Molecular Plant Advance Access published May 6, 2014 SPOTLIGHT
Molecular Plant
To Grow or Not to Grow: FERONIA Has Her Say
FER ON CELL GROWTH: PROMOTION OR INHIBITION? FER was first hinted as a growth inhibitor because its loss of function (hereafter referred to as fer) resulted in pollen tube overgrowth within the embryo sac, leading to reduced fertility (Escobar-Restrepo et al., 2007). However, fer also displayed reduced growth during vegetative stages (Keinath et al., 2010; Kessler et al., 2010), of root hairs (Duan et al., 2010; Huang et al., 2013), and of dark- or blue-light-induced hypocotyl elongation (Guo et al., 2009; Deslauriers and Larsen, 2010), implying a growth promoting role. In addition, studies to understand the interactions between FER and hormonal signaling also hinted at a promoting role of FER on cell growth. For example, it was shown that auxin-promoted root hair elongation depends on FER (Duan et al., 2010; Huang et al., 2013). In darkgrown seedlings, FER promotes hypocotyl elongation, in parallel and in concert with ethylene and brassinosteroid
(BR)-signaling pathways (Guo et al., 2009; Deslauriers and Larsen, 2010). Nonetheless, an enlightening study recently demonstrated that FER acts as a growth inhibitor in root post-elongation zone upon the perception of its ligand, a small secreted peptide RAPID ALKALIZATION FACTOR (RALF) (Haruta et al., 2014). RALF specifically interacted with the extracellular domain of FER and its binding induced FER autophosphorylation (Haruta et al., 2014). The activated FER causes phosphorylation and inactivation of a plasma membrane (PM) H + -ATPase (AHA), finally an increase in apoplastic pH (Haruta et al., 2014). Apoplastic pH has long been known as a driving force for cell growth by influencing cell wall properties. In root hairs, it was demonstrated that high pH resulted in growth arrest due to global rigidification of wall while low pH resulted in cell burst possibly due to unregulated cell expansion (Monshausen et al., 2007), indicating that apoplastic pH has to be delicately controlled. As a result of RALF-induced FER activation, root cell elongation is arrested and overall root growth reduced (Haruta et al., 2014). This new finding shows that both root cells and pollen tubes may use a common FER-mediated signaling pathway to suppress cell growth. Consistently with its growth promoting or inhibiting activities, FER promotes or inhibits the production of ROS. FER is required for ROS production in root hairs, whose mutations lead to reduced cell elongation (Duan et al., 2010; Huang et al., 2013). A recent report demonstrates that the inhibitory role of FER on pollen tube overgrowth in the embryo sac relies on its ability to induce local ROS elevation, which is critical for pollen tube burst (Duan et al., 2014). By contrast, fer shows enhanced ROS production in leaves (Keinath et al., 2010; Kessler et al., 2010) and in guard cells (Yu et al., 2012). The enhanced ROS level in fer is also reflected by spontaneous cell death at unchallenged leaves (Keinath et al., 2010; Kessler et al., 2010). Thus, the distinct functions of FER, either promoting or inhibiting ROS production, are cell-specific and context-dependent.
© The Author 2014. Published by the Molecular Plant Shanghai Editorial Office in association with Oxford University Press on behalf of CSPB and IPPE, SIBS, CAS. doi:10.1093/mp/ssu031 Received 26 February 2014; accepted 16 March 2014
Downloaded from http://mplant.oxfordjournals.org/ at Universidade de BrasÃ-lia on May 10, 2014
Plant cells differ from their animal counterparts such that they are encased in a complex wall structure, crucial for cell growth through a dynamic equilibrium of rigidity and flexibility. Cell wall extensibility can be greatly influenced by apoplastic pH and reactive oxygen species (ROS) (Duan et al., 2014; Haruta et al., 2014). Several recent works demonstrated that the receptor-like kinase (RLK) FERONIA (FER) is critical to fine-tune cell growth in a spatiotemporal and context-dependent manner by controlling apoplastic pH (Haruta et al., 2014) and ROS (Duan et al., 2010, 2014), likely balancing wall rigidity for cell integrity and flexibility for cell expansion. FER belongs to the Catharanthus roseus RLK1-like kinase family (CrRLK1Ls) characterized by their extracellular carbohydrate-binding malectin (ML) domains (Escobar-Restrepo et al., 2007). FER was first identified for its role in fertilization (Escobar-Restrepo et al., 2007), but later implicated in various processes such as pathogen resistance (Keinath et al., 2010; Kessler et al., 2010), vegetative growth (Guo et al., 2009; Deslauriers and Larsen, 2010), root hair elongation (Duan et al., 2010; Huang et al., 2013), and seed development (Yu et al., 2014). In this Spotlight, we highlight some new findings and point out several unanswered questions whose resolution will help fill the gaps in the FER-mediated signaling pathway (Figure 1).
2
Molecular Plant
Spotlight
REGULATORY MECHANISMS UNDERLYING FER-MEDIATED GROWTH CONTROL Diverse regulatory mechanisms have been evolved to ensure fine-tuned FER signaling. First, FER is regulated transcriptionally. FER is constitutively expressed in all tissues except pollen tubes. Its expression is particularly strong in regions undergoing rapid cell elongation, such as root hairs, hypocotyls, and leaf petioles (Guo et al., 2009; Duan et al., 2010). FER expression is induced by auxin, ethylene, and BR, but repressed by abscisic acid (Guo et al., 2009; Deslauriers and Larsen, 2010; Yu et al., 2012), implying its central role in integrating developmental cues. Second, membrane partition of FER might be a key step toward signaling specification. FER is asymmetrically distributed at the PM of synergid cells (Escobar-Restrepo et al., 2007) and its enrichment at the filliform apparatus is critical for pollen tube reception and may mediate membrane asymmetry of other proteins such as NORTIA (Kessler et al., 2010). In response to flg22, FER rapidly translocates to detergent-resistant membranes (DRMs) (Keinath et al., 2010), being recognized as signaling platforms in eukaryotic cells. Third, although FER is uniformly localized in many cell types such as root hairs and hypocotyls (Duan et al., 2010; Haruta et al., 2014), ligand availability and concentrations might attribute to its activation asymmetry crucial for their asymmetric growth. For example, the expression of the RALF precursor gene is enriched in roots at the maturation zone, distal to the elongation zone (Haruta et al., 2014). It
is perceivable that a ligand gradient might be formed to allow asymmetric FER activation, resulting in local growth inhibition. Last but not least, distinct signaling outputs may depend on different intracellular partners of FER. Guanine nucleotide exchange factor (GEF)-mediated ROP activation seems a common theme in FER-mediated intracellular signaling (Duan et al., 2010; Yu et al., 2012; Huang et al., 2013). It remains to be seen whether cell-specific and context-dependent GEF– ROP pairs contribute to the distinct outputs of FER.
FUTURE DIRECTIONS The identification of RALF as a ligand for FER raises more questions than it answers. Are other RALF family members also ligands for FER? Genes encoding RALF precursors are present throughout the plant kingdom (Haruta et al., 2014). So are genes encoding for FER homologs (EscobarRestrepo et al., 2007), implying the evolutionary conservation of the RALF–FER signaling. Appropriately for its role in fertilization, the extracellular sequences of FER were fast evolving (Escobar-Restrepo et al., 2007). However, members of the RALF polypeptides are highly conserved (Haruta et al., 2014). It remains to be seen whether they are diversified in residues crucial for FER recognition specificity. Furthermore, putative ligands of sugar properties as indicated by the ML domains of the CrRLK1Ls have yet to be discovered. How FER signaling is specified in a cell-specific and context-dependent manner is another intriguing question. Transcriptional regulation of the ligand-coding
Downloaded from http://mplant.oxfordjournals.org/ at Universidade de BrasÃ-lia on May 10, 2014
Figure 1 FER-Mediated Signaling Promotes or Inhibits Growth.
Molecular Plant
Spotlight
genes as demonstrated by the RALF precursors (Haruta et al., 2014) would certainly not be the only answer. Another issue to be resolved in the future is the interaction between FER and its cytosolic partners, such as RopGEFs, in a spatiotemporal resolution in planta. Finally, it will be informative that FER-mediated dynamic apoplastic pH and ROS as well as cell wall organization are visualized in spatial resolution. The quests for these unresolved issues will finally allow us to understand FER-controlled cell growth in plants.
3
of root hair development. Proc. Natl Acad. Sci. U S A. 107, 17821–17826. Escobar-Restrepo, J.-M., Huck, N., Kessler, S., Gagliardini, V., Gheyselinck, J., Yang, W.-C., and Grossniklaus, U. (2007). The FERONIA receptor-like kinase mediates male–female interactions during pollen tube reception. Science. 317, 656–660. Guo, H., Li, L., Ye, H., Yu, X., Algreen, A., and Yin, Y. (2009). Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc. Natl Acad. Sci. U S A. 106, 7648–7653. Haruta., M., Sabat, G., Stecker, K., Minkoff, B.B., and Sussman, M.R. (2014). A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science. 343, 408–411.
FUNDING
Sha Li and Yan Zhang
1
State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Daizong St. 61, Tai’an, Shandong, China 1 To whom correspondence should be addressed. E-mail [email protected], tel. 86-538-8246365, fax +86-538-8248696.
References Deslauriers, S.D., and Larsen, P.B. (2010). FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in Arabidopsis hypocotyls. Mol. Plant. 3, 626–640. Duan, Q., Kita, D., Johnson, E.A., Aggarwal, M., Gates, L., Wu, H.-M., and Cheung, A.Y. (2014). Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat. Comms. 5, 3129. Duan, Q., Kita, D., Li, C., Cheung, A.Y., and Wu, H.-M. (2010). FERONIA receptor-like kinase regulates RHO GTPase signaling
Huang, G.-Q., Li, E., Ge F.-R., Li, S., Wang, Q., Zhang, C.-Q., and Zhang, Y. (2013). Arabidopsis RopGEF4 and RopGEF10 are important for FERONIA-mediated developmental but not environmental regulation of root hair growth. New Phytol. 200, 1089–1101. Keinath, N.F., Kierszniowska, S., Lorek, J., Bourdais, G., Kessler, S.A., Shimosato-Asano, H., Grossniklaus, U., Schulze, W.X., Robatzek, S., and Panstruga, R. (2010). PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveals novel components of plant immunity. J. Biol. Chem. 285, 39140–39149. Kessler, S.A., Shimosato-Asano, H., Keinath, N.F., Wuest, S.E., Ingram, G., Panstruga, R., and Grossniklaus, U. (2010). Conserved molecular components for pollen tube reception and fungal invasion. Science. 330, 968–971. Monshausen, G.B., Bibikova, T.N., Messerli, M.A., and Gilroy, S. (2007). Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc. Natl Acad. Sci. U S A. 104, 20996–21001. Yu, F., Li, Li, J., Huang, Y., Liu, L., Li, D., Chen, L., and Luan, S. (2014). FERONIA receptor kinase controls seed size in Arabidopsis thaliana. Mol. Plant., published online on Jan 30, 2014, 10.1093/mp/ssu010. Yu, F., Qian, L., Nibau, C., Duan, Q., Kita, D., Levasseur, K., Li, X., Lu, C., Li, H., Hou, C., et al. (2012). FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. Proc. Natl Acad. Sci. U S A. 109, 14693–14698.
Downloaded from http://mplant.oxfordjournals.org/ at Universidade de BrasÃ-lia on May 10, 2014
This work was supported by the Major Research Plant (2013CB945102) from the Ministry of Science and Technology of China to Y.Z. No conflict of interest declared.
Molecular Plant
To Grow or Not to Grow: FERONIA Has Her Say
FER ON CELL GROWTH: PROMOTION OR INHIBITION? FER was first hinted as a growth inhibitor because its loss of function (hereafter referred to as fer) resulted in pollen tube overgrowth within the embryo sac, leading to reduced fertility (Escobar-Restrepo et al., 2007). However, fer also displayed reduced growth during vegetative stages (Keinath et al., 2010; Kessler et al., 2010), of root hairs (Duan et al., 2010; Huang et al., 2013), and of dark- or blue-light-induced hypocotyl elongation (Guo et al., 2009; Deslauriers and Larsen, 2010), implying a growth promoting role. In addition, studies to understand the interactions between FER and hormonal signaling also hinted at a promoting role of FER on cell growth. For example, it was shown that auxin-promoted root hair elongation depends on FER (Duan et al., 2010; Huang et al., 2013). In darkgrown seedlings, FER promotes hypocotyl elongation, in parallel and in concert with ethylene and brassinosteroid
(BR)-signaling pathways (Guo et al., 2009; Deslauriers and Larsen, 2010). Nonetheless, an enlightening study recently demonstrated that FER acts as a growth inhibitor in root post-elongation zone upon the perception of its ligand, a small secreted peptide RAPID ALKALIZATION FACTOR (RALF) (Haruta et al., 2014). RALF specifically interacted with the extracellular domain of FER and its binding induced FER autophosphorylation (Haruta et al., 2014). The activated FER causes phosphorylation and inactivation of a plasma membrane (PM) H + -ATPase (AHA), finally an increase in apoplastic pH (Haruta et al., 2014). Apoplastic pH has long been known as a driving force for cell growth by influencing cell wall properties. In root hairs, it was demonstrated that high pH resulted in growth arrest due to global rigidification of wall while low pH resulted in cell burst possibly due to unregulated cell expansion (Monshausen et al., 2007), indicating that apoplastic pH has to be delicately controlled. As a result of RALF-induced FER activation, root cell elongation is arrested and overall root growth reduced (Haruta et al., 2014). This new finding shows that both root cells and pollen tubes may use a common FER-mediated signaling pathway to suppress cell growth. Consistently with its growth promoting or inhibiting activities, FER promotes or inhibits the production of ROS. FER is required for ROS production in root hairs, whose mutations lead to reduced cell elongation (Duan et al., 2010; Huang et al., 2013). A recent report demonstrates that the inhibitory role of FER on pollen tube overgrowth in the embryo sac relies on its ability to induce local ROS elevation, which is critical for pollen tube burst (Duan et al., 2014). By contrast, fer shows enhanced ROS production in leaves (Keinath et al., 2010; Kessler et al., 2010) and in guard cells (Yu et al., 2012). The enhanced ROS level in fer is also reflected by spontaneous cell death at unchallenged leaves (Keinath et al., 2010; Kessler et al., 2010). Thus, the distinct functions of FER, either promoting or inhibiting ROS production, are cell-specific and context-dependent.
© The Author 2014. Published by the Molecular Plant Shanghai Editorial Office in association with Oxford University Press on behalf of CSPB and IPPE, SIBS, CAS. doi:10.1093/mp/ssu031 Received 26 February 2014; accepted 16 March 2014
Downloaded from http://mplant.oxfordjournals.org/ at Universidade de BrasÃ-lia on May 10, 2014
Plant cells differ from their animal counterparts such that they are encased in a complex wall structure, crucial for cell growth through a dynamic equilibrium of rigidity and flexibility. Cell wall extensibility can be greatly influenced by apoplastic pH and reactive oxygen species (ROS) (Duan et al., 2014; Haruta et al., 2014). Several recent works demonstrated that the receptor-like kinase (RLK) FERONIA (FER) is critical to fine-tune cell growth in a spatiotemporal and context-dependent manner by controlling apoplastic pH (Haruta et al., 2014) and ROS (Duan et al., 2010, 2014), likely balancing wall rigidity for cell integrity and flexibility for cell expansion. FER belongs to the Catharanthus roseus RLK1-like kinase family (CrRLK1Ls) characterized by their extracellular carbohydrate-binding malectin (ML) domains (Escobar-Restrepo et al., 2007). FER was first identified for its role in fertilization (Escobar-Restrepo et al., 2007), but later implicated in various processes such as pathogen resistance (Keinath et al., 2010; Kessler et al., 2010), vegetative growth (Guo et al., 2009; Deslauriers and Larsen, 2010), root hair elongation (Duan et al., 2010; Huang et al., 2013), and seed development (Yu et al., 2014). In this Spotlight, we highlight some new findings and point out several unanswered questions whose resolution will help fill the gaps in the FER-mediated signaling pathway (Figure 1).
2
Molecular Plant
Spotlight
REGULATORY MECHANISMS UNDERLYING FER-MEDIATED GROWTH CONTROL Diverse regulatory mechanisms have been evolved to ensure fine-tuned FER signaling. First, FER is regulated transcriptionally. FER is constitutively expressed in all tissues except pollen tubes. Its expression is particularly strong in regions undergoing rapid cell elongation, such as root hairs, hypocotyls, and leaf petioles (Guo et al., 2009; Duan et al., 2010). FER expression is induced by auxin, ethylene, and BR, but repressed by abscisic acid (Guo et al., 2009; Deslauriers and Larsen, 2010; Yu et al., 2012), implying its central role in integrating developmental cues. Second, membrane partition of FER might be a key step toward signaling specification. FER is asymmetrically distributed at the PM of synergid cells (Escobar-Restrepo et al., 2007) and its enrichment at the filliform apparatus is critical for pollen tube reception and may mediate membrane asymmetry of other proteins such as NORTIA (Kessler et al., 2010). In response to flg22, FER rapidly translocates to detergent-resistant membranes (DRMs) (Keinath et al., 2010), being recognized as signaling platforms in eukaryotic cells. Third, although FER is uniformly localized in many cell types such as root hairs and hypocotyls (Duan et al., 2010; Haruta et al., 2014), ligand availability and concentrations might attribute to its activation asymmetry crucial for their asymmetric growth. For example, the expression of the RALF precursor gene is enriched in roots at the maturation zone, distal to the elongation zone (Haruta et al., 2014). It
is perceivable that a ligand gradient might be formed to allow asymmetric FER activation, resulting in local growth inhibition. Last but not least, distinct signaling outputs may depend on different intracellular partners of FER. Guanine nucleotide exchange factor (GEF)-mediated ROP activation seems a common theme in FER-mediated intracellular signaling (Duan et al., 2010; Yu et al., 2012; Huang et al., 2013). It remains to be seen whether cell-specific and context-dependent GEF– ROP pairs contribute to the distinct outputs of FER.
FUTURE DIRECTIONS The identification of RALF as a ligand for FER raises more questions than it answers. Are other RALF family members also ligands for FER? Genes encoding RALF precursors are present throughout the plant kingdom (Haruta et al., 2014). So are genes encoding for FER homologs (EscobarRestrepo et al., 2007), implying the evolutionary conservation of the RALF–FER signaling. Appropriately for its role in fertilization, the extracellular sequences of FER were fast evolving (Escobar-Restrepo et al., 2007). However, members of the RALF polypeptides are highly conserved (Haruta et al., 2014). It remains to be seen whether they are diversified in residues crucial for FER recognition specificity. Furthermore, putative ligands of sugar properties as indicated by the ML domains of the CrRLK1Ls have yet to be discovered. How FER signaling is specified in a cell-specific and context-dependent manner is another intriguing question. Transcriptional regulation of the ligand-coding
Downloaded from http://mplant.oxfordjournals.org/ at Universidade de BrasÃ-lia on May 10, 2014
Figure 1 FER-Mediated Signaling Promotes or Inhibits Growth.
Molecular Plant
Spotlight
genes as demonstrated by the RALF precursors (Haruta et al., 2014) would certainly not be the only answer. Another issue to be resolved in the future is the interaction between FER and its cytosolic partners, such as RopGEFs, in a spatiotemporal resolution in planta. Finally, it will be informative that FER-mediated dynamic apoplastic pH and ROS as well as cell wall organization are visualized in spatial resolution. The quests for these unresolved issues will finally allow us to understand FER-controlled cell growth in plants.
3
of root hair development. Proc. Natl Acad. Sci. U S A. 107, 17821–17826. Escobar-Restrepo, J.-M., Huck, N., Kessler, S., Gagliardini, V., Gheyselinck, J., Yang, W.-C., and Grossniklaus, U. (2007). The FERONIA receptor-like kinase mediates male–female interactions during pollen tube reception. Science. 317, 656–660. Guo, H., Li, L., Ye, H., Yu, X., Algreen, A., and Yin, Y. (2009). Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc. Natl Acad. Sci. U S A. 106, 7648–7653. Haruta., M., Sabat, G., Stecker, K., Minkoff, B.B., and Sussman, M.R. (2014). A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science. 343, 408–411.
FUNDING
Sha Li and Yan Zhang
1
State Key Laboratory of Crop Biology, College of Life Sciences, Shandong Agricultural University, Daizong St. 61, Tai’an, Shandong, China 1 To whom correspondence should be addressed. E-mail [email protected], tel. 86-538-8246365, fax +86-538-8248696.
References Deslauriers, S.D., and Larsen, P.B. (2010). FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in Arabidopsis hypocotyls. Mol. Plant. 3, 626–640. Duan, Q., Kita, D., Johnson, E.A., Aggarwal, M., Gates, L., Wu, H.-M., and Cheung, A.Y. (2014). Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat. Comms. 5, 3129. Duan, Q., Kita, D., Li, C., Cheung, A.Y., and Wu, H.-M. (2010). FERONIA receptor-like kinase regulates RHO GTPase signaling
Huang, G.-Q., Li, E., Ge F.-R., Li, S., Wang, Q., Zhang, C.-Q., and Zhang, Y. (2013). Arabidopsis RopGEF4 and RopGEF10 are important for FERONIA-mediated developmental but not environmental regulation of root hair growth. New Phytol. 200, 1089–1101. Keinath, N.F., Kierszniowska, S., Lorek, J., Bourdais, G., Kessler, S.A., Shimosato-Asano, H., Grossniklaus, U., Schulze, W.X., Robatzek, S., and Panstruga, R. (2010). PAMP (pathogen-associated molecular pattern)-induced changes in plasma membrane compartmentalization reveals novel components of plant immunity. J. Biol. Chem. 285, 39140–39149. Kessler, S.A., Shimosato-Asano, H., Keinath, N.F., Wuest, S.E., Ingram, G., Panstruga, R., and Grossniklaus, U. (2010). Conserved molecular components for pollen tube reception and fungal invasion. Science. 330, 968–971. Monshausen, G.B., Bibikova, T.N., Messerli, M.A., and Gilroy, S. (2007). Oscillations in extracellular pH and reactive oxygen species modulate tip growth of Arabidopsis root hairs. Proc. Natl Acad. Sci. U S A. 104, 20996–21001. Yu, F., Li, Li, J., Huang, Y., Liu, L., Li, D., Chen, L., and Luan, S. (2014). FERONIA receptor kinase controls seed size in Arabidopsis thaliana. Mol. Plant., published online on Jan 30, 2014, 10.1093/mp/ssu010. Yu, F., Qian, L., Nibau, C., Duan, Q., Kita, D., Levasseur, K., Li, X., Lu, C., Li, H., Hou, C., et al. (2012). FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. Proc. Natl Acad. Sci. U S A. 109, 14693–14698.
Downloaded from http://mplant.oxfordjournals.org/ at Universidade de BrasÃ-lia on May 10, 2014
This work was supported by the Major Research Plant (2013CB945102) from the Ministry of Science and Technology of China to Y.Z. No conflict of interest declared.
