CLE Peptide Signaling Molecules in Plants

Abstract

Abstract: Peptide ligands have long been recognized as signaling molecules which are involved in diverse developmental and physiological processes in animal systems. In recent years, peptide ligands have also well been known signaling molecules in plants, indicating that the function of peptides as singling molecules in inter-cellular communication is evolutionarily conserved. Recently, CLE（CLAVATA3/EMBRYO SURROUNDING REGION）family is well be researched of signaling molecules in plants. Similar to peptide ligands maturation in animals, the CLE peptides are matured by post-translational proteolysis and modification by studying the CLV3 from Arabidopsis and TDIF from Zinnia. In this review, we outline the molecular characteristics, biological functions and the post-translational maturation of CLE gene family members. We also provide prospective vision in this field.

Key words: Peptide signaling molecule , CLE peptide family, Receptor kinase , Signaling pathway , Arabidopsis

Gao Li. CLE Peptide Signaling Molecules in Plants[J]. Biotechnology Bulletin, 2014, 0(11): 14-23.

References

[1]Bliss M. The discovery of insulin[M]. Chicago：University of Chicago Press, 1982.
[2]Brivanlou AH, Darnell JE. Signal transduction and the control of gene expression[J]. Science, 2002, 295（5556）：813-818.
[3]Todorovica V, Jurukovskia V, Chena Y, et al. Latent TGF- β binding proteins[J]. Int J Biochem Cell Biol, 2005, 37（1）：38-41.
[4]Gaspar TH, Kevers C, Faivre-Rampant O, et al. Changing concepts in plant hormone action[J]. In Vitro Cell Dev Biol Plant, 2003, 39（2）：85-106.
[5]Pearce G, Strydom D, Johnson S, et al. A polypeptide from tomato leaves activates the expression of proteinase inhibitor genes[J]. Science, 1991, 253（5022）：895-898.
[6]Matsubayashi Y, Sakagami Y. Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L[J]. Proc Natl Acad Sci USA, 1996, 93（15）：7623-7627.
[7]Casson SA, Chilley PM, Topping JE, et al. The POLARIS gene of Arabidopsis encodes a predicted peptide required for correct root growth and leaf vascular patterning[J]. Plant Cell, 2002, 14（8）：1705-1721.
[8]Butenko MA, Patterson SE, Grini PE, et al. INFLORESCENCE DEFICIENT IN ABSCISSION controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants[J]. Plant Cell, 2003, 15（10）：2296-2307.
[9]Narita NN, Moore S, Horiguchi G, et al. Overexpression of a novel small peptide ROTUNDIFOLIA4 decreases cell proliferation and alters leaf shape in Arabidopsis thaliana[J]. Plant J, 2004, 38（4）：699-713.
[10]Strabala TJ, O'Donnell PJ, Smit AM, et al. Gain-of-function phenotypes for many CLAVATA3/ESR genes, including four new family members, correlate with tandem variations in the conserved CLAVATA3/ESR domain[J]. Plant Physiol, 2006, 140（4）：1331-1344.
[11]Fletcher JC, Brand U, Running MP, et al. Signaling of cell fate decisions by CLAVATA3 in Arabidopsis shoot meristem[J]. Science, 1999, 283（5409）：1911-1914.
[12]Opsahl-Ferstad HG, Le Deunff E, Dumas C, et al. ZmEsr, a novel endosperm-specific gene expressed in restricted region around the maize embryo[J]. Plant J, 1997, 12（1）：235-246.
[13]Chu H, Qian Q, Liang W, et al. The FLORAL ORGAN NUMBER4 gene encoding a putative ortholog of Arabidopsis CLAVATA3 regulates apical meristem size in rice[J]. Plant Physiol, 2006, 142（3）：1039-1052.
[14]Cock JM, Mccormick S. A large family of genes that share homology with CLAVATA3[J]. Plant Physiol, 2001, 126：939-942.
[15]Kondo T, Sawa S, Kinoshita A, et al. A plant peptide encoded by CLV3 identified by in situ MALDI-TOF MS analysis[J]. Science, 2006, 313：845-848.
[16]Bowers JE, Chapman BA, Rong JK, et al. Unravelling angiosperm genome evolution by phylogenetic analysis of chromosomal duplication events[J]. Nature, 2003, 422（6930）：433-438.
[17]Sharma VK, Ramirez J, Fletcher JC. The Arabidopsis CLV3-like（CLE）genes are expressed in diverse tissues and encode secreted proteins[J]. Plant Mol Biol, 2003, 51（3）：415-425.
[18]Ito Y, Nakanomyo I, Motose H, et al. Dodeca-CLE peptides as suppressors of plant stem cell differentiation[J]. Science, 2006, 313（5788）：842-845.
[19]Fiers M, Golemiec E, Xu J, et al. The 14-amino acid CLV3, CLE19, and CLE40 peptides trigger consumption of the root meristem in Arabidopsis through a CLAVATA2-dependent pathway[J]. Plant Cell, 2005, 17：2542-2553.
[20]Ni J, Clark SE. Evidence for functional conservation, sufficiency, and proteolytic processing of the CLAVATA3 CLE domain[J]. Plant Physiol, 2006, 140（2）：726-733.
[21]Durbak AR, Tax FE. CLAVATA signaling pathway receptors of Arabidopsis regulate cell proliferation in fruit organ formation as well as in meristem[J]. Genetics, 2011, 189：177-194.
[22]Yadav RK, Reddy GV. WUSCHEL protein movement and stem cell homeostasis[J]. Plant Signal Behav, 2012, 7（5）：592-594.
[23] Jonsson H, Heisler M, Reddy GV, et al. Modeling the organization of the WUSCHEL expression domain in the shoot apical meristem[J]. Bioinformatics, 2005, 21（Suppl. 1）：i232-i240.
[24]Müller R, Borghi L, Kwiatkowska D, et al. Dynamic and compensa-tory responses of Arabidopsis shoot and floral meristem to CLV3 sig-naling[J]. The Plant Cell, 2006, 18：1188-1198.
[25]Yadav RK, Perales M, Gruel J, et al. WUSCHEL protein movement mediates stem cell homeostasis in the Arabidopsis shoot apex[J]. Genes Dev, 2011, 25：2025-2030.
[26]Deyoung BJ, Bickle KL, Schrage KJ, et al. The CLAVATA1-related BAM1, BAM2 and BAM3 receptor kinase-like proteins are required for meristem function in Arabidopsis[J]. Plant J, 2006, 45：1-16.
[27]Guo YF, Han LQ, Hymes M, et al. CLAVATA2 forms a distinct CLE-binding receptor complex regulating Arabidopsis stem cell specification[J]. Plant J, 2010, 63（6）：889-900.
[28]Müller R, Bleckmann A, Simon R. The receptor kinase CORYNE of Arabidopsis transmits the stem cell-limiting signal CLAVATA3 independently of CLAVATA1[J]. Plant Cell, 2008, 20（4）：934-946.
[29]Zhu YF, Wang YQ, Li R, et al. Analysis of interactions among the CLAVATA3 receptors reveals a direct interaction between CLAVATA2 and CORYNE in Arabidopsis[J]. Plant J, 2010, 61：223-233.
[30]Kinoshita A, Betsuyaku S, Osakabe Y, et al. RPK2 is an essential receptor-like kinase that transmits the CLV3 signal in Arabidopsis[J]. Development, 2010, 137（2）：3911-3920.
[31]Stone JM, Trotochaud AE, Walker JC, et al. Control of meristem development by CLAVATA1 receptor kinase and kinase-associated protein phosphatase interactions[J]. Plant Physiol, 1998, 117（4）：1217-1225.
[32]Yu LP, Miller AK, Clark SE. POLTERGEIST encodes a protein phosphatase 2C that regulates CLAVATA pathways controlling stem cell identity at Arabidopsis shoot and flower meristems[J]. Curr Biol, 2003, 13：179-188.
[33]Song SK, Lee MM, Clark SE. POL and PLL1 phosphatases are CLAVATA1 signaling intermediates required for Arabidopsis shoot and floral stem cells[J]. Development, 2006, 133：4691-4698.
[34]Trotochaud AE, Hao T, Wu G, et al. The CLAVATA1 receptor-like kinase requires CLAVATA3 for its assembly into a signaling complex that includes KAPP and a Rho-related protein[J]. Plant Cell, 1999, 11（3）：393-406.
[35]Betsuyaku S, Takahashi F, Kinoshita A, et al. Mitogen-activated protein kinase regulated by the CLAVATA receptors contributes to shoot apical meristem homeostasis[J]. Plant Cell Physiol, 2011, 52（1）：14-29.
[36]Gish LA, Gagne JM, Brody LH, et al. WUSCHEL-responsive At5g65480 interacts with CLAVATA components in vitro and in transient expression[J]. PLoS One, 2013, 8（6）：e66345.
[37]Yadav RK, Perales M, Gruel J, et al. Plant stem cell maintenance involves direct transcriptional repression of differentiation program[J]. Mol Syst Biol, 2013, 9：654.
[38]Suzaki T, Sato M, Ashikari M, et al. The gene FLORAL ORGAN NUMBER1 regulates floral meristem size in rice and encodes a leucine rich repeat receptor kinase orthologous to Arabidopsis CLAVATA1[J]. Development, 2004, 131（22）：5649-5657.
[39]Kim C, Jeong DH, An G. Molecular cloning and characterization of OsLRK1 encoding a putative receptor-like protein kinase from Oryza sativa[J]. Plant Sci, 2000, 152：17-26.
[40]Hobe M, Müller R, Grünewald M, et al. Loss of CLE40, a protein functionally equivalent to the stem cell restricting signal CLV3, enhances root waving in Arabidopsis[J]. Dev Genes Evol, 2003, 213（8）：371-381.
[41]Stahl Y, Wink RH, Ingram GC, et al. A signaling module controlling the stem cell niche in Arabidopsis root meristems[J]. Curr Biol, 2009, 19（11）：909-914.
[42]Chu HW, Liang WQ, Li J, et al. A CLE-WOX signaling module regulates root meristem maintenance and vascular tissue developm-ent in rice[J]. J Exper Botany, 2013, 64（17）：5359-5369.
[43]Fiers M, Hause G, Boutilier K, et al. Mis-expression of the CLV3/ESR-like gene CLE19 in Arabidopsis leads to a consumption of root meristem[J]. Gene, 2004, 327（1）：37-49.
[44]Wang GD, Long YC, Thomma BP, et al. Functional analyses of the CLAVATA2-like proteins and their domains that contribute to CALVATA2 specificity[J]. Plant Physiol, 2010, 152（1）：320-331.
[45]Jun J, Fiume E, Roeder AH, et al. Comprehensive analysis of CLE polypeptide signaling gene expression and overexpression activity in Arabidopsis[J]. Plant Physiol, 2010, 154（4）：1721-1736.
[46]Etchells JP, Turner SR. The PXY-CLE41 receptor ligand pair defines a multifunctional pathway that controls the rate and orientation of vascular cell division[J]. Development, 2010, 137（5）：767-774.
[47]Hirakawa Y, Kondo Y, Fukuda H. TDIF peptide signaling regulates vascular stem cell proliferation via the WOX4 homeobox gene in Arabidopsis[J]. Plant Cell, 2010, 22（8）：2618-2629.
[48]Qiang Y, Wu JB, Han HB, et al. CLE peptides in vascular development[J]. J Integrative Plant Biol, 2013, 55（4）：389-394.
[49]Wang JH, Kucukoglu M, Zhang LB, et al. The Arabidopsis LRR-RLK, PXC1, is a regulator of secondary wall formation correlated with the TDIF-PXY/TDR-WOX4 signaling pathway[J]. BMC Plant Biol, 2013, 13：94.
[50]Fiume E, Fletcher JC. Regulation of Arabidopsis embryo and endosperm development by the polypeptide signaling molecule CLE8[J]. Plant Cell, 2012, 24（3）：1000-1012.
[51]Song XF, Guo P, Ren SC, et al. Antagonistic peptide technology for functional dissection of CLV3/ESR genes in Arabidopsis[J]. Plant Physiol, 2013, 161：1076-1085.
[52]Bonello JF, Opsahl-Ferstad HG, Perez P, et al. Esr genes show different levels of expression in the same region of maize endosperm[J]. Gene, 2000, 246（1-2）：219-227.
[53]Balandín M, Royo J, Gómez E, et al. A protective role for the embryo surrounding region of the maize endosperm, as evidenced by the characterisation of ZmESR-6, a defensin gene specifically expressed in this region[J]. Plant Mol Biol, 2005, 58（2）：269-282.
[54]Floyd SK, Bowman JL. The ancestral developmental tool kit of land plants[J]. Int J Plant Sci, 2007, 168（1）：1-35.
[55]Strabala TJ, Phillips L, West M, et al. Bioinformatic and phylogenetic analysis of CLAVATA3/EMBRYO-SURROUNDING REGION（CLE）and the CLE-LIKE signal peptide genes in the Pinophyta[J]. BMC Plant Biol, 2014, 14：47.
[56] Wang X, Mitchum MG, Gao B, et al. A parasitism gene from a plant-parasitic nematode with function similar to CLAVATA3/ESR（CLE）of Arabidopsis thaliana[J]. Mol Plant Pathol, 2005, 6（2）：187-191.
[57] Fiers M, Golemiec E, van der Schors R, et al. The CLAVATA3/ESR motif of CLAVATA3 is functionally independent from the noncons-erved flanking sequences[J]. Plant Physiol, 2006, 141（4）：1284-1292.
[58]Djordjevic MA, Oakes M, Wong CE, et al. Border sequences of Medicago truncatula CLE36 are specifically cleaved by endoproteases common to the extracellular fluids of Medicago and soybean[J]. J Exp Bot, 2011, 62（13）：4649-4659.
[59]Casamitjana-Martínez E, Hofhuis HF, Xu J, et al. Root-specific CLE19 overexpression and the sol1/2 suppressors implicate a CLV-like pathway in the control of Arabidopsis root meristem maintenance[J]. Curr Biol, 2003, 13（16）：1435-1441.
[60] Sawa S, Kinoshita A, Betsuyaku S, et al. A large family of genes that share homology with CLE domain in Arabidopsis and rice[J]. Plant Signal Behav, 2008, 3（5）：337-339.
[61] Lu SW, Chen S, Wang J, et al. Structural and functional diversity of CLAVATA3/ESR（CLE）-like genes from the potato cyst nematode Globodera rostochiensis[J]. Mol Plant Microbe Interact, 2009, 22（9）：1128-1142.
[62]Ohyama K, Shinohara H, Ogawa-Ohnishi M, et al. A glycopeptide regulating stem cell fate in Arabidopsis thaliana[J]. Nat Chem Biol, 2009, 5（8）：578-580.
[63]Shiu SH, Bleecker AB. Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases[J]. Proc Natl Acad Sci USA, 2001, 98（19）：10763-10768.
[64]Matsumoto N, Okada K. A homeobox gene, PRESSED FLOWER, regulates lateral axis-dependent development of Arabidopsis flowers[J]. Genes Dev, 2001, 15（24）：3355-3364.
[65]Wu X, Dabi T, Weigel D. Requirement of homeobox, gene STIMPY/WOX9 for Arabidopsis meristem growth and maintenance[J]. Curr Biol, 2005, 15（5）：436-440.
[66]Haecker A, Gross-Hardt R, Geiges B, et al. Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana[J]. Development, 2004, 131（3）：657-668.
[67]Yang H, Matsubayashi Y, Nakamura K, et al. Oryza sativa PSK gene encodes a precursor of phytosulfokine-alpha, a sulfated peptide growth factor found in plants[J]. Proc Natl Acad Sci USA, 1999, 96（23）：13560-13565.
[68]Kondo Y, Hirakawa Y, Kieber JJ, et al. CLE peptides can negatively regulate protoxylem vessel formation via cytokinin signaling[J]. Plant Cell Physiol, 2011, 52（1）：37-48.
[69]Bidadi H, Matsuoka K, Sage-Ono K, et al. CLE6 expression recovers gibberellin deficiency to promote shoot growth in Arabidopsis[J]. Plant J, 2014, 78（2）：241-252.