PLANT SIGNALING & BEHAVIOR 2016, VOL. 11, NO. 10, e1238546 (3 pages) http://dx.doi.org/10.1080/15592324.2016.1238546
ARTICLE ADDENDUM
Asymmetric zygote division: A mystery starting point of embryogenesis Jing Zhao and Meng-Xiang Sun College of Life Science, State Key Laboratory of Hybrid Rice, Wuhan University, Wuhan, China
ABSTRACT
ARTICLE HISTORY
In angiosperm, asymmetric zygote division is critical for embryogenesis. The molecular mechanism underlying this process has gained a great attention recently. Some players involve in the control of both accurate position and correct orientation of zygote division plane have been found, which provide useful clues for the extensive investigations. It is getting clear that both internal and external factors are involved in this complex regulatory mechanism and the asymmetric zygote division seems with great impact in cell fate determination and embryo pattern formation.
Received 6 September 2016 Revised 8 September 2016 Accepted 15 September 2016
Zygote is usually considered as the starting point of embryogenesis and the beginning of a new diploid or sporophytic generation in plant life cycle. According to current opinion, once the zygote is divided the embryogenesis process has been visibly activated. In dicot plants, such as tobacco and Arabidopsis, the predictable pattern is elaborated precisely for embryogenesis. The elongated zygote usually divides asymmetrically, giving rise to a larger basal cell and a smaller apical cell with distinct developmental fates. Subsequently, the apical cell divides twice longitudinally and once transversely to form an 8-cell proembryo, whereas the basal cell divides transversely to form a suspensor composed of several cells. Thus, the initial apical and basal domains of a proembryo are stablished. During this process, asymmetric division of the zygote is essential for normal embryogenesis and seed formation. Successful asymmetric zygote division requires the mechanism that ensures both accurate position and correct orientation of cell division plane. In spite of our obscure knowledge, some of the key players involved in this process have emerged, and what’s more, recent works have focused on the variations of the zygote divisions and their influence on the developmental fate of different cell lineages. According to the role that the players are involved in zygote division, 2 categories could be classified in general. One is the genes for regulating accurate position of zygotic division, and the other is the gene regulating proper orientation of zygote division plane, associated with microtubules or cytokinesis. For the former category, YDA MAPK signaling and the WRKY2-WOX genetic network set the stage for better understanding of the asymmetric zygote division.1,2 In the mutants of MAPKK kinase YDA and its downstream AP3/MAP6, the elongation of the zygote is inhibited, producing an apical and basal cells in similar size.3,4 The MAPKK kinase cascade is activated
KEY WORDS
Asymmetric cell division; cell fate; embryogenesis; zygote
by paternal originated SHORT SUSPENSOR (SSP) after fertilization.5 SSP transcripts are produced in sperm, whereas SSP protein is translated after egg-sperm fusion. SSP mutants showed weaker phenotypes than that with loss of YDA or MAP3/MAP6, suggesting existence of other activator for MAPKK kinase cascade. Meanwhile, it is dramatic to identify the direct target of YDA phosphorylation cascade. Recently, the RWP-RK-type transcription factor GROUNDED (GRD)/ RKD4 was revealed as an indirect, but crucial effector of YDA signaling.6,7 Loss of GRD resembles yda mutant, blocking zygote elongation and suppressing suspensor formation. It is noteworthy that loss of GRD eliminates the dominant effects of hyperactive YDA variants, suggesting that GRD may function downstream in the MAP kinase cascade. In addition, recent researches indicated that both CLAVATA3-like peptide CLE88 and EMBRYO SURROUNDING FACTOR 19 are expressed in the endosperm and associated with suspensor development, implying that the YDA pathway is under the control of extracellular maternal effective regulator besides paternal effect.10 The other network which regulates zygotic asymmetric division is WRKY2-WOX pathway.11 The zygotes of WRKY2 Mutant elongate normally, but fail to divide asymmetrically, resulting in apical and basal daughters with similar size and distorted embryo development. WRKY2 is known to function as a transcription factor to activate WOX8/WOX9 transcription directly to establish zygote polarity. More recently, another mutant, zygotic arrest 1 (zar1),12 with a failure in accurate positioning of zygote division plane was identified. ZAR1 was supposed to integrate extracellular stimuli with intracellular Ca2C and Gprotein signaling, to modulate zygotic division in Arabidopsis. Except the position control of zygote division plane, the orientation control of the plane is also a critical issue for accurate asymmetric zygote division. In most plant cells, including
CONTACT Meng-Xiang Sun [email protected] This is an addendum to: Zhao J, Xin H, Cao L, Fu Y, Sun M-X. NtDRP is necessary for maintaining accurate zygotic division orientation and differentiation of embryo and suspensor domains in embryo pattern formation. New Phytologist 2016; http://dx.doi.org/10.1111/nph.14060. © 2016 Taylor & Francis Group, LLC
e1238546-2
J. ZHAO AND M.-X. SUN
embryonic cells, preprophase band (PPB) is essential for a proper division orientation. SABRE,13 CLASP, FASS,14 TONNEAU15 has been shown to be required for PPB establishment1. During the formation and disappearance of PPB, 2 kinesin-12 proteins POK1 and POK216,17 cooperate with microtubules by binding protein TANGLED (TAN)17 to guide the expanding phragmoplast maintaining the division plane. In the telophase, TPLATE protein is together with Clathrin Light Chain2 (CLC2) for cell plate maturation.18 The proteins mentioned above are related to microtubules and directly or indirectly modulate the orientation of cell division plane. However, the defects of mutants for microtubules related genes are mainly described in root and embryos at later stage. Few are related to zygote division. In our previous work, we reported a dynamin related protein, NtDRP, which has a persistent ability of binding microtubules throughout the cell cycle.19 Loss of NtDRP function results in various abnormal orientations of zygote division plane and disturbance of embryo pattern formation. Horizontal, oblique and even vertical orientations could be observed during the zygote division. As the development of the embryo, the RNAi effects at later embryos were still apparent even though the expression of NtDRP was decreased. The aberrant divisions of zygote and early proembryos finally result in the failure of differentiation of basal cell lineage toward suspensor formation. It suggests that accurate asymmetric zygote division is likely critical to the cell fate determination. Up to know, it is clear that both accurate position and orientation control of the zygote division plane are necessary for the proper asymmetric zygote division and both internal genetic factors and microenvironmental cues are involved in this complex regulatory process. However, much more works are required for a clear understanding of the molecular mechanism underlying this process. It is possible that the alterations of the cell division positions or orientations result in different cytoplasmic components portioned into the apical or basal cell, thus modifying their further differentiation. It has been proposed that some cell fate determinants may show a polar distribution in the zygote and be differentially portioned into the apical or basal cell to guide their development.20 We have previously confirmed the uneven distribution of specific transcripts in apical and basal cells of tobacco, which provides each daughter cell a specific transcription program.21 The disorganized distribution of cytoplasmic components may disturb the cell-specific transcription programs and thus modify the cell fate. In addition, for more than one century, there is an accepted rule that the newly formed walls should be perpendicular to existing walls along the long axis of the cell at 90 degree with minimum energy during cell division.22 This seems indicating a cell shape related mechanism and the cell wall, as an external cue, plays a critical role in positioning new cell wall. In fact, the mechanic force from cell wall could indeed regulate position of the nucleus, where cell division will occurs.23 However, genetic regulation in embryo can create patterns by overriding the default rule.24 As revealed in our previous work, NtDRP is involved in regulating the zygotic division plane orientation by binding to microtubules and modulating microtubule spatial organization and spindle orientation. In this case, both cell shape and cell division pattern are modified. These works point
to a mechanism that cytoskeleton-directed cell shaping and cell wall deposition may control cell division pattern, in which both internal and external factors are involved and interacted. Obviously, how the factors cooperate with each other is still a longstanding question to be resolved. Although asymmetric zygote division is generally considered critical for embryogenesis it is still debatable that if the proper asymmetric zygote division is essential to the apical and basal cell fate determination and subsequent embryo pattern formation, or in another word, the real role of the asymmetric zygote division itself in early embryogenesis is not clear yet. To address this question we actually need a cell division regulator that specifically expressed in zygote and only modify the position or orientation of zygote division plane without any influence on cell shape and cell polarity. Alternatively, it is also useful to find a similar regulator that expressed in all embryo cells, but not in zygote only. The mutants of the genes encoding these regulators will greatly facilitate our understanding on the developmental impact of the zygote asymmetric division in embryogenesis and revealing the answer for the mystery. Hopefully, these unique materials will be available in the near future.
Disclosure of potential conflicts of interest No potential conflicts of interest were disclosed.
References 1. van Dop M, Liao CY, Weijers D. Control of oriented cell division in the Arabidopsis embryo. Curr Opin Plant Biol 2015; 23:25-30; PMID:25449723; http://dx.doi.org/10.1016/j.pbi.2014.10.004 2. Ueda M, Laux T. The origin of the plant body axis. Curr Opin Plant Biol 2012; 15:578-84; PMID:22921364; http://dx.doi.org/10.1016/j. pbi.2012.08.001 3. Lukowitz W, Roeder A, Parmenter D, Somerville C. A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 2004; 116:109-19; PMID:14718171; http://dx.doi.org/10.1016/S0092-8674 (03)01067-5 4. Wang HC, Ngwenyama N, Liu YD, Walker JC, Zhang SQ. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 2007; 19:63-73; PMID:17259259; http://dx.doi.org/10.1105/tpc.106.048298 5. Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W. Paternal control of embryonic patterning in Arabidopsis thaliana. Science 2009; 323:1485-8; PMID:19286558; http://dx.doi.org/10.1126/ science.1167784 6. Jeong S, Palmer TM, Lukowitz W. The RWP-RK factor GROUNDED promotes embryonic polarity by facilitating YODA MAP kinase signaling. Curr Biol 2011; 21:1268-76; PMID:21802295; http://dx.doi. org/10.1016/j.cub.2011.06.049 7. Waki T, Hiki T, Watanabe R, Hashimoto T, Nakajima K. The Arabidopsis RWP-RK protein RKD4 triggers gene expression and pattern formation in early embryogenesis. Curr Biol 2011; 21:1277-81; PMID:21802301; http://dx.doi.org/10.1016/j.cub.2011.07.001 8. Fiume E, Fletcher JC. Regulation of Arabidopsis embryo and endosperm development by the polypeptide signaling molecule CLE8. Plant Cell 2012; 24:1000-12; PMID:22427333; http://dx.doi.org/ 10.1105/tpc.111.094839 9. Costa LM, Marshall E, Tesfaye M, Silverstein KAT, Mori M, Umetsu Y, Otterbach SL, Papareddy R, Dickinson HG, Boutiller K, et al. Central cell-derived peptides regulate early embryo patterning in flowering plants. Science 2014; 344:168-72; PMID:24723605; http://dx.doi. org/10.1126/science.1243005
PLANT SIGNALING & BEHAVIOR
10. Jeong S, Eilbert E, Bolbol A, Lukowitz W. Going mainstream: How is the body axis of plants first initiated in the embryo? Dev Biol 2016; S0012-1606:30158-0; http://dx.doi.org/10.1016/j.ydbio.2016.05.002 11. Ueda M, Zhang ZJ, Laux T. Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev Cell 2011; 20:264-70; PMID:21316593; http://dx.doi.org/ 10.1016/j.devcel.2011.01.009 12. Yu TY, Shi DQ, Jia PF, Tang J, Li HJ, Liu J, Yang WC. The Arabidopsis receptor kinase ZAR1 is required for zygote asymmetric division and its daughter cell fate. Plos Genet 2016; 12:e1005933; http://dx.doi. org/10.1371/journal.pgen.1005933 13. Pietra S, Gustavsson A, Kiefer C, Kalmbach L, Horstedt P, Ikeda Y, Stepanova AN, Alonso JM, Grebe M. Arabidopsis SABRE and CLASP interact to stabilize cell division plane orientation and planar polarity. Nat Commun 2013; 4:2779; PMID:24240534; http://dx.doi.org/ 10.1038/ncomms3779 14. Spinner L, Gadeyne A, Belcram K, Goussot M, Moison M, Duroc Y, Eeckhout D, De Winne N, Schaefer E, Van De Slijke E, et al. A protein phosphatase 2A complex spatially controls plant cell division. Nature Commun 2013; 4:1863; http://dx.doi.org/10.1038/ncomms2831 15. Drevensek S, Goussot M, Duroc Y, Christodoulidou A, Steyaert S, Schaefer E, Duvernois E, Grandjean O, Vantard M, Bouchez D, et al. The Arabidopsis TRM1-TON1 interaction reveals a recruitment network common to plant cortical microtubule arrays and eukaryotic centrosomes. Plant Cell 2012; 24:178-91; PMID:22286137; http://dx. doi.org/10.1105/tpc.111.089748 16. Muller S, Han SC, Smith LG. Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr Biol 2006; 16:88894; PMID:16682350; http://dx.doi.org/10.1016/j.cub.2006.03.034 17. Lipka E, Gadeyne A, Stockle D, Zimmermann S, De Jaeger G, Ehrhardt DW, Kirik V, Van Damme D, M€ uller S. The phragmoplast-
18.
19.
20.
21.
22. 23.
24.
e1238546-3
orienting kinesin-12 class proteins translate the positional information of the preprophase band to establish the cortical division zone in Arabidopsis thaliana. Plant Cell 2014; 26:2617-32; PMID:24972597; http://dx.doi.org/10.1105/tpc.114.124933 Gadeyne A, Sanchez-Rodriguez C, Vanneste S, Di Rubbo S, Zauber H, Vanneste K, Van Leene J, De Winne N, Eeckhout D, Persiau G, et al. The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants. Cell 2014; 156:691-704; PMID:24529374; http://dx.doi.org/ 10.1016/j.cell.2014.01.039 Zhao J, Xin H, Cao L, Fu Y, Sun MX. NtDRP is necessary for maintaining accurate zygotic division orientation and differentiation of embryo and suspensor domains in embryo pattern formation. New Phytologist 2016; http://dx.doi.org/10.1111/ nph.14060 Mayer U, B€ uttner G, J€ urgens G. Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 1993; 117:149-62 Ma LG, Xin HP, Qu LH, Zhao J, Yang LB, Zhao P, Sun M. Transcription profile analysis reveals that zygotic division results in uneven distribution of specific transcripts in apical/basal cells of tobacco. PloS One 2011; 6:e15971; PMID:21249132; http://dx.doi.org/10.1371/ journal.pone.0015971 € Sachs J. Uber die Anordnung der Zellen in j€ ungsten Pflanzentheilen. Stahel’schen 1877 Qu LH, Sun MX. The plant cell nucleus is constantly alert and highly sensitive to repetitive local mechanical stimulations. Plant Cell Rep 2007; 26:1187-1193; PMID:17396239; http://dx.doi.org/10.1007/ s00299-007-0343-6 Besson S, Dumais J. Universal rule for the symmetric division of plant cells. Proc Natl Acad Sci USA 2011; 108:6294-9; PMID:21383128; http://dx.doi.org/10.1073/pnas.1011866108
ARTICLE ADDENDUM
Asymmetric zygote division: A mystery starting point of embryogenesis Jing Zhao and Meng-Xiang Sun College of Life Science, State Key Laboratory of Hybrid Rice, Wuhan University, Wuhan, China
ABSTRACT
ARTICLE HISTORY
In angiosperm, asymmetric zygote division is critical for embryogenesis. The molecular mechanism underlying this process has gained a great attention recently. Some players involve in the control of both accurate position and correct orientation of zygote division plane have been found, which provide useful clues for the extensive investigations. It is getting clear that both internal and external factors are involved in this complex regulatory mechanism and the asymmetric zygote division seems with great impact in cell fate determination and embryo pattern formation.
Received 6 September 2016 Revised 8 September 2016 Accepted 15 September 2016
Zygote is usually considered as the starting point of embryogenesis and the beginning of a new diploid or sporophytic generation in plant life cycle. According to current opinion, once the zygote is divided the embryogenesis process has been visibly activated. In dicot plants, such as tobacco and Arabidopsis, the predictable pattern is elaborated precisely for embryogenesis. The elongated zygote usually divides asymmetrically, giving rise to a larger basal cell and a smaller apical cell with distinct developmental fates. Subsequently, the apical cell divides twice longitudinally and once transversely to form an 8-cell proembryo, whereas the basal cell divides transversely to form a suspensor composed of several cells. Thus, the initial apical and basal domains of a proembryo are stablished. During this process, asymmetric division of the zygote is essential for normal embryogenesis and seed formation. Successful asymmetric zygote division requires the mechanism that ensures both accurate position and correct orientation of cell division plane. In spite of our obscure knowledge, some of the key players involved in this process have emerged, and what’s more, recent works have focused on the variations of the zygote divisions and their influence on the developmental fate of different cell lineages. According to the role that the players are involved in zygote division, 2 categories could be classified in general. One is the genes for regulating accurate position of zygotic division, and the other is the gene regulating proper orientation of zygote division plane, associated with microtubules or cytokinesis. For the former category, YDA MAPK signaling and the WRKY2-WOX genetic network set the stage for better understanding of the asymmetric zygote division.1,2 In the mutants of MAPKK kinase YDA and its downstream AP3/MAP6, the elongation of the zygote is inhibited, producing an apical and basal cells in similar size.3,4 The MAPKK kinase cascade is activated
KEY WORDS
Asymmetric cell division; cell fate; embryogenesis; zygote
by paternal originated SHORT SUSPENSOR (SSP) after fertilization.5 SSP transcripts are produced in sperm, whereas SSP protein is translated after egg-sperm fusion. SSP mutants showed weaker phenotypes than that with loss of YDA or MAP3/MAP6, suggesting existence of other activator for MAPKK kinase cascade. Meanwhile, it is dramatic to identify the direct target of YDA phosphorylation cascade. Recently, the RWP-RK-type transcription factor GROUNDED (GRD)/ RKD4 was revealed as an indirect, but crucial effector of YDA signaling.6,7 Loss of GRD resembles yda mutant, blocking zygote elongation and suppressing suspensor formation. It is noteworthy that loss of GRD eliminates the dominant effects of hyperactive YDA variants, suggesting that GRD may function downstream in the MAP kinase cascade. In addition, recent researches indicated that both CLAVATA3-like peptide CLE88 and EMBRYO SURROUNDING FACTOR 19 are expressed in the endosperm and associated with suspensor development, implying that the YDA pathway is under the control of extracellular maternal effective regulator besides paternal effect.10 The other network which regulates zygotic asymmetric division is WRKY2-WOX pathway.11 The zygotes of WRKY2 Mutant elongate normally, but fail to divide asymmetrically, resulting in apical and basal daughters with similar size and distorted embryo development. WRKY2 is known to function as a transcription factor to activate WOX8/WOX9 transcription directly to establish zygote polarity. More recently, another mutant, zygotic arrest 1 (zar1),12 with a failure in accurate positioning of zygote division plane was identified. ZAR1 was supposed to integrate extracellular stimuli with intracellular Ca2C and Gprotein signaling, to modulate zygotic division in Arabidopsis. Except the position control of zygote division plane, the orientation control of the plane is also a critical issue for accurate asymmetric zygote division. In most plant cells, including
CONTACT Meng-Xiang Sun [email protected] This is an addendum to: Zhao J, Xin H, Cao L, Fu Y, Sun M-X. NtDRP is necessary for maintaining accurate zygotic division orientation and differentiation of embryo and suspensor domains in embryo pattern formation. New Phytologist 2016; http://dx.doi.org/10.1111/nph.14060. © 2016 Taylor & Francis Group, LLC
e1238546-2
J. ZHAO AND M.-X. SUN
embryonic cells, preprophase band (PPB) is essential for a proper division orientation. SABRE,13 CLASP, FASS,14 TONNEAU15 has been shown to be required for PPB establishment1. During the formation and disappearance of PPB, 2 kinesin-12 proteins POK1 and POK216,17 cooperate with microtubules by binding protein TANGLED (TAN)17 to guide the expanding phragmoplast maintaining the division plane. In the telophase, TPLATE protein is together with Clathrin Light Chain2 (CLC2) for cell plate maturation.18 The proteins mentioned above are related to microtubules and directly or indirectly modulate the orientation of cell division plane. However, the defects of mutants for microtubules related genes are mainly described in root and embryos at later stage. Few are related to zygote division. In our previous work, we reported a dynamin related protein, NtDRP, which has a persistent ability of binding microtubules throughout the cell cycle.19 Loss of NtDRP function results in various abnormal orientations of zygote division plane and disturbance of embryo pattern formation. Horizontal, oblique and even vertical orientations could be observed during the zygote division. As the development of the embryo, the RNAi effects at later embryos were still apparent even though the expression of NtDRP was decreased. The aberrant divisions of zygote and early proembryos finally result in the failure of differentiation of basal cell lineage toward suspensor formation. It suggests that accurate asymmetric zygote division is likely critical to the cell fate determination. Up to know, it is clear that both accurate position and orientation control of the zygote division plane are necessary for the proper asymmetric zygote division and both internal genetic factors and microenvironmental cues are involved in this complex regulatory process. However, much more works are required for a clear understanding of the molecular mechanism underlying this process. It is possible that the alterations of the cell division positions or orientations result in different cytoplasmic components portioned into the apical or basal cell, thus modifying their further differentiation. It has been proposed that some cell fate determinants may show a polar distribution in the zygote and be differentially portioned into the apical or basal cell to guide their development.20 We have previously confirmed the uneven distribution of specific transcripts in apical and basal cells of tobacco, which provides each daughter cell a specific transcription program.21 The disorganized distribution of cytoplasmic components may disturb the cell-specific transcription programs and thus modify the cell fate. In addition, for more than one century, there is an accepted rule that the newly formed walls should be perpendicular to existing walls along the long axis of the cell at 90 degree with minimum energy during cell division.22 This seems indicating a cell shape related mechanism and the cell wall, as an external cue, plays a critical role in positioning new cell wall. In fact, the mechanic force from cell wall could indeed regulate position of the nucleus, where cell division will occurs.23 However, genetic regulation in embryo can create patterns by overriding the default rule.24 As revealed in our previous work, NtDRP is involved in regulating the zygotic division plane orientation by binding to microtubules and modulating microtubule spatial organization and spindle orientation. In this case, both cell shape and cell division pattern are modified. These works point
to a mechanism that cytoskeleton-directed cell shaping and cell wall deposition may control cell division pattern, in which both internal and external factors are involved and interacted. Obviously, how the factors cooperate with each other is still a longstanding question to be resolved. Although asymmetric zygote division is generally considered critical for embryogenesis it is still debatable that if the proper asymmetric zygote division is essential to the apical and basal cell fate determination and subsequent embryo pattern formation, or in another word, the real role of the asymmetric zygote division itself in early embryogenesis is not clear yet. To address this question we actually need a cell division regulator that specifically expressed in zygote and only modify the position or orientation of zygote division plane without any influence on cell shape and cell polarity. Alternatively, it is also useful to find a similar regulator that expressed in all embryo cells, but not in zygote only. The mutants of the genes encoding these regulators will greatly facilitate our understanding on the developmental impact of the zygote asymmetric division in embryogenesis and revealing the answer for the mystery. Hopefully, these unique materials will be available in the near future.
Disclosure of potential conflicts of interest No potential conflicts of interest were disclosed.
References 1. van Dop M, Liao CY, Weijers D. Control of oriented cell division in the Arabidopsis embryo. Curr Opin Plant Biol 2015; 23:25-30; PMID:25449723; http://dx.doi.org/10.1016/j.pbi.2014.10.004 2. Ueda M, Laux T. The origin of the plant body axis. Curr Opin Plant Biol 2012; 15:578-84; PMID:22921364; http://dx.doi.org/10.1016/j. pbi.2012.08.001 3. Lukowitz W, Roeder A, Parmenter D, Somerville C. A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell 2004; 116:109-19; PMID:14718171; http://dx.doi.org/10.1016/S0092-8674 (03)01067-5 4. Wang HC, Ngwenyama N, Liu YD, Walker JC, Zhang SQ. Stomatal development and patterning are regulated by environmentally responsive mitogen-activated protein kinases in Arabidopsis. Plant Cell 2007; 19:63-73; PMID:17259259; http://dx.doi.org/10.1105/tpc.106.048298 5. Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W. Paternal control of embryonic patterning in Arabidopsis thaliana. Science 2009; 323:1485-8; PMID:19286558; http://dx.doi.org/10.1126/ science.1167784 6. Jeong S, Palmer TM, Lukowitz W. The RWP-RK factor GROUNDED promotes embryonic polarity by facilitating YODA MAP kinase signaling. Curr Biol 2011; 21:1268-76; PMID:21802295; http://dx.doi. org/10.1016/j.cub.2011.06.049 7. Waki T, Hiki T, Watanabe R, Hashimoto T, Nakajima K. The Arabidopsis RWP-RK protein RKD4 triggers gene expression and pattern formation in early embryogenesis. Curr Biol 2011; 21:1277-81; PMID:21802301; http://dx.doi.org/10.1016/j.cub.2011.07.001 8. Fiume E, Fletcher JC. Regulation of Arabidopsis embryo and endosperm development by the polypeptide signaling molecule CLE8. Plant Cell 2012; 24:1000-12; PMID:22427333; http://dx.doi.org/ 10.1105/tpc.111.094839 9. Costa LM, Marshall E, Tesfaye M, Silverstein KAT, Mori M, Umetsu Y, Otterbach SL, Papareddy R, Dickinson HG, Boutiller K, et al. Central cell-derived peptides regulate early embryo patterning in flowering plants. Science 2014; 344:168-72; PMID:24723605; http://dx.doi. org/10.1126/science.1243005
PLANT SIGNALING & BEHAVIOR
10. Jeong S, Eilbert E, Bolbol A, Lukowitz W. Going mainstream: How is the body axis of plants first initiated in the embryo? Dev Biol 2016; S0012-1606:30158-0; http://dx.doi.org/10.1016/j.ydbio.2016.05.002 11. Ueda M, Zhang ZJ, Laux T. Transcriptional activation of Arabidopsis axis patterning genes WOX8/9 links zygote polarity to embryo development. Dev Cell 2011; 20:264-70; PMID:21316593; http://dx.doi.org/ 10.1016/j.devcel.2011.01.009 12. Yu TY, Shi DQ, Jia PF, Tang J, Li HJ, Liu J, Yang WC. The Arabidopsis receptor kinase ZAR1 is required for zygote asymmetric division and its daughter cell fate. Plos Genet 2016; 12:e1005933; http://dx.doi. org/10.1371/journal.pgen.1005933 13. Pietra S, Gustavsson A, Kiefer C, Kalmbach L, Horstedt P, Ikeda Y, Stepanova AN, Alonso JM, Grebe M. Arabidopsis SABRE and CLASP interact to stabilize cell division plane orientation and planar polarity. Nat Commun 2013; 4:2779; PMID:24240534; http://dx.doi.org/ 10.1038/ncomms3779 14. Spinner L, Gadeyne A, Belcram K, Goussot M, Moison M, Duroc Y, Eeckhout D, De Winne N, Schaefer E, Van De Slijke E, et al. A protein phosphatase 2A complex spatially controls plant cell division. Nature Commun 2013; 4:1863; http://dx.doi.org/10.1038/ncomms2831 15. Drevensek S, Goussot M, Duroc Y, Christodoulidou A, Steyaert S, Schaefer E, Duvernois E, Grandjean O, Vantard M, Bouchez D, et al. The Arabidopsis TRM1-TON1 interaction reveals a recruitment network common to plant cortical microtubule arrays and eukaryotic centrosomes. Plant Cell 2012; 24:178-91; PMID:22286137; http://dx. doi.org/10.1105/tpc.111.089748 16. Muller S, Han SC, Smith LG. Two kinesins are involved in the spatial control of cytokinesis in Arabidopsis thaliana. Curr Biol 2006; 16:88894; PMID:16682350; http://dx.doi.org/10.1016/j.cub.2006.03.034 17. Lipka E, Gadeyne A, Stockle D, Zimmermann S, De Jaeger G, Ehrhardt DW, Kirik V, Van Damme D, M€ uller S. The phragmoplast-
18.
19.
20.
21.
22. 23.
24.
e1238546-3
orienting kinesin-12 class proteins translate the positional information of the preprophase band to establish the cortical division zone in Arabidopsis thaliana. Plant Cell 2014; 26:2617-32; PMID:24972597; http://dx.doi.org/10.1105/tpc.114.124933 Gadeyne A, Sanchez-Rodriguez C, Vanneste S, Di Rubbo S, Zauber H, Vanneste K, Van Leene J, De Winne N, Eeckhout D, Persiau G, et al. The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants. Cell 2014; 156:691-704; PMID:24529374; http://dx.doi.org/ 10.1016/j.cell.2014.01.039 Zhao J, Xin H, Cao L, Fu Y, Sun MX. NtDRP is necessary for maintaining accurate zygotic division orientation and differentiation of embryo and suspensor domains in embryo pattern formation. New Phytologist 2016; http://dx.doi.org/10.1111/ nph.14060 Mayer U, B€ uttner G, J€ urgens G. Apical-basal pattern formation in the Arabidopsis embryo: studies on the role of the gnom gene. Development 1993; 117:149-62 Ma LG, Xin HP, Qu LH, Zhao J, Yang LB, Zhao P, Sun M. Transcription profile analysis reveals that zygotic division results in uneven distribution of specific transcripts in apical/basal cells of tobacco. PloS One 2011; 6:e15971; PMID:21249132; http://dx.doi.org/10.1371/ journal.pone.0015971 € Sachs J. Uber die Anordnung der Zellen in j€ ungsten Pflanzentheilen. Stahel’schen 1877 Qu LH, Sun MX. The plant cell nucleus is constantly alert and highly sensitive to repetitive local mechanical stimulations. Plant Cell Rep 2007; 26:1187-1193; PMID:17396239; http://dx.doi.org/10.1007/ s00299-007-0343-6 Besson S, Dumais J. Universal rule for the symmetric division of plant cells. Proc Natl Acad Sci USA 2011; 108:6294-9; PMID:21383128; http://dx.doi.org/10.1073/pnas.1011866108
