Patterning the embryo in higher plants: Emerging pathways and challenges

Abstract

Embryogenesis, which establishes the basic body plan for the post-embryonic organs after stereotyped cell divisions, initiates the first step of the plant life cycle. Studies in the last two decades indicate that embryogenesis is a precisely controlled process, and any defect would result in abnormalities. Here we discuss the recent progresses, with a focus on the cellular pathways governing early embryogenesis in the model species BoldItalic.

Keywords

Arabidopsis embryogenesis / auxin signaling / receptor-like kinases (RLKs) / non-cell-autonomous transcription factors and microRNA

References

[1] Abe M, Katsumata H, Komeda Y, Takahashi T (2003). Regulation of shoot epidermal cell differentiation by a pair of homeodomain proteins in Arabidopsis. Development, 130(4): 635-643

[2] Abe M, Takahashi T, Komeda Y (1999). Cloning and characterization of an L1 layer-specific gene in Arabidopsis thaliana. Plant Cell Physiol, 40(6): 571-580

[3] Abrash E B, Bergmann D C (2009). Asymmetric cell divisions: a view from plant development. Dev Cell, 16(6): 783-796

[4] Aida M, Beis D, Heidstra R, Willemsen V, Blilou I, Galinha C, Nussaume L, Noh Y S, Amasino R, Scheres B (2004). The PLETHORA genes mediate patterning of the Arabidopsis root stem cell niche. Cell, 119(1): 109-120

[5] Aida M, Vernoux T, Furutani M, Traas J, Tasaka M (2002). Roles of PIN-FORMED1 and MONOPTEROS in pattern formation of the apical region of the Arabidopsis embryo. Development, 129(17): 3965-3974

[6] Bayer M, Nawy T, Giglione C, Galli M, Meinnel T, Lukowitz W (2009). Paternal control of embryonic patterning in Arabidopsis thaliana. Science, 323(5920): 1485-1488

[7] Benková E, Michniewicz M, Sauer M, Teichmann T, Seifertová D, Jürgens G, Friml J (2003). Local, efflux-dependent auxin gradients as a common module for plant organ formation. Cell, 115(5): 591-602

[8] Berger D, Altmann T (2000). A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. Genes Dev, 14(9): 1119-1131

[9] Blilou I, Xu J, Wildwater M, Willemsen V, Paponov I, Friml J, Heidstra R, Aida M, Palme K, Scheres B (2005). The PIN auxin efflux facilitator network controls growth and patterning in Arabidopsis roots. Nature, 433(7021): 39-44

[10] Brand U, Fletcher J C, Hobe M, Meyerowitz E M, Simon R (2000). Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science, 289(5479): 617-619

[11] Breuninger H, Rikirsch E, Hermann M, Ueda M, Laux T (2008). Differential expression of WOX genes mediates apical-basal axis formation in the Arabidopsis embryo. Dev Cell, 14(6): 867-876

[12] Carlsbecker A, Lee J Y, Roberts C J, Dettmer J, Lehesranta S, Zhou J, Lindgren O, Moreno-Risueno M A, Vatén A, Thitamadee S, Campilho A, Sebastian J, Bowman J L, Helariutta Y, Benfey P N (2010). Cell signalling by microRNA165/6 directs gene dose-dependent root cell fate. Nature, 465(7296): 316-321

[13] Cartwright H N, Humphries J A, Smith L G (2009). PAN1: a receptor-like protein that promotes polarization of an asymmetric cell division in maize. Science, 323(5914): 649-651

[14] Chandler J W, Cole M, Flier A, Grewe B, Werr W (2007). The AP2 transcription factors DORNROSCHEN and DORNROSCHEN-LIKE redundantly control Arabidopsis embryo patterning via interaction with PHAVOLUTA. Development, 134(9): 1653-1662

[15] Cheng Y, Dai X, Zhao Y (2007). Auxin synthesized by the YUCCA flavin monooxygenases is essential for embryogenesis and leaf formation in Arabidopsis. Plant Cell, 19(8): 2430-2439

[16] Cole M, Chandler J, Weijers D, Jacobs B, Comelli P, Werr W (2009). DORNROSCHEN is a direct target of the auxin response factor MONOPTEROS in the Arabidopsis embryo. Development, 136(10): 1643-1651

[17] De Smet I, Lau S, Mayer U, Jürgens G (2010). Embryogenesis–the humble beginnings of plant life. Plant J, 61(6): 959-970

[18] De Smet I, Vassileva V, De Rybel B, Levesque M P, Grunewald W, Van Damme D, Van Noorden G, Naudts M, Van Isterdael G, De Clercq R, Wang J Y, Meuli N, Vanneste S, Friml J, Hilson P, Jürgens G, Ingram G C, Inzé D, Benfey P N, Beeckman T (2008). Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science, 322(5901): 594-597

[19] De Smet I, Voss U, Jürgens G, Beeckman T (2009). Receptor-like kinases shape the plant. Nat Cell Biol, 11(10): 1166-1173

[20] DeYoung B J, Bickle K L, Schrage K J, Muskett P, Patel K, Clark S E (2006). The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis. Plant J, 45(1): 1-16

[21] Deyoung B J, Clark S E (2008). BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics, 180(2): 895-904

[22] Dhonukshe P, Tanaka H, Goh T, Ebine K, Mähönen A P, Prasad K, Blilou I, Geldner N, Xu J, Uemura T, Chory J, Ueda T, Nakano A, Scheres B, Friml J (2008). Generation of cell polarity in plants links endocytosis, auxin distribution and cell fate decisions. Nature, 456(7224): 962-966

[23] Dong J, MacAlister C A, Bergmann D C (2009). BASL controls asymmetric cell division in Arabidopsis. Cell, 137(7): 1320-1330

[24] Etchells J P, Turner S R (2010). The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development, 137(5): 767-774

[25] Friml J, Vieten A, Sauer M, Weijers D, Schwarz H, Hamann T, Offringa R, Jürgens G (2003). Efflux-dependent auxin gradients establish the apical-basal axis of Arabidopsis. Nature, 426(6963): 147-153

[26] Friml J, Yang X, Michniewicz M, Weijers D, Quint A, Tietz O, Benjamins R, Ouwerkerk P B, Ljung K, Sandberg G, Hooykaas P J, Palme K, Offringa R (2004). A PINOID-dependent binary switch in apical-basal PIN polar targeting directs auxin efflux. Science, 306(5697): 862-865

[27] Furutani M, Vernoux T, Traas J, Kato T, Tasaka M, Aida M (2004). PIN-FORMED1 and PINOID regulate boundary formation and cotyledon development in Arabidopsis embryogenesis. Development, 131(20): 5021-5030

[28] Galinha C, Hofhuis H, Luijten M, Willemsen V, Blilou I, Heidstra R, Scheres B (2007). PLETHORA proteins as dose-dependent master regulators of Arabidopsis root development. Nature, 449(7165): 1053-1057

[29] Gehring M, Huh J H, Hsieh T F, Penterman J, Choi Y, Harada J J, Goldberg R B, Fischer R L (2006). DEMETER DNA glycosylase establishes MEDEA polycomb gene self-imprinting by allele-specific demethylation. Cell, 124(3): 495-506

[30] Geldner N, Anders N, Wolters H, Keicher J, Kornberger W, Muller P, Delbarre A, Ueda T, Nakano A, Jürgens G (2003). The Arabidopsis GNOM ARF-GEF mediates endosomal recycling, auxin transport, and auxin-dependent plant growth. Cell, 112(2): 219-230

[31] Gifford M L, Robertson F C, Soares D C, Ingram G C (2005). ARABIDOPSIS CRINKLY4 function, internalization, and turnover are dependent on the extracellular crinkly repeat domain. Plant Cell, 17(4): 1154-1166

[32] Goldstein B, Takeshita H, Mizumoto K, Sawa H (2006). Wnt signals can function as positional cues in establishing cell polarity. Dev Cell, 10(3): 391-396

[33] Green K A, Prigge M J, Katzman R B, Clark S E (2005). CORONA, a member of the class III homeodomain leucine zipper gene family in Arabidopsis, regulates stem cell specification and organogenesis. Plant Cell, 17(3): 691-704

[34] Grossniklaus U, Vielle-Calzada J P, Hoeppner M A, Gagliano W B (1998). Maternal control of embryogenesis by MEDEA, a polycomb group gene in Arabidopsis. Science, 280(5362): 446-450

[35] Grunewald W, Friml J (2010). The march of the PINs: developmental plasticity by dynamic polar targeting in plant cells. EMBO J, 29(16): 2700-2714

[36] Haecker A, Gross-Hardt R, Geiges B, Sarkar A, Breuninger H, Herrmann M, Laux T (2004). Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development, 131(3): 657-668

[37] Hall Q, Cannon M C (2002). The cell wall hydroxyproline-rich glycoprotein RSH is essential for normal embryo development in Arabidopsis. Plant Cell, 14(5): 1161-1172

[38] Hamann T, Benkova E, Bäurle I, Kientz M, Jürgens G (2002). The Arabidopsis BODENLOS gene encodes an auxin response protein inhibiting MONOPTEROS-mediated embryo patterning. Genes Dev, 16(13): 1610-1615

[39] Hamann T, Mayer U, Jürgens G (1999). The auxin-insensitive bodenlos mutation affects primary root formation and apical-basal patterning in the Arabidopsis embryo. Development, 126(7): 1387-1395

[40] Hardtke C S, Berleth T (1998). The Arabidopsis gene MONOPTEROS encodes a transcription factor mediating embryo axis formation and vascular development. EMBO J, 17(5): 1405-1411

[41] Hazak O, Bloch D, Poraty L, Sternberg H, Zhang J, Friml J, Yalovsky S, Leyser O (2010). A rho scaffold integrates the secretory system with feedback mechanisms in regulation of auxin distribution. PLoS Biol, 8(1): e1000282

[42] Helariutta Y, Fukaki H, Wysocka-Diller J, Nakajima K, Jung J, Sena G, Hauser M T, Benfey P N (2000). The SHORT-ROOT gene controls radial patterning of the Arabidopsis root through radial signaling. Cell, 101(5): 555-567

[43] Hirakawa Y, Shinohara H, Kondo Y, Inoue A, Nakanomyo I, Ogawa M, Sawa S, Ohashi-Ito K, Matsubayashi Y, Fukuda H (2008). Non-cell-autonomous control of vascular stem cell fate by a CLE peptide/receptor system. Proc Natl Acad Sci U S A, 105(39): 15208-15213

[44] Hobe M, Müller R, Grünewald M, Brand U, Simon R (2003). Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis. Dev Genes Evol, 213(8): 371-381

[45] Huang F, Zago M K, Abas L, van Marion A, Galván-Ampudia C S, Offringa R (2010). Phosphorylation of conserved PIN motifs directs Arabidopsis PIN1 polarity and auxin transport. Plant Cell, 22(4): 1129-1142

[46] Kemphues K J, Priess J R, Morton D G, Cheng N S (1988). Identification of genes required for cytoplasmic localization in early C. elegans embryos. Cell, 52(3): 311-320

[47] Kim I, Cho E, Crawford K, Hempel F D, Zambryski P C (2005a). Cell-to-cell movement of GFP during embryogenesis and early seedling development in Arabidopsis. Proc Natl Acad Sci USA, 102(6): 2227-2231

[48] Kim I, Hempel F D, Sha K, Pfluger J, Zambryski P C (2002). Identification of a developmental transition in plasmodesmatal function during embryogenesis in Arabidopsis thaliana. Development, 129(5): 1261-1272

[49] Kim I, Kobayashi K, Cho E, Zambryski P C (2005b). Subdomains for transport via plasmodesmata corresponding to the apical-basal axis are established during Arabidopsis embryogenesis. Proc Natl Acad Sci USA, 102(33): 11945-11950

[50] Kleine-Vehn J, Huang F, Naramoto S, Zhang J, Michniewicz M, Offringa R, Friml J (2009). PIN auxin efflux carrier polarity is regulated by PINOID kinase-mediated recruitment into GNOM-independent trafficking in Arabidopsis. Plant Cell, 21(12): 3839-3849

[51] Kobayashi K, Otegui M S, Krishnakumar S, Mindrinos M, Zambryski P (2007). INCREASED SIZE EXCLUSION LIMIT 2 encodes a putative DEVH box RNA helicase involved in plasmodesmata function during Arabidopsis embryogenesis. Plant Cell, 19(6): 1885-1897

[52] Laufs P, Peaucelle A, Morin H, Traas J (2004). MicroRNA regulation of the CUC genes is required for boundary size control in Arabidopsis meristems. Development, 131(17): 4311-4322

[53] Leyser O (2005). Auxin distribution and plant pattern formation: how many angels can dance on the point of PIN? Cell, 121(6): 819-822

[54] Li H J, Liu N Y, Shi D Q, Liu J, Yang W C (2010). YAO is a nucleolar WD40-repeat protein critical for embryogenesis and gametogenesis in Arabidopsis. BMC Plant Biol, 10: 169

[55] Long J A (2006). TOPLESS Regulates Apical Embryonic Fate in Arabidopsis. Science, 312(5779): 1520-1523

[56] Lukowitz W, Roeder A, Parmenter D, Somerville C (2004). A MAPKK kinase gene regulates extra-embryonic cell fate in Arabidopsis. Cell, 116(1): 109-119

[57] Mallory A C, Dugas D V, Bartel D P, Bartel B (2004). MicroRNA regulation of NAC-domain targets is required for proper formation and separation of adjacent embryonic, vegetative, and floral organs. Curr Biol, 14(12): 1035-1046

[58] Mattsson J, Ckurshumova W, Berleth T (2003). Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol, 131(3): 1327-1339

[59] Mayer K F, Schoof H, Haecker A, Lenhard M, Jürgens G, Laux T (1998). Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell, 95(6): 805-815

[60] Menke F L H, Scheres B (2009). Plant asymmetric cell division, vive la différence! Cell, 137(7): 1189-1192

[61] Michniewicz M, Zago M K, Abas L, Weijers D, Schweighofer A, Meskiene I, Heisler M G, Ohno C, Zhang J, Huang F, Schwab R, Weigel D, Meyerowitz E M, Luschnig C, Offringa R, Friml J (2007). Antagonistic regulation of PIN phosphorylation by PP2A and PINOID directs auxin flux. Cell, 130(6): 1044-1056

[62] Miwa H, Kinoshita A, Fukuda H, Sawa S (2009). Plant meristems: CLAVATA3/ESR-related signaling in the shoot apical meristem and the root apical meristem. J Plant Res, 122(1): 31-39

[63] Moussian B, Schoof H, Haecker A, Jürgens G, Laux T (1998). Role of the ZWILLE gene in the regulation of central shoot meristem cell fate during Arabidopsis embryogenesis. EMBO J, 17(6): 1799-1809

[64] Müller R, Bleckmann A, Simon R (2008). The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1. Plant Cell, 20(4): 934-946

[65] Nakajima K, Sena G, Nawy T, Benfey P N (2001). Intercellular movement of the putative transcription factor SHR in root patterning. Nature, 413(6853): 307-311

[66] Nodine M D, Tax F E (2008). Two receptor-like kinases required together for the establishment of Arabidopsis cotyledon primordia. Dev Biol, 314(1): 161-170

[67] Nodine M D, Yadegari R, Tax F E (2007). RPK1 and TOAD2 are two receptor-like kinases redundantly required for Arabidopsis embryonic pattern formation. Dev Cell, 12(6): 943-956

[68] Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008). Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science, 319(5861): 294

[69] Pillitteri L J, Sloan D B, Bogenschutz N L, Torii K U (2007). Termination of asymmetric cell division and differentiation of stomata. Nature, 445(7127): 501-505

[70] Prigge M J, Otsuga D, Alonso J M, Ecker J R, Drews G N, Clark S E (2005). Class III homeodomain-leucine zipper gene family members have overlapping, antagonistic, and distinct roles in Arabidopsis development. Plant Cell, 17(1): 61-76

[71] Sabatini S, Beis D, Wolkenfelt H, Murfett J, Guilfoyle T, Malamy J, Benfey P, Leyser O, Bechtold N, Weisbeek P, Scheres B (1999). An auxin-dependent distal organizer of pattern and polarity in the Arabidopsis root. Cell, 99(5): 463-472

[72] Sarkar A K, Luijten M, Miyashima S, Lenhard M, Hashimoto T, Nakajima K, Scheres B, Heidstra R, Laux T (2007). Conserved factors regulate signalling in Arabidopsis thaliana shoot and root stem cell organizers. Nature, 446(7137): 811-814

[73] Sauer M, Friml J (2004). In vitro culture of Arabidopsis embryos within their ovules. Plant J, 40(5): 835-843

[74] Scheres B (2001). Plant cell identity. The role of position and lineage. Plant Physiol, 125(1): 112-114

[75] Schlereth A, Möller B, Liu W, Kientz M, Flipse J, Rademacher E H, Schmid M, Jürgens G, Weijers D (2010). MONOPTEROS controls embryonic root initiation by regulating a mobile transcription factor. Nature, 464(7290): 913-916

[76] Schuetz M, Berleth T, Mattsson J (2008). Multiple MONOPTEROS-dependent pathways are involved in leaf initiation. Plant Physiol, 148(2): 870-880

[77] Shevell D E, Leu W M, Gillmor C S, Xia G, Feldmann K A, Chua N H (1994). EMB30 is essential for normal cell division, cell expansion, and cell adhesion in Arabidopsis and encodes a protein that has similarity to Sec7. Cell, 77(7): 1051-1062

[78] Smith Z R, Long J A (2010). Control of Arabidopsis apical-basal embryo polarity by antagonistic transcription factors. Nature, 464(7287): 423-426

[79] St Johnston D, Ahringer J (2010). Cell polarity in eggs and epithelia: parallels and diversity. Cell, 141(5): 757-774

[80] Stahl Y, Wink R H, Ingram G C, Simon R (2009). A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol, 19(11): 909-914

[81] Steinmann T, Geldner N, Grebe M, Mangold S, Jackson C L, Paris S, Gälweiler L, Palme K, Jürgens G (1999). Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science, 286(5438): 316-318

[82] Suzuki A, Ohno S (2006). The PAR-aPKC system: lessons in polarity. J Cell Sci, 119(Pt 6): 979-987

[83] Szemenyei H, Hannon M, Long J A (2008). TOPLESS mediates auxin-dependent transcriptional repression during Arabidopsis embryogenesis. Science, 319(5868): 1384-1386

[84] Takada S, Jürgens G (2007). Transcriptional regulation of epidermal cell fate in the Arabidopsis embryo. Development, 134(6): 1141-1150

[85] Tanaka H, Onouchi H, Kondo M, Hara-Nishimura I, Nishimura M, Machida C, Machida Y (2001). A subtilisin-like serine protease is required for epidermal surface formation in Arabidopsis embryos and juvenile plants. Development, 128(23): 4681-4689

[86] Tanaka H, Watanabe M, Sasabe M, Hiroe T, Tanaka T, Tsukaya H, Ikezaki M, Machida C, Machida Y (2007). Novel receptor-like kinase ALE2 controls shoot development by specifying epidermis in Arabidopsis. Development, 134(9): 1643-1652

[87] Torres-Ruiz R A, Jürgens G (1994). Mutations in the FASS gene uncouple pattern formation and morphogenesis in Arabidopsis development. Development, 120(10): 2967-2978

[88] Tsuwamoto R, Fukuoka H, Takahata Y (2008). GASSHO1 and GASSHO2 encoding a putative leucine-rich repeat transmembrane-type receptor kinase are essential for the normal development of the epidermal surface in Arabidopsis embryos. Plant J, 54(1): 30-42

[89] Tucker M R, Hinze A, Tucker E J, Takada S, Jürgens G, Laux T (2008). Vascular signalling mediated by ZWILLE potentiates WUSCHEL function during shoot meristem stem cell development in the Arabidopsis embryo. Development, 135(17): 2839-2843

[90] Wang G, Fiers M (2010). CLE peptide signaling during plant development. Protoplasma, 240(1-4): 33-43

[91] Watanabe M, Tanaka H, Watanabe D, Machida C, Machida Y (2004). The ACR4 receptor-like kinase is required for surface formation of epidermis-related tissues in Arabidopsis thaliana. Plant J, 39(3): 298-308

[92] Weijers D, Schlereth A, Ehrismann J S, Schwank G, Kientz M, Jürgens G (2006). Auxin triggers transient local signaling for cell specification in Arabidopsis embryogenesis. Dev Cell, 10(2): 265-270

[93] West M, Harada J J (1993). Embryogenesis in higher Plants: An overview. Plant Cell, 5(10): 1361-1369

[94] Willemsen V, Wolkenfelt H, de Vrieze G, Weisbeek P, Scheres B (1998). The HOBBIT gene is required for formation of the root meristem in the Arabidopsis embryo. Development, 125(3): 521-531

[95] Willmann M R (2000). CLV1 and CLV3: negative regulators of SAM stem cell accumulation. Trends Plant Sci, 5(10): 416

[96] Wisniewska J, Xu J, Seifertová D, Brewer P B, Ruzicka K, Blilou I, Rouquié D, Benková E, Scheres B, Friml J (2006). Polar PIN localization directs auxin flow in plants. Science, 312(5775): 883

[97] Wysocka-Diller J W, Helariutta Y, Fukaki H, Malamy J E, Benfey P N (2000). Molecular analysis of SCARECROW function reveals a radial patterning mechanism common to root and shoot. Development, 127(3): 595-603

[98] Yang S, Johnston N, Talideh E, Mitchell S, Jeffree C, Goodrich J, Ingram G (2008). The endosperm-specific ZHOUPI gene of Arabidopsis thaliana regulates endosperm breakdown and embryonic epidermal development. Development, 135(21): 3501-3509

[99] Zhang J, Nodzynski T, Pencík A, Rolcík J, Friml J (2010). PIN phosphorylation is sufficient to mediate PIN polarity and direct auxin transport. Proc Natl Acad Sci U S A, 107(2): 918-922

Acknowledgments

This work was supported by grants from the Chinese Academy of Sciences (No. KSCX2-YW-N-048) and the National Natural Sciences Foundation of China (Grant Nos. 30830063, 30921003).

RIGHTS & PERMISSIONS

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg