Combining a modelling with a genetic approach in establishing associations between genetic and physiological effects in relation to phosphorus uptake

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.

Stress Response Versus Stress Tolerance: A Transcriptome Analysis of Two Rice Lines Contrasting in Tolerance to Phosphorus Deficiency

“…This release is mediated by specific efflux transporters, and their level of activity was shown to be directly linked to malate or citratemediated tolerance to excess aluminum (Delhaize et al 2004;Magalhaes et al 2007). However, putative efflux transporters were not among the root-specific genes differentially expressed between genotypes, corroborating earlier results that neither genotype exuded citrate or malate at high enough concentrations to have a significant effect on P solubilization (Wissuwa 2005).…”

“…The higher expression for many root cell- Only genes with informative annotation and that are "present" in at least one tissue are shown a Localized within Kasalath introgressions present on chromosomes 1, 7, 10, and 12 (Torabi et al 2009) b Genes present in shoot and root Only genes with informative annotation and that are "present" in at least one tissue are shown a Localized within Kasalath introgressions present on chromosomes 1, 7, 10, and 12 (Torabi et al 2009) b Genes present in shoot and root wall-associated genes would support our third hypothesis that tolerance to P deficiency in NIL6-4 is due to modifications in root growth that maximize Pi interception. This is further corroborated by phenotypic data showing that the most consistent difference between Nipponbare and NIL6-4 is a far more pronounced reduction in root biomass and surface area due to P deficiency in Nipponbare (Wissuwa and Ae 2001b;Wissuwa 2005). Presumably, the increased P uptake by NIL6-4 under P-deficient conditions allowed further root growth compared to Nipponbare: however, under P-replete conditions, both genotypes acquire sufficient P for unrestricted root growth, and hence root biomass did not differ between genotypes.…”

“…However, we cannot conclude that this observation assigns a critical role to these transporters in stress tolerance because expression levels in our tolerant line NIL6-4 were consistently lower than in Nipponbare. That transporter activity (in addition to transcript level) was indeed not limiting in Nipponbare could be deduced from P depletion experiments showing that Nipponbare is capable of depleting Pi from nutrient solutions as rapidly and to an equally low level (0.16 µM P) as a Pup1-NIL (Wissuwa 2005). Similarly, barley lines overexpressing a Pi transporter did not show improved tolerance to P deficiency (Rae et al 2004), most likely because substrate (Pi) availability rather than transporter activity is the limiting step in P-deficient soils.…”

“…Considerable genotypic variation in the ability to acquire P under P-deficient field conditions was observed in rice (Fageria and Baligar 1997;Wissuwa and Ae 2001a), and a major QTL for P deficiency tolerance, Pup1 for P-uptake 1, was fine-mapped to a region between 15.1 and 15.6 Mb on chromosome 12 (Wissuwa et al 2002). Near-isogenic lines (NILs) carrying the Pup1 allele from tolerant donor parent "Kasalath" consistently showed up to fourfold higher P uptake, dry weight, and grain yield compared to the intolerant recurrent parent "Nipponbare" (Wissuwa and Ae 2001b;Wissuwa 2005). Because P deficiency is a major problem in upland or drought-prone rain-fed lowland (nonirrigated) systems, previous studies (Wissuwa and Ae 2001b;Wissuwa 2005) and the study presented here were conducted under "upland" conditions.…”

“…Near-isogenic lines (NILs) carrying the Pup1 allele from tolerant donor parent "Kasalath" consistently showed up to fourfold higher P uptake, dry weight, and grain yield compared to the intolerant recurrent parent "Nipponbare" (Wissuwa and Ae 2001b;Wissuwa 2005). Because P deficiency is a major problem in upland or drought-prone rain-fed lowland (nonirrigated) systems, previous studies (Wissuwa and Ae 2001b;Wissuwa 2005) and the study presented here were conducted under "upland" conditions. While the intolerant donor parent "Nipponbare" is a lowland cultivar, NIL6-4 is near identical; hence, studies under upland conditions characterize the response of the Pup1 locus in typical droughtprone environments.…”