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Mapping and cloning of quantitative trait loci for phosphorus efficiency in crops: opportunities and challenges

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ABSTRACT

Background

Phosphorus (P) is an essential mineral element required in large quantities by plants. Globally, the availability of P in many soils is poor. Breeding crops that can acquire and utilise this limited resource with high efficiency is an important goal for agricultural sustainability in the future. The mapping and cloning of quantitative trait loci (QTLs) provides an effective tool in analyzing the genetic mechanisms underlying P efficiency and breeding P-efficient varieties.

Scope

This paper describes the QTL mapping of traits related to P efficiency which impact on shoot biomass or yield of crops in the past 20 years. It summarises the progress of studies on crop P-efficiency related QTLs and discusses the challenges for the cloning of QTLs. It proposes a scheme to develop crop genotypes with improved P efficiency. It also describes emerging methods, such as QTL-seq, genome-wide association analysis, and RNA-seq, that aid the rapid identification of P-efficiency related genes in crops.

Conclusion

Traits conferring P efficiency are heritable. Thus, it is feasible to incorporate phenotyping and selection for P efficiency in crop breeding programs. Identification of QTLs for target traits is a key step to enhancing the P efficiency of crops. Numerous QTLs have been identified that affect P efficiency in key crops, but few causal genes have been identified and breeding P-efficient crop varieties using marker-assisted selection (MAS) has not progressed far. The challenge now is to identify the specific genes controlling P-efficiency related traits. The availability of complete genome sequences for more crops, and the combination of conventional linkage mapping, association mapping, QTL-seq, transcriptomics and gene editing technologies can accelerate the cloning and confirmation of genes underlying QTL affecting P-efficiency related traits. Knowledge of these genes will be helpful in revealing the molecular mechanisms underlying P efficiency in crops, as well as providing the opportunity to improve crop P efficiency through MAS or gene manipulation.

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Abbreviations

APA:

acid phosphatase activity

DH:

double haploid

GWAS:

genome-wide association analysis

LRL:

lateral root length

LRN:

lateral root number

MAS:

marker-assisted selection

NIL:

near-isogenic line

P:

phosphorus

Pi:

phosphate

PRL:

primary root length

PUpE:

phosphorus uptake efficiency

PUtE:

phosphorus utilization efficiency

PVE:

phenotypic variation explained

QTL:

quantitative trait loci

RAPA:

relative acid phosphatase activity

RDW:

root dry weight

RIL:

recombinant inbred line

RPC:

relative plant phosphorus concentration

RRDW:

relative root dry weight

RSA:

root system architecture

RSDW:

relative shoot dry weight

SDW:

shoot dry weight

SNP:

single nucleotide polymorphism

SPC:

shoot phosphorus content

SRL:

seminal root length

SRN:

seminal root number

TDW:

total dry weight

TRL:

total root length

References

  • Adu MO, Chatot A, Wiesel L, Bennett MJ, Broadley MR, White PJ, Dupuy LX (2014) A scanner system for high-resolution quantification of variation in root growth dynamics of Brassica rapa genotypes. J Exp Bot 65:2039–2048

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Azevedo GC, Cheavegatti-Gianotto A, Negri BF, Hufnagel B, Silva LDCE, Magalhaes JV, Garcia AAF, Lana UGP, de Sousa SM, Guimaraes CT (2015) Multiple interval QTL mapping and searching for PSTOL1 homologs associated with root morphology, biomass accumulation and phosphorus content in maize seedlings under low-P. BMC Plant Biol 15:172

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Beebe SE, Rojas-Pierce M, Yan X, Blair MW, Pedraza F, Muñoz F, Tohme J, Lynch JP (2006) Quantitative trait loci for root architecture traits correlated with phosphorus acquisition in common bean. Crop Sci 46:413–423

    Article  CAS  Google Scholar 

  • Blair G (1993) Genetic aspects of plant mineral nutrition. In: Randall PJ, Delhaize E, Richards RA, Munns R (eds) Nutrient efficiency – what do we really mean? Kluwer Academic Publishers, Dordrecht, pp 205–213

    Google Scholar 

  • Brooker RW, Bennett AE, Cong W-F, Daniell TJ, George TS, Hallett PD, Hawes C, Ianetta PPM, Jones HG, Karley AJ, Li L, McKenzie BM, Pakeman RJ, Paterson E, Schöb C, Shen J, Squire G, Watson CA, Zhang C, Zhang F, Zhang J, White PJ (2015) Improving intercropping: a synthesis of research in agronomy, plant physiology and ecology. New Phytol 206:107–117

    Article  PubMed  Google Scholar 

  • Brown LK, George TS, Neugebauer K, White PJ (2017) The rhizosheath – a potential trait for future agricultural sustainability occurs in orders throughout the angiosperms. Plant Soil 418:115–128

    Article  CAS  Google Scholar 

  • Bulgarelli D, Schlaeppi K, Spaepen S, Ver Loren van Themaat E, Schulze-Lefert P (2013) Structure and functions of the bacterial microbiota of plants. Annu Rev Plant Biol 64:807–838

    Article  CAS  PubMed  Google Scholar 

  • Cai H, Chu Q, Yuan L, Liu J, Chen X, Chen F, Mi G, Zhang F (2012a) Identification of quantitative trait loci for leaf area and chlorophyll content in maize (Zea mays) under low nitrogen and low phosphorus supply. Mol Breed 30:251–266

    Article  CAS  Google Scholar 

  • Cai H, Chen F, Mi G, Zhang F, Maurer HP, Liu W, Reif JC, Yuan L (2012b) Mapping QTLs for root system architecture of maize (Zea mays L.) in the field at different developmental stages. Theor Appl Genet 125:1313–1324

    Article  PubMed  Google Scholar 

  • Cai H, Chu Q, Gu R, Yuan L, Liu J, Zhang X, Chen F, Mi G, Zhang F (2012c) Identification of QTLs for plant height, ear height and grain yield in maize (Zea mays L.) in response to nitrogen and phosphorus supply. Plant Breed 131:502–510

    Article  CAS  Google Scholar 

  • Cao WD, Jia JZ, Jin JY (2001) Identification and interaction analysis of QTL for phosphorus use efficiency in wheat. Plant Nutr Fertil Sci 7:285–292

    Google Scholar 

  • Cao P, Ren Y, Zhang K, Teng W, Zhao X, Dong Z, Liu X, Qin H, Li Z, Wang D, Tong Y (2014) Further genetic analysis of a major quantitative trait locus controlling root length and related traits in common wheat. Mol Breed 33:975–985

    Article  Google Scholar 

  • Chen J, Xu L (2011a) Comparative mapping of QTLs for H+ secretion of root in maize (Zea mays L.) and cross phosphorus levels on two growth stages. Front Agric China 5:284–290

    Article  CAS  Google Scholar 

  • Chen J, Xu L (2011b) The candidate QTLs affecting phosphorus absorption efficiency and root weight in maize (Zea mays L.). Front Agric China 5:456–462

    Article  Google Scholar 

  • Chen J, Xu L, Cai Y, Xu J (2008) QTL mapping of phosphorus efficiency and relative biologic characteristics in maize (Zea mays L.) at two sites. Plant Soil 313:251–266

    Article  CAS  Google Scholar 

  • Chen J, Xu L, Cai Y, Xu J (2009) Identification of QTLs for phosphorus utilization efficiency in maize (Zea mays L.) across P levels. Euphytica 167:245–252

    Article  CAS  Google Scholar 

  • Chen J, Cai Y, Xu L, Wang J, Zhang W, Wang G, Xu D, Chen T, Lu X, Sun H, Huang A, Liang Y, Dai G, Qin H, Huang Z, Zhu Z, Yang Z, Xu J, Kuang S (2011) Identification of QTLs for biomass production in maize (Zea mays L.) under different phosphorus levels at two sites. Front Agric China 5:152–161

    Article  Google Scholar 

  • Cheng L, Bucciarelli B, Liu J, Zinn K, Miller S, Patton-Vogt J, Allan D, Shen J, Vance CP (2011) White lupin cluster root acclimation to phosphorus deficiency and root hair development involve unique glycerophosphodiester phosphodiesterases. Plant Physiol 156:1131–1148

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chin JH, Lu X, Haefele SM, Gamuyao R, Ismail A, Wissuwa M, Heuer S (2010) Development and application of gene-based markers for the major rice QTL Phosphorus uptake 1. Theor Appl Genet 120:1073–1086

    Article  CAS  PubMed  Google Scholar 

  • Chin JH, Gamuyao R, Dalid C, Bustamam M, Prasetiyono J, Moeljopawiro S, Wissuwa M, Heuer S (2011) Developing rice with high yield under phosphorus deficiency: Pup1 sequence to application. Plant Physiol 156:1202–1216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cichy KA, Blair MW, Galeano Mendoza CH, Snapp SS, Kelly JD (2009) QTL analysis of root architecture traits and low phosphorus tolerance in an Andean bean population. Crop Sci 49:59–68

    Article  CAS  Google Scholar 

  • Cordell D, Drangert JO, White S (2009) The story of phosphorus: global food security and food for thought. Glob Environ Chang 19:292–305

    Article  Google Scholar 

  • Corrales I, Amenós M, Poschenrieder C, Barceló J (2007) Phosphorus efficiency and root exudates in two contrasting tropical maize varieties. J Plant Nutr 30:887–900

    Article  CAS  Google Scholar 

  • Crossa J, Pérez-Rodríguez P, Cuevas J, Montesinos-López O, Jarquín D, de Los Campos G, Burgueño J, González-Camacho JM, Pérez-Elizalde S, Beyene Y, Dreisigacker S, Singh R, Zhang X, Gowda M, Roorkiwal M, Rutkoski J, Varshney RK (2017) Genomic selection in plant breeding: methods, models, and perspectives. Trends Plant Sci 22:961–975

    Article  CAS  PubMed  Google Scholar 

  • Cui SY, Geng LY, Meng QC, Yu DY (2007) QTL mapping of phosphorus deficiency tolerance in soybean ( Glycine max L.) during seedling stage. Acta Agron Sin 33:378–383

    CAS  Google Scholar 

  • Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510

    Article  CAS  PubMed  Google Scholar 

  • Delgado M, Zúñiga-Feest A, Almonacid L, Lambers H, Borie F (2015) Cluster roots of Embothrium coccineum (Proteaceae) affect enzyme activities and phosphorus lability in rhizosphere soil. Plant Soil 395:189–200

    Article  CAS  Google Scholar 

  • Delhaize E, James RA, Ryan PR (2012) Aluminium tolerance of root hairs underlies genotypic differences in rhizosheath size of wheat (Triticum aestivum) grown on acid soil. New Phytol 195:609–619

    Article  CAS  PubMed  Google Scholar 

  • Delhaize E, Rathjen TM, Cavanagh CR (2015) The genetics of rhizosheath size in a multiparent mapping population of wheat. J Exp Bot 66:4527–4536

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Diaz LM, Ricaurte J, Cajiao C, Galeano CH, Rao I, Beebe S, Raatz B (2017) Phenotypic evaluation and QTL analysis of yield and symbiotic nitrogen fixation in a common bean population grown with two levels of phosphorus supply. Mol Breed 37:76

    Article  CAS  Google Scholar 

  • Ding G, Zhao Z, Liao Y, Hu Y, Shi L, Long Y, Xu F (2012) Quantitative trait loci for seed yield and yield-related traits, and their responses to reduced phosphorus supply in Brassica napus. Ann Bot 109:747–759

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Downie HF, Adu MO, Schmidt S, Otten W, Dupuy LX, White PJ, Valentine TA (2015) Challenges and opportunities for quantifying roots and rhizosphere interactions through imaging and image analysis. Plant Cell Environ 38:1213–1232

    Article  CAS  PubMed  Google Scholar 

  • Duan HY, Shi L, Ye XS, Wang YH, Xu FS (2009) Identification of phosphorous efficient germplasm in oilseed rape. J Plant Nutr 32:1148–1163

    Article  CAS  Google Scholar 

  • Dupuy L, Wright G, Thompson JA, Taylor A, Dekeyser S, White CP, Thomas WTB, Nightingale M, Hammond JP, Graham NS, Thomas CL, Broadley MR, White PJ (2017) Accelerating root system phenotyping through a computer-assisted processing pipeline. Plant Methods 13:57

    Article  PubMed  PubMed Central  Google Scholar 

  • Flint-Garcia SA, Thuillet AC, Yu J, Pressoir G, Romero SM, Mitchell SE, Doebley J, Kresovich S, Goodman MM, Buckler ES (2005) Maize association population: a high-resolution platform for quantitative trait locus dissection. Plant J 44:1054–1064

    Article  CAS  PubMed  Google Scholar 

  • Florez-Sarasa I, Lambers H, Wang X, Finnegan PM, Ribas-Carbo M (2014) The alternative respiratory pathway mediates carboxylate synthesis in white lupin cluster roots under phosphorus deprivation. Plant Cell Environ 37:922–928

    Article  CAS  PubMed  Google Scholar 

  • Fu Y, Wei D, Dong H, He Y, Cui Y, Mei J, Wan H, Li J, Snowdon R, Friedt W, Li X, Qian W (2015) Comparative quantitative trait loci for silique length and seed weight in Brassica napus. Sci Rep 5:14407

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furbank RT, Tester M (2011) Phenomics-technologies to relieve the phenotyping bottleneck. Trends Plant Sci 16:635–644

    Article  CAS  PubMed  Google Scholar 

  • Gamuyao R, Chin JH, Pariasca-Tanaka J, Pesaresi P, Catausan S, Dalid C, Slamet-Loedin I, Tecson-Mendoza EM, Wissuwa M, Heuer S (2012) The protein kinase Pstol1 from traditional rice confers tolerance of phosphorus deficiency. Nature 488:535–539

    Article  CAS  PubMed  Google Scholar 

  • Geng LY, Cui SY, Zhang D, Xing H, Gai JY, Yu DY (2007) QTL mapping and epistasis analysis for P-efficiency in soybean (Glycine max L.). Soybean Sci 26:460–466

    Google Scholar 

  • Gu R, Chen F, Long L, Cai H, Liu Z, Yang J, Wang L, Li H, Li J, Liu W, Mi G, Zhang F, Yuan L (2016) Enhancing phosphorus uptake efficiency through QTL-based selection for root system architecture in maize. J Genet Genomics 43:663–672

    Article  PubMed  Google Scholar 

  • Guo Y, Kong FM, Xu YF, Zhao Y, Liang X, Wang YY, An DG, Li SS (2012) QTL mapping for seedling traits in wheat grown under varying concentrations of N, P and K nutrients. Theor Appl Genet 124:851–865

    Article  CAS  PubMed  Google Scholar 

  • Haefele SM, Nelson A, Hijmans RJ (2014) Soil quality and constraints in global rice production. Geoderma 235–236:250–259

    Article  CAS  Google Scholar 

  • Hajabbasi MA, Schumacher TE (1994) Phosphorus effects on root growth and development in two maize genotypes. Plant Soil 158:39–46

    Article  CAS  Google Scholar 

  • Hammond JP, White PJ (2008) Sucrose transport in the phloem: integrating root responses to phosphorus starvation. J Exp Bot 59:93–109

    Article  CAS  PubMed  Google Scholar 

  • Hammond JP, Broadley MR, White PJ, King GJ, Bowen HC, Hayden R, Meacham MC, Mead A, Overs T, Spracklen WP, Greenwood DJ (2009) Shoot yield drives phosphorus use efficiency in Brassica oleracea and correlates with root architecture traits. J Exp Bot 60:1953–1968

    Article  CAS  PubMed  Google Scholar 

  • Harjes CE, Rocheford TR, Bai L, Brutnell TP, Kandianis CB, Sowinski SG, Stapleton AE, Vallabhaneni R, Williams M, Wurtzel ET, Yan J, Buckler ES (2008) Natural genetic variation in lycopene epsilon cyclase tapped for maize biofortification. Science 319:330–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hawkesford M, Horst W, Kichey T, Lambers H, Schjoerring J, Skrumsager Møller I, White P (2012) Chapter 6: Functions of macronutrients. In: Marschner P (ed) Marschner’s Mineral Nutrition of Higher Plants, Third edn. Academic Press, London, pp 135–189

  • He Y, Liao H, Yan X (2003) Localized supply of phosphorus induces root morphological and architectural changes of rice in split and stratified soil cultures. Plant Soil 248:247–256

    Article  CAS  Google Scholar 

  • Heuer S, Lu X, Chin JH, Tanaka JP, Kanamori H, Matsumoto T, De Leon T, Ulat VJ, Ismail AM, Yano M, Wissuwa M (2009) Comparative sequence analyses of the major quantitative trait locus phosphorus uptake 1 (Pup1) reveal a complex genetic structure. Plant Biotechnol J 7:456–471

    Article  CAS  PubMed  Google Scholar 

  • Hirel B, Bertin P, Quilleré I, Bourdoncle W, Attagnant C, Dellay C, Gouy A, Cadiou S, Retailliau C, Falque M, Gallais A (2001) Towards a better understanding of the genetic and physiological basis for nitrogen use efficiency in maize. Plant Physiol 125:1258–1270

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hu B, Wu P, Liao CY, Zhang WP, Ni JJ (2001) QTLs and epistasis underlying activity of acid phosphatase under phosphorus sufficient and deficient condition in rice (Oryza sativa L.). Plant Soil 230:99–105

    Article  CAS  Google Scholar 

  • Hua Y, Zhang D, Zhou T, He M, Ding G, Shi L, Xu F (2016) Transcriptomics-assisted QTL fine mapping for the rapid identification of a nodulin 26-like intrinsic protein gene regulating boron efficiency in allotetraploid rapeseed. Plant Cell Environ 39:1601–1618

    Article  CAS  PubMed  Google Scholar 

  • Hufnagel B, de Sousa SM, Assis L, Guimaraes CT, Leiser W, Azevedo GC, Negri B, Larson BG, Shaff JE, Pastina MM, Barros BA, Weltzien E, Rattunde HFW, Viana JH, Clark RT, Falcão A, Gazaffi R, Garcia AAF, Schaffert RE, Kochian LV, Magalhaes JV (2014) Duplicate and conquer: multiple homologs of PHOSPHORUS-STARVATION TOLERANCE1 enhance phosphorus acquisition and sorghum performance on low-phosphorus soils. Plant Physiol 166:659–677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hund A, Reimer R, Messmer R (2011) A consensus map of QTLs controlling the root length of maize. Plant Soil 344:143–158

    Article  CAS  Google Scholar 

  • Illa-Berenguer E, Van Houten J, Huang Z, van der Knaap E (2015) Rapid and reliable identification of tomato fruit weight and locule number loci by QTL-seq. Theor Appl Genet 128:1329–1342

    Article  PubMed  Google Scholar 

  • Jain A, Vasconcelos MJ, Raghothama KG (2007) Molecular mechanisms of plant adaptation to phosphate deficiency. In: Janick J (ed) Plant Breeding Reviews, vol 29. Wiley, Hoboken, pp 359–419

    Chapter  Google Scholar 

  • James RA, Weligama C, Verbyla K, Ryan PR, Rebetzke GJ, Rattey A, Richardson AE, Delhaize E (2016) Rhizosheaths on wheat grown in acid soils: phosphorus acquisition efficiency and genetic control. J Exp Bot 67:3709–3718

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jonas E, de Koning DJ (2013) Does genomic selection have a future in plant breeding? Trends Biotechnol 31:497–504

    Article  CAS  PubMed  Google Scholar 

  • Kaeppler SM, Parke JL, Mueller SM, Senior L, Stuber C, Tracy WF (2000) Variation among maize inbred lines and detection of quantitative trait loci for growth at low phosphorus and responsiveness to arbuscular mycorrhizal fungi. Crop Sci 40:358–364

    Article  Google Scholar 

  • Kochian LV (2012) Plant nutrition: rooting for more phosphorus. Nature 488:466–467

    Article  CAS  PubMed  Google Scholar 

  • Koide Y, Pariasca Tanaka J, Rose T, Fukuo A, Konisho K, Yanagihara S, Fukuta Y, Wissuwa M (2013) QTLs for phosphorus deficiency tolerance detected in upland NERICA varieties. Plant Breed 132:259–265

    Article  CAS  Google Scholar 

  • Lambers H, Clements JC, Nelson MN (2013) How a phosphorus-acquisition strategy based on carboxylate exudation powers the success and agronomic potential of lupines (Lupinus, Fabaceae). Am J Bot 100:263–288

    Article  CAS  PubMed  Google Scholar 

  • Lapis-Gaza HR, Jost R, Finnegan PM (2014) Arabidopsis PHOSPHATE TRANSPORTER1 genes PHT1;8 and PHT1;9 are involved in root-to-shoot translocation of orthophosphate. BMC Plant Biol 14:334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li YD, Wang YJ, Tong YP, Gao JG, Zhang JS, Chen SY (2005) QTL mapping of phosphorus deficiency tolerance in soybean (Glycine max L. Merr.). Euphytica 142:137–142

    Article  CAS  Google Scholar 

  • Li J, Xie Y, Dai A, Liu L, Li Z (2009) Root and shoot traits responses to phosphorus deficiency and QTL analysis at seedling stage using introgression lines of rice. J Genet Genomics 36:173–183

    Article  CAS  PubMed  Google Scholar 

  • Li M, Guo X, Zhang M, Wang X, Zhang G, Tian Y, Wang Z (2010) Mapping QTLs for grain yield and yield components under high and low phosphorus treatments in maize (Zea mays L.). Plant Sci 178:454–462

    Article  CAS  Google Scholar 

  • Li Y, Zhang J, Zhang X, Fan H, Gu M, Qu H, Xu G (2015) Phosphate transporter OsPht1;8 in rice plays an important role in phosphorus redistribution from source to sink organs and allocation between embryo and endosperm of seeds. Plant Sci 230:23–32

    Article  CAS  PubMed  Google Scholar 

  • Li H, Yang Y, Zhang H, Chu S, Zhang X, Yin D, Yu D, Zhang D (2016) A genetic relationship between phosphorus efficiency and photosynthetic traits in soybean as revealed by QTL analysis using a high-density genetic map. Front Plant Sci 7:924

    PubMed  PubMed Central  Google Scholar 

  • Li X, Guo Z, Lv Y, Cen X, Ding X, Wu H, Li X, Huang J, Xiong L (2017) Genetic control of the root system in rice under normal and drought stress conditions by genome-wide association study. PLoS Genet 13:e1006889

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang C, Tian J, Lam HM, Lim BL, Yan X, Liao H (2010a) Biochemical and molecular characterization of PvPAP3, a novel purple acid phosphatase isolated from common bean enhancing extracellular ATP utilization. Plant Physiol 152:854–865

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liang Q, Cheng X, Mei M, Yan X, Liao H (2010b) QTL analysis of root traits as related to phosphorus efficiency in soybean. Ann Bot 106:223–234

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liao H, Yan X (2000) Molecular mapping of QTLs conferring root architecture of common bean in response to phosphorus deficiency. J Agric. Biotech 8:67–70

    Google Scholar 

  • Liao H, Yan X, Rubio G, Beebe SE, Blair MW, Lynch JP (2004) Genetic mapping of basal root gravitropism and phosphorus acquisition efficiency in common bean. Funct Plant Biol 31:959–970

    Article  CAS  PubMed  Google Scholar 

  • Lim JH, Chung IM, Ryu SS, Park MR, Yun SJ (2003) Differential responses of rice acid phosphatase activities and isoforms to phosphorus deprivation. J Biochem Mol Biol 36:597–602

    CAS  PubMed  Google Scholar 

  • Liu J, Li J, Chen F, Zhang F, Ren T, Zhuang Z, Mi G (2008) Mapping QTLs for root traits under different nitrate levels at the seedling stage in maize (Zea mays, L.). Plant Soil 305:253–265

    Article  CAS  Google Scholar 

  • Liu J, Hua W, Hu Z, Yang H, Zhang L, Li R, Deng L, Sun X, Wang X, Wang H (2015a) Natural variation in ARF18 gene simultaneously affects seed weight and silique length in polyploid rapeseed. Proc Natl Acad Sci 112:E5123–E5132

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu L, Du Y, Shen X, Li M, Sun W, Huang J, Liu Z, Tao Y, Zheng Y, Yan J, Zhang Z (2015b) KRN4 controls quantitative variation in maize kernel row number. PLoS Genet 11:e1005670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu F, Xu Y, Jiang H, Jiang C, Du Y, Gong C, Wang W, Zhu S, Han G, Cheng B (2016) Systematic identification, evolution and expression analysis of the Zea mays PHT1 gene family reveals several new members involved in root colonization by arbuscular mycorrhizal fungi. Int J Mol Sci 17:930

    Article  CAS  PubMed Central  Google Scholar 

  • Liu Z, Gao K, Shan S, Gu R, Wang Z, Craft EJ, Mi G, Yuan L, Chen F (2017) Comparative analysis of root traits and the associated QTLs for maize seedlings grown in paper roll, hydroponics and vermiculite culture system. Front Plant Sci 8:436

    PubMed  PubMed Central  Google Scholar 

  • López-Arredondo DL, Leyva-González MA, González-Morales SI, López-Bucio J, Herrera-Estrella L (2014) Phosphate nutrition: improving low-phosphate tolerance in crops. Annu Rev Plant Biol 65:95–123

    Article  CAS  PubMed  Google Scholar 

  • Lu H, Lin T, Klein J, Wang S, Qi J, Zhou Q, Sun J, Zhang Z, Weng Y, Huang S (2014) QTL-seq identifies an early flowering QTL located near Flowering Locus T in cucumber. Theor Appl Genet 127:1491–1499

    Article  PubMed  Google Scholar 

  • Luo XD, Liu J, Dai LF, Zhang FT, Wan Y, Xie JK (2017) Linkage map construction and QTL identification of P-deficiency tolerance in Oryza rufipogon Griff. at early seedling stage. Euphytica 213:96

    Article  CAS  Google Scholar 

  • Lynch JP (2007) Roots of the second green revolution. Aust J Bot 55:493–512

    Article  Google Scholar 

  • Lynch JP (2011) Root phenes for enhanced soil exploration and phosphorus acquisition: tools for future crops. Plant Physiol 156:1041–1049

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lynch JP (2015) Root phenes that reduce the metabolic costs of soil exploration: opportunities for 21st century agriculture. Plant Cell Environ 38:1775–1784

    Article  PubMed  Google Scholar 

  • Mendes FF, Guimarães LJM, Souza JC, Guimarães PEO, Magalhaes JV, Garcia AAF, Parentoni SN, Guimaraes CT (2014) Genetic architecture of phosphorus use efficiency in tropical maize cultivated in a low-P soil. Crop Sci 54:1530–1538

    Article  CAS  Google Scholar 

  • Messmer R, Fracheboud Y, Bänziger M, Vargas M, Stamp P, Ribaut JM (2009) Drought stress and tropical maize: QTL-by-environment interactions and stability of QTLs across environments for yield components and secondary traits. Theor Appl Genet 119:913–930

    Article  PubMed  Google Scholar 

  • Miklas PN, Kelly JD, Beebe SE, Blair MW (2006) Common bean breeding for resistance against biotic and abiotic stresses: from classical to MAS breeding. Euphytica 147:105–131

    Article  CAS  Google Scholar 

  • Ming F, Zheng X, Mi G, He P, Zhu L, Zhang F (2000) Identification of quantitative trait loci affecting tolerance to low phosphorus in rice (Oryza Sativa L.). Chinese Sci Bull 45:520–525

    Article  Google Scholar 

  • Ming F, Zheng X, Mi G, Zhu L, Zhang F (2001) Detection and verification of quantitative trait loci affecting tolerance to low phosphorus in rice. J Plant Nutr 24:1399–1408

    Article  Google Scholar 

  • Mu P, Huang C, Li JX, Liu LF, Liu UJ, Li ZC (2008) Yield trait variation and QTL mapping in a DH population of rice under phosphorus deficiency. Acta Agron Sin 34:1137–1142

    CAS  Google Scholar 

  • Navea IP, Dwiyanti MS, Park J, Kim B, Lee S, Huang X, Koh HJ, Chin JH (2017) Identification of quantitative trait loci for panicle length and yield related traits under different water and P application conditions in tropical region in rice (Oryza sativa, L.). Euphytica 213(37)

  • Ni JJ, Wu P, Senadhira D, Huang N (1998) Mapping QTLs for phosphorus deficiency tolerance in rice (Oryza sativa L.). Theor Appl Genet 97:1361–1369

    Article  CAS  Google Scholar 

  • Ning L, Kan G, Du W, Guo S, Wang Q, Zhang G, Cheng H, Yu D (2016) Association analysis for detecting significant single nucleotide polymorphisms for phosphorus-deficiency tolerance at the seedling stage in soybean [Glycine max (L) Merr]. Breed Sci 66:191–203

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Niu YF, Chai RS, Jin GL, Wang H, Tang CX, Zhang YS (2013) Responses of root architecture development to low phosphorus availability: a review. Ann Bot 112:391–408

    Article  CAS  PubMed  Google Scholar 

  • Ochoa IE, Blair MW, Lynch JP (2006) QTL analysis of adventitious root formation in common bean under contrasting phosphorus availability. Crop Sci 46:1609–1621

    Article  CAS  Google Scholar 

  • Ogawa S, Selvaraj MG, Fernando AJ, Lorieux M, Ishitani M, McCouch S, Arbelaez JD (2014) N- and P-mediated seminal root elongation response in rice seedlings. Plant Soil 375:303–315

    Article  CAS  Google Scholar 

  • Plaxton WC, Tran HT (2011) Metabolic adaptations of phosphate-starved plants. Plant Physiol 156:1006–1015

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qin H, Cai Y, Sun H, Wang J, Wang G, Liu Z (2011) QTL mapping of root exudates related to phosphorus efficiency in maize (Zea mays L.). J Agr. Biotechnol 19:93–101

    CAS  Google Scholar 

  • Qiu F, Zheng Y, Zhang Z, Xu S (2007) Mapping of QTL associated with waterlogging tolerance during the seedling stage in maize. Ann Bot 99:1067–1081

    Article  PubMed  PubMed Central  Google Scholar 

  • Qiu H, Mei X, Liu C, Wang J, Wang G, Wang X, Liu Z, Cai Y (2013) Fine mapping of quantitative trait loci for acid phosphatase activity in maize leaf under low phosphorus stress. Mol Breed 32:629–639

    Article  CAS  Google Scholar 

  • Qiu H, Liu C, Yu T, Mei X, Wang G, Wang J, Cai Y (2014) Identification of QTL for acid phosphatase activity in root and rhizosphere soil of maize under low phosphorus stress. Euphytica 197:133–143

    Article  CAS  Google Scholar 

  • Reiter RS, Coors JG, Sussman MR, Gabelman WH (1991) Genetic analysis of tolerance to low-phosphorus stress in maize using restriction fragment length polymorphisms. Theor Appl Genet 82:561–568

    Article  CAS  PubMed  Google Scholar 

  • Ren Y, He X, Liu D, Li J, Zhao X, Li B, Tong Y, Zhang A, Li Z (2012) Major quantitative trait loci for seminal root morphology of wheat seedlings. Mol Breed 30:139–148

    Article  Google Scholar 

  • Ren ZY, Su SZ, Zhang SZ, Liu HL, Luo BW, Liu D, Wu L, Rong TZ, Gao SB (2015) Characterization and QTL mapping of yield trait under two phosphorus regimes in maize. Acta Agric Boreali sin 30:9–14

    CAS  Google Scholar 

  • Rodríguez-Leal D, Lemmon ZH, Man J, Bartlett ME, Lippman ZB (2017) Engineering quantitative trait variation for crop improvement by genome editing. Cell 171:1–11

    Article  CAS  Google Scholar 

  • Rose TJ, Rose MT, Pariasca-Tanaka J, Heuer S, Wissuwa M (2011) The frustration with utilization: why have improvements in internal phosphorus utilization efficiency in crops remained so elusive? Front Plant Sci 2:73

    PubMed  PubMed Central  Google Scholar 

  • Ryan PR, Liao M, Delhaize E, Rebetzke GJ, Weligama C, Spielmeyer W, James RA (2015) Early vigour improves phosphate uptake in wheat. J Exp Bot 66:7089–7100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shi L, Liang HL, Xu FS, Wang YH (2008) Genotypic variation in phosphorus fractions and its relation to phosphorus efficiency in seedlings of Brassica napus L. Plant Nutr Fertil Sci 14:351–356

    CAS  Google Scholar 

  • Shi L, Shi T, Broadley MR, White PJ, Long Y, Meng J, Xu F, Hammond JP (2013a) High-throughput root phenotyping screens identify genetic loci associated with root architectural traits in Brassica napus under contrasting phosphate availabilities. Ann Bot 112:381–389

    Article  CAS  PubMed  Google Scholar 

  • Shi T, Li R, Zhao Z, Ding G, Long Y, Meng J, Xu F, Shi L (2013b) QTL for yield traits and their association with functional genes in response to phosphorus deficiency in Brassica napus. PLoS One 8:e54559

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Shimizu A, Yanagihara S, Kawasaki S, IKehashi H (2004) Phosphorus deficiency-induced root elongation and its QTL in rice (Oryza sativa L.). Theor Appl Genet 109:1361–1368

    Article  CAS  PubMed  Google Scholar 

  • Shimizu A, Kato K, Komatsu A, Motomura K, Ikehashi H (2008) Genetic analysis of root elongation induced by phosphorus deficiency in rice (Oryza sativa L.): fine QTL mapping and multivariate analysis of related traits. Theor Appl Genet 117:987–996

    Article  CAS  PubMed  Google Scholar 

  • Song H, Yin Z, Chao M, Ning L, Zhang D, Yu D (2014) Functional properties and expression quantitative trait loci for phosphate transporter GmPT1 in soybean. Plant Cell Environ 37:462–472

    Article  CAS  PubMed  Google Scholar 

  • Spindel J, Wright M, Chen C, Cobb J, Gage J, Harrington S, Lorieux M, Ahmadi N, McCouch S (2013) Bridging the genotyping gap: using genotyping by sequencing (GBS) to add high-density SNP markers and new value to traditional bi-parental mapping and breeding populations. Theor Appl Genet 126:2699–2716

    Article  CAS  PubMed  Google Scholar 

  • Stutter MI, Shand CA, George TS, Blackwell MSA, Bol R, MacKay RL, Richardson AE, Condron LM, Turner BL, Haygarth PM (2012) Recovering phosphorus from soil: a root solution? Environ Sci Technol 46:1977–1978

    Article  CAS  PubMed  Google Scholar 

  • Su J, Xiao Y, Li M, Liu Q, Li B, Tong Y, Jia J, Li Z (2006) Mapping QTLs for phosphorus-deficiency tolerance at wheat seedling stage. Plant Soil 281:25–36

    Article  CAS  Google Scholar 

  • Su JY, Zheng Q, Li HW, Li B, Jing RL, Tong YP, Li ZS (2009a) Detection of QTLs for phosphorus use efficiency in relation to agronomic performance of wheat grown under phosphorus sufficient and limited conditions. Plant Sci 176:824–836

    Article  CAS  Google Scholar 

  • Su H, Li Z, Song S (2009b) Molecular mapping of QTLs major agronomic traits in soybean (Glycine max L.) under phosphorus deficiency stress. Acta Agric Bor-Occid Sin 18:98–101

    Google Scholar 

  • Takagi H, Abe A, Yoshida K, Kosugi S, Natsume S, Mitsuoka C, Uemura A, Utsushi H, Tamiru M, Takuno S, Innan H, Cano LM, Kamoun S, Terauchi R (2013) QTL-seq: rapid mapping of quantitative trait loci in rice by whole genome resequencing of DNA from two bulked populations. Plant J 74:174–183

    Article  CAS  PubMed  Google Scholar 

  • Thomas CL, Graham NS, Hayden R, Meacham MC, Neugebauer K, Nightingale M, Dupuy LX, Hammond JP, White PJ, Broadley MR (2016) High-throughput phenotyping (HTP) identifies seedling root traits linked to variation in seed yield and nutrient capture in field-grown oilseed rape (Brassica napus L.). Ann Bot 118:655–665

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Tian J, Wang X, Tong Y, Chen X, Liao H (2012) Bioengineering and management for efficient phosphorus utilization in crops and pastures. Curr Opin Biotechnol 23:866–871

    Article  CAS  PubMed  Google Scholar 

  • Tiessen H (2008) Phosphorus in the global environment. In: White PJ, Hammond JP (eds) The ecophysiology of plant-phosphorus interactions. Springer, Dordrecht, pp 1–7

    Google Scholar 

  • Ubbens JR, Stavness I (2017) Deep plant phenomics: a deep learning platform for complex plant phenotyping tasks. Front Plant Sci 8:1190

    Article  PubMed  PubMed Central  Google Scholar 

  • van de Wiel CCM, van der Linden CG, Scholten OE (2016) Improving phosphorus use efficiency in agriculture: opportunities for breeding. Euphytica 207:1–22

    Article  Google Scholar 

  • Van Kauwenbergh SJ (2010) World phosphate rock reserves and resources. International Fertilizer Development Center, Muscle Shoals, Alabama 35662, USA. ISBN 978-0-88090-167-3

  • Veneklaas EJ, Lambers H, Bragg J, Finnegan PM, Lovelock CE, Plaxton WC, Price CA, Scheible WR, Shane MW, White PJ, Raven JA (2012) Opportunities for improving phosphorus-use efficiency in crop plants. New Phytol 195:306–320

    Article  CAS  PubMed  Google Scholar 

  • Walder F, Brulé D, Koegel S, Wiemken A, Boller T, Courty PE (2015) Plant phosphorus acquisition in a common mycorrhizal network: regulation of phosphate transporter genes of the Pht1 family in sorghum and flax. New Phytol 205:1632–1645

    Article  CAS  PubMed  Google Scholar 

  • Wang Y, Sun YJ, Chen DY, Yu SB (2009a) Quantitative trait loci analysis of responses to nitrogen and phosphorus deficiency in rice chromosomal segment substitution lines. Acta Agron Sin 35:580–587

    CAS  Google Scholar 

  • Wang X, Wang Y, Tian J, Lim BL, Yan X, Liao H (2009b) Overexpressing AtPAP15 enhances phosphorus efficiency in soybean. Plant Physiol 151:233–240

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Yan X, Liao H (2010a) Genetic improvement for phosphorus efficiency in soybean: a radical approach. Ann Bot 106:215–222

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang X, Shen J, Liao H (2010b) Acquisition or utilization, which is more critical for enhancing phosphorus efficiency in modern crops? Plant Sci 179:302–306

    Article  CAS  Google Scholar 

  • Wang K, Cui K, Liu G, Xie W, Yu H, Pan J, Huang J, Nie L, Shah F, Peng S (2014) Identification of quantitative trait loci for phosphorus use efficiency traits in rice using a high density SNP map. BMC Genet 15:155

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang H, Cheng H, Wang W, Liu J, Hao M, Mei D, Zhou R, Fu L, Hu Q (2016) Identification of BnaYUCCA6 as a candidate gene for branch angle in Brassica napus by QTL-seq. Sci Rep 6:38493

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang X, Chen Y, Thomas CL, Ding G, Xu P, Shi D, Grandke F, Jin K, Cai H, Xu F, Yi B, Broadley MR, Shi L (2017) Genetic variants associated with the root system architecture of oilseed rape (Brassica napus L.) under contrasting phosphate supply. DNA Res 24:407–417

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wasaki J, Shinano T, Onishi K, Yonetani R, Yazaki J, Fujii F, Shimbo K, Ishikawa M, Shimatani Z, Nagata Y, Hashimoto A, Ohta T, Sato Y, Miyamoto C, Honda S, Kojima K, Sasaki T, Kishimoto N, Kikuchi S, Osaki M (2006) Transcriptomic analysis indicates putative metabolic changes caused by manipulation of phosphorus availability in rice leaves. J Exp Bot 57:2049–2059

    Article  CAS  PubMed  Google Scholar 

  • Wei QZ, Fu WY, Wang YZ, Qin XD, Wang J, Li J, Lou QF, Chen JF (2016) Rapid identification of fruit length loci in cucumber (Cucumis sativus L.) using next-generation sequencing (NGS)-based QTL analysis. Sci Rep 6:27496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White PJ, Broadley MR, Gregory PJ (2012) Managing the nutrition of plants and people. Appl Environ Soil Sci 2012:104826

    Google Scholar 

  • White PJ, George TS, Gregory PJ, Bengough AG, Hallett PD, McKenzie BM (2013a) Matching roots to their environment. Ann Bot 112:207–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • White PJ, George TS, Dupuy LX, Karley AJ, Valentine TA, Wiesel L, Wishart J (2013b) Root traits for infertile soils. Front Plant Sci 4:193

    Article  PubMed  PubMed Central  Google Scholar 

  • Wissuwa M, Ae N (2001) Genotypic variation for tolerance to phosphorus deficiency in rice and the potential for its exploitation in rice improvement. Plant Breed 120:43–48

    Article  CAS  Google Scholar 

  • Wissuwa M, Yano M, Ae N (1998) Mapping of QTLs for phosphorus-deficiency tolerance in rice (Oryza sativa L.). Theor Appl Genet 97:777–783

    Article  CAS  Google Scholar 

  • Wissuwa M, Wegner J, Ae N, Yano M (2002) Substitution mapping of Pup1: a major QTL increasing phosphorus uptake of rice from a phosphorus-deficient soil. Theor Appl Genet 105:890–897

    Article  CAS  PubMed  Google Scholar 

  • Wissuwa M, Kondo K, Fukuda T, Mori A, Rose MT, Pariasca-Tanaka J, Kretzschmar T, Haefele SM, Rose TJ (2015) Unmasking novel loci for internal phosphorus utilization efficiency in rice germplasm through genome-wide association analysis. PloS One 10:e0124215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Withers PJ, Sylvester-Bradley R, Jones DL, Healey JR, Talboys PJ (2014) Feed the crop not the soil: rethinking phosphorus management in the food chain. Environ Sci Technol 48:6523–6530

    Article  CAS  PubMed  Google Scholar 

  • Xiang C, Ren J, Zhao XQ, Ding ZS, Zhang J, Wang C, Zhang JW, Joseph CA, Zhang Q, Pang YL, Gao YM, Shi YY (2015) Genetic dissection of low phosphorus tolerance related traits using selected introgression lines in rice. Rice Sci 22:264–274

    Article  Google Scholar 

  • Xiao Y, Liu H, Wu L, Warburton M, Yan J (2017) Genome-wide association studies in maize: praise and stargaze. Mol Plant 10:359–374

    Article  CAS  PubMed  Google Scholar 

  • Xu Y, Wang R, Tong Y, Zhao H, Xie Q, Liu D, Zhang A, Li B, Xu H, An D (2014) Mapping QTLs for yield and nitrogen-related traits in wheat: influence of nitrogen and phosphorus fertilization on QTL expression. Theor Appl Genet 127:59–72

    Article  CAS  PubMed  Google Scholar 

  • Yan X, Liao H, Trull MC, Beebe SE, Lynch JP (2001) Induction of a major leaf acid phosphatase does not confer adaptation to low phosphorus availability in common bean. Plant Physiol 125:1901–1911

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yan X, Liao H, Beebe SE, Blair MW, Lynch JP (2004) QTL mapping of root hair and acid exudation traits and their relationship to phosphorus uptake in common bean. Plant Soil 265:17–29

    Article  CAS  Google Scholar 

  • Yan J, Kandianis CB, Harjes CE, Bai L, Kim EH, Yang X, Skinner DJ, Fu Z, Mitchell S, Li Q, Fernandez MGS, Zaharieva M, Babu R, Fu Y, Palacios N, Li J, DellaPenna D, Brutnell T, Buckler ES, Warburton ML, Rocheford T (2010) Rare genetic variation at Zea mays crtRB1 increases β-carotene in maize grain. Nat Genet 42:322–327

    Article  CAS  PubMed  Google Scholar 

  • Yan J, Warburton M, Crouch J (2011) Association mapping for enhancing maize (Zea mays L.) genetic improvement. Crop Sci 51:433–449

    Article  Google Scholar 

  • Yang M, Ding G, Shi L, Feng J, Xu F, Meng J (2010) Quantitative trait loci for root morphology in response to low phosphorus stress in Brassica napus. Theor Appl Genet 121:181–193

    Article  CAS  PubMed  Google Scholar 

  • Yang M, Ding G, Shi L, Xu F, Meng J (2011) Detection of QTL for phosphorus efficiency at vegetative stage in Brassica napus. Plant Soil 339:97–111

    Article  CAS  Google Scholar 

  • Yang W, Guo Z, Huang C, Duan L, Chen G, Jiang N, Fang W, Feng H, Xie W, Lian X, Wang G, Luo Q, Zhang Q, Liu Q, Xiong L (2014) Combining high-throughput phenotyping and genome-wide association studies to reveal natural genetic variation in rice. Nat Commun 5:5087

    Article  CAS  PubMed  Google Scholar 

  • Yuan Y, Gao M, Zhang M, Zheng H, Zhou X, Guo Y, Zhao Y, Kong F, Li S (2017) QTL mapping for phosphorus efficiency and morphological traits at seedling and maturity stages in wheat. Front Plant Sci 8:614

    Article  PubMed  PubMed Central  Google Scholar 

  • Zeng H, Wang G, Zhang Y, Hu X, Pi E, Zhu Y, Wang H, Du L (2016) Genome-wide identification of phosphate-deficiency-responsive genes in soybean roots by high-throughput sequencing. Plant Soil 398:207–227

    Article  CAS  Google Scholar 

  • Zhang H, Wang H (2015) QTL mapping for traits related to P-deficient tolerance using three related RIL populations in wheat. Euphytica 203:505–520

    Article  Google Scholar 

  • Zhang Q, Wing R (2013) Genome studies and molecular genetics: understanding the functional genome based on the rice model. Curr Opin Plant Biol 16:129–132

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Cheng H, Geng L, Kan G, Cui S, Meng Q, Gai J, Yu D (2009) Detection of quantitative trait loci for phosphorus deficiency tolerance at soybean seedling stage. Euphytica 167:313–322

    Article  CAS  Google Scholar 

  • Zhang H, Huang Y, Ye X, Xu F (2010a) Analysis of the contribution of acid phosphatase to P efficiency in Brassica napus under low phosphorus conditions. Sci China Life Sci 53:709–717

    Article  CAS  PubMed  Google Scholar 

  • Zhang D, Liu C, Cheng H, Kan G, Cui S, Meng Q, Gai J, Yu D (2010b) Quantitative trait loci associated with soybean tolerance to low phosphorus stress based on flower and pod abscission. Plant Breed 129:243–249

    Article  CAS  Google Scholar 

  • Zhang G, Wang X, Wang B, Tian Y, Li M, Nie Y, Peng Q, Wang Z (2013a) Fine mapping a major QTL for kernel number per row under different phosphorus regimes in maize (Zea mays L.). Theor Appl Genet 126:1545–1553

    Article  CAS  PubMed  Google Scholar 

  • Zhang K, Wang J, Zhang L, Rong C, Zhao F, Peng T, Li H, Cheng D, Liu X, Qin H, Zhang A, Tong Y, Wang D (2013b) Association analysis of genomic loci important for grain weight control in elite common wheat varieties cultivated with variable water and fertiliser supply. PLoS One 8:e57853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Chen F, Li X, Li C (2013c) Higher leaf area and post-silking P uptake conferred by introgressed DNA segments in the backcross maize line 224. Field Crops Res 151:78–84

    Article  Google Scholar 

  • Zhang J, Xiang C, Zhang J, Ren J, Liu Z, Wang C, Qu L, Shi Y (2014a) Mapping QTL controlling yield traits using low phosphorus tolerance selected backcrossing introgression lines of rice (Oryza sativa L.). Chin Agric Sci Bull 30:56–65

    Google Scholar 

  • Zhang D, Song H, Cheng H, Hao D, Wang H, Kan G, Jin H, Yu D (2014b) The acid phosphatase-encoding gene GmACP1 contributes to soybean tolerance to low-phosphorus stress. PLoS Genet 10:e1004061

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang D, Li H, Wang J, Zhang H, Hu Z, Chu S, Lv H, Yu D (2016a) High-density genetic mapping identifies new major loci for tolerance to low-phosphorus stress in soybean. Front Plant Sci 7:372

    PubMed  PubMed Central  Google Scholar 

  • Zhang Y, Thomas CL, Xiang J, Long Y, Wang X, Zou J, Luo Z, Ding G, Cai H, Graham NS, Hammond JP, King GJ, White PJ, Xu F, Broadley MR, Shi L, Meng J (2016b) QTL meta-analysis of root traits in Brassica napus under contrasting phosphorus supply in two growth systems. Sci Rep 6:33113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang D, Zhang H, Chu S, Li H, Chi Y, Triebwasser-Freese D, Lv H, Yu D (2017a) Integrating QTL mapping and transcriptomics identifies candidate genes underlying QTLs associated with soybean tolerance to low-phosphorus stress. Plant Mol Biol 93:137–150

    Article  CAS  PubMed  Google Scholar 

  • Zhang X, Huang C, Wu D, Qiao F, Li W, Duan L, Wang K, Xiao Y, Chen G, Liu Q, Xiong L, Yang W, Yan J (2017b) High-throughput phenotyping and QTL mapping reveals the genetic architecture of maize plant growth. Plant Physiol 173:1554–1564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhao CF, Zhang YD, Chen T, Zhao QY, Zhu Z, Zhou LH, Yao S, Yu X, Wang CL (2013) QTL mapping for root elongation traits related to phosphorus-deficiency tolerance at seedling stage in rice. Acta Agric Boreali sin 28:6–10

    CAS  Google Scholar 

  • Zheng W, Wang Y, Wang L, Ma Z, Zhao J, Wang P, Zhang L, Liu Z, Lu X (2016) Genetic mapping and molecular marker development for Pi65(t), a novel broad-spectrum resistance gene to rice blast using next-generation sequencing. Theor Appl Genet 129:1035–1044

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Kaeppler SM, Lynch JP (2005a) Mapping of QTLs for lateral root branching and length in maize (Zea mays L.) under differential phosphorus supply. Theor Appl Genet 111:688–695

    Article  CAS  PubMed  Google Scholar 

  • Zhu J, Kaeppler SM, Lynch JP (2005b) Mapping of QTL controlling root hair length in maize (Zea mays L.) under phosphorus deficiency. Plant Soil 270:299–310

    Article  CAS  Google Scholar 

  • Zhu J, Mickelson SM, Kaeppler SM, Lynch JP (2006) Detection of quantitative trait loci for seminal root traits in maize (Zea mays L.) seedlings grown under differential phosphorus levels. Theor Appl Genet 113:1–10

    Article  CAS  PubMed  Google Scholar 

  • Zhu C, Bortesi L, Baysal C, Twyman RM, Fischer R, Capell T, Schillberg S, Christou P (2017) Characteristics of genome editing mutations in cereal crops. Trends Plant Sci 22:38–52

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

The authors thank Prof. Sibing Yu for his valuable discussions on the relative traits. We thank two anonymous reviewers for their useful and constructive comments on the manuscript. This research was supported by the National Key R&D Program of China (Grant No. 2017YFD0200200), National Nature Science Foundation of China (Grant No. 31471933, 31672215), Natural and Fundamental Research Funds for the Central Universities of China (Grant No. 2662015PY105) and the Rural and Environment Science and Analytical Services Division (RESAS) of the Scottish Government.

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  1. National Key Laboratory of Crop Genetic Improvement, Huazhong Agricultural University, Wuhan, 430070, China

    Wei Wang, Guang-Da Ding, Xiao-Hua Wang, Ke-Mo Jin, Fang-Sen Xu & Lei Shi

  2. Key Laboratory of Arable Land Conservation (Middle and Lower Reaches of Yangtze River), Ministry of Agriculture, Huazhong Agricultural University, Wuhan, 430070, China

    Wei Wang, Guang-Da Ding, Xiao-Hua Wang, Ke-Mo Jin, Fang-Sen Xu & Lei Shi

  3. The James Hutton Institute, Invergowrie, Dundee, DD2 5DA, UK

    Philip John White

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Wang, W., Ding, GD., White, P.J. et al. Mapping and cloning of quantitative trait loci for phosphorus efficiency in crops: opportunities and challenges. Plant Soil 439, 91–112 (2019). https://doi.org/10.1007/s11104-018-3706-6

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