Journal of Experimental Botany, Vol. 53, No. 366, pp. 39-43,
January 1, 2002
© 2002 Oxford University Press
Short Papers |
The role of long-distance signalling in plant responses to nitrate and other nutrients
Department of Biological Sciences, Lancaster University, Lancaster LA1 4YQ, UK
Received 17 September 2001; Accepted 25 September 2001
Abstract
The phenotypic plasticity that plants display in response to changes in their nutrient supply requires the operation of both short- and long-range signalling pathways. Long-distance signals arising in the root can provide the shoot with an early warning of fluctuations in external nutrient concentrations, while signals in the reverse direction are needed to ensure that root physiology and development are integrated with the nutritional demands of the shoot. In this review, the focus is on recent advances in the understanding of these long-distance signalling pathways with an emphasis on nitrate nutrition, and a personal view of the key issues for future research is put forward.
Key words: Auxin, cytokinins, iron deficiency, lateral roots, nitrate transport, phosphorus deficiency, sulphur deficiency.
Introduction
Plants display a high degree of physiological and developmental plasticity in response to changing nutritional conditions (Clarkson and Lüttge, 1990
; Robinson, 1994; Forde and Lorenzo, 2001). Some nutritional responses are restricted to those roots directly exposed to the nutrient signal: for example, the localized proliferation of lateral roots that occurs in 
or phosphate (Pi)-rich soil patches (Robinson, 1994), and the increased root hair production which is associated with Fe or P deprivation (Bates and Lynch, 1996; Schikora and Schmidt, 2001). However, many other nutritional responses are systemic and must involve the transmission of long-distance signals, usually between the root and the shoot.
Two types of systemic response can be distinguished. One depends on the nutrient status of the whole plant (or specifically the shoot), while the other results from short-term fluctuations in the nutrient supply to the root. An example of the former is the regulation of nutrient transport systems in the root by ‘demand’ from the shoot (Marschner, 1995). Systemic responses of the second kind can provide the shoot with an early warning of changes in nutrient availability. This is seen, for example, in the rapid decline in leaf expansion rates that follows withdrawal of from the roots (McDonald and Davies, 1996).
This article examines the importance of long-distance signalling in plant nutrition and what is known of the processes involved, with an emphasis on nutrition.
Recent advances
Shoot-to-root signalling in the feedback regulation of uptake
The high-affinity uptake system (HATS) in roots is both substrate-inducible and feedback-regulated according to the shoot's demand for N (Clarkson and Lüttge, 1990). Feedback regulation of the NRT2 genes that specify components of the HATS for occurs at least partly at the mRNA level (Forde, 2000; Orsel et al., 2002), and recent studies with split roots of Arabidopsis have confirmed the involvement of long-range signals from the shoot in regulating expression of the AtNRT2-1 gene (Gansel et al., 2001).
It has been proposed that the recycling of amino acids that occurs between the shoot and the root could provide a mechanism for communicating changes in the N status of the shoot (Cooper and Clarkson, 1989; Imsande and Touraine, 1994). However, a study with split-roots of Ricinus communis found that up-regulation of the influx system was not correlated with changes in the amino acid composition of the phloem sap nor with the absolute rates of amino acid transport into the root (Tillard et al., 1998). Nevertheless, it still cannot be ruled out that there are subtle short-term fluctuations in phloem amino acid composition or fluxes to which the NRT2 genes are sensitive.
Shoot-to-root signalling in the developmental response to plant N status
Studies with tobacco have revealed a strong negative correlation between the shoot content and the allocation of resources to root growth and branching (Scheible et al., 1997; Stitt and Feil, 1999). In Arabidopsis the negative effect of the plant's status was specifically on the outgrowth of the laterals (Zhang et al., 1999). Since auxin transported from the shoot is a positive regulator of lateral root development (Reed et al., 1998), it has been tentatively suggested that accumulation in the shoot might negatively regulate root branching by inhibiting auxin biosynthesis or its transport to the root (Forde, 2002).
Sugars as long-distance signals interacting with -regulated processes in roots
Sugars are important signals controlling many aspects of plant metabolism and development (Smeekens, 2000). Nitrate uptake systems are diurnally regulated, with activities generally being highest during the light period and lowest in the dark, and there is evidence that this regulation may be mediated at least in part by sugars (reviewed in Forde, 2002). Lateral root development is also stimulated by sugars, supplied either externally or through the phloem (Bingham et al., 1998; Crookshanks et al., 1998), and an increase in the sucrose concentration in the medium can overcome the inhibitory effect of high concentrations (Zhang et al., 1999). Thus, sugars transported in the phloem may play a significant role as positive regulators of both physiological and developmental responses to the shoot status. Operating in parallel with feedback regulation by the N status of the shoot, this can be seen as providing a mechanism for modulating these responses in accordance with the plant's N/C balance.
The role of cytokinin as a long-distance signal modulating the shoot's response to changes in supply
Some genes expressed in shoots are -inducible only if the is supplied through the roots. Examples are the C4Ppc1 gene for phosphoenolpyruvate (PEP) carboxylase in maize (Sugiharto et al., 1992) and a subgroup of genes belonging to the response regulator family in maize and Arabidopsis (the ZRR and ARR genes, respectively) (Taniguchi et al., 1998; Kiba et al., 1999). Although not inducible if is supplied directly to detached leaves, these genes are rapidly induced by cytokinin treatment (Taniguchi et al., 1998; Kiba et al., 1999). When coupled with the evidence that resupply to N-deprived roots rapidly stimulates cytokinin biosynthesis and transport to the shoot (Samuelson and Larsson, 1993; Walch-Liu et al., 2000; Takei et al., 2001), these observations suggest that cytokinins are long-distance signals mediating the molecular response to changes in availability (Sakakibara et al., 2000; Takei et al., 2001).
Nitrate responses in the shoot also include rapid changes in the rate of leaf expansion: when roots are deprived of , leaf expansion rapidly slows down (McDonald and Davies, 1996). Given the known role of cytokinins as regulators of growth and cell division (D'Agostino and Kieber, 1999), the -dependent changes in cytokinin production in roots could provide a mechanism for regulating leaf expansion in response to short-term fluctuations in availability. The finding that response regulator genes (the ARR/ZRR genes) are also up-regulated by this /cytokinin signalling pathway is of particular interest because response regulators are components of the His-to-Asp phospho-relay signal transduction pathways (Sakakibara et al., 2000). Thus, as discussed previously (Forde, 2002), it is possible that one or more of the cytokinin-inducible ARR/ZRR gene family are components of a signal transduction pathway linking the signal in roots to increased rates of leaf expansion.
Long-distance signals in the regulation of responses to other nutrients
Like the influx system, the uptake systems for other nutrients are regulated by demand from the shoot (Marschner, 1995). This feedback regulation also extends to enzymes involved in nutrient assimilation and the mobilization of nutrients from the rhizosphere (Leustek et al., 2000; Raghothama, 2000; Schmidt and Steinbach, 2000). The role of long-distance signals from the shoot in regulating gene expression in the root has been demonstrated for the responses to deficiencies in phosphorus (Burleigh and Harrison, 1999), iron (Grusak and Pezeshgi, 1996; Li et al., 2000) and sulphur (Lappartient et al., 1999). A remarkable feature of these systemic responses is that each appears to be specific to the nutrient in question, in as far as this has been tested (Martin et al., 2000).
As is the case for the -regulated responses discussed above, clear evidence for how these long-distance signalling pathways operate is largely lacking. The S-metabolite glutathione, transported in the phloem, has been suggested to act as a negative regulator of S starvation-inducible genes in Arabidopsis and Brassica napus (Lappartient et al., 1999). However, later studies in rice and poplar suggest that glutathione concentrations in the phloem sap are quite stable and that the 
to glutathione ratio is more closely correlated with the response to S deprivation (Herschbach et al., 2000; Kuzuhara et al., 2000).
Whereas auxin and sugars have both been discussed above as possible long-range regulators of the root's developmental response to , a recent study has found that the root architectural response to shoot Pi status was independent of the sucrose supply and auxin signalling (Williamson et al., 2001). The lack of correlation between root Pi concentrations and expression of P starvation-inducible genes in split roots and in a mutant (pho1) defective in Pi translocation to the shoot, has been taken as evidence that Pi itself is not the long-distance signal (Burleigh and Harrison, 1999). However, a different conclusion was reached in a later study, where a P starvation-inducible promoter was fused to the GUS reporter gene and its expression studied at the cell level in the wild-type and a pho1 mutant (Martin et al., 2000). Thus it remains plausible that Pi recycling between the shoot and the root (Drew et al., 1984) provides the signal that reports on the Pi status of the shoot.
In an exciting new development the Arabidopsis PHR1 gene, which is part of the systemic response pathway for P starvation, has been shown to encode a MYB transcription factor that is homologous to a P regulatory gene (PSR1) in Chlamydomonas (Rubio et al., 2001). The putative riboregulators encoded by the P starvation-inducible At4/Mt4/AtIPS1 gene family (Burleigh and Harrison, 1999; Martin et al., 2000) may be upstream components of the same systemic response pathway.
Studies of the Fe starvation-induced expression of Fe(III) reductase in pea roots led to the conclusion that the shoot-derived signal is not Fe itself (Grusak and Pezeshgi, 1996). Shoot-derived auxin is a candidate for a positive regulatory signal for Fe(III) reductase in Phaseolus vulgaris L. (Li et al., 2000), but the same study failed to find evidence for auxin regulation of Fe(III) reductase in cucumber. In Arabidopsis, hormone signalling does not appear to be involved in the regulation of Fe(III) reductase (Schmidt et al., 2000).
Issues for the future
Table 1 summarizes the current picture of long-distance signalling pathways in higher plants. One of the key questions about these long-distance signalling pathways concerns the nature of the inter-organ signals. From the discussion above it can be seen that the nutrients themselves, their assimilation products and phytohormones have all been implicated. Novel signal molecules transported in the phloem such as peptides and ribonucleoprotein complexes might also be involved (Lucas, 1997; Xoconostle-Cazares et al., 2000). One pre-requisite for further progress in this area will be improved techniques for accurately monitoring changes in phloem sap composition, possibly by extending the use of sap-feeding aphids beyond the few plant species in which this is currently possible, as discussed previously (Forde and Clarkson, 1999). This might be combined with improved microanalytical methods currently being applied to solutes sampled from individual plant cells (Tomos and Sharrock, 2001).
|
Novel screens to identify nutrient signalling mutants in Arabidopsis, similar to those that have already yielded lesions in the P starvation response (Chen et al., 2000
; Rubio et al., 2001; Zakhleniuk et al., 2001) will be of enormous value in elucidating the signalling pathways. It is expected that the sequencing of the Arabidopsis genome and the use of microarrays to monitor global changes in gene expression, combined with reverse genetics, will further accelerate progress in this area. Given the extensive interactions and crosstalk known to occur between signalling pathways (Genoud and Métraux, 1999), it should also be profitable to test the nutrient-responsiveness of signalling mutants isolated in other screening programmes.
Concluding remarks
The homology between phosphate regulatory genes from higher plants and algae (Martin et al., 2000), and the conservation of the PII nitrogen regulatory gene between plants and prokaryotes (Hsieh et al., 1998), indicate that nutrient regulatory pathways in plants have ancient origins. However the need for long-distance signalling pathways of the kind considered here would presumably only have arisen with the evolution of vascular plants. The finding that a homologue of the Chlamydomonas PSR1 phosphate response gene is part of the systemic P response pathway in Arabidopsis (Martin et al., 2000) suggests that long-range signalling systems may have been superimposed on existing intracellular signal transduction pathways.
Acknowledgments
Work in the author's laboratory is supported by the Biotechnology and Biological Research Council and by Norsk Hydro ASA.
Notes
1 Fax: +44 (0)1524843854. E-mail: b.g.forde{at}lancaster.ac.uk 
References
Bates TR, Lynch JP. 1996. Stimulation of root hair elongation in Arabidopsis thaliana by low phosphorus availability. Plant Cell and Environment 19, 529–538.
Bingham IJ, Blackwood JM, Stevenson EA. 1998. Relationship between tissue sugar content, phloem import and lateral root initiation in wheat. Physiologia Plantarum 103, 107–113.
Burleigh SH, Harrison MJ. 1999. The down-regulation of Mt4-like genes by phosphate fertilization occurs systemically and involves phosphate translocation to the shoots. Plant Physiology 119, 241–248.
Chen DL, Delatorre CA, Bakker A, Abel S. 2000. Conditional identification of phosphate-starvation-response mutants in Arabidopsis thaliana. Planta 211, 13–22.[Web of Science][Medline]
Clarkson DT, Lüttge U. 1990. Mineral nutrition: inducible and repressible nutrient transport systems. Progress in Botany 52, 61–83.
Cooper HD, Clarkson DT. 1989. Cycling of amino nitrogen and other nutrients between shoots and roots in cereals: a possible mechanism integrating shoot and root in the regulation of nutrient uptake. Journal of Experimental Botany 40, 753–762.
Crookshanks M, Taylor G, Dolan L. 1998. A model system to study the effects of elevated CO2 on the developmental physiology of roots: the use of Arabidopsis thaliana. Journal of Experimental Botany 49, 593–597.
D'Agostino IB, Kieber JJ. 1999. Molecular mechanisms of cytokinin action. Current Opinion in Plant Biology 2, 359–364.[Web of Science][Medline]
Drew MC, Saker LR, Barber SA, Jenkins W. 1984. Changes in the kinetics of phosphate and potassium absorption in nutrient-deficient barley roots measured by a solution-depletion technique. Planta 160, 490–499.
Forde BG, Lorenzo H. 2001. The nutritional control of root development. Plant and Soil 232, 51–68.[Web of Science]
Forde BG. 2000. Nitrate transporters in plants: structure, function and regulation. Biochimica et Biophysica Acta 1465, 219–235.[Medline]
Forde BG. 2002. Local and long-range signaling pathways regulating plant responses to nitrate. Annual Review of Plant Physiology and Plant Molecular Biology (in press).
Forde BG, Clarkson DT. 1999. Nitrate and ammonium nutrition of plants: physiological and molecular perspectives. Advances in Botanical Research 30, 1–90.
Gansel X, Munos S, Tillard P, Gojon A. 2001. Differential regulation of the and 
transporter genes AtNrt2 1 and AtAmt1 1 in Arabidopsis: relation with long-distance and local controls by N status of the plant. The Plant Journal 26, 143–155.[Web of Science][Medline]
Genoud T, Métraux J-P. 1999. Crosstalk in plant cell signaling: structure and function of the genetic network. Trends in Plant Science 4, 503–507.[Web of Science][Medline]
Grusak MA, Pezeshgi S. 1996. Shoot-to-root signal transmission regulates root Fe(III) reductase activity in the dgl mutant of pea. Plant Physiology 110, 329–334.[Abstract]
Herschbach C, van der Zalm E, Schneider A, Jouanin L, De Kok LJ, Rennenberg H. 2000. Regulation of sulfur nutrition in wild-type and transgenic poplar over-expressing gamma-glutamylcysteine synthetase in the cytosol as affected by atmospheric H2S. Plant Physiology 124, 461–473.
Hsieh M-H, Lam H-M, Van De Loo FJ, Coruzzi G. 1998. A PII-like protein in Arabidopsis: putative role in nitrogen sensing. Proceedings of the National Academy of Sciences, USA 95, 13965–13970.
Imsande J, Touraine B. 1994. N demand and the regulation of nitrate uptake. Plant Physiology 105, 3–7.[Web of Science][Medline]
Kiba T, Taniguchi M, Imamura A, Ueguchi C, Mizuno T, Sugiyama T. 1999. Differential expression of genes for response regulators in response to cytokinins and nitrate in Arabidopsis thaliana. Plant and Cell Physiology 40, 767–771.
Kuzuhara Y, Isobe A, Awazuhara M, Fujiwara T, Hayashi H. 2000. Glutathione levels in phloem sap of rice plants under sulfur-deficient conditions. Soil Science and Plant Nutrition 46, 265–270.
Lappartient AG, Vidmar JJ, Leustek T, Glass ADM, Touraine B. 1999. Inter-organ signaling in plants: regulation of ATP sulfurylase and sulfate transporter genes expression in roots mediated by phloem-translocated compound. The Plant Journal 18, 89–95.[Web of Science][Medline]
Leustek T, Martin MN, Bick JA, Davies JP. 2000. Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annual Review of Plant Physiology and Plant Molecular Biology 51, 141–165.[Web of Science]
Li CJ, Zhu XP, Zhang FS. 2000. Role of shoot in regulation of iron deficiency responses in cucumber and bean plants. Journal of Plant Nutrition 23, 1809–1818.
Lucas WJ. 1997. Application of microinjection techniques to plant nutrition. Plant and Soil 196, 175–189.
Marschner H. 1995. Mineral nutrition of higher plants. London: Academic Press.
Martin AC, del Pozo JC, Iglesias J, Rubio V, Solano R, de la Pena A, Leyva A, Paz-Ares J. 2000. Influence of cytokinins on the expression of phosphate starvation responsive genes in Arabidopsis. The Plant Journal 24, 559–567.[Web of Science][Medline]
McDonald AJS, Davies WJ. 1996. Keeping in touch: responses of the whole plant to deficits in water and nitrogen supply. Advances in Botanical Research 22, 229–300.
Orsel M, Filleur S, Fraisier V, Daniel-Vedele F. 2002. Nitrate transport in plants: which gene and which control? Journal of Experimental Botany 53, (in press).
Raghothama KG. 2000. Phosphate transport and signaling. Current Opinion in Plant Biology 3, 182–187.[Web of Science][Medline]
Reed RC, Brady SR, Muday GK. 1998. Inhibition of auxin movement from the shoot into the root inhibits lateral root development in Arabidopsis. Plant Physiology 118, 1369–1378.
Robinson D. 1994. The responses of plants to non-uniform supplies of nutrients. New Phytologist 127, 635–674.[Web of Science]
Rubio V, Linhares F, Solano R, Martin AC, Iglesias J, Leyva A, Paz-Ares J. 2001. A conserved MYB transcription factor involved in phosphate-starvation signaling both in vascular plants and in unicellular algae. Genes and Development 15, 2122–2133.
Sakakibara H, Taniguchi M, Sugiyama T. 2000. His-Asp phosphorelay signaling: a communication avenue between plants and their environment. Plant Molecular Biology 42, 273–278.[Web of Science][Medline]
Samuelson ME, Larsson CM. 1993. Nitrate regulation of zeatin riboside levels in barley roots: effects of inhibitors of N-assimilation and comparison with ammonium. Plant Science 93, 77–84.
Scheible WR, Lauerer M, Schulze ED, Caboche M, Stitt M. 1997. Accumulation of nitrate in the shoot acts as a signal to regulate shoot–root allocation in tobacco. The Plant Journal 11, 671–691.
Schikora A, Schmidt W. 2001. Iron stress-induced changes in root epidermal cell fate are regulated independently from physiological responses to low iron availability. Plant Physiology 125, 1679–1687.
Schmidt W, Steinbach S. 2000. Sensing iron—a whole plant approach. Annals of Botany 86, 589–593.
Schmidt W, Tittel J, Schikora A. 2000. Role of hormones in the induction of iron deficiency responses in Arabidopsis roots. Plant Physiology 122, 1109–1118.
Smeekens S. 2000. Sugar-induced signal transduction in plants. Annual Review of Plant Physiology and Plant Molecular Biology 51, 49–81.[Web of Science]
Stitt M, Feil R. 1999. Lateral root frequency decreases when nitrate accumulates in tobacco transformants with low nitrate reductase activity: consequences for the regulation of biomass partitioning between shoots and root. Plant and Soil 215, 143–153.
Sugiharto B, Burnell JN, Sugiyama T. 1992. Cytokinin is required to induce the nitrogen-dependent accumulation of messenger-RNAs for phosphoenolpyruvate carboxylase and carbonic anhydrase in detached maize leaves. Plant Physiology 100, 153–156.
Takei K, Sakakibara H, Taniguchi M, Sugiyama T. 2001. Nitrogen-dependent accumulation of cytokinins in root and the translocation to leaf: implication of cytokinin species that induces gene expression of maize response regulator. Plant and Cell Physiology 42, 85–93.
Taniguchi M, Kiba T, Sakakibara H, Ueguchi C, Mizuno T, Sugiyama T. 1998. Expression of Arabidopsis response regulator homologs is induced by cytokinins and nitrate. FEBS Letters 429, 259–262.[Web of Science][Medline]
Tillard P, Passama L, Gojon A. 1998. Are phloem amino acids involved in the shoot to root control of uptake in Ricinus communis plants? Journal of Experimental Botany 49, 1371–1379.
Tomos AD, Sharrock RA. 2001. Cell sampling and analysis (SiCSA): metabolites measured at single cell resolution. Journal of Experimental Botany 52, 623–630.
Walch-Liu P, Neumann G, Bangerth F, Engels C. 2000. Rapid effects of nitrogen form on leaf morphogenesis in tobacco. Journal of Experimental Botany 51, 227–237.
Williamson LC, Ribrioux S, Fitter AH, Leyser HMO. 2001. Phosphate availability regulates root system architecture in Arabidopsis. Plant Physiology 126, 875–882.
Xoconostle-Cazares B, Ruiz-Medrano R, Lucas WJ. 2000. Proteolytic processing of CmPP36, a protein from the cytochrome b5reductase family, is required for entry into the phloem translocation pathway. The Plant Journal 24, 735–747.[Web of Science][Medline]
Zakhleniuk OV, Raines CA, Lloyd JC. 2001. pho3: a phosphorus-deficient mutant of Arabidopsis thaliana (L.) Heynh. Planta 212, 529–534.[Web of Science][Medline]
Zhang HM, Jennings A, Barlow PW, Forde BG. 1999. Dual pathways for regulation of root branching by nitrate. Proceedings of the National Academy of Sciences, USA 96, 6529–6534.
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  S.-I Lin, S.-F. Chiang, W.-Y. Lin, J.-W. Chen, C.-Y. Tseng, P.-C. Wu, and T.-J. Chiou Regulatory Network of MicroRNA399 and PHO2 by Systemic Signaling Plant Physiology, June 1, 2008; 147(2): 732 - 746. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. Ruffel, S. Freixes, S. Balzergue, P. Tillard, C. Jeudy, M. L. Martin-Magniette, M. J. van der Merwe, K. Kakar, J. Gouzy, A. R. Fernie, et al. Systemic Signaling of the Plant Nitrogen Status Triggers Specific Transcriptome Responses Depending on the Nitrogen Source in Medicago truncatula Plant Physiology, April 1, 2008; 146(4): 2020 - 2035. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Zhang, H. Rong, and D. Pilbeam Signalling mechanisms underlying the morphological responses of the root system to nitrogen in Arabidopsis thaliana J. Exp. Bot., July 1, 2007; 58(9): 2329 - 2338. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Jain, M. D. Poling, A. S. Karthikeyan, J. J. Blakeslee, W. A. Peer, B. Titapiwatanakun, A. S. Murphy, and K. G. Raghothama Differential Effects of Sucrose and Auxin on Localized Phosphate Deficiency-Induced Modulation of Different Traits of Root System Architecture in Arabidopsis Plant Physiology, May 1, 2007; 144(1): 232 - 247. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. J. BLOOM, J. FRENSCH, and A. R. TAYLOR Influence of Inorganic Nitrogen and pH on the Elongation of Maize Seminal Roots Ann. Bot., May 1, 2006; 97(5): 867 - 873. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. C. Dodd and C. A. Beveridge Xylem-borne cytokinins: still in search of a role? J. Exp. Bot., January 1, 2006; 57(1): 1 - 4. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. He, M. Osaki, M. Takebe, T. Shinano, and J. Wasaki Endogenous hormones and expression of senescence-related genes in different senescent types of maize J. Exp. Bot., April 1, 2005; 56(414): 1117 - 1128. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Lemaire, J-C. Avice, T-H. Kim, and A. Ourry Developmental changes in shoot N dynamics of lucerne (Medicago sativa L.) in relation to leaf growth dynamics as a function of plant density and hierarchical position within the canopy J. Exp. Bot., March 1, 2005; 56(413): 935 - 943. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. R. Kinghorn, J. Sloan, G. J. M. Kana'n, E. R. DaSilva, D. A. Rouch, and S. E. Unkles Missense Mutations That Inactivate the Aspergillus nidulans nrtA Gene Encoding a High-Affinity Nitrate Transporter Genetics, March 1, 2005; 169(3): 1369 - 1377. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 K. Takei, N. Ueda, K. Aoki, T. Kuromori, T. Hirayama, K. Shinozaki, T. Yamaya, and H. Sakakibara AtIPT3 is a Key Determinant of Nitrate-Dependent Cytokinin Biosynthesis in Arabidopsis Plant Cell Physiol., August 15, 2004; 45(8): 1053 - 1062. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Loque and N. von Wiren Regulatory levels for the transport of ammonium in plant roots J. Exp. Bot., June 1, 2004; 55(401): 1293 - 1305. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. H. Macduff and A. K. Bakken Diurnal variation in uptake and xylem contents of inorganic and assimilated N under continuous and interrupted N supply to Phleum pratense and Festuca pratensis J. Exp. Bot., January 2, 2003; 54(381): 431 - 444. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. A. Kreps, Y. Wu, H.-S. Chang, T. Zhu, X. Wang, and J. F. Harper Transcriptome Changes for Arabidopsis in Response to Salt, Osmotic, and Cold Stress Plant Physiology, December 1, 2002; 130(4): 2129 - 2141. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y.-H. Wang, D. F. Garvin, and L. V. Kochian Rapid Induction of Regulatory and Transporter Genes in Response to Phosphorus, Potassium, and Iron Deficiencies in Tomato Roots. Evidence for Cross Talk and Root/Rhizosphere-Mediated Signals Plant Physiology, November 1, 2002; 130(3): 1361 - 1370. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||