- Email: [email protected]
Local Auxin Biosynthesis Mediates Plant Growth and Development
TRPLSC 1751 No. of Pages 3
Spotlight
Local Auxin Biosynthesis Mediates Plant Growth and Development Bingsheng Lv,1,4 Zhenwei Yan,1,4 Huiyu Tian,1,* Xiansheng Zhang,2,* and Zhaojun Ding1,3,* Auxin is one of the most important plant hormones controlling various aspects of plant growth and development. Here, we highlight three recent papers that shed light on how local auxin biosynthesis contributes to plant growth and development in response to endogenous developmental signals and exogenous environmental cues, such as shade and aluminum stress. Introduction Auxin is one of the most important plant hormones mediating endogenous developmental signals and exogenous environmental cues to control various plant growth and developmental responses. As a plant hormone, formation of an appropriate auxin gradient is critical for its function. A model based on PIN proteins together with other transporter classes suggests that redistribution of shoot-derived auxin is sufficient to generate an auxin gradient with an auxin maximum in the root [1]. It is widely accepted that the coordinated actions of auxin biosynthesis and/or metabolism and transport have an essential role in establishing the auxin gradient. Disruption of polar auxin transport strongly affects auxin gradient formation [2], suggesting the crucial role of polar auxin transport in the generation of auxin gradients. By contrast, mutation of auxin
biosynthesis-related genes also affects auxin gradient formation [3]. A growing body of recent studies further demonstrates that local auxin biosynthesis has an important role in auxin gradient formation and, thus, triggers various plant development and growth responses [4–9].
Local Auxin Biosynthesis Mediates Plant Development Remarkable progress over the past decade demonstrated that indole-3-acetic acid (IAA) is synthesized from both tryptophan (Trp)-dependent and -independent pathways. In addition to CYTOCHROME P450, FAMILY 79, SUBFAMILY B, POLYPEPTIDE 2/3 (CYP79B2/3), the YUCCA (YUC) family of flavin-containing mono-oxygenases and the TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA) family of aminotransferases are the best-characterized enzymes expressed in various tissues and involved in the regulation of numerous aspects of plant growth and development though the regulation of Trp-dependent auxin biosynthesis [3,10]. Mutant analyses together with analyses of the expression pattern of these enzymes suggest that local auxin biosynthesis has an important role in the generation of the auxin gradient and the resulting plant organogenesis [3]. Although the role of polar auxin transport has been highlighted [11], the origin of auxin that triggers initial embryogenesis has remained obscure. Recently, Robert et al. reported that the maternal auxin supply has an important role in early embryo patterning in arabidopsis (Arabidopsis thaliana) [4]. By monitoring DIIVENUS and DR5:GFP auxin signaling reporters, the authors observed an accumulation of auxin in ovules 24 h after pollination, indicating that pollination leads to increased auxin levels in maternal tissues surrounding the embryo [4]. To address how this auxin was produced, the authors
analyzed the expression of auxin biosynthesis-related genes and found that expression of TAA1, YUC8, and YUC9 was increased in integuments after pollination. Mutant analysis showed a strong reduction of IAA levels 24 h after pollination in weak ethylene insensitive8/tryptophan aminotransferase related1 (wei8tar1) ovules compared with wildtype (WT) [4]. In reciprocal cross tests, compared with WT, embryos from wei8-1 mutant mother plants displayed defective embryo phenotypes, indicating that auxin production in maternal tissues has an important role in embryo development [4]. Integument-specific expression of bacterial IAA-lysine synthetase (iaaL), which inactivates free auxin through conjugation, reduces auxin signal responses in the integument and affects embryo development [4]. Taken together, the results of this study suggest that maternal auxin production in the integuments contributes to early embryo development [4]. As well as a critical role in early embryo patterning, local auxin biosynthesis is also involved in early stages of pollen development. Yao et al. recently demonstrated that auxin production in diploid microsporocytes was necessary and sufficient for early stages of pollen development [5]. Although it is well known that sporophytic cells can provide nutrients and cell wall materials for gametophytic development in arabidopsis, whether auxin produced by sporophytic tissues is required in this process requires clarification. Yao et al. found that microspore development in yuc2yuc6 double mutants arrested before the first asymmetric mitotic division and failed to produce viable pollen [5]. YUC2/6 are expressed in microspores, tapetum, meiocytes, middle layer, and endothecium in anthers. To investigate the source of auxin during pollen development, the authors used various promoters to drive YUC2-GFP expression in yuc2yuc6 mutants. Their results
Trends in Plant Science, Month Year, Vol. xx, No. yy
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TRPLSC 1751 No. of Pages 3
Local auxin biosynthesis was also reported to regulatefloralmeristemidentity.SUPERMAN (SUP) was proposed to function as a boundary gene to separate the stamen-producing whorl 3 from the carpel-producing whorl 4. The sup mutant displayed prolonged maintenance of floral stem cells, which led to an
(B)
(A)
PMII
Mp
Bc
Tc
YUC8/9
Msp
(C)
(D)
Aux
in
Meiosis PMI
SUP
SUP
YUC1/4
YUC1/4
Light
Shade
PIF
PIF
YUC
YUC
(E)
increase in the number of reproductive organs. By monitoring the activity of auxin reporters, including pDR5rev::2xGFP-N7, pDR5rev::GFP-ER, and DII-VENUS, Xu et al. observed that the loss of SUP function led to auxin accumulation at the boundary between whorl 3 and whorl 4 [6]. Expressing the bacterial auxin biosynthetic enzyme IAAH, which converts the auxin precursor, indole acetamide (IAM) to the active form of auxin, with the SUP promoter, resulted in flowers of transgenic plants showing weak to strong sup-like phenotypes in the presence of 1 mM IAM. This suggests that local increases in auxin biosynthesis at the boundary region between the third and fourth whorl are sufficient to trigger sup-like phenotypes [6].The alteredauxin gradients insup resulted from the derepressed local YUC1/4 activity, which was inhibited by SUP through interaction with components of polycomb repressive complex 2 [6]. The authors proposed that SUP coordinates floral organogenesis and floral meristem size through regulation of YUC1/4-mediated local auxin biosynthesis. In addition to its vital role in aboveground Al stress tissues, local auxin biosynthesis was also reported to be involved in root development. TAA1/YUCs It was found that auxin overproduction in shoots was unable to rescue auxin deficienAuxin cies in arabidopsis roots [12]. Integument
showed that only auxin produced in microsporocytes and microspores rescued the sterile phenotypes of yuc2yuc6 mutants [5], demonstrating that auxin produced in diploid microsporocytes has a critical role during the early stages of pollen development (Figure 1).
Local Auxin Biosynthesis Mediates Plant Growth Responses to Shade and Aluminum Stress
Figure 1. A Proposed Model of Local Auxin Biosynthesis in Plant Growth and Development. (A) Auxin produced in microsporocyte and microspores through YUCCA (YUC)-2/6 has a critical role during the early stages of pollen development. (B) During early embryo pattern, the expression of YUC8 and YUC9 are induced after pollination, which increases auxin levels in the integument. Maternal auxin production in integuments is necessary for early embryo development. (C) A boundary gene, SUPERMAN (SUP), controls proper floral patterning through the regulation of YUC1/4-mediated local auxin biosynthesis at the boundary between whorl 3 and whorl 4. (D) PHYTOCHROME-INTERACTING FACTOR (PIF)-YUC-mediated local auxin biosynthesis provides a mechanism whereby local shade responses mediate plant adaptation to heterogeneous environments. (E) The expression of TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1 (TAA1) and YUC3/5/7/8/9 in the root apex transition zone is upregulated in response to aluminum stress, which eventually leads to auxin accumulation in the root apex transition zone and inhibition of root growth. Orange yellow means high levels of auxin; arrows indicate positive regulation; bars indicate negative regulation. Abbreviations: Bc, bicellular pollen; Mp, microspores; Msp, microsporocytes; PM, pollen mitosis; Tc, tricellular pollen.
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Trends in Plant Science, Month Year, Vol. xx, No. yy
Competition for light triggers shade avoidance syndrome (SAS) in plants. In response to shade, auxin levels are induced, a process that is dependent on TAA1-mediated auxin biosynthesis. Auxin produced in the shaded leaf is transported toward the lower parts of the plant, where it influences the growth of hypocotyls [10]. Two recent reports provide more evidence about how shade signals affect only part of a plant and lead to a local response. The reports demonstrated that local induction of auxin biosynthesis in one leaf only led to SAS in that
TRPLSC 1751 No. of Pages 3
leaf and did not affect the development of other leaves on the same plant [7,8]. A further study showed that the PHYTOCHROME-INTERACTING FACTOR (PIF)-YUC regulation module was essential for shade-induced leaf hyponasty [7,8], indicating that local auxin biosynthesis has a profound impact on the shade response of plants.
However, some questions remain. For example, because polar auxin transport also has an important role in plant growth and development, how do plants balance the local auxin biosynthesis and polar auxin transport in this process? Are these two processes connected or dissected during plant growth and development? There are five TAA genes and 11 YUC genes in arabidopsis, with diverse expression patterns in various tissues. It will be interesting to elucidate the precise function of local auxin biosynthesis in each tissue. In addition to local auxin biosynthesis, auxin metabolism also has important roles in the establishment of local auxin gradients, it will be interesting to study the relationship between local auxin biosynthesis and metabolism in plant growth and development.
Local auxin biosynthesis also has an important role in root growth in response to aluminum stress. In addition to TAA1mediated local auxin biosynthesis, Liu et al. reported that YUCCAs also regulated local auxin biosynthesis in the root apex transition zone in response to aluminum stress [9]. Similar to TAA1, the expression of YUC3/5/7/8/9 in the root apex transition zone was upregulated in response to aluminum stress, which eventually led to the accumulation of Acknowledgements auxin in the root apex transition zone This work is supported by the Shandong Province and inhibition of root growth [9]. The Natural Science Foundation of Major Basic Research PIF4 transcription factor binds directly Program (2017C03), the National Natural Science to promoters of YUC5/8/9 and functions Foundation of China (Projects 31770305 and 31870252). as a transcriptional activator to promote local auxin biosynthesis in the root apex 1The Key Laboratory of Plant Development and transition zone under aluminum stress [9]. Environmental Adaptation Biology, Ministry of Education,
Concluding Remarks and Open Questions In summary, recent studies highlight the important role of local auxin biosynthesis in plant growth and development.
College of Life Sciences, Shandong University, Qingdao, 266237, Shandong, China 2 State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Taian, 271018, Shandong, China
*Correspondence: [email protected] (H. Tian), [email protected] (X. Zhang), [email protected] (Z. Ding). https://doi.org/10.1016/j.tplants.2018.10.014 References 1. Armengot, L. et al. (2016) Regulation of polar auxin transport by protein and lipid kinases. J. Exp. Bot. 67, 4015– 4037 2. Robert, H.S. and Friml, J. (2009) Auxin and other signals on the move in plants. Nat. Chem. Biol. 5, 325–332 3. Zhao, Y.D. (2010) Auxin biosynthesis and its role in plant development. Annu. Rev. Plant Biol. 61, 49–64 4. Robert, H.S. et al. (2018) Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nat. Plants 4, 548–553 5. Yao, X. et al. (2018) Auxin production in diploid microsporocytes is necessary and sufficient for early stages of pollen development. PLoS Genet. 14, e1007397 6. Xu, Y.F. et al. (2018) SUPERMAN regulates floral whorl boundaries through control of auxin biosynthesis. EMBO J. 37, e97499 7. Michaud, O. et al. (2017) Local auxin production underlies a spatially restricted neighbor-detection response in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 114, 7444– 7449 8. Pantazopoulou, C.K. et al. (2017) Neighbor detection at the leaf tip adaptively regulates upward leaf movement through spatial auxin dynamics. Proc. Natl. Acad. Sci. U. S. A. 114, 7450–7455 9. Liu, G. et al. (2016) Local transcriptional control of YUCCA regulates auxin promoted root-growth inhibition in response to aluminium stress in Arabidopsis. PLoS Genet. 12, e1006360 10. Tao, Y. et al. (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133, 164–176 11. Friml, J. et al. (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147–153 12. Chen, Q.G. et al. (2014) Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots. Plant Cell Physiol. 55, 1072–1079
3 State Key Laboratory of Microbial Technology, Shandong University, Qingdao, 266237, Shandong, China 4 These authors contributed equally to this work
Trends in Plant Science, Month Year, Vol. xx, No. yy
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Spotlight
Local Auxin Biosynthesis Mediates Plant Growth and Development Bingsheng Lv,1,4 Zhenwei Yan,1,4 Huiyu Tian,1,* Xiansheng Zhang,2,* and Zhaojun Ding1,3,* Auxin is one of the most important plant hormones controlling various aspects of plant growth and development. Here, we highlight three recent papers that shed light on how local auxin biosynthesis contributes to plant growth and development in response to endogenous developmental signals and exogenous environmental cues, such as shade and aluminum stress. Introduction Auxin is one of the most important plant hormones mediating endogenous developmental signals and exogenous environmental cues to control various plant growth and developmental responses. As a plant hormone, formation of an appropriate auxin gradient is critical for its function. A model based on PIN proteins together with other transporter classes suggests that redistribution of shoot-derived auxin is sufficient to generate an auxin gradient with an auxin maximum in the root [1]. It is widely accepted that the coordinated actions of auxin biosynthesis and/or metabolism and transport have an essential role in establishing the auxin gradient. Disruption of polar auxin transport strongly affects auxin gradient formation [2], suggesting the crucial role of polar auxin transport in the generation of auxin gradients. By contrast, mutation of auxin
biosynthesis-related genes also affects auxin gradient formation [3]. A growing body of recent studies further demonstrates that local auxin biosynthesis has an important role in auxin gradient formation and, thus, triggers various plant development and growth responses [4–9].
Local Auxin Biosynthesis Mediates Plant Development Remarkable progress over the past decade demonstrated that indole-3-acetic acid (IAA) is synthesized from both tryptophan (Trp)-dependent and -independent pathways. In addition to CYTOCHROME P450, FAMILY 79, SUBFAMILY B, POLYPEPTIDE 2/3 (CYP79B2/3), the YUCCA (YUC) family of flavin-containing mono-oxygenases and the TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS (TAA) family of aminotransferases are the best-characterized enzymes expressed in various tissues and involved in the regulation of numerous aspects of plant growth and development though the regulation of Trp-dependent auxin biosynthesis [3,10]. Mutant analyses together with analyses of the expression pattern of these enzymes suggest that local auxin biosynthesis has an important role in the generation of the auxin gradient and the resulting plant organogenesis [3]. Although the role of polar auxin transport has been highlighted [11], the origin of auxin that triggers initial embryogenesis has remained obscure. Recently, Robert et al. reported that the maternal auxin supply has an important role in early embryo patterning in arabidopsis (Arabidopsis thaliana) [4]. By monitoring DIIVENUS and DR5:GFP auxin signaling reporters, the authors observed an accumulation of auxin in ovules 24 h after pollination, indicating that pollination leads to increased auxin levels in maternal tissues surrounding the embryo [4]. To address how this auxin was produced, the authors
analyzed the expression of auxin biosynthesis-related genes and found that expression of TAA1, YUC8, and YUC9 was increased in integuments after pollination. Mutant analysis showed a strong reduction of IAA levels 24 h after pollination in weak ethylene insensitive8/tryptophan aminotransferase related1 (wei8tar1) ovules compared with wildtype (WT) [4]. In reciprocal cross tests, compared with WT, embryos from wei8-1 mutant mother plants displayed defective embryo phenotypes, indicating that auxin production in maternal tissues has an important role in embryo development [4]. Integument-specific expression of bacterial IAA-lysine synthetase (iaaL), which inactivates free auxin through conjugation, reduces auxin signal responses in the integument and affects embryo development [4]. Taken together, the results of this study suggest that maternal auxin production in the integuments contributes to early embryo development [4]. As well as a critical role in early embryo patterning, local auxin biosynthesis is also involved in early stages of pollen development. Yao et al. recently demonstrated that auxin production in diploid microsporocytes was necessary and sufficient for early stages of pollen development [5]. Although it is well known that sporophytic cells can provide nutrients and cell wall materials for gametophytic development in arabidopsis, whether auxin produced by sporophytic tissues is required in this process requires clarification. Yao et al. found that microspore development in yuc2yuc6 double mutants arrested before the first asymmetric mitotic division and failed to produce viable pollen [5]. YUC2/6 are expressed in microspores, tapetum, meiocytes, middle layer, and endothecium in anthers. To investigate the source of auxin during pollen development, the authors used various promoters to drive YUC2-GFP expression in yuc2yuc6 mutants. Their results
Trends in Plant Science, Month Year, Vol. xx, No. yy
1
TRPLSC 1751 No. of Pages 3
Local auxin biosynthesis was also reported to regulatefloralmeristemidentity.SUPERMAN (SUP) was proposed to function as a boundary gene to separate the stamen-producing whorl 3 from the carpel-producing whorl 4. The sup mutant displayed prolonged maintenance of floral stem cells, which led to an
(B)
(A)
PMII
Mp
Bc
Tc
YUC8/9
Msp
(C)
(D)
Aux
in
Meiosis PMI
SUP
SUP
YUC1/4
YUC1/4
Light
Shade
PIF
PIF
YUC
YUC
(E)
increase in the number of reproductive organs. By monitoring the activity of auxin reporters, including pDR5rev::2xGFP-N7, pDR5rev::GFP-ER, and DII-VENUS, Xu et al. observed that the loss of SUP function led to auxin accumulation at the boundary between whorl 3 and whorl 4 [6]. Expressing the bacterial auxin biosynthetic enzyme IAAH, which converts the auxin precursor, indole acetamide (IAM) to the active form of auxin, with the SUP promoter, resulted in flowers of transgenic plants showing weak to strong sup-like phenotypes in the presence of 1 mM IAM. This suggests that local increases in auxin biosynthesis at the boundary region between the third and fourth whorl are sufficient to trigger sup-like phenotypes [6].The alteredauxin gradients insup resulted from the derepressed local YUC1/4 activity, which was inhibited by SUP through interaction with components of polycomb repressive complex 2 [6]. The authors proposed that SUP coordinates floral organogenesis and floral meristem size through regulation of YUC1/4-mediated local auxin biosynthesis. In addition to its vital role in aboveground Al stress tissues, local auxin biosynthesis was also reported to be involved in root development. TAA1/YUCs It was found that auxin overproduction in shoots was unable to rescue auxin deficienAuxin cies in arabidopsis roots [12]. Integument
showed that only auxin produced in microsporocytes and microspores rescued the sterile phenotypes of yuc2yuc6 mutants [5], demonstrating that auxin produced in diploid microsporocytes has a critical role during the early stages of pollen development (Figure 1).
Local Auxin Biosynthesis Mediates Plant Growth Responses to Shade and Aluminum Stress
Figure 1. A Proposed Model of Local Auxin Biosynthesis in Plant Growth and Development. (A) Auxin produced in microsporocyte and microspores through YUCCA (YUC)-2/6 has a critical role during the early stages of pollen development. (B) During early embryo pattern, the expression of YUC8 and YUC9 are induced after pollination, which increases auxin levels in the integument. Maternal auxin production in integuments is necessary for early embryo development. (C) A boundary gene, SUPERMAN (SUP), controls proper floral patterning through the regulation of YUC1/4-mediated local auxin biosynthesis at the boundary between whorl 3 and whorl 4. (D) PHYTOCHROME-INTERACTING FACTOR (PIF)-YUC-mediated local auxin biosynthesis provides a mechanism whereby local shade responses mediate plant adaptation to heterogeneous environments. (E) The expression of TRYPTOPHAN AMINOTRANSFERASE OF ARABIDOPSIS 1 (TAA1) and YUC3/5/7/8/9 in the root apex transition zone is upregulated in response to aluminum stress, which eventually leads to auxin accumulation in the root apex transition zone and inhibition of root growth. Orange yellow means high levels of auxin; arrows indicate positive regulation; bars indicate negative regulation. Abbreviations: Bc, bicellular pollen; Mp, microspores; Msp, microsporocytes; PM, pollen mitosis; Tc, tricellular pollen.
2
Trends in Plant Science, Month Year, Vol. xx, No. yy
Competition for light triggers shade avoidance syndrome (SAS) in plants. In response to shade, auxin levels are induced, a process that is dependent on TAA1-mediated auxin biosynthesis. Auxin produced in the shaded leaf is transported toward the lower parts of the plant, where it influences the growth of hypocotyls [10]. Two recent reports provide more evidence about how shade signals affect only part of a plant and lead to a local response. The reports demonstrated that local induction of auxin biosynthesis in one leaf only led to SAS in that
TRPLSC 1751 No. of Pages 3
leaf and did not affect the development of other leaves on the same plant [7,8]. A further study showed that the PHYTOCHROME-INTERACTING FACTOR (PIF)-YUC regulation module was essential for shade-induced leaf hyponasty [7,8], indicating that local auxin biosynthesis has a profound impact on the shade response of plants.
However, some questions remain. For example, because polar auxin transport also has an important role in plant growth and development, how do plants balance the local auxin biosynthesis and polar auxin transport in this process? Are these two processes connected or dissected during plant growth and development? There are five TAA genes and 11 YUC genes in arabidopsis, with diverse expression patterns in various tissues. It will be interesting to elucidate the precise function of local auxin biosynthesis in each tissue. In addition to local auxin biosynthesis, auxin metabolism also has important roles in the establishment of local auxin gradients, it will be interesting to study the relationship between local auxin biosynthesis and metabolism in plant growth and development.
Local auxin biosynthesis also has an important role in root growth in response to aluminum stress. In addition to TAA1mediated local auxin biosynthesis, Liu et al. reported that YUCCAs also regulated local auxin biosynthesis in the root apex transition zone in response to aluminum stress [9]. Similar to TAA1, the expression of YUC3/5/7/8/9 in the root apex transition zone was upregulated in response to aluminum stress, which eventually led to the accumulation of Acknowledgements auxin in the root apex transition zone This work is supported by the Shandong Province and inhibition of root growth [9]. The Natural Science Foundation of Major Basic Research PIF4 transcription factor binds directly Program (2017C03), the National Natural Science to promoters of YUC5/8/9 and functions Foundation of China (Projects 31770305 and 31870252). as a transcriptional activator to promote local auxin biosynthesis in the root apex 1The Key Laboratory of Plant Development and transition zone under aluminum stress [9]. Environmental Adaptation Biology, Ministry of Education,
Concluding Remarks and Open Questions In summary, recent studies highlight the important role of local auxin biosynthesis in plant growth and development.
College of Life Sciences, Shandong University, Qingdao, 266237, Shandong, China 2 State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Taian, 271018, Shandong, China
*Correspondence: [email protected] (H. Tian), [email protected] (X. Zhang), [email protected] (Z. Ding). https://doi.org/10.1016/j.tplants.2018.10.014 References 1. Armengot, L. et al. (2016) Regulation of polar auxin transport by protein and lipid kinases. J. Exp. Bot. 67, 4015– 4037 2. Robert, H.S. and Friml, J. (2009) Auxin and other signals on the move in plants. Nat. Chem. Biol. 5, 325–332 3. Zhao, Y.D. (2010) Auxin biosynthesis and its role in plant development. Annu. Rev. Plant Biol. 61, 49–64 4. Robert, H.S. et al. (2018) Maternal auxin supply contributes to early embryo patterning in Arabidopsis. Nat. Plants 4, 548–553 5. Yao, X. et al. (2018) Auxin production in diploid microsporocytes is necessary and sufficient for early stages of pollen development. PLoS Genet. 14, e1007397 6. Xu, Y.F. et al. (2018) SUPERMAN regulates floral whorl boundaries through control of auxin biosynthesis. EMBO J. 37, e97499 7. Michaud, O. et al. (2017) Local auxin production underlies a spatially restricted neighbor-detection response in Arabidopsis. Proc. Natl. Acad. Sci. U. S. A. 114, 7444– 7449 8. Pantazopoulou, C.K. et al. (2017) Neighbor detection at the leaf tip adaptively regulates upward leaf movement through spatial auxin dynamics. Proc. Natl. Acad. Sci. U. S. A. 114, 7450–7455 9. Liu, G. et al. (2016) Local transcriptional control of YUCCA regulates auxin promoted root-growth inhibition in response to aluminium stress in Arabidopsis. PLoS Genet. 12, e1006360 10. Tao, Y. et al. (2008) Rapid synthesis of auxin via a new tryptophan-dependent pathway is required for shade avoidance in plants. Cell 133, 164–176 11. Friml, J. et al. (2003) Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature 426, 147–153 12. Chen, Q.G. et al. (2014) Auxin overproduction in shoots cannot rescue auxin deficiencies in Arabidopsis roots. Plant Cell Physiol. 55, 1072–1079
3 State Key Laboratory of Microbial Technology, Shandong University, Qingdao, 266237, Shandong, China 4 These authors contributed equally to this work
Trends in Plant Science, Month Year, Vol. xx, No. yy
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