biomassallocation? Trends in Plant Science, 11, 610-617

[19]Hinsinger P. 2001. Bioavailability of soil inorganic P in therhizosphere as affected by root-induced chemicalchanges: a review. Plant and Soil, 237, 173-195

[20]Kochian L V, Hoekenga O A, Piñeros M A. 2004. How docrop plants tolerate acid soils? Mechanisms ofaluminum tolerance and phosphorous efficiency.Annual Review of Plant Biology, 55, 459-493

[21]Lambers H, Shane M W, Cramer M D, Pearse S J, VeneklaasE J. 2006. Root structure and functioning for efficientacquisition of phosphorus: matching morphologicaland physiological traits. Annals of Botany, 98, 693-713

[22]Li H G, Shen J B, Zhang F S, Marschner P, Cawthray G Z R.2010. Phosphorus uptake and rhizosphere propertiesof intercropped and monocropped maize, faba bean,and white lupin in acidic soil. Biology and Fertility ofSoils, 46, 79-91

[23]Li K P, Xu Z P, Zhang K W, Yang A F, Zhang J R. 2007.Efficient production and characterization for maizeinbred lines with low-phosphorus tolerance. PlantScience, 172, 255-264

[24]Li M, Guo X G, Zhang M, Wang X P, Zhang G D, Tian Y C,Wang Z L. 2010. Mapping QTLs for grain yield andyield components under high and low phosphorustreatments in maize (Zea mays L.). Plant Science, 178,454-462

[25]Liu H, Trieu A T, Blaylock L A, Harrison M J. 1998. Cloningand characterization of two phosphate transporters fromMedicago truncatula roots: Regulation in response tophospate and to colonization by arbuscular mycorrhizal(AM) fungi. Molecular Plant-Microbe Interactions,11, 14-22

[26]Liu J C, Cai H G, Chu Q, Chen X H, Chen F J, Yuan L X, MiG H, Zhang F S. 2011. Genetic analysis of vertical rootpulling resistance (VRPR) in maize using two geneticpopulations. Molecular Breeding, 28, 463-474

[27]Liu Y, Mi G H, Chen F J, Zhang J H, Zhang F S. 2004.Rhizosphere effect and root growth of two maize (Zeamays L.) genotypes with contrasting P efficiency atlow P availability. Plant Science, 167, 217-223

[28]Lynch J P, Brown K M. 2008. Root strategies for phosphorusacquisition. In White P, Hammond J, eds., TheEcophysiology of Plant-Phosphorus Interactions.Springer Science, Dordrecht, the Netherlands. pp. 83-116

[29]Lynch J P. 2007. Roots of the second green revolution.Australian Journal of Botany, 55, 493-512

[30]Lynch J P. 2011. Root phenes for enhanced soil explorationand phosphorus acquisition: tools for future crops.Plant Physiology, 156, 1041-1049

[31]Ma Z, Lynch J P, Bielenberg D G, Brown K M. 2001.Regulation of root hair density by phosphorusavailability in arabidopsis thaliana. Plant Cell andEnvironment, 24, 459-467

[32]Marschner H. 1995. Rhizosphere pH effects on phosphorusnutrition. In: Genetic Manipulation of Crop Plants toEnhance Integrated Nutrient Management inCropping Systems-1 Phosphorus: Proceedings of anFAO/ICRISAT Expert Consultancy Worshop, ICRISATAsia Center, India. pp. 107-115

[33]Murphy J, Riley J P. 1962. A modified single solution methodfor the determination of phosphate in natural waters. Analytical Chemica Acta, 27, 31-36

[34]Nagarajah S, Posner A M, Quirk J P. 1970. Competitiveadsorption of phosphate with polygalacturonate andother organic anions on kaolinite and oxide surfaces.Nature, 228, 83-85

[35]Neumann G, Massonneau A, Martinoia E, Römheld V. 1999.Physiological adaptations to phosphorus deficiencyduring proteoid root development in white lupin.Planta, 208, 373-382

[36]Neumann G, Römheld V. 1999. Root excretion of carboxylicacids and protons in phosphorus-deficient plants. Plantand Soil, 211, 121-130

[37]Postma J A, Lynch J P. 2010. Theoretical evidence for thefunctional benefit of root cortical aerenchyma in soilswith low phosphorus availability. Annals of Botany,107, 829-841

[38]Raghothama K G. 1999. Phosphorus acquisition. AnnualReview of Plant Physiology and Plant MolecularBiology, 50, 665-693

[39]Ramaekers L, Remans R, Rao I M, Blair M W, VanderleydenJ. 2010. Strategies for improving phosphorus acquisitionefficiency of crop plants. Field Crops Research, 117,169-176

[40]Richardson A E. 2009. Regulating the phosphorus nutritionof plants: molecular biology meeting agronomic needs.Plant and Soil, 322, 17-24

[41]Sanderson J B, Daynard T B, Tollenaar M. 1981. Amathematical model of the shape of corn leaves.Canadian Journal of Plant Science, 61, 1009-1011

[42]Schweiger P F, Robson A D, Barrow N J, Abbott L K. 2007.Arbuscular mycorrhizal fungi from three genera inducetwo-phase plant growth responses on a high P-fixingsoil. Plant and Soil, 292, 181-192

[43]Shen H, Yan X. 2001. Exudation and accumulation of organicacids by the roots of common bean (Phaseolus vulgarisL.) in response to low phosphorus and aluminumtoxicity stress. Acta Ecologica Sinica, 21, 1892-1898

[44](in Chinese).Shen J B, Li H G, Neumann G, Zhang F S. 2005. Nutrientuptake, cluster root formation and exudation of protonsand citrate in Lupinus albus as affected by localizedsupply of phosphorus in a split-root system. PlantScience, 168, 837-845

[45]Silva A E D, Gabelman W H. 1992. Screening maize inbredlines for tolerance to low-P stress condition. Plant andSoil, 146, 181-187

[46]Tang C, Qiao Y F, Han X Z, Zheng S J. 2007. Genotypicvariation in phosphorus utilisation of soybean Glycinemax (L.) Murr. grown in various sparingly soluble Psources. Australian Journal of Agricultural Research,58, 443-451

[47]Tian Q Y, Chen F J, Zhang F S, Mi G H. 2006. Genotypicdifference in nitrogen acquisition ability in maize plantsis related to the coordination of leaf and root growth.Journal of Plant Nutrition, 29, 317-330

[48]Tuberosa R, Salvi S, Sanguineti M C, Landi P, MacCaferriM, Conti S. 2002. Mapping QTLs regulating morphophysiologicaltraits and yield: case studies,shortcomings and perspectives in drought-stressedmaize. Annals of Botany, 89, 941-963

[49]Wang Y, Mi G H, Chen F J, Zhang J H, Zhang F S. 2004.Response of root morphology to nitrate supply and itscontribution to nitrogen accumulation in maize. Journalof Plant Nutrition, 27, 2189-2202

[50]Wang Z Y, Xiao K, Katagi H, Harrison M. 2006. Improvedphosphorus acquisition and biomass production inArabidopsis by transgenic expression of a purple acidphosphatase gene from M. truncatula. Plant Science,170, 191-202

[51]Wissuwa M. 2003. How do plants achieve tolerance tophosphorus deficiency? Small causes with big effects.Plant Physiology, 133, 1947-1958

[52]Zhu J, Kaeppler S M, Lynch J P. 2005. Mapping of QTL forlateral root branching and length in maize (Zea mays L.)under differential phosphorus supply. Theoretical andApplied Genetics, 111, 688-695

[53]Zhu J, Lynch J P. 2004. The contribution of lateral rootingto phosphorus acquisition efficiency in maize (Zeamays) seedlings. Functional Plant Biology, 31, 949-958.
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