- Email: [email protected]
Locally Sourced: Auxin Biosynthesis and Transport in the Root Meristem
Developmental Cell
Previews titer, confirming that EcI is indeed necessary to import steroid hormones into cells. Finally, co-expression of EcI and the ecdysone receptor (EcR) in mammalian cells cultured in the presence of ecdysone activated expression of an EcRresponsive reporter, thereby convincingly demonstrating that EcI is both necessary and sufficient for ecdysone import into cells. So, how do steroid hormones enter cells? These findings by Okamoto and colleagues reopen a debate that was considered closed decades ago, as the identification and validation of a bona fide steroid hormone transporter now forces us to reconsider the validity of the passive diffusion model of steroid entry. From a biological perspective, transporter-mediated steroid hormone entry provides a new mechanism for cells to control how much, if any, steroid hormone they will import, adding an additional layer of regulation and complexity to steroid hormone signaling. However, the hydrophobicity profile of different steroid hormones varies considerably, making it difficult to directly extrapolate these findings with ecdysone to mammalian steroid hormones. Nevertheless, this study by Okamoto et al. (2018) creates reasonable doubt regarding the validity of the passive
diffusion model of steroid hormone entry, making it necessary to now determine whether transporters are required for entry of steroid hormones into mammalian cells. Given the wide evolutionary conservation of SLCO transporters among animals, it is possible that these proteins may also be required for steroid hormone uptake in mammalian cells. In fact, OATPs are already known to transport some steroid hormone precursors and conjugates in vivo, and these proteins have also been shown to transport steroid hormones in vitro (Hagenbuch and Stieger, 2013), raising the tantalizing possibility that careful in vivo studies may identify OATPs, and/or other transporter proteins, that are required for steroid hormone uptake in mammalian cells. If such transporters are confirmed, the implications for human health would be tremendous, as the presence of steroid hormone transporters would lead to revolutionary changes in the therapeutic approaches used to manage human endocrinerelated diseases.
REFERENCES Giorgi, E.P., and Stein, W.D. (1981). The transport of steroids into animal cells in culture. Endocrinology 108, 688–697.
Gorski, J., and Gannon, F. (1976). Current models of steroid hormone action: a critique. Annu. Rev. Physiol. 38, 425–450. Hagenbuch, B., and Stieger, B. (2013). The SLCO (former SLC21) superfamily of transporters. Mol. Aspects Med. 34, 396–412. Kalliokoski, A., and Niemi, M. (2009). Impact of OATP transporters on pharmacokinetics. Br. J. Pharmacol. 158, 693–705. Milgrom, E., Atger, M., and Baulieu, E.-E. (1973). Studies on estrogen entry into uterine cells and on estradiol-receptor complex attachment to the nucleus–is the entry of estrogen into uterine cells a protein-mediated process? Biochim. Biophys. Acta 320, 267–283. Nakagawa, Y. (2005). Nonsteroidal ecdysone agonists. Vitam. Horm. 73, 131–173. Okamoto, N., Viswanatha, R., Bittar, R., Li, Z., Haga-Yamanaka, S., Perrimon, N., and Yamanaka, N. (2018). A membrane transporter is required for steroid hormone uptake in Drosophila. Dev. Cell 47, this issue, 294–305. Pietras, R.J., and Szego, C.M. (1977). Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells. Nature 265, 69–72. Plagemann, P.G.W., and Erbe, J. (1976). Glucocorticoids–uptake by simple diffusion by cultured Reuber and Novikoff rat hepatoma cells. Biochem. Pharmacol. 25, 1489–1494. Yamanaka, N., Marque´s, G., and O’Connor, M.B. (2015). Vesicle-mediated steroid hormone secretion in Drosophila melanogaster. Cell 163, 907–919.
Locally Sourced: Auxin Biosynthesis and Transport in the Root Meristem Nicholas J. Morffy1 and Lucia C. Strader1,2,* 1Department
of Biology, Washington University, St. Louis, MO 63130, USA for Engineering MechanoBiology, Washington University, St. Louis, MO 63130, USA *Correspondence: [email protected] https://doi.org/10.1016/j.devcel.2018.10.018 2Center
Localized maxima of the plant hormone auxin are crucial to root development and meristem maintenance. In this issue of Developmental Cell, Brumos et al. used elegant genetic and grafting experiments to distinguish between the contributions of local and distal auxin sources to auxin maxima generation and root meristem maintenance. Plants rely on a diverse array of endogenous signaling molecules to drive their development and responses to the environment. One of these signaling
molecules, auxin, impacts nearly every aspect of plant growth and development, including shoot growth, branching, and root growth (reviewed in Enders and
262 Developmental Cell 47, November 5, 2018 ª 2018 Elsevier Inc.
Strader, 2015). An auxin maximum is required for root meristem maintenance; auxin homeostasis models rely on the coordination of auxin biosynthesis, both
Developmental Cell
Previews C organized meristem
disorganized meristem
disorganized meristem
organized meristem
A
Wild-type/ wei8 tar2/ Wild-type/ wei8 tar2/ Wild-type wei8 tar2 wei8 tar2 Wild-Type B
WEI8pro:: WEI8Genomic
WEI8pro:: WEI8cDNA
Figure 1. Locally Sourced Auxin Regulates Root Meristem Development (A) A cartoon representing the results of the root grafting experiment. Wild-type tissues are shaded in blue, and wei8 tar2 double mutant tissues are shaded in red. (B) The expression domains of WEI8Genomic and WEI8cDNA reported in Brumos et al. (2018) are shaded in light green and differ from one another. (C) A model of auxin maxima generation in the root meristem. Both auxin biosynthesis through the IPyA (WEI8/TAA) pathway (green) and auxin transport (red arrows) contribute to auxin maxima (blue and green areas) in the root meristem.
in shoot tissues and root tissues, and its cell-to-cell transport via influx and efflux carriers to generate these auxin maxima. It was believed that shootderived auxin and its downward transport accounted for the majority of auxin found in the roots that drives root growth and development. However, several recent studies have shown that there are locally generated sources of auxin in the root (Ljung et al., 2002, 2005; Stepanova et al., 2008) and that shoot-produced auxin is unable to rescue deficiencies in auxin production in roots (Chen et al., 2014). These developments raised the possibility that root-synthesized auxin contributes to root development by generating an auxin maximum in the root meristem. It is within this context that Brumos et al. (2018) tested the hypothesis that root-synthesized auxin was necessary for generating root meristem auxin maxima, shedding light on the relative contributions of auxin transport and biosynthesis to root stem cell niche maintenance.
The main auxin biosynthesis pathway involves conversion of tryptophan to indole-3-pyruvic acid (IPyA) to indole-3acetic acid (auxin). WEI8 and its homolog TAR2 are enzymes in the auxin biosynthetic pathway that are required for proper auxin levels and root meristem maintenance; the wei8 tar2 double mutant displays the loss of the root meristem and reduced auxin activity in roots. Brumos et al. (2018) used root-shoot grafts to determine whether root-synthesized auxin was necessary for meristem maintenance. Wild-type root stocks had normal root meristems regardless of the genotype of the grafted shoot, whereas wei8 tar2 root stocks failed to maintain the root meristem even when fused to wild-type shoots (Figure 1A). These results suggest that auxin transport from the shoots is insufficient for generating maxima in root meristems and that rootsynthesized auxin is necessary for this process. The authors then used a heatinduced auxin biosynthetic circuit to rescue auxin deficiency in wei8 tar2;
heating the aerial portions of the wei8 tar2 double mutant failed to rescue root meristem degeneration, whereas inducing auxin biosynthesis in roots was sufficient to maintain the root meristem. These studies suggest a model in which locally synthesized auxin is required for the generation of auxin maxima and the maintenance of root meristems. Examination of WEI8 expression domains revealed that WEI8 is natively expressed in the quiescent center, a small niche of cells in the root meristem that are stem cell precursors. Previous studies provided conflicting reports for WEI8 expression domains (Stepanova et al., 2008; Yamada et al., 2009); however, these studies used constructs that differed in the presence of WEI8 introns (i.e., genomic versus cDNA copies of WEI8). Brumos et al. (2018) show that the genomic sequence for WEI8 contains an element required for expression in the quiescent center in the root meristem, whereas the WEI8 coding sequence fails to express in the root meristem,
Developmental Cell 47, November 5, 2018 263
Developmental Cell
Previews uncovering the source of discrepancy in previous reports. Interestingly, when driven behind its native upstream regulatory element, WEI8 expressed from cDNA and WEI8 expressed from genomic sequence are in distinct tissues, with WEI8 quiescent center expression from the genomic construct and WEI8 more broadly expressed in root tissues when expressed from the cDNA construct (Figure 1B). The distinct expression patterns of WEI8 when sourced from cDNA or genomic DNA provided a tool exploited by this study. With mutant lines expressing either a cDNA or genomic copy of WEI8 rescue constructs, the authors could specifically determine the effects of loss of WEI8 function solely in the quiescent center (i.e., using lines expressing the cDNA rescue construct). Plants expressing the WEI8 cDNA construct were unable to maintain a meristem when auxin transport was inhibited, whereas plants expressing the genomic copy rescued the wei8 mutation in the presence of auxin transport inhibitors, suggesting that auxin biosynthesis in the quiescent center can compensate for loss of auxin provision through transport mechanisms. Taken together, these results suggest that local auxin biosynthesis in the root is necessary for the maintenance of auxin maxima in the root meristem. The contribution of the root-derived IPyA biosynthesis pathway is consistent with work showing that auxin biosynthetic pathways are active in the root meristem early in development. Previous reports showed that auxin biosynthesis in root meristems was under feedback inhibition from auxin transport and that excised roots showed decreases in total auxin accumulation suggesting redundancy between auxin biosynthetic pathways and auxin transport in maintaining auxin levels in the root (Bhalerao et al., 2002; Ljung et al., 2005). The results presented by Brumos et al. (2018) raise the possibility that root meri-
stem synthesized auxin, in addition to auxin transport, affect auxin homeostasis and root growth more generally. Moving forward, determining the relative contribution of distinct auxin sources in different cell types and regions of the root will be critical to understanding auxin regulation of developmental events. Under optimal growth conditions, auxin transport and biosynthesis work cooperatively to promote root meristematic function. Under less favorable growth conditions, localized auxin biosynthesis could supplement auxin transport. In either case, new layers of auxin regulation, such as sequestration, metabolism, and transport, should be considered at each cell layer and condition. In addition to the root meristem, auxin maxima occur in the tips of developing leaves, shoot apices, and the sites of lateral root initiation. Determining the relative contributions of local auxin biosynthesis and transport from distal sources to the maintenance of these auxin maxima will illuminate the mechanisms underlying the associated developmental processes. Varying rates of biosynthesis, transport, and metabolism could act to tune auxin levels at auxin maxima, controlling development. For example, studies similar to that from Brumos et al. (2018) could shed light on the contribution of local biosynthesis to auxin maxima in the shoot apex, where auxin transport is well studied. In the case of lateral root initiation, the coordination of shoot-, root meristem-, and root cap-derived (Xuan et al., 2015) auxin may play differential roles in priming, generating, and elongating lateral roots to ensure that root tissues respond appropriately to environmental conditions and improve the robustness of auxin responses. Further, these studies would be better informed by auxin sensors that report auxin levels directly, as opposed to indirectly by measuring auxin signaling events. Brumos et al. (2018) showcase the power of combining genetic, chemical,
264 Developmental Cell 47, November 5, 2018
and synthetic biological approaches to address a difficult problem. In the process, they have uncovered new sources for a crucial plant signaling molecule in the root meristem and its contribution to plant growth and development.
REFERENCES Bhalerao, R.P., Eklo¨f, J., Ljung, K., Marchant, A., Bennett, M., and Sandberg, G. (2002). Shootderived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J. 29, 325–332. Brumos, J., Robles, L.M., Yun, J., Vu, T.C., Jackson, S., Alonso, J.M., and Stepanova, A.N. (2018). Local auxin biosynthesis is a key regulator of plant development. Dev. Cell 47, this issue, 306–318. Chen, Q., Dai, X., De-Paoli, H., Cheng, Y., Takebayashi, Y., Kasahara, H., Kamiya, Y., and Zhao, Y. (2014). Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots. Plant Cell Physiol. 55, 1072–1079. Enders, T.A., and Strader, L.C. (2015). Auxin activity: past, present, and future. Am. J. Bot. 102, 180–196. Ljung, K., Hul, A.K., Kowalczyk, M., Marchant, A., Celenza, J., Cohen, J.D., and Sandberg, G. (2002). Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol. Biol. 50, 309–332. Ljung, K., Hull, A.K., Celenza, J., Yamada, M., Estelle, M., Normanly, J., and Sandberg, G. (2005). Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17, 1090–1104. Stepanova, A.N., Robertson-Hoyt, J., Yun, J., Benavente, L.M., Xie, D.-Y., Dolezal, K., Schlereth, €rgens, G., and Alonso, J.M. (2008). TAA1A., Ju mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133, 177–191. Xuan, W., Audenaert, D., Parizot, B., Mo¨ller, B.K., Njo, M.F., De Rybel, B., De Rop, G., €ho¨nen, A.P., Vanneste, Van Isterdael, G., Ma S., and Beeckman, T. (2015). Root capderived auxin pre-patterns the longitudinal axis of the Arabidopsis root. Curr. Biol. 25, 1381–1388. Yamada, M., Greenham, K., Prigge, M.J., Jensen, P.J., and Estelle, M. (2009). The TRANSPORT INHIBITOR RESPONSE2 gene is required for auxin synthesis and diverse aspects of plant development. Plant Physiol. 151, 168–179.
Previews titer, confirming that EcI is indeed necessary to import steroid hormones into cells. Finally, co-expression of EcI and the ecdysone receptor (EcR) in mammalian cells cultured in the presence of ecdysone activated expression of an EcRresponsive reporter, thereby convincingly demonstrating that EcI is both necessary and sufficient for ecdysone import into cells. So, how do steroid hormones enter cells? These findings by Okamoto and colleagues reopen a debate that was considered closed decades ago, as the identification and validation of a bona fide steroid hormone transporter now forces us to reconsider the validity of the passive diffusion model of steroid entry. From a biological perspective, transporter-mediated steroid hormone entry provides a new mechanism for cells to control how much, if any, steroid hormone they will import, adding an additional layer of regulation and complexity to steroid hormone signaling. However, the hydrophobicity profile of different steroid hormones varies considerably, making it difficult to directly extrapolate these findings with ecdysone to mammalian steroid hormones. Nevertheless, this study by Okamoto et al. (2018) creates reasonable doubt regarding the validity of the passive
diffusion model of steroid hormone entry, making it necessary to now determine whether transporters are required for entry of steroid hormones into mammalian cells. Given the wide evolutionary conservation of SLCO transporters among animals, it is possible that these proteins may also be required for steroid hormone uptake in mammalian cells. In fact, OATPs are already known to transport some steroid hormone precursors and conjugates in vivo, and these proteins have also been shown to transport steroid hormones in vitro (Hagenbuch and Stieger, 2013), raising the tantalizing possibility that careful in vivo studies may identify OATPs, and/or other transporter proteins, that are required for steroid hormone uptake in mammalian cells. If such transporters are confirmed, the implications for human health would be tremendous, as the presence of steroid hormone transporters would lead to revolutionary changes in the therapeutic approaches used to manage human endocrinerelated diseases.
REFERENCES Giorgi, E.P., and Stein, W.D. (1981). The transport of steroids into animal cells in culture. Endocrinology 108, 688–697.
Gorski, J., and Gannon, F. (1976). Current models of steroid hormone action: a critique. Annu. Rev. Physiol. 38, 425–450. Hagenbuch, B., and Stieger, B. (2013). The SLCO (former SLC21) superfamily of transporters. Mol. Aspects Med. 34, 396–412. Kalliokoski, A., and Niemi, M. (2009). Impact of OATP transporters on pharmacokinetics. Br. J. Pharmacol. 158, 693–705. Milgrom, E., Atger, M., and Baulieu, E.-E. (1973). Studies on estrogen entry into uterine cells and on estradiol-receptor complex attachment to the nucleus–is the entry of estrogen into uterine cells a protein-mediated process? Biochim. Biophys. Acta 320, 267–283. Nakagawa, Y. (2005). Nonsteroidal ecdysone agonists. Vitam. Horm. 73, 131–173. Okamoto, N., Viswanatha, R., Bittar, R., Li, Z., Haga-Yamanaka, S., Perrimon, N., and Yamanaka, N. (2018). A membrane transporter is required for steroid hormone uptake in Drosophila. Dev. Cell 47, this issue, 294–305. Pietras, R.J., and Szego, C.M. (1977). Specific binding sites for oestrogen at the outer surfaces of isolated endometrial cells. Nature 265, 69–72. Plagemann, P.G.W., and Erbe, J. (1976). Glucocorticoids–uptake by simple diffusion by cultured Reuber and Novikoff rat hepatoma cells. Biochem. Pharmacol. 25, 1489–1494. Yamanaka, N., Marque´s, G., and O’Connor, M.B. (2015). Vesicle-mediated steroid hormone secretion in Drosophila melanogaster. Cell 163, 907–919.
Locally Sourced: Auxin Biosynthesis and Transport in the Root Meristem Nicholas J. Morffy1 and Lucia C. Strader1,2,* 1Department
of Biology, Washington University, St. Louis, MO 63130, USA for Engineering MechanoBiology, Washington University, St. Louis, MO 63130, USA *Correspondence: [email protected] https://doi.org/10.1016/j.devcel.2018.10.018 2Center
Localized maxima of the plant hormone auxin are crucial to root development and meristem maintenance. In this issue of Developmental Cell, Brumos et al. used elegant genetic and grafting experiments to distinguish between the contributions of local and distal auxin sources to auxin maxima generation and root meristem maintenance. Plants rely on a diverse array of endogenous signaling molecules to drive their development and responses to the environment. One of these signaling
molecules, auxin, impacts nearly every aspect of plant growth and development, including shoot growth, branching, and root growth (reviewed in Enders and
262 Developmental Cell 47, November 5, 2018 ª 2018 Elsevier Inc.
Strader, 2015). An auxin maximum is required for root meristem maintenance; auxin homeostasis models rely on the coordination of auxin biosynthesis, both
Developmental Cell
Previews C organized meristem
disorganized meristem
disorganized meristem
organized meristem
A
Wild-type/ wei8 tar2/ Wild-type/ wei8 tar2/ Wild-type wei8 tar2 wei8 tar2 Wild-Type B
WEI8pro:: WEI8Genomic
WEI8pro:: WEI8cDNA
Figure 1. Locally Sourced Auxin Regulates Root Meristem Development (A) A cartoon representing the results of the root grafting experiment. Wild-type tissues are shaded in blue, and wei8 tar2 double mutant tissues are shaded in red. (B) The expression domains of WEI8Genomic and WEI8cDNA reported in Brumos et al. (2018) are shaded in light green and differ from one another. (C) A model of auxin maxima generation in the root meristem. Both auxin biosynthesis through the IPyA (WEI8/TAA) pathway (green) and auxin transport (red arrows) contribute to auxin maxima (blue and green areas) in the root meristem.
in shoot tissues and root tissues, and its cell-to-cell transport via influx and efflux carriers to generate these auxin maxima. It was believed that shootderived auxin and its downward transport accounted for the majority of auxin found in the roots that drives root growth and development. However, several recent studies have shown that there are locally generated sources of auxin in the root (Ljung et al., 2002, 2005; Stepanova et al., 2008) and that shoot-produced auxin is unable to rescue deficiencies in auxin production in roots (Chen et al., 2014). These developments raised the possibility that root-synthesized auxin contributes to root development by generating an auxin maximum in the root meristem. It is within this context that Brumos et al. (2018) tested the hypothesis that root-synthesized auxin was necessary for generating root meristem auxin maxima, shedding light on the relative contributions of auxin transport and biosynthesis to root stem cell niche maintenance.
The main auxin biosynthesis pathway involves conversion of tryptophan to indole-3-pyruvic acid (IPyA) to indole-3acetic acid (auxin). WEI8 and its homolog TAR2 are enzymes in the auxin biosynthetic pathway that are required for proper auxin levels and root meristem maintenance; the wei8 tar2 double mutant displays the loss of the root meristem and reduced auxin activity in roots. Brumos et al. (2018) used root-shoot grafts to determine whether root-synthesized auxin was necessary for meristem maintenance. Wild-type root stocks had normal root meristems regardless of the genotype of the grafted shoot, whereas wei8 tar2 root stocks failed to maintain the root meristem even when fused to wild-type shoots (Figure 1A). These results suggest that auxin transport from the shoots is insufficient for generating maxima in root meristems and that rootsynthesized auxin is necessary for this process. The authors then used a heatinduced auxin biosynthetic circuit to rescue auxin deficiency in wei8 tar2;
heating the aerial portions of the wei8 tar2 double mutant failed to rescue root meristem degeneration, whereas inducing auxin biosynthesis in roots was sufficient to maintain the root meristem. These studies suggest a model in which locally synthesized auxin is required for the generation of auxin maxima and the maintenance of root meristems. Examination of WEI8 expression domains revealed that WEI8 is natively expressed in the quiescent center, a small niche of cells in the root meristem that are stem cell precursors. Previous studies provided conflicting reports for WEI8 expression domains (Stepanova et al., 2008; Yamada et al., 2009); however, these studies used constructs that differed in the presence of WEI8 introns (i.e., genomic versus cDNA copies of WEI8). Brumos et al. (2018) show that the genomic sequence for WEI8 contains an element required for expression in the quiescent center in the root meristem, whereas the WEI8 coding sequence fails to express in the root meristem,
Developmental Cell 47, November 5, 2018 263
Developmental Cell
Previews uncovering the source of discrepancy in previous reports. Interestingly, when driven behind its native upstream regulatory element, WEI8 expressed from cDNA and WEI8 expressed from genomic sequence are in distinct tissues, with WEI8 quiescent center expression from the genomic construct and WEI8 more broadly expressed in root tissues when expressed from the cDNA construct (Figure 1B). The distinct expression patterns of WEI8 when sourced from cDNA or genomic DNA provided a tool exploited by this study. With mutant lines expressing either a cDNA or genomic copy of WEI8 rescue constructs, the authors could specifically determine the effects of loss of WEI8 function solely in the quiescent center (i.e., using lines expressing the cDNA rescue construct). Plants expressing the WEI8 cDNA construct were unable to maintain a meristem when auxin transport was inhibited, whereas plants expressing the genomic copy rescued the wei8 mutation in the presence of auxin transport inhibitors, suggesting that auxin biosynthesis in the quiescent center can compensate for loss of auxin provision through transport mechanisms. Taken together, these results suggest that local auxin biosynthesis in the root is necessary for the maintenance of auxin maxima in the root meristem. The contribution of the root-derived IPyA biosynthesis pathway is consistent with work showing that auxin biosynthetic pathways are active in the root meristem early in development. Previous reports showed that auxin biosynthesis in root meristems was under feedback inhibition from auxin transport and that excised roots showed decreases in total auxin accumulation suggesting redundancy between auxin biosynthetic pathways and auxin transport in maintaining auxin levels in the root (Bhalerao et al., 2002; Ljung et al., 2005). The results presented by Brumos et al. (2018) raise the possibility that root meri-
stem synthesized auxin, in addition to auxin transport, affect auxin homeostasis and root growth more generally. Moving forward, determining the relative contribution of distinct auxin sources in different cell types and regions of the root will be critical to understanding auxin regulation of developmental events. Under optimal growth conditions, auxin transport and biosynthesis work cooperatively to promote root meristematic function. Under less favorable growth conditions, localized auxin biosynthesis could supplement auxin transport. In either case, new layers of auxin regulation, such as sequestration, metabolism, and transport, should be considered at each cell layer and condition. In addition to the root meristem, auxin maxima occur in the tips of developing leaves, shoot apices, and the sites of lateral root initiation. Determining the relative contributions of local auxin biosynthesis and transport from distal sources to the maintenance of these auxin maxima will illuminate the mechanisms underlying the associated developmental processes. Varying rates of biosynthesis, transport, and metabolism could act to tune auxin levels at auxin maxima, controlling development. For example, studies similar to that from Brumos et al. (2018) could shed light on the contribution of local biosynthesis to auxin maxima in the shoot apex, where auxin transport is well studied. In the case of lateral root initiation, the coordination of shoot-, root meristem-, and root cap-derived (Xuan et al., 2015) auxin may play differential roles in priming, generating, and elongating lateral roots to ensure that root tissues respond appropriately to environmental conditions and improve the robustness of auxin responses. Further, these studies would be better informed by auxin sensors that report auxin levels directly, as opposed to indirectly by measuring auxin signaling events. Brumos et al. (2018) showcase the power of combining genetic, chemical,
264 Developmental Cell 47, November 5, 2018
and synthetic biological approaches to address a difficult problem. In the process, they have uncovered new sources for a crucial plant signaling molecule in the root meristem and its contribution to plant growth and development.
REFERENCES Bhalerao, R.P., Eklo¨f, J., Ljung, K., Marchant, A., Bennett, M., and Sandberg, G. (2002). Shootderived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J. 29, 325–332. Brumos, J., Robles, L.M., Yun, J., Vu, T.C., Jackson, S., Alonso, J.M., and Stepanova, A.N. (2018). Local auxin biosynthesis is a key regulator of plant development. Dev. Cell 47, this issue, 306–318. Chen, Q., Dai, X., De-Paoli, H., Cheng, Y., Takebayashi, Y., Kasahara, H., Kamiya, Y., and Zhao, Y. (2014). Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots. Plant Cell Physiol. 55, 1072–1079. Enders, T.A., and Strader, L.C. (2015). Auxin activity: past, present, and future. Am. J. Bot. 102, 180–196. Ljung, K., Hul, A.K., Kowalczyk, M., Marchant, A., Celenza, J., Cohen, J.D., and Sandberg, G. (2002). Biosynthesis, conjugation, catabolism and homeostasis of indole-3-acetic acid in Arabidopsis thaliana. Plant Mol. Biol. 50, 309–332. Ljung, K., Hull, A.K., Celenza, J., Yamada, M., Estelle, M., Normanly, J., and Sandberg, G. (2005). Sites and regulation of auxin biosynthesis in Arabidopsis roots. Plant Cell 17, 1090–1104. Stepanova, A.N., Robertson-Hoyt, J., Yun, J., Benavente, L.M., Xie, D.-Y., Dolezal, K., Schlereth, €rgens, G., and Alonso, J.M. (2008). TAA1A., Ju mediated auxin biosynthesis is essential for hormone crosstalk and plant development. Cell 133, 177–191. Xuan, W., Audenaert, D., Parizot, B., Mo¨ller, B.K., Njo, M.F., De Rybel, B., De Rop, G., €ho¨nen, A.P., Vanneste, Van Isterdael, G., Ma S., and Beeckman, T. (2015). Root capderived auxin pre-patterns the longitudinal axis of the Arabidopsis root. Curr. Biol. 25, 1381–1388. Yamada, M., Greenham, K., Prigge, M.J., Jensen, P.J., and Estelle, M. (2009). The TRANSPORT INHIBITOR RESPONSE2 gene is required for auxin synthesis and diverse aspects of plant development. Plant Physiol. 151, 168–179.