Abstract
The Pup1 locus confers tolerance to phosphorus (P) deficiency in rice (Oryza sativa L.). Transferring the Pup1 locus to an intolerant genotype increased P uptake by a factor 3 to 4. Lines with the Pup1 locus maintained higher root growth rates under P deficiency, but only as they started to diverge from intolerant lines in P uptake. It was thus not possible to determine if differences in root growth preceded and caused differences in P uptake or whether high root growth was the result of higher external P uptake efficiency (P influx per root size). The purpose of this paper is to review experimental evidence on the effect of Pup1 in light of recent results in modelling cause-and-effect relations between root growth, external efficiency and P uptake. Model simulations suggested that only very small changes in factors enhancing root growth were needed to explain the effect of Pup1 on P uptake. A 22% increase in root fineness or in internal P utilization efficiency (root dry matter per root P) was sufficient to triple P uptake . External root efficiency had to increase by 33 to account for the effect of Pup1. However, the most noticeable effect of increases in external efficiency was a subsequent stimulation of root growth that contributed eight times more to final P uptake compared to the change in external efficiency. Comparisons of model simulations with empirical data suggested that measured differences in external efficiency between Nipponbare and NIL-Pup1 were sufficiently large to account for the increase in P uptake. A segregation analysis using several pairs of contrasting NILs (at the Pup1 locus) further confirmed this as Pup1 co-segregated with external efficiency but not with seedling root growth or internal efficiency.
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References
N Ae J Arihara K Okada T Yoshihara C Johansen (1990) ArticleTitlePhosphorus uptake by pigeon pea and its role in cropping systems of the Indian subcontinent Science 248 477–480 Occurrence Handle1:CAS:528:DyaK3cXkslOitbw%3D
A Dobermann K G Cassman C P Mamaril J E Sheehy (1998) ArticleTitleManagement of phosphorus, potassium, and sulfur in intensive, irrigated lowland rice Field Crops Res. 56 113–138 Occurrence Handle10.1016/S0378-4290(97)00124-X
J M Franco-Zorrilla E Gonzalez R Bustos F Linhares A Leyva J Paz-Ares (2004) ArticleTitleThe transcriptional control of plant responses to phosphate limitation J. Exp. Bot. 55 285–293 Occurrence Handle10.1093/jxb/erh009 Occurrence Handle1:CAS:528:DC%2BD2cXms1eguw%3D%3D Occurrence Handle14718495
T Gahoonia N Claassen A Jungk (1992) ArticleTitleMobilization of residual phosphate of different phosphate fertilizers in relation to pH in the rhizosphere of ryegrass Fertilizer Res. 33 229–237 Occurrence Handle1:CAS:528:DyaK3sXksVynu74%3D
J P Hammond M J Bennett H C Bowen M R Broadley D C Eastwood S T May C Rahn R Swarup K E Woolaway P J White (2003) ArticleTitleChanges in gene expression in Arabidopsis shoots during phosphate starvation and the potential for developing smart plants Plant Physiol. 132 578–596 Occurrence Handle10.1104/pp.103.020941 Occurrence Handle1:CAS:528:DC%2BD3sXkslersbo%3D Occurrence Handle12805589
W J Horst M Kamh J M Jibrin V O Chude (2001) ArticleTitleAgronomic measures for increasing P availability to crops Plant Soil 237 211–223 Occurrence Handle10.1023/A:1013353610570 Occurrence Handle1:CAS:528:DC%2BD38XovVWltw%3D%3D
G J D Kirk T George B Courtois D Senadhira (1998) ArticleTitleOpportunities to improve phosphorus efficiency and soil fertility in rainfed lowland and upland rice ecosystems Field Crops Res. 56 73–92 Occurrence Handle10.1016/S0378-4290(97)00141-X
G J D Kirk E E Santos G R Findenegg (1999a) ArticleTitlePhosphate solubilization by organic anion excretion from rice (Oryza sativa L.) growing in aerobic soil Plant Soil 211 11–18 Occurrence Handle10.1023/A:1004539212083 Occurrence Handle1:CAS:528:DyaK1MXnt1Krtrk%3D
G J D Kirk E E Santos M B Santos (1999) ArticleTitlePhosphate solubilization by organic anion excretion from rice growing in aerobic soil: rates of excretion and decomposition, effects on rhizosphere pH and effects on phosphate solubility and uptake New Phytol. 142 185–200 Occurrence Handle10.1046/j.1469-8137.1999.00400.x Occurrence Handle1:CAS:528:DyaK1MXkslOmsr8%3D
H Koyama E Takita A Kawamura T Hara D Shibata (1999) ArticleTitleOver expression of mitochondrial citrate synthase gene improves the growth of carrot cells in Al-phosphate medium Plant Cell Physiol. 40 482–488 Occurrence Handle1:CAS:528:DyaK1MXjsVOit7o%3D Occurrence Handle10427772
J Lopez-Bucio E Hernandez-Abreu L Sanchez-Calderon M F Nieto-Jacobo J Simpson L Herrera-Estrella (2002) ArticleTitlePhosphate availability alters architecture and causes changes in hormone sensitivity in the Arabidopsis root system Plant Physiol. 129 244–256 Occurrence Handle10.1104/pp.010934 Occurrence Handle1:CAS:528:DC%2BD38XjvFSmsro%3D Occurrence Handle12011355
J P Lynch K M Brown (2001) ArticleTitleTopsoil foraging – An architectural adaptation of plants to low phosphorus availability Plant Soil 237 225–237 Occurrence Handle10.1023/A:1013324727040 Occurrence Handle1:CAS:528:DC%2BD38XovVWltA%3D%3D
Z Ma D G Bielenberg K M Brown J P Lynch (2001) ArticleTitleRegulation of root hair density by phosphorus availability in Arabidopsis thaliana Plant Cell Environ. 24 459–467 Occurrence Handle10.1046/j.1365-3040.2001.00695.x Occurrence Handle1:CAS:528:DC%2BD3MXjtFyjtb0%3D
J F Ma R Shen Z Zhao M Wissuwa Y Takeuchi T Ebitani M Yano (2002) ArticleTitleResponse of rice to Al stress and identification of quantitative trait loci for Al tolerance Plant Cell Physiol. 43 652–659 Occurrence Handle10.1093/pcp/pcf081 Occurrence Handle1:CAS:528:DC%2BD38XkvVChtLw%3D Occurrence Handle12091719
S S Miller J Liu D L Allan C J Menzhuber M Fedorova C P Vance (2001) ArticleTitleMolecular control of acid phosphatase secretion into the rhizosphere of proteoid roots from phosphorus-stressed white lupin Plant Physiol. 127 594–606 Occurrence Handle10.1104/pp.127.2.594 Occurrence Handle1:CAS:528:DC%2BD3MXnslGlurY%3D Occurrence Handle11598233
N Mitsukawa S Okumura Y Shirano S Sato T Kato S Harashimi D Shibata (1997) ArticleTitleOverexpression of an Arabidopsis thaliana high-affinity phosphate transporter gene in tobacco cultured cells enhances cell growth under phosphate-limited conditions Proc. Nat. Acad. Sci. USA 94 7098–7102 Occurrence Handle10.1073/pnas.94.13.7098 Occurrence Handle1:CAS:528:DyaK2sXktF2qsbo%3D Occurrence Handle9192698
G Neumann V Romheld (1999) ArticleTitleRoot excretion of carboxylic acids and protons in phosphorus-deficient plants Plant Soil 211 121–130 Occurrence Handle10.1023/A:1004380832118 Occurrence Handle1:CAS:528:DyaK1MXnt1Kqsr4%3D
T Otani N Ae (1996) ArticleTitleSensitivity of phosphorus uptake to changes in root length and soil volume Agron. J. 88 371–375
A L Rae J M Jarmey S R Mudge F W Smith (2004) ArticleTitleOver-expression of a high-affinity phosphate transporter in transgenic barley plants does not enhance phosphate uptake rates Funct. Plant Biol. 31 141–148 Occurrence Handle10.1071/FP03159 Occurrence Handle1:CAS:528:DC%2BD2cXhsl2gtro%3D
K G Raghothama (2000) ArticleTitlePhosphate transport and signaling Curr. Opin. Plant Biol. 3 182–187 Occurrence Handle1:CAS:528:DC%2BD3cXktVOnsrw%3D Occurrence Handle10837272
A E Richardson P A Hadobas J E Hayes (2001) ArticleTitleExtracellular secretion of Aspergillus phytase from Arabidopsis roots enables plants to obtain phosphorus from phytate Plant J. 25 641–649 Occurrence Handle10.1046/j.1365-313x.2001.00998.x Occurrence Handle1:CAS:528:DC%2BD3MXjvVOisro%3D Occurrence Handle11319031
G Rubio H Liao X Yan J P Lynch (2003) ArticleTitleTopsoil foraging and its role in plant competitiveness for phosphorus in common bean Crop Sci. 43 598–607
M A Saleque G J D Kirk (1995) ArticleTitleRoot-induced solubilization of phosphate in the rhizosphere of lowland rice New Phytol. 129 325–336 Occurrence Handle1:CAS:528:DyaK2MXltlamu74%3D
M Silberbush S A Barber (1983) ArticleTitleSensitivity of simulated phosphorus uptake to parameters used by a mechanistic-mathematical model Plant Soil 74 93–100 Occurrence Handle10.1007/BF02178744 Occurrence Handle1:CAS:528:DyaL2cXit1SrsA%3D%3D
F W Smith S R Mudge A L Rae D Glassop (2003) ArticleTitlePhosphate transport in plants Plant Soil 248 71–83 Occurrence Handle10.1023/A:1022376332180 Occurrence Handle1:CAS:528:DC%2BD3sXhtFCqs74%3D
S E Smith D J Read (1997) Mycorrhizal Symbiosis Academic Press San Diego.
Y H Teo C A Beyrouty E E Gbur (1992) ArticleTitleEvaluating a model for predicting nutrient uptake by rice during vegetative growth Agron J. 84 1064–1070 Occurrence Handle1:CAS:528:DyaK3sXhvFSks7k%3D
C P Vance C Uhde-Stone D L Allan (2003) ArticleTitlePhosphorus acquisition and use: Critical adaptations by plants for securing a nonrenewable resource New Phytol. 157 423–447 Occurrence Handle10.1046/j.1469-8137.2003.00695.x Occurrence Handle1:CAS:528:DC%2BD3sXisF2gu70%3D
J Wasaki T Yamamura T Shinano M Osaki (2003a) ArticleTitleSecreted acid phosphatase is expressed in cluster roots of lupin in response to phosphorus deficiency Plant Soil 248 129–136 Occurrence Handle10.1023/A:1022332320384 Occurrence Handle1:CAS:528:DC%2BD3sXhtFCru7c%3D
J Wasaki R Yonetani S Kuroda T Shinano J Yazaki F Fujii K Shimbo K Yamamoto K Sakata T Sasaki (2003b) ArticleTitleTranscriptomic analysis of metabolic changes by phosphorus stress in rice plant roots Plant Cell Environ. 26 1515–1523 Occurrence Handle10.1046/j.1365-3040.2003.01074.x Occurrence Handle1:CAS:528:DC%2BD3sXotFyqsr8%3D
M Wissuwa (2003) ArticleTitleHow do plants achieve tolerance to phosphorus deficiency – Small causes with big effects Plant Physiol. 133 1947–1958 Occurrence Handle10.1104/pp.103.029306 Occurrence Handle1:CAS:528:DC%2BD2cXhvFKn Occurrence Handle14605228
M Wissuwa N Ae (2001a) ArticleTitleFurther characterization of two QTLs that increase phosphorus uptake of rice (Oryza sativa L.) under phosphorus deficiency Plant Soil 237 275–286 Occurrence Handle10.1023/A:1013385620875 Occurrence Handle1:CAS:528:DC%2BD38XovVWksw%3D%3D
M Wissuwa N Ae (2001b) ArticleTitleGenotypic variation for tolerance to phosphorus deficiency in rice and the potential for its exploitation in rice improvement Plant Breed. 120 43–48 Occurrence Handle10.1046/j.1439-0523.2001.00561.x Occurrence Handle1:CAS:528:DC%2BD3MXitleqsbs%3D
M Wissuwa J Wegner N Ae M Yano (2002) ArticleTitleSubstitution mapping of Pup1: A major QTL increasing phosphorus uptake of rice from a phosphorus-deficient soil Theor. Appl. Genet. 105 890–897 Occurrence Handle1:CAS:528:DC%2BD38XosVCntLs%3D Occurrence Handle12582914
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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, 57–68 (2005). https://doi.org/10.1007/s11104-004-2026-1
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DOI: https://doi.org/10.1007/s11104-004-2026-1