- Email: [email protected]
Nitrate Contra Auxin: Nutrient Sensing by Roots
Developmental Cell
Previews Nitrate Contra Auxin: Nutrient Sensing by Roots Tom Beeckman1,2 and Jirˇı´ Friml1,2,3,* 1Department
of Plant Systems Biology, VIB, 9052 Gent, Belgium of Plant Biotechnology and Genetics, Ghent University, 9052 Gent, Belgium 3Division of Functional Genomics and Proteomics, Department of Experimental Biology, Masaryk University, 62500 Brno, Czech Republic *Correspondence: [email protected] DOI 10.1016/j.devcel.2010.05.020 2Department
In a new study published in this issue of Developmental Cell, Krouk et al. reveal a surprising mechanism by which plant root systems adapt their architecture for soil exploitation. The dual transporter NRT1.1 uses both nitrate and the plant hormone auxin as substrates, enabling soil nitrate availability to regulate auxin-driven lateral root development.
The sessile life style of plants makes them vulnerable to changing environmental conditions and, in contrast to animals, prevents them from moving to more favorable habitats. Uptake of water and nutrients from the soil is controlled by the root system, in which many lateral roots covered with numerous root hairs branch off from the main axes. Roots are capable of responding to local soil conditions, mainly by proliferating in enriched soil patches by the development of extra lateral roots. This phenomenon has been designated as foraging behavior and represents, to a certain extent, a compensation for the lack of mobility. The high level of root plasticity has fascinated numerous plant scientists over the years because it determines the efficiency with which plants compete with their neighbors and other organisms for the use of limited mineral resources. Obviously, foraging behavior implies the deployment of nutrient sensors in the root that translate the external nutrient conditions into appropriate growth responses. Up to date, molecular data demystifying the mechanisms of these adaptive responses in plants are largely missing. The main nitrogen source for plant nutrition is nitrate (NO3 ) and studies with the plant model Arabidopsis thaliana have shown that nitrate-rich soil patches induce new lateral root development (Zhang and Forde, 1998). This proliferation occurs by stimulating the elongation of preformed lateral root primordia and appears not to be a nutritional effect due to improved nitrogen assimilation, but rather to result from the action of a specific nitrate signaling pathway. In Arabidopsis
thaliana, this nitrate signaling pathway had been shown to require the same protein that also mediates nitrate uptake itself, namely the plasma membrane NITRATE TRANSPORTER1;1 (NRT1.1) (Remans et al. (2006)). Indeed, loss-offunction mutants of NRT1.1 are seriously affected in their ability to colonize nitraterich zones. However, it has remained unclear how a nitrate transporter would couple to a signaling pathway controlling root development. Now, Krouk et al. (2010) in this issue of Developmental Cell link the nutrientsensing capacity of NRT1.1 to the regulation of the distribution of the plant hormone auxin (Vanneste and Friml, 2009), which, among other effects, controls the formation and outgrowth of lateral roots. Formation of lateral roots is characterized by several consecutive developmental steps; each of them is subjected to hormonal control, in which auxin plays a dominant role (Benkova´ et al., 2003; Dubrovsky et al., 2008; Pe´ret et al., 2009). After the initiation from pericycle cells inside the main root, a lateral root primordium is generated following a regular division pattern. The further growth of the primordium involves separation of the overlying tissue layers as the primordium forces its way to the root surface prior to its emergence from the parent root (Swarup et al., 2008). Various studies have shown the existence of a developmental checkpoint at this step, because unfavorable growth conditions will stop the primordium outgrowth (De Smet et al., 2006). One of the endogenous factors controlling this checkpoint is auxin that accumulates at the tip of the primordium,
thus regulating the unidirectional cell expansion (Benkova et al., 2003) that ultimately leads to the outgrowth of the lateral root into the surrounding rhizosphere. It is this regulated elongation that represents the driving force for the foraging behavior of the root system and that mediates growth into nitraterich soil patches. Mutant phenotypes revealed that under low nitrate conditions, NRT1.1dependent signaling inhibits and at high nitrate concentrations stimulates the outgrowth of lateral roots. Krouk et al. (2010) quite unexpectedly accounted for this observation by finding that NRT1.1 functions as a dual uptake transporter for both nitrate and auxin (Figure 1). The two substrates seem to compete for NRT1.1 transport activity, meaning that at low nitrate concentrations, the NRT1.1 capacity to transport auxin is high, whereas at high nitrate concentrations, the auxin uptake into cells is low. Localization studies demonstrated the presence of NRT1.1 at the anticlinal membranes of the primordium epidermis cells, where NRT1.1 is perfectly positioned to regulate the auxin flow away from the primordium tip. Hence, under low nitrate conditions, NRT1.1 transport activity would shunt auxin into the epidermal flow away from the tip of the primordium (Figure 1, left panel); auxin accumulation at the tip is low and the outgrowth of lateral roots is inhibited. In contrast, under high nitrate conditions, NRT1.1 is compelled to transport nitrate, preventing auxin uptake. The outward epidermal auxin flow would therefore be expected to decrease; auxin accumulates at the tip (Figure 1, right panel),
Developmental Cell 18, June 15, 2010 ª2010 Elsevier Inc. 877
Developmental Cell
Previews
NR
De Smet, I., Zhang, H., Inze´, D., and stimulating primordium outLow NO₃High NO₃Beeckman, T. (2006). Trends Plant growth. In contrast, in nrt1.1 Sci. 11, 434–439. mutants, auxin levels in the tip are constantly high, leadDubrovsky, J.G., Sauer, M., Napsucialy-Mendivil, S., Ivanchenko, ing to outgrowth of lateral NO₃M.G., Friml, J., Shishkova, S., Celeroots even at low nitrate nza, J., and Benkova´, E. (2008). NRT1 .1 Proc. Natl. Acad. Sci. USA 105, concentrations, which abro8790–8794. gates the ability of roots to respond to nitrate availability Krouk, G., Lacombe, B., Bielach, .1 T1 in the soil and undermines A., Perrine-Walker, F., Malinska, NR .1 NRT1 K., Mounier, E., Hoyerova´, K., Tillthe foraging behavior of ard, P., Leon, S., Ljung, K., et al. nrt1.1 roots. (2010). Dev. Cell 18, this issue, This elegant mechanism of 927–937. NO₃root regulation by nutrients is Pe´ret, B., De Rybel, B., Casimiro, I., based on the dual transport Benkova´, E., Swarup, R., Laplaze, specificity of the NRT1.1 L., Beeckman, T., and Bennett, transporter for the endogeM.J. (2009). Trends Plant Sci. 14, 399–408. Figure 1. NRT1.1-Dependent Mechanism of Lateral Root Outgrowth nous hormonal signal auxin At low nitrate concentration, NRT1.1-dependent signaling inhibits outgrowth and for the exogenous nuof lateral roots (left panel). Under such soil conditions, the NRT1.1 transporter Remans, T., Nacry, P., Pervent, M., trient nitrate. This study conappears to supply auxin to the epidermis flow, moving auxin away from the Filleur, S., Diatloff, E., Mounier, E., lateral root primordium tip and restraining primordium outgrowth. Under stitutes an important step Tillard, P., Forde, B.G., and Gojon, high nitrate conditions (right panel), NRT1.1-dependent auxin transport is inA. (2006). Proc. Natl. Acad. Sci. forward in our understanding hibited. This would be expected to reduce contribution to the auxin flow in USA 103, 19206–19211. of nutrient sensing in plants the epidermis; more auxin accumulates at the tip, and this, in turn, stimulates and provides a first molecular lateral root outgrowth. Auxin fluxes and accumulations contributing to lateral Swarup, K., Benkova´, E., Swarup, root outgrowth are indicated in blue; epidermal flow diverting auxin from this basis for the foraging beR., Casimiro, I., Pe´ret, B., Yang, Y., purpose is indicated in yellow. Parry, G., Nielsen, E., De Smet, I., havior of roots. It is intriguing Vanneste, S., et al. (2008). Nat. Cell to speculate whether a similar Biol. 10, 946–954. mechanism of dual transport Vanneste, S., and Friml, J. (2009). Cell 136, or perception specificities can be utilized REFERENCES 1005–1016. to modulate plant development by other Benkova´, E., Michniewicz, M., Sauer, M., Teichnutrients or even by nutrient-unrelated mann, T., Seifertova´, D., Ju¨rgens, G., and Friml, Zhang, H., and Forde, B.G. (1998). Science 279, external signals. 407–409. J. (2003). Cell 115, 591–602. T1
.1
The DUBle Life of Polycomb Complexes Bernd Schuettengruber1 and Giacomo Cavalli1,* 1Institut
de Ge´ne´tique Humaine, CNRS, 141, rue de la Cardonille, 34396 Montpellier Cedex 5, France *Correspondence: [email protected] DOI 10.1016/j.devcel.2010.06.001
Many Polycomb group (PcG) proteins assemble into complexes containing histone-modifying enzymes that act in concert to control developmental regulators. In a recent study in Nature, Scheuermann et al. report the identification of a PcG complex with histone H2A-specific deubiquitinase activity that may be a key player in PcG-target gene regulation. Originally identified in Drosophila melanogaster as regulators of homeotic (HOX) genes, Polycomb group (PcG) proteins are conserved chromatin silencing factors that dynamically define cellular identities and behaviors during development as well as in stem cell biology and cancer
(reviewed in Schuettengruber and Cavalli, 2009). Large multimeric PcG complexes associate with specific DNA regulatory elements (termed Polycomb response elements, PREs) and silence chromatin via histone-modifying activities. Among those, the Polycomb repressive complex
878 Developmental Cell 18, June 15, 2010 ª2010 Elsevier Inc.
2 (PRC2) has histone methyltransferase activity specific for histone H3 on lysine 27 (H3K27me3), whereas the Polycomb repressive complex 1 (PRC1) and the related dRing-associated factor (dRAF) complex can ubiquitinate histone H2A on lysine 119 (H2AK119ub1) through
Previews Nitrate Contra Auxin: Nutrient Sensing by Roots Tom Beeckman1,2 and Jirˇı´ Friml1,2,3,* 1Department
of Plant Systems Biology, VIB, 9052 Gent, Belgium of Plant Biotechnology and Genetics, Ghent University, 9052 Gent, Belgium 3Division of Functional Genomics and Proteomics, Department of Experimental Biology, Masaryk University, 62500 Brno, Czech Republic *Correspondence: [email protected] DOI 10.1016/j.devcel.2010.05.020 2Department
In a new study published in this issue of Developmental Cell, Krouk et al. reveal a surprising mechanism by which plant root systems adapt their architecture for soil exploitation. The dual transporter NRT1.1 uses both nitrate and the plant hormone auxin as substrates, enabling soil nitrate availability to regulate auxin-driven lateral root development.
The sessile life style of plants makes them vulnerable to changing environmental conditions and, in contrast to animals, prevents them from moving to more favorable habitats. Uptake of water and nutrients from the soil is controlled by the root system, in which many lateral roots covered with numerous root hairs branch off from the main axes. Roots are capable of responding to local soil conditions, mainly by proliferating in enriched soil patches by the development of extra lateral roots. This phenomenon has been designated as foraging behavior and represents, to a certain extent, a compensation for the lack of mobility. The high level of root plasticity has fascinated numerous plant scientists over the years because it determines the efficiency with which plants compete with their neighbors and other organisms for the use of limited mineral resources. Obviously, foraging behavior implies the deployment of nutrient sensors in the root that translate the external nutrient conditions into appropriate growth responses. Up to date, molecular data demystifying the mechanisms of these adaptive responses in plants are largely missing. The main nitrogen source for plant nutrition is nitrate (NO3 ) and studies with the plant model Arabidopsis thaliana have shown that nitrate-rich soil patches induce new lateral root development (Zhang and Forde, 1998). This proliferation occurs by stimulating the elongation of preformed lateral root primordia and appears not to be a nutritional effect due to improved nitrogen assimilation, but rather to result from the action of a specific nitrate signaling pathway. In Arabidopsis
thaliana, this nitrate signaling pathway had been shown to require the same protein that also mediates nitrate uptake itself, namely the plasma membrane NITRATE TRANSPORTER1;1 (NRT1.1) (Remans et al. (2006)). Indeed, loss-offunction mutants of NRT1.1 are seriously affected in their ability to colonize nitraterich zones. However, it has remained unclear how a nitrate transporter would couple to a signaling pathway controlling root development. Now, Krouk et al. (2010) in this issue of Developmental Cell link the nutrientsensing capacity of NRT1.1 to the regulation of the distribution of the plant hormone auxin (Vanneste and Friml, 2009), which, among other effects, controls the formation and outgrowth of lateral roots. Formation of lateral roots is characterized by several consecutive developmental steps; each of them is subjected to hormonal control, in which auxin plays a dominant role (Benkova´ et al., 2003; Dubrovsky et al., 2008; Pe´ret et al., 2009). After the initiation from pericycle cells inside the main root, a lateral root primordium is generated following a regular division pattern. The further growth of the primordium involves separation of the overlying tissue layers as the primordium forces its way to the root surface prior to its emergence from the parent root (Swarup et al., 2008). Various studies have shown the existence of a developmental checkpoint at this step, because unfavorable growth conditions will stop the primordium outgrowth (De Smet et al., 2006). One of the endogenous factors controlling this checkpoint is auxin that accumulates at the tip of the primordium,
thus regulating the unidirectional cell expansion (Benkova et al., 2003) that ultimately leads to the outgrowth of the lateral root into the surrounding rhizosphere. It is this regulated elongation that represents the driving force for the foraging behavior of the root system and that mediates growth into nitraterich soil patches. Mutant phenotypes revealed that under low nitrate conditions, NRT1.1dependent signaling inhibits and at high nitrate concentrations stimulates the outgrowth of lateral roots. Krouk et al. (2010) quite unexpectedly accounted for this observation by finding that NRT1.1 functions as a dual uptake transporter for both nitrate and auxin (Figure 1). The two substrates seem to compete for NRT1.1 transport activity, meaning that at low nitrate concentrations, the NRT1.1 capacity to transport auxin is high, whereas at high nitrate concentrations, the auxin uptake into cells is low. Localization studies demonstrated the presence of NRT1.1 at the anticlinal membranes of the primordium epidermis cells, where NRT1.1 is perfectly positioned to regulate the auxin flow away from the primordium tip. Hence, under low nitrate conditions, NRT1.1 transport activity would shunt auxin into the epidermal flow away from the tip of the primordium (Figure 1, left panel); auxin accumulation at the tip is low and the outgrowth of lateral roots is inhibited. In contrast, under high nitrate conditions, NRT1.1 is compelled to transport nitrate, preventing auxin uptake. The outward epidermal auxin flow would therefore be expected to decrease; auxin accumulates at the tip (Figure 1, right panel),
Developmental Cell 18, June 15, 2010 ª2010 Elsevier Inc. 877
Developmental Cell
Previews
NR
De Smet, I., Zhang, H., Inze´, D., and stimulating primordium outLow NO₃High NO₃Beeckman, T. (2006). Trends Plant growth. In contrast, in nrt1.1 Sci. 11, 434–439. mutants, auxin levels in the tip are constantly high, leadDubrovsky, J.G., Sauer, M., Napsucialy-Mendivil, S., Ivanchenko, ing to outgrowth of lateral NO₃M.G., Friml, J., Shishkova, S., Celeroots even at low nitrate nza, J., and Benkova´, E. (2008). NRT1 .1 Proc. Natl. Acad. Sci. USA 105, concentrations, which abro8790–8794. gates the ability of roots to respond to nitrate availability Krouk, G., Lacombe, B., Bielach, .1 T1 in the soil and undermines A., Perrine-Walker, F., Malinska, NR .1 NRT1 K., Mounier, E., Hoyerova´, K., Tillthe foraging behavior of ard, P., Leon, S., Ljung, K., et al. nrt1.1 roots. (2010). Dev. Cell 18, this issue, This elegant mechanism of 927–937. NO₃root regulation by nutrients is Pe´ret, B., De Rybel, B., Casimiro, I., based on the dual transport Benkova´, E., Swarup, R., Laplaze, specificity of the NRT1.1 L., Beeckman, T., and Bennett, transporter for the endogeM.J. (2009). Trends Plant Sci. 14, 399–408. Figure 1. NRT1.1-Dependent Mechanism of Lateral Root Outgrowth nous hormonal signal auxin At low nitrate concentration, NRT1.1-dependent signaling inhibits outgrowth and for the exogenous nuof lateral roots (left panel). Under such soil conditions, the NRT1.1 transporter Remans, T., Nacry, P., Pervent, M., trient nitrate. This study conappears to supply auxin to the epidermis flow, moving auxin away from the Filleur, S., Diatloff, E., Mounier, E., lateral root primordium tip and restraining primordium outgrowth. Under stitutes an important step Tillard, P., Forde, B.G., and Gojon, high nitrate conditions (right panel), NRT1.1-dependent auxin transport is inA. (2006). Proc. Natl. Acad. Sci. forward in our understanding hibited. This would be expected to reduce contribution to the auxin flow in USA 103, 19206–19211. of nutrient sensing in plants the epidermis; more auxin accumulates at the tip, and this, in turn, stimulates and provides a first molecular lateral root outgrowth. Auxin fluxes and accumulations contributing to lateral Swarup, K., Benkova´, E., Swarup, root outgrowth are indicated in blue; epidermal flow diverting auxin from this basis for the foraging beR., Casimiro, I., Pe´ret, B., Yang, Y., purpose is indicated in yellow. Parry, G., Nielsen, E., De Smet, I., havior of roots. It is intriguing Vanneste, S., et al. (2008). Nat. Cell to speculate whether a similar Biol. 10, 946–954. mechanism of dual transport Vanneste, S., and Friml, J. (2009). Cell 136, or perception specificities can be utilized REFERENCES 1005–1016. to modulate plant development by other Benkova´, E., Michniewicz, M., Sauer, M., Teichnutrients or even by nutrient-unrelated mann, T., Seifertova´, D., Ju¨rgens, G., and Friml, Zhang, H., and Forde, B.G. (1998). Science 279, external signals. 407–409. J. (2003). Cell 115, 591–602. T1
.1
The DUBle Life of Polycomb Complexes Bernd Schuettengruber1 and Giacomo Cavalli1,* 1Institut
de Ge´ne´tique Humaine, CNRS, 141, rue de la Cardonille, 34396 Montpellier Cedex 5, France *Correspondence: [email protected] DOI 10.1016/j.devcel.2010.06.001
Many Polycomb group (PcG) proteins assemble into complexes containing histone-modifying enzymes that act in concert to control developmental regulators. In a recent study in Nature, Scheuermann et al. report the identification of a PcG complex with histone H2A-specific deubiquitinase activity that may be a key player in PcG-target gene regulation. Originally identified in Drosophila melanogaster as regulators of homeotic (HOX) genes, Polycomb group (PcG) proteins are conserved chromatin silencing factors that dynamically define cellular identities and behaviors during development as well as in stem cell biology and cancer
(reviewed in Schuettengruber and Cavalli, 2009). Large multimeric PcG complexes associate with specific DNA regulatory elements (termed Polycomb response elements, PREs) and silence chromatin via histone-modifying activities. Among those, the Polycomb repressive complex
878 Developmental Cell 18, June 15, 2010 ª2010 Elsevier Inc.
2 (PRC2) has histone methyltransferase activity specific for histone H3 on lysine 27 (H3K27me3), whereas the Polycomb repressive complex 1 (PRC1) and the related dRing-associated factor (dRAF) complex can ubiquitinate histone H2A on lysine 119 (H2AK119ub1) through