Abstract
Although there are hundreds of genes encoding receptor-like kinases and putative secreted ligands, to date less that ten have been matched and been shown to control plant growth or development. Brassionsteroids (BRs) and peptide ligands are involved in signaling between cells in the close vicinity to each other, and not transported over long distances. BRs and sulfated peptide ligands (PSK and PSY) have growth-promoting activities, while cysteine-rich and proline-rich peptide ligands identified so far are involved in specific processes such as self-incompatibility, differentiation, meristem maintenance and cell separation. Here we review how ligands in development and their respective receptors have been identified, how they interact, as well as the functional redundancy found in ligand gene families.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
Abrash EB, Bergmann DC (2010) Regional specification of stomatal production by the putative ligand CHALLAH. Development 137:447–455
Amano Y, Tsubouchi H, Shinohara H, Ogawa M, Matsubayashi Y (2007) Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc Natl Acad Sci USA 104:18333–18338
Azpiroz R, Wu Y, LoCascio JC, Feldmann KA (1998) An Arabidopsis brassinosteroid-dependent mutant is blocked in cell elongation. Plant Cell 10:219–230
Bajguz A (2007) Metabolism of brassinosteroids in plants. Plant Physiol Biochem 45:95–107
Bergmann DC, Sack FD (2007) Stomatal development. Ann Rev Plant Biol 58:163–181
Bhave N, Veley K, Nadeau J, Lucas J, Bhave S, Sack F (2009) TOO MANY MOUTHS promotes cell fate progression in stomatal development of Arabidopsis stems. Planta 229:357–367
Bleckmann A, Weidtkamp-Peters S, Seidel CAM, Simon R (2010) Stem cell signaling in Arabidopsis requires CRN to localize CLV2 to the plasma membrane. Plant Physiol 152:166–176
Brand U, Fletcher JC, Hobe M, Meyerowitz EM, Simon R (2000) Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289:617–619
Butenko MA, Patterson SE, Grini PE, Stenvik GE, Amundsen SS, Mandal A, Aalen RB (2003) INFLORESCENCE DEFICIENT IN ABSCISSION controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell 15:2296–2307
Butenko MA, Stenvik G-E, Alm V, Sæther B, Patterson SE, Aalen RB (2006) Ethylene dependent and -independent pathways controlling floral abscission are revelaed to converge using promoter::reporter gene constructs in the ida abscission mutant. J Exp Bot 57:3627–3637
Butenko MA, Vie AK, Brembu T, Aalen RB, Bones AM (2009) Plant peptides in signalling: looking for new partners. Trends Plant Sci 14:255–263
Chen YF, Matsubayashi Y, Sakagami Y (2000) Peptide growth factor phytosulfokine-alpha contributes to the pollen population effect. Planta 211:752–755
Cho SK, Larue CT, Chevalier D, Wang H, Jinn TL, Zhang S, Walker JC (2008) Regulation of floral organ abscission in Arabidopsis thaliana. Proc Natl Acad Sci USA 105:15629–15634
Choe S, Dilkes BP, Fujioka S, Takatsuto S, Sakurai A, Feldmann KA (1998) The DWF4 gene of Arabidopsis encodes a Cytochrome P450 that mediates multiple 22a-hydroxylation steps in brassinosteroid biosynthesis. Plant Cell 10:231–244
Chory J, Nagpal P, Peto CA (1991) Phenotypic and genetic analysis of det2, a new mutant that affects light-regulated seedling development in Arabidopsis. Plant Cell 3:445–459
Clark SE, Running MP, Meyerowitz EM (1995) CLAVATA3 is a specific regulator of shoot and floral meristem development affecting the same processes as CLAVATA1. Development 121:2057–2067
Clouse SD, Langford M, McMorris TC (1996) A brassinosteroid-insensitive mutant in Arabidopsis thaliana exhibits multiple defects in growth and development. Plant Physiol 111:671–678
De Smet I, Vassileva V, De Rybel B, Levesque MP, Grunewald W, Van Damme D, Van Noorden G, Naudts M, Van Isterdael G, De Clercq R, Wang JY, Meuli N, Vanneste S, Friml J, Hilson P, Jurgens G, Ingram GC, Inze D, Benfey PN, Beeckman T (2008) Receptor-like kinase ACR4 restricts formative cell divisions in the Arabidopsis root. Science 322:594–597
De Smet I, Voss U, Jurgens G, Beeckman T (2009) Receptor-like kinases shape the plant. Nat Cell Biol 11:1166–1173
DeYoung BJ, Clark SE (2008) BAM receptors regulate stem cell specification and organ development through complex interactions with CLAVATA signaling. Genetics 180:895–904
Etchells JP, Turner SR (2010) The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division. Development 137:767–774
Fiers M, Golemiec E, Xu J, van der Geest L, Heidstra R, Stiekema W, Liu C-M (2005) The 14-Amino Acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway. Plant Cell 17:2542–2553
Fiers M, Golemiec E, van der Schors R, van der Geest L, Li KW, Stiekema WJ, Liu C-M (2006) The CLAVATA3/ESR motif of CLAVATA3 is functionally independent from the nonconserved flanking sequences. Plant Physiol 141:1284–1292
Fisher K, Turner S (2007) PXY, a receptor-like kinase essential for maintaining polarity during plant vascular-tissue development. Curr Biol 17:1061–1066
Fletcher JC, Brand U, Hobe M, Meyerowitz EM, Simon R (2000) Stem cell fate in Arabidopsis thaliana depends on a feedback loop regulated by CLV3 activity. Mol Biol Cell 11:1497
Franklin-Tong N (2002) Receptor-ligand interaction demonstrated in Brassica self-incompatibility. Trends Genet 18:113–115
Fujioka S, Yokota T (2003) Biosynthesis and metabolism of brassinosteroids. Annu Rev Plant Biol 54:137–164
Fukuda H, Hirakawa Y, Sawa S (2007) Peptide signaling in vascular development. Curr Opin Plant Biol 10:477–482
Geisler M, Nadeau J, Sack FD (2000) Oriented asymmetric divisions that generate the stomatal spacing pattern in Arabidopsis are disrupted by the too many mouths mutation. Plant Cell 12:2075–2086
Grove MD, Spencer GF, Rohwedder WK, Mandava N, Worley JF, Warthen JD, Steffens GL, Flippenanderson JL, Cook JC (1979) Brassinolide, a plant growth-promoting steroid isolated from Brassica napus pollen. Nature 281:216–217
Guo Y, Han L, Hymes M, Denver R, Clark SE (2010) CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification. Plant J 63:889–900
Hara K, Yokoo T, Kajita R, Onishi T, Yahata S, Peterson KM, Torii KU, Kakimoto T (2009) Epidermal cell density is autoregulated via a secretory peptide, EPIDERMAL PATTERNING FACTOR 2 in Arabidopsis leaves. Plant Cell Physiol 50:1019–1031
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 USA 105:15208–15213
Hirakawa Y, Kondo Y, Fukuda H (2010) Regulation of vascular development by CLE peptide-receptor systems. J Integr Plant Biol 52:8–16
Hobe M, Muller R, Grunewald 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 213:371–381
Hunt L, Gray JE (2009) The signaling peptide EPF2 controls asymmetric cell divisions during stomatal development. Curr Biol 19:864–869
Hunt L, Bailey KJ, Gray JE (2010) The signalling peptide EPFL9 is a positive regulator of stomatal development. New Phytol 186:609–614
Ito Y, Nakanomyo I, Motose H, Iwamoto K, Sawa S, Dohmae N, Fukuda H (2006) Dodeca-CLE peptides as suppressors of plant stem cell differentiation. Science 313:842–845
Jia G, Liu X, Owen HA, Zhao D (2008) Signaling of cell fate determination by the TPD1 small protein and EMS1 receptor kinase. Proc Natl Acad Sci USA 105:2220–2225
Jun J, Fiume E, Roeder A, Meng L, Sharma VK, Osmont KS, Baker C, Ha CM, Meyerowitz EM, Feldman LJ, Fletcher J (2010) Comprehensive analysis of CLE polypeptide signaling gene expression and over-expression activity in Arabidopsis. Plant Physiol 154:1721–1736
Kauschmann A, Jessop A, Koncz C, Szekeres M, Willmitzer L, Altmann T (1996) Genetic evidence for an essential role of brassinosteroids in plant development. Plant J 9:701–713
Kayes JM, Clark SE (1998) CLAVATA2, a regulator of meristem and organ development in Arabidopsis. Development 125:3843–3851
Kim TW, Wang ZY (2010) Brassinosteroid signal transduction from receptor kinases to transcription factors. Annu Rev Plant Biol 61:681–704
Kinoshita T, Cano-Delgado A, Seto H, Hiranuma S, Fujioka S, Yoshida S, Chory J (2005) Binding of brassinosteroids to the extracellular domain of plant receptor kinase BRI1. Nature 433:167–171
Kinoshita A, Betsuyaku S, Osakabe Y, Mizuno S, Nagawa S, Stahl Y, Simon R, Yamaguchi-Shinozaki K, Fukuda H, Sawa S (2010) RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis. Development 137:3911–3920
Kobayashi T, Eun CH, Hanai H, Matsubayashi Y, Sakagami Y, Kamada H (1999) Phytosulphokine-alpha, a peptidyl plant growth factor, stimulates somatic embryogenesis in carrot. J Exp Bot 50:1123–1128
Komori R, Amano Y, Ogawa-Ohnishi M, Matsubayashi Y (2009) Identification of tyrosylprotein sulfotransferase in Arabidopsis. Proc Natl Acad Sci USA 106:15067–15072
Kondo T, Sawa S, Kinoshita A, Mizuno S, Kakimoto T, Fukuda H, Sakagami Y (2006) A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis. Science 313:845–848
Kondo T, Nakamura T, Yokomine K, Sakagami Y (2008) Dual assay for MCLV3 activity reveals structure-activity relationship of CLE peptides. Biochem Biophys Res Commun 377:312–316
Kondo T, Kajita R, Miyazaki A, Hokoyama M, Nakamura-Miura T, Mizuno S, Masuda Y, Irie K, Tanaka Y, Takada S, Kakimoto T, Sakagami Y (2010) Stomatal density is controlled by a mesophyll-derived signaling molecule. Plant Cell Physiol 51:1–8
Lease KA, Walker JC (2006) The Arabidopsis unannotated secreted peptide database, a resource for plant peptidomics. Plant Physiol 142:831–838
Lenhard M, Laux T (2003) Stem cell homeostasis in the Arabidopsis shoot meristem is regulated by intercellular movement of CLAVATA3 and its sequestration by CLAVATA1. Development 130:3163–3173
Li J, Nagpal P, Vitart V, McMorris TC, Chory J (1996) A role for brassinosteroids in light-dependent development of Arabidopsis. Science 272:398–401
Malinowski R, Higgins R, Luo Y, Piper L, Nazir A, Bajwa VS, Clouse SD, Thompson PR, Stratmann JW (2009) The tomato brassinosteroid receptor BRI1 increases binding of systemin to tobacco plasma membranes, but is not involved in systemin signaling. Plant Mol Biol 70:603–616
Matsubayashi Y (2003) Ligand-receptor pairs in plant peptide signaling. J Cell Sci 116:3863–3870
Matsubayashi Y, Sakagami Y (1996) Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc Natl Acad Sci USA 93:7623–7627
Matsubayashi Y, Sakagami Y (2006) Peptide hormones in plants. Annu Rev Plant Biol 57:649–674
Matsubayashi Y, Takagi L, Omura N, Morita A, Sakagami Y (1999) The endogenous sulfated pentapeptide phytosulfokine-alpha stimulates tracheary element differentiation of isolated mesophyll cells of Zinnia. Plant Physiol 120:1043–1048
Matsubayashi Y, Ogawa M, Morita A, Sakagami Y (2002) An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science 296:1470–1472
Matsubayashi Y, Ogawa M, Sakagami Y (2005) Analysis of pskr1-1, an Arabidopsis knockout mutant of PSK receptor gene. Plant Cell Physiol 46:S177–S177
Matsubayashi Y, Shinohara H, Ogawa M (2006) Identification and functional characterization of phytosulfokine receptor using a ligand-based approach. Chem Rec 6:356–364
Mishima M, Takayama S, Sasaki K, Jee J, Kojima C, Isogai A, Shirakawa M (2003) Structure of the male determinant factor for Brassica self-incompatibility. J Biol Chem 278:36389–36395
Miwa H, Betsuyaku S, Iwamoto K, Kinoshita A, Fukuda H, Sawa S (2008) The receptor-like kinase SOL2 mediates CLE signaling in Arabidopsis. Plant Cell Physiol 49:1752–1757
Moore KL (2003) The biology and enzymology of protein tyrosine O-sulfation. J Biol Chem 278:24243–24246
Müller R, Borghi L, Kwiatkowska D, Laufs P, Simon R (2006) Dynamic and compensatory responses of Arabidopsis shoot and floral meristems to CLV3 signaling. Plant Cell 18:1188–1198
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 20:934–946
Nakaya M, Tsukaya H, Murakami N, Kato M (2002) Brassinosteroids control the proliferation of leaf cells of Arabidopsis thaliana. Plant Cell Physiol 43:239–244
Ni J, Clark SE (2006) Evidence for functional conservation, sufficiency, and proteolytic processing of the CLAVATA3 CLE domain. Plant Physiol 140:726–733
Oelkers K, Goffard N, Weiller G, Gresshoff P, Mathesius U, Frickey T (2008) Bioinformatic analysis of the CLE signaling peptide family. BMC Plant Biol 8:1
Ogawa M, Shinohara H, Sakagami Y, Matsubayashi Y (2008) Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319:294
Ohyama K, Ogawa M, Matsubayashi Y (2008) Identification of a biologically active, small, secreted peptide in Arabidopsis by in silico gene screening, followed by LC-MS-based structure analysis. Plant J 55:152–160
Ohyama K, Shinohara H, Ogawa-Ohnishi M, Matsubayashi Y (2009) A glycopeptide regulating stem cell fate in Arabidopsis thaliana. Nat Chem Biol 5:578–580
Peret B, Larrieu A, Bennett MJ (2009) Lateral root emergence: a difficult birth. J Exp Bot 60:3637–3643
Poppenberger B, Fujioka S, Soeno K, George GL, Vaistij FnE, Hiranuma S, Seto H, Takatsuto S, Adam G, Yoshida S, Bowles D (2005) The UGT73C5 of Arabidopsis thaliana glucosylates brassinosteroids. Proc Natl Acad Sci USA 102:15253–15258
Rowe MH, Bergmann DC (2010) Complex signals for simple cells: the expanding ranks of signals and receptors guiding stomatal development. Curr Opin Plant Biol 13:548–555
Rychel AL, Peterson KM, Torii KU (2010) Plant twitter: ligands under 140 amino acids enforcing stomatal patterning. J Plant Res 123:275–280
Sanders PM, Bui AQ, Weterings K, McIntire KN, Hsu YC, Lee PY, Truong MT, Beals TP, Goldberg RB (1999) Anther developmental defects in Arabidopsis thaliana male-sterile mutants. Sex Plant Reprod 11:297–322
Scheer JM, Ryan CA (2002) The systemin receptor SR160 from Lycopersicon peruvianum is a member of the LRR receptor kinase family. Proc Natl Acad Sci USA 99:9585–9590
Schoof H, Lenhard M, Haecker A, Mayer KFX, Jurgens G, Laux T (2000) The stem cell population of Arabidopsis shoot meristems is maintained by a regulatory loop between the CLAVATA and WUSCHEL genes. Cell 100:635–644
Schopfer CR, Nasrallah ME, Nasrallah JB (1999) The male determinant of self-incompatibility in Brassica. Science 286:1697–1700
Sharma VK, Carles C, Fletcher JC (2003) Maintenance of stem cell populations in plants. Proc Natl Acad Sci USA 100:11823–11829
Shiba H, Takayama S, Iwano M, Shimosato H, Funato M, Nakagawa T, Che FS, Suzuki G, Watanabe M, Hinata K, Isogai A (2001) A pollen coat protein, SP11/SCR, determines the pollen S-specificity in the self-incompatibility of Brassica species. Plant Physiol 125:2095–2103
Shimada Y, Fujioka S, Miyauchi N, Kushiro M, Takatsuto S, Nomura T, Yokota T, Kamiya Y, Bishop GJ, Yoshida S (2001) Brassinosteroid-6-oxidases from Arabidopsis and tomato catalyze multiple C-6 oxidations in brassinosteroid biosynthesis. Plant Physiol 126:770–779
Shimada Y, Goda H, Nakamura A, Takatsuto S, Fujioka S, Yoshida S (2003) Organ-specific expression of brassinosteroid-biosynthetic genes and distribution of endogenous brassinosteroids in Arabidopsis. Plant Physiol 131:287–297
Shinohara H, Ogawa M, Sakagami Y, Matsubayashi Y (2007) Identification of ligand binding site of phytosulfokine receptor by on-column photoaffinity labeling. J Biol Chem 282:124–131
Shiu SH, Bleecker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci USA 98:10763–10768
Shpak ED, McAbee JM, Pillitteri LJ, Torii KU (2005) Stomatal patterning and differentiation by synergistic interactions of receptor kinases. Science 309:290–293
Sieburth LE (2007) Plant development: PXY and polar cell division in the procambium. Curr Biol 17:R594–R596
Silverstein KAT, Moskal WA, Wu HC, Underwood BA, Graham MA, Town CD, VandenBosch KA (2007) Small cysteine-rich peptides resembling antimicrobial peptides have been under-predicted in plants. Plant J 51:262–280
Stahl Y, Simon R (2010) Plant primary meristems: shared functions and regulatory mechanisms. Curr Opin Plant Biol 13:53–58
Stahl Y, Wink RH, Ingram GC, Simon R (2009) A signaling module controlling the stem cell niche in Arabidopsis root meristems. Curr Biol 19:909–914
Stenvik G-E, Butenko MA, Urbanowicz BR, Rose JK, Aalen RB (2006) Overexpression of INFLORESCENCE DEFICIENT IN ABSCISSION activates cell separation in vestigial abscission zones in Arabidopsis. Plant Cell 18:1467–1476
Stenvik G-E, Tandstad NM, Guo Y, Shi C-L, Kristiansen W, Holmgren A, Clark SE, Aalen RB, Butenko MA (2008) The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 20:1805–1817
Sugano SS, Shimada T, Imai Y, Okawa K, Tamai A, Mori M, Hara-Nishimura I (2010) Stomagen positively regulates stomatal density in Arabidopsis. Nature 463:241–U130
Symons GM, Reid JB (2004) Brassinosteroids do not undergo long-distance transport in pea. implications for the regulation of endogenous brassinosteroid levels. Plant Physiol 135:2196–2206
Symons GM, Ross JJ, Jager CE, Reid JB (2008) Brassinosteroid transport. J Exp Bot 59:17–24
Szekeres M (2003) Brassinosteroid and systemin: two hormones perceived by the same receptor. Trends Plant Sci 8:102–104
Szekeres M, Németh K, Koncz-Kálmán Z, Mathur J, Kauschmann A, Altmann T, Rédei GP, Nagy F, Schell J, Koncz C (1996) Brassinosteroids rescue the deficiency of CYP90, a Cytochrome P450, controlling cell elongation and de-etiolation in Arabidopsis. Cell 85:171–182
Takayama S, Isogai A (2005) Self-incompatibility in plants. Annu Rev Plant Biol 56:467–489
Takayama S, Shiba H, Iwano M, Shimosato H, Che FS, Kai N, Watanabe M, Suzuki G, Hinata K, Isogai A (2000) The pollen determinant of self-incompatibility in Brassica campestris. Proc Natl Acad Sci USA 97:1920–1925
Takayama S, Shimosato H, Shiba H, Funato M, Che FS, Watanabe M, Iwano M, Isogai A (2001) Direct ligand-receptor complex interaction controls Brassica self-incompatibility. Nature 413:534–538
Trotochaud AE, Hao T, Wu G, Yang ZB, Clark SE (1999) The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein. Plant Cell 11:393–405
Tsuchimatsu T, Suwabe K, Shimizu-Inatsugi R, Isokawa S, Pavlidis P, Stadler T, Suzuki G, Takayama S, Watanabe M, Shimizu KK (2010) Evolution of self-compatibility in Arabidopsis by a mutation in the male specificity gene. Nature 464:1342–1346
Turk EM, Fujioka S, Seto H, Shimada Y, Takatsuto S, Yoshida S, Denzel MA, Torres QI, Neff MM (2003) CYP72B1 inactivates brassinosteroid hormones: an intersection between photomorphogenesis and plant steroid signal transduction. Plant Physiol 133:1643–1653
Ubeda-Tomas S, Bennett MJ (2010) Plant development: size matters, and it's all down to hormones. Curr Biol 20:R511–R513
Vanoosthuyse V, Miege C, Dumas C, Cock JM (2001) Two large Arabidopsis thaliana gene families are homologous to the Brassica gene superfamily that encodes pollen coat proteins and the male component of the self-incompatibility response. Plant Mol Biol 46:17–34
Vert Gg, Nemhauser JL, Geldner N, Hong F, Chory J (2005) Molecular mechanisms of steroid hormone signaling in plants. Annu Rev Cell Dev Biol 21:177–201
Whitford R, Fernandez A, De Groodt R, Ortega E, Hilson P (2008) Plant CLE peptides from two distinct functional classes synergistically induce division of vascular cells. Proc Natl Acad Sci USA 105:18625–18630
Yamaguchi Y, Pearce G, Ryan CA (2006) The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc Natl Acad Sci USA 103:10104–10109
Yamakawa S, Sakuta C, Matsubayashi Y, Sakagami Y, Kamada H, Satoh S (1998) The promotive effects of a peptidyl plant growth factor, phytosulfokine-alpha, on the formation of adventitious roots and expression of a gene for a root-specific cystatin in cucumber hypocotyls. J Plant Res 111:453–458
Yang H, Matsubayashi Y, Nakamura K, Sakagami Y (2001) Diversity of Arabidopsis genes encoding precursors for phytosulfokine, a peptide growth factor. Plant Physiol 127:842–851
Yang S-L, Xie L-F, Mao H-Z, Puah CS, Yang W-C, Jiang L, Sundaresan V, Ye D (2003) TAPETUM DETERMINANT1 is required for cell specialization in the Arabidopsis anther. Plant Cell 15:2792–2804
Yang S-L, Jiang L, Puah CS, Xie L-F, Zhang X-Q, Chen L-Q, Yang W-C, Ye D (2005) Overexpression of TAPETUM DETERMINANT1 alters the cell fates in the Arabidopsis carpel and tapetum via genetic interaction with EXCESS MICROSPOROCYTES1/EXTRA SPOROGENOUS CELLS. Plant Physiol 139:186–191
Yuan T, Fujioka S, Takatsuto S, Matsumoto S, Gou X, He K, Russell SD, Li J (2007) BEN1, a gene encoding a dihydroflavonol 4-reductase (DFR)-like protein, regulates the levels of brassinosteroids in Arabidopsis thaliana. Plant J 51:220–233
Zhu Y, Wang Y, Li R, Song X, Wang Q, Huang S, Jin JB, Liu C-M, Lin J (2010) Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis. Plant J 61:223–233
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2012 Springer-Verlag Berlin Heidelberg
About this chapter
Cite this chapter
Butenko, M.A., Aalen, R.B. (2012). Receptor Ligands in Development. In: Tax, F., Kemmerling, B. (eds) Receptor-like Kinases in Plants. Signaling and Communication in Plants, vol 13. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-23044-8_11
Download citation
DOI: https://doi.org/10.1007/978-3-642-23044-8_11
Published:
Publisher Name: Springer, Berlin, Heidelberg
Print ISBN: 978-3-642-23043-1
Online ISBN: 978-3-642-23044-8
eBook Packages: Biomedical and Life SciencesBiomedical and Life Sciences (R0)