- Email: [email protected]
Ligand mimicry? Plant-parasitic nematode polypeptide with similarity to CLAVATA3
Update
TRENDS in Plant Science
2 Johnson, L. et al. (2002) Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr. Biol. 12, 1360 3 Richards, E.J. and Elgin, S.C. (2002) Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108, 489– 500 4 Bartee, L. et al. (2001) Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev. 15, 1753– 1758 5 Lindroth, A.M. et al. (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292, 2077– 2080 6 Jackson, J.P. et al. (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416, 556 – 560 7 Tamaru, H. and Selker, E.U. (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414, 277– 283
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8 Volpe, T.A. et al. (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297, 1833 – 1837 9 Pal-Bhadra, M. et al. (2002) RNAi related mechanisms affect both transcriptional and posttranscriptional transgene silencing in Drosophila. Mol. Cell 9, 315 – 327 10 Richards, E.J. (1997) DNA methylation and plant development. Trends Genet. 13, 319 – 323 11 Vaucheret, H. et al. (2001) Post-transcriptional gene silencing in plants. J. Cell Sci. 114, 3083– 3091 12 Dernburg, A.F. and Karpen, G.H. (2002) A chromosome RNAissance. Cell 111, 159– 162
1360-1385/03/$ - see front matter q 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S1360-1385(03)00005-0
| Letters
Ligand mimicry? Plant-parasitic nematode polypeptide with similarity to CLAVATA3 Addie Nina Olsen and Karen Skriver Institute of Molecular Biology, University of Copenhagen, Øster, Farimagsgade 2A, DK-1353 Copenhagen K, Denmark
The importance of peptides in plant intercellular signaling has become apparent during the past decade. Among recently identified peptide signals is CLAVATA3 (CLV3), which is involved in cell-fate determination in the shoot apical meristem of Arabidopsis. There is evidence that CLV3 is a ligand for CLAVATA1 (CLV1), a receptor kinase with an extracellular domain containing leucine-rich repeats (LRRs) [1]. The Arabidopsis genome contains a large gene family, called CLE for CLAVATA3/ESR-related, encoding polypeptides with similarity to CLV3. These small polypeptides are characterized by a short, C-terminal motif and an N-terminal signal peptide or signal anchor [2]. Similar sequences are encoded by expressed sequence tag (EST) clones from various plants. Using motif-based database search methods, we have discovered sequence similarity between the CLE polypeptides and an esophageal gland cell polypeptide from Heterodera glycines, the soybean cyst nematode (Fig. 1). The sequence similarity between the plant polypeptide family and the H. glycines polypeptide, here referred to as HgCLE, was evident from a position-specific iterative BLAST (PSI-BLAST) [3] database search with the CLV3 sequence. Furthermore, the motif-discovery tool MEME [4] was applied to the CLE sequences, and the resulting file was used as input to the MAST algorithm [5] in a database search. The high-scoring sequences were CLV3-like plant polypeptides, but also included HgCLE. H. glycines is a sedentary plant-parasitic nematode. The infective juvenile stage penetrates the root and Corresponding author: Karen Skriver ([email protected]). http://plants.trends.com
migrates to a site near the vascular tissue to establish a permanent feeding site. The nematode induces the transformation of plant cells into metabolically active feeding cells. Secretions from the esophageal gland cells of the nematode are released through the stylet, a mouth spear that is used to pierce plant cell walls. These secretions are thought to contain the substances that cause the transformation of root cells by altering gene expression in the cells [6]. HgCLE is a hypothetical polypeptide predicted from cDNA sequences cloned from esophageal gland cells [7,8]. The cDNA clone hybridized to genomic DNA of H. glycines, and expression of the gene was specifically detected in the dorsal esophageal gland cell of parasitic stages of H. glycines [7]. The dorsal gland cell is the predominate gland of the parasitic stages of H. glycines [6]. HgCLE contains the C-terminal motif and the N-terminal signal peptide that characterize the CLE sequences (Fig. 1). Predicted signal peptide cleavage produces a polypeptide of 117 amino acids, but further processing cannot be excluded. It has yet to be determined whether the CLE polypeptides are processed subsequent to signal peptide cleavage [2]. Indeed, several EST clones from wheat encode sequences containing multiple CLE motifs (Fig. 1). The striking resemblance to a polyprotein precursor could suggest that the conserved motif constitutes the mature CLE peptides. Based on the similarity between a bioactive plant peptide and a plant-parasite polypeptide, we hypothesize that the nematode has co-opted the plant signaling peptide for parasitic modification of host
Update
56
BE401912 CLE41 CLE9 CLE10 CLE13 CLE12 CLE11 CLAVATA3 HgCLE CLE3 CLE4 CLE6 CLE5 CLE1 CLE2 CLE7 CLE40 CLE18 CLE21 CLE19 CLE8 CLE17 CLE16 CLE22 CLE20 CLE14 CLE25 CLE26 CLE27 Consensus
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
BE401912 CLE41 CLE9 CLE10 CLE13 CLE12 CLE11 CLAVATA3 HgCLE CLE3 CLE4 CLE6 CLE5 CLE1 CLE2 CLE7 CLE40 CLE18 CLE21 CLE19 CLE8 CLE17 CLE16 CLE22 CLE20 CLE14 CLE25 CLE26 CLE27 Consensus
86 71 87 75 76 77 67 66 97 59 57 57 57 51 51 56 54 26 81 91 49 54 78 76 62 55 45 64 64 109
TRENDS in Plant Science
Vol.8 No.2 February 2003
--------MAAMHESTPSLLVLFLSLMLFFTASS---------------ARHMTGDPPPVIPSPPPHMASPTMEEAWEGVMVAPRPVPSGPDPIHHRPHAPPPHRPXP ------------MATSNDQTNTKSSHSRTLLLLFIFLSLLLFSSLT---------IPMTRHQS----------------TSMVAPFKRVLLESS-VPASSTMDLRPKA -------------MTHLNRLILISLLFVSLLLKSSTASSTVVDEGNRTSRNFRYRTHRFVPRFNHHPYHVT--------PHRSCDSFIRPYARS-MCIELQRIHRSSR --------------MKTNRNRPINILIVFFLLTTARA----------ATRNWTNRTHRTVPKV-QHAYYAY--------PHRSCESFSRPYARS-MCIELERIHRSSR ------------MATTRVSHVLGFLLWISLLIFVSIGLFG-------------NFSSKPINPFPSPVITLPA-------LYYRPGRRALAVKTF-DFTPFLKDLRRSN -------------MALKFSQILFIVLWLSLFFLLLHHLYSLNFRRLYS----------LNAVEPSLLKQHY--------RSYRLVSRKVLSDRF-DFTPFHSRDNSRH ------MTKQPKPCSFLFHISLLSALFVFLLISFAFTTS-------------------------YKLKSG----------INSLGHKRILASNF-DFTPFLKNKDRTQ ------------MDSKSFLLLLLLFCFLFLHDASG-----------------LTLSFTPLYVYN-------------SYLTQAHAHVQGLSNRK-MMMMKMESEWVGA -----------MPNIFKILLIVLLAVVSFRLSASTGDKKTANDGSGNNSSAGIGTKIKRIVTAGLLFTSLATGGAEAIGRSNAQGGNAAGLVPS-HLTNRSMAPPPPP ----------------MASLKLWVCLVLLLVLELTSVHEC-----------------RPLVAEE----------------RFSGSSRLKKIRRE-LFERLKEMKGRSE ----------------MASFKLWVCLILLLLEFSVHQC-------------------RPLVAEE----------------SPSDSGNIRKIMRE-LLKRSEELKVRSK ----------------MANLILKQSLIILLIIYSTPILSSQA---------------RILR--------------------TYRPTTMGDMDSQ-VLLRELGIDLSKF ----------------MATLILKQTLIILLIIFSLQTLSSQA---------------RILR--------------------SYRAVSMGNMDSQ-VLLHELGFDLSKF ----------------MANLKFLLCLFLICVSLSRSSA----------------------------------------SRPMFPNADGIKRGR--MMIEAEEVLKASM ----------------MAKLSFTFCFLLFLLLSSIAA-----------------------------------------GSRPLEGARVGVKVRG-LSPSIEATSPTVE -------------MASKALLLFVMLTFLLVIEMEG----------------------RILRVN-----------------SKTKDGESNDLLKR-LGYNVSELKRIGR -------------MAAMKYKGSVFIILVILLLSSSLLA-----------------------------------------HSSSTKSFFWLGETQ-DTKAMKKEKKIDG ------------MHLLKGGVVLIITLILFLITSSIVA---------------------------------------------------------------------------MLILSSRYAMKRDVLIIVIFTVLVLIIISRSSS----------------IQAGRFMTTGRNRNLSVAR------SLYYKNHHKVVITEM-SNFNKVRRRSSRF ------MLHLFILYAPYSLYINISILILFALLSNVAIYNN-----------PAFAFLHIISPSNKQKQYLTKNRQMKIKGLMILASSLLILAFI-HQSESASMRSLLM ------------MKVLKRDSMLLLITLYFLLTTSMA-----------------------------------------------RQDPFLVGVEK-DVVPAGTDLKQNK -------------MTMCFFLFFFVFYVSFQIVLS-----------------------------------------SSASVGYSRLHLVASPPPP-PPRKALRYSTAPF -MEACSRKRRRRRAYTTSTTGYAAVFFCGIFVFAQFGISSSA-----------------------------LFAPDHYPSLPRKAGHFHEMASF-QAPKATVSFTGQR MGNYYSRRKSRKHITTVALIILLLLLFLFLYAKASSS--------------------------------SPNIHHHSTHGSLKKSGNLDPKLHD-LDSNAASSRGSKY --------MKNKNMNPSRPRLLCLIVFLFLVIVLSKA--------------------------------------SRIHVERRRFSSKPSGENR-EFLPSQPTFPVVD --------------MKVWSQRLSFLIVMIFILAGLHSSSA---------------------------------------GRKLPSMTTTEEFQR-LSFDGKRILSEVT ----------------MGGNGIRALVGVIASLGLIVFLLVGILA-----------------------------------------------NSA-PSVPSSENVKTLR -----------MRNNHSLRLQLWFRTLFTVGVVTLLMIDAFVL---------------------------------QNNKEDDKTKEITTAVNM-NNSDAKEIQQELE -----------MTHAREWRSSLTTTLLMVILLSYMLHLFCVYSRVGA---------------------------------IRIFPETPASGKRQ-EEDLMKKYFGAGK L L LIL LLL S
STEEAREG------------------VMVAPRPVPSGPNPIHHFPAPAPQPHHHHRCHDLPPASTEEACEGDIVAPRPVPFGSHPIHNHPAPVPQPNQQRRRKAHRLHL STRRSRTS------RRRE--------FGNDAHEVPSGPNPISN-----------------------------------------------------------------KQPLLSPPPP---EIDPR--------YGVDKRLVPSGPNPLHN------------------------------------------------------------------QPLFSPPPPPT-EIDQR--------YGVEKRLVPSGPNPLHN-----------------------------------------------------------------HRKALPAGGS---EIDPR--------YGVEKRLVPSGPNPLHH-----------------------------------------------------------------NHRSGEQYDGD--EIDPR--------YGVEKRRVPSGPNPLHH-----------------------------------------------------------------RQRQSPSLTVK--ENGFW--------YNDEERVVPSGPNPLHH-----------------------------------------------------------------NGEAEKAKTKG-----LG--------LHEELRTVPSGPDPLHHHVNPPRQPRNNFQLP--------------------------------------------------AQFEKGAATRVEKMRAQLRELAEKMTDKDPKRLSPSGPDPHHH-----------------------------------------------------------------GEETILGN------------------TLDSKRLSPGGPDPRHH-----------------------------------------------------------------DGQTVLG-------------------TLDSKRLSPGGPDPRHH-----------------------------------------------------------------KGQDERRF------------------LVDSERVSPGGPDPQHH-----------------------------------------------------------------KGHNERRF------------------LVSSDRVSPGGPDPQHH-----------------------------------------------------------------EKLMERG-------------------FNESMRLSPGGPDPRHH-----------------------------------------------------------------DDQAAGSHG------------------KSPERLSPGGPDPQHH------------------------------------------------------------------ELSVQN---------------------EVDRFSPGGPDPQHHSYPLSSKPRI----------------------------------------------------------GTAN--------------------EVEERQVPTGSDPLHHKHIPFTP------------------------------------------------------------------------------IREDPSLIGVDRQIPTGPDPLHNPPQPSPKHHHWIGVEENNIDRSWNYVDYESHHAHSPIHNSPEPAPLYRHLIGV------------RRKTDGDE------------------EEEEKRSIPTGPNPLHNK----------------------------------------------------------------NNGSYEEEEQVLKYDSMG--TIANSSALDSKRVIPTGPNPLHNR----------------------------------------------------------------AKPHLPN-------------------LFRTMRRVPTGPNPLHHISPPQPGSLNYARN---------------------------------------------------RGPLSRDD-----------------IYGDDKRVVHTGPNPLHN-----------------------------------------------------------------REEENRDE-----------------VYKDDKRLVHTGPNPLHN-----------------------------------------------------------------TNYEGGGED----------------VFEDGKRRVFTGPNPLHNR----------------------------------------------------------------AGEILPD-----------------------KRKVKTGSNPLHNKR---------------------------------------------------------------ADKKYDR------------------IYGASARLVPKGPNPLHNK----------------------------------------------------------------FSGKDVN------------------LFHVSKRKVPNGPDPIHNRFLSLLSRIFNLLLLLL------------------------------------------------DGSRNDDLS-----------------YVASKRKVPRGPDPIHNRFLLLSRFILSLLTNPYPYLHICVLDVSV------------------------------------FPPVDSFVGKG---------------ISESKRIVPSCPDPLHN-----------------------------------------------------------------KRLVPSGPNPLHH TRENDS in Plant Science
Fig. 1. Alignment of the esophageal gland cell polypeptide from Heterodera glycines (GenBank Accession number: AAG21331, here referred to as HgCLE) with CLAVATA3 and Arabidopsis CLE sequences. Also included in the alignment is the sequence encoded by wheat EST clone BE401912, exemplifying a sequence encoding multiple CLE motifs. CLE1 –CLE27 were identified by J. Mark Cock and Sheila McCormick [2]. CLE40 and CLE41 are included in the annotation of the Arabidopsis genome performed by The Institute for Genomic Research, Rockville, MD, USA (http://www.tigr.org); the sequences are encoded by loci At5g12990 and At3g24770, respectively. Residues highlighted in red are common to at least half of the sequences, and residues highlighted in blue are chemically similar in more than half of the sequences or similar to the dominating residue. The last line shows the consensus residues. Predicted signal peptides are underlined. CLE16, CLE25, CLE26 and CLE27 are predicted to contain an N-terminal signal anchor instead of a signal peptide [2]. The three occurrences of the conserved motif in the sequence encoded by EST clone BE401912 are highlighted in gray.
plant cells. HgCLE might thus function as a ligand for a host LRR receptor kinase, possibly imitating or inhibiting the function of an endogenous peptide ligand. This hypothesis concurs with a model proposed by David McKenzie Bird [9] to explain the development of nematode-induced feeding sites. Moreover, it has been demonstrated that a low-molecular-weight peptide component of potato cyst nematode secretions can costimulate the proliferation of tobacco protoplasts in the http://plants.trends.com
presence of phytohormones [10]. It would be interesting to determine the effects of HgCLE in a plant protoplast proliferation assay. Furthermore, doublestranded RNA-mediated interference of HgCLE gene expression could be applied to investigate the role of HgCLE in the plant – parasite interaction [11]. Database searches revealed no sequences from Caenorhabditis elegans or other non-plant organisms with the characteristics of HgCLE or of the plant CLE sequences.
Update
TRENDS in Plant Science
The intriguing similarity between host and parasite sequences could be an example of adaptive molecular mimicry, defined by Roger Hall [12] as ‘a parasite molecule mimics a host molecule for a biological reason’. Although lateral gene transfer influences the evolution of archeal and bacterial genomes, the transfer of genes between two multicellular eukaryotes is not expected to be common [13]. Considering the simplicity of the features shared by HgCLE and the CLE sequences, a more likely explanation of the sequence similarity is convergent evolution. If indeed this is an example of ligand mimicry, it emphasizes the importance of peptide ligands in plant biology and constitutes a convergence of research in nematode parasitism and peptide signaling. References 1 DeYoung, B.J. and Clark, S.E. (2001) Signaling through the CLAVATA1 receptor complex. Plant Mol. Biol. 46, 505 – 513 2 Cock, J.M. and McCormick, S. (2001) A large family of genes that share homology with CLAVATA3. Plant Physiol. 126, 939 – 942 3 Altschul, S.F. et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389 – 3402 4 Bailey, T.L. and Elkan, C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2, 28– 36
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5 Bailey, T.L. and Gribskov, M. (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14, 48 – 54 6 Davis, E.L. et al. (2000) Nematode parasitism genes. Annu. Rev. Phytopathol. 38, 365 – 396 7 Wang, X. et al. (2001) Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol. Plant – Microbe Interact. 14, 536 – 544 8 Gao, B. et al. (2001) Identification of putative parasitism genes expressed in the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol. Plant – Microbe Interact. 14, 1247 – 1254 9 Bird, D.M. (1996) Manipulation of host gene expression by root-knot nematodes. J. Parasitol. 82, 881– 888 10 Goverse, A. et al. (1999) Naturally induced secretions of the potato cyst nematode co-stimulate the proliferation of both tobacco leaf protoplasts and human peripheral blood mononuclear cells. Mol. Plant – Microbe Interact. 12, 872 – 881 11 Urwin, P.E. et al. (2002) Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Mol. Plant –Microbe Interact. 15, 747 – 752 12 Hall, R. (1994) Molecular mimicry. Adv. Parasitol. 34, 81 – 132 13 Doolittle, W.F. (1999) Phylogenetic classification and the universal tree. Science 284, 2124 – 2128 1360-1385/03/$ - see front matter q 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S1360-1385(03)00003-7
Articles of interest in other Trends journals 21st century wheat breeding: plot selection or plate detection? Robert M.D. Koebner and Richard W. Summers. Trends in Biotechnology (19 December 2002) DOI: 10.1016/S0167-7799(02)00036-7 Inducible systems see the light William M. Keyes and Alea A. Mills. Trends in Biotechnology (2 December 2002) DOI: 10.1016/S0167-7799(02)00022-7 Progress towards commercialization of plastid transformation technology Pal Maliga. Trends in Biotechnology (2003) 21, 20 – 28 The genes of the Green Revolution Peter Hedden. Trends in Genetics (2003) 19, 5– 9 Macro effects of microRNAs in plants Catherine A. Kidner and Robert A. Martienssen. Trends in Genetics (2003) 19, 13 –16 Chloroplast research in the genomic age Dario Leister. Trends in Genetics (2003) 19, 47 –56 Pharmacological effects of garlic extract Ruomei Qi and Zhengang Wang. Trends in Pharmacological Sciences (14 December 2002) DOI: 10.1016/S0165-6147(02)00014-7 http://plants.trends.com
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2 Johnson, L. et al. (2002) Interplay between two epigenetic marks. DNA methylation and histone H3 lysine 9 methylation. Curr. Biol. 12, 1360 3 Richards, E.J. and Elgin, S.C. (2002) Epigenetic codes for heterochromatin formation and silencing: rounding up the usual suspects. Cell 108, 489– 500 4 Bartee, L. et al. (2001) Arabidopsis cmt3 chromomethylase mutations block non-CG methylation and silencing of an endogenous gene. Genes Dev. 15, 1753– 1758 5 Lindroth, A.M. et al. (2001) Requirement of CHROMOMETHYLASE3 for maintenance of CpXpG methylation. Science 292, 2077– 2080 6 Jackson, J.P. et al. (2002) Control of CpNpG DNA methylation by the KRYPTONITE histone H3 methyltransferase. Nature 416, 556 – 560 7 Tamaru, H. and Selker, E.U. (2001) A histone H3 methyltransferase controls DNA methylation in Neurospora crassa. Nature 414, 277– 283
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8 Volpe, T.A. et al. (2002) Regulation of heterochromatic silencing and histone H3 lysine-9 methylation by RNAi. Science 297, 1833 – 1837 9 Pal-Bhadra, M. et al. (2002) RNAi related mechanisms affect both transcriptional and posttranscriptional transgene silencing in Drosophila. Mol. Cell 9, 315 – 327 10 Richards, E.J. (1997) DNA methylation and plant development. Trends Genet. 13, 319 – 323 11 Vaucheret, H. et al. (2001) Post-transcriptional gene silencing in plants. J. Cell Sci. 114, 3083– 3091 12 Dernburg, A.F. and Karpen, G.H. (2002) A chromosome RNAissance. Cell 111, 159– 162
1360-1385/03/$ - see front matter q 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S1360-1385(03)00005-0
| Letters
Ligand mimicry? Plant-parasitic nematode polypeptide with similarity to CLAVATA3 Addie Nina Olsen and Karen Skriver Institute of Molecular Biology, University of Copenhagen, Øster, Farimagsgade 2A, DK-1353 Copenhagen K, Denmark
The importance of peptides in plant intercellular signaling has become apparent during the past decade. Among recently identified peptide signals is CLAVATA3 (CLV3), which is involved in cell-fate determination in the shoot apical meristem of Arabidopsis. There is evidence that CLV3 is a ligand for CLAVATA1 (CLV1), a receptor kinase with an extracellular domain containing leucine-rich repeats (LRRs) [1]. The Arabidopsis genome contains a large gene family, called CLE for CLAVATA3/ESR-related, encoding polypeptides with similarity to CLV3. These small polypeptides are characterized by a short, C-terminal motif and an N-terminal signal peptide or signal anchor [2]. Similar sequences are encoded by expressed sequence tag (EST) clones from various plants. Using motif-based database search methods, we have discovered sequence similarity between the CLE polypeptides and an esophageal gland cell polypeptide from Heterodera glycines, the soybean cyst nematode (Fig. 1). The sequence similarity between the plant polypeptide family and the H. glycines polypeptide, here referred to as HgCLE, was evident from a position-specific iterative BLAST (PSI-BLAST) [3] database search with the CLV3 sequence. Furthermore, the motif-discovery tool MEME [4] was applied to the CLE sequences, and the resulting file was used as input to the MAST algorithm [5] in a database search. The high-scoring sequences were CLV3-like plant polypeptides, but also included HgCLE. H. glycines is a sedentary plant-parasitic nematode. The infective juvenile stage penetrates the root and Corresponding author: Karen Skriver ([email protected]). http://plants.trends.com
migrates to a site near the vascular tissue to establish a permanent feeding site. The nematode induces the transformation of plant cells into metabolically active feeding cells. Secretions from the esophageal gland cells of the nematode are released through the stylet, a mouth spear that is used to pierce plant cell walls. These secretions are thought to contain the substances that cause the transformation of root cells by altering gene expression in the cells [6]. HgCLE is a hypothetical polypeptide predicted from cDNA sequences cloned from esophageal gland cells [7,8]. The cDNA clone hybridized to genomic DNA of H. glycines, and expression of the gene was specifically detected in the dorsal esophageal gland cell of parasitic stages of H. glycines [7]. The dorsal gland cell is the predominate gland of the parasitic stages of H. glycines [6]. HgCLE contains the C-terminal motif and the N-terminal signal peptide that characterize the CLE sequences (Fig. 1). Predicted signal peptide cleavage produces a polypeptide of 117 amino acids, but further processing cannot be excluded. It has yet to be determined whether the CLE polypeptides are processed subsequent to signal peptide cleavage [2]. Indeed, several EST clones from wheat encode sequences containing multiple CLE motifs (Fig. 1). The striking resemblance to a polyprotein precursor could suggest that the conserved motif constitutes the mature CLE peptides. Based on the similarity between a bioactive plant peptide and a plant-parasite polypeptide, we hypothesize that the nematode has co-opted the plant signaling peptide for parasitic modification of host
Update
56
BE401912 CLE41 CLE9 CLE10 CLE13 CLE12 CLE11 CLAVATA3 HgCLE CLE3 CLE4 CLE6 CLE5 CLE1 CLE2 CLE7 CLE40 CLE18 CLE21 CLE19 CLE8 CLE17 CLE16 CLE22 CLE20 CLE14 CLE25 CLE26 CLE27 Consensus
1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1
BE401912 CLE41 CLE9 CLE10 CLE13 CLE12 CLE11 CLAVATA3 HgCLE CLE3 CLE4 CLE6 CLE5 CLE1 CLE2 CLE7 CLE40 CLE18 CLE21 CLE19 CLE8 CLE17 CLE16 CLE22 CLE20 CLE14 CLE25 CLE26 CLE27 Consensus
86 71 87 75 76 77 67 66 97 59 57 57 57 51 51 56 54 26 81 91 49 54 78 76 62 55 45 64 64 109
TRENDS in Plant Science
Vol.8 No.2 February 2003
--------MAAMHESTPSLLVLFLSLMLFFTASS---------------ARHMTGDPPPVIPSPPPHMASPTMEEAWEGVMVAPRPVPSGPDPIHHRPHAPPPHRPXP ------------MATSNDQTNTKSSHSRTLLLLFIFLSLLLFSSLT---------IPMTRHQS----------------TSMVAPFKRVLLESS-VPASSTMDLRPKA -------------MTHLNRLILISLLFVSLLLKSSTASSTVVDEGNRTSRNFRYRTHRFVPRFNHHPYHVT--------PHRSCDSFIRPYARS-MCIELQRIHRSSR --------------MKTNRNRPINILIVFFLLTTARA----------ATRNWTNRTHRTVPKV-QHAYYAY--------PHRSCESFSRPYARS-MCIELERIHRSSR ------------MATTRVSHVLGFLLWISLLIFVSIGLFG-------------NFSSKPINPFPSPVITLPA-------LYYRPGRRALAVKTF-DFTPFLKDLRRSN -------------MALKFSQILFIVLWLSLFFLLLHHLYSLNFRRLYS----------LNAVEPSLLKQHY--------RSYRLVSRKVLSDRF-DFTPFHSRDNSRH ------MTKQPKPCSFLFHISLLSALFVFLLISFAFTTS-------------------------YKLKSG----------INSLGHKRILASNF-DFTPFLKNKDRTQ ------------MDSKSFLLLLLLFCFLFLHDASG-----------------LTLSFTPLYVYN-------------SYLTQAHAHVQGLSNRK-MMMMKMESEWVGA -----------MPNIFKILLIVLLAVVSFRLSASTGDKKTANDGSGNNSSAGIGTKIKRIVTAGLLFTSLATGGAEAIGRSNAQGGNAAGLVPS-HLTNRSMAPPPPP ----------------MASLKLWVCLVLLLVLELTSVHEC-----------------RPLVAEE----------------RFSGSSRLKKIRRE-LFERLKEMKGRSE ----------------MASFKLWVCLILLLLEFSVHQC-------------------RPLVAEE----------------SPSDSGNIRKIMRE-LLKRSEELKVRSK ----------------MANLILKQSLIILLIIYSTPILSSQA---------------RILR--------------------TYRPTTMGDMDSQ-VLLRELGIDLSKF ----------------MATLILKQTLIILLIIFSLQTLSSQA---------------RILR--------------------SYRAVSMGNMDSQ-VLLHELGFDLSKF ----------------MANLKFLLCLFLICVSLSRSSA----------------------------------------SRPMFPNADGIKRGR--MMIEAEEVLKASM ----------------MAKLSFTFCFLLFLLLSSIAA-----------------------------------------GSRPLEGARVGVKVRG-LSPSIEATSPTVE -------------MASKALLLFVMLTFLLVIEMEG----------------------RILRVN-----------------SKTKDGESNDLLKR-LGYNVSELKRIGR -------------MAAMKYKGSVFIILVILLLSSSLLA-----------------------------------------HSSSTKSFFWLGETQ-DTKAMKKEKKIDG ------------MHLLKGGVVLIITLILFLITSSIVA---------------------------------------------------------------------------MLILSSRYAMKRDVLIIVIFTVLVLIIISRSSS----------------IQAGRFMTTGRNRNLSVAR------SLYYKNHHKVVITEM-SNFNKVRRRSSRF ------MLHLFILYAPYSLYINISILILFALLSNVAIYNN-----------PAFAFLHIISPSNKQKQYLTKNRQMKIKGLMILASSLLILAFI-HQSESASMRSLLM ------------MKVLKRDSMLLLITLYFLLTTSMA-----------------------------------------------RQDPFLVGVEK-DVVPAGTDLKQNK -------------MTMCFFLFFFVFYVSFQIVLS-----------------------------------------SSASVGYSRLHLVASPPPP-PPRKALRYSTAPF -MEACSRKRRRRRAYTTSTTGYAAVFFCGIFVFAQFGISSSA-----------------------------LFAPDHYPSLPRKAGHFHEMASF-QAPKATVSFTGQR MGNYYSRRKSRKHITTVALIILLLLLFLFLYAKASSS--------------------------------SPNIHHHSTHGSLKKSGNLDPKLHD-LDSNAASSRGSKY --------MKNKNMNPSRPRLLCLIVFLFLVIVLSKA--------------------------------------SRIHVERRRFSSKPSGENR-EFLPSQPTFPVVD --------------MKVWSQRLSFLIVMIFILAGLHSSSA---------------------------------------GRKLPSMTTTEEFQR-LSFDGKRILSEVT ----------------MGGNGIRALVGVIASLGLIVFLLVGILA-----------------------------------------------NSA-PSVPSSENVKTLR -----------MRNNHSLRLQLWFRTLFTVGVVTLLMIDAFVL---------------------------------QNNKEDDKTKEITTAVNM-NNSDAKEIQQELE -----------MTHAREWRSSLTTTLLMVILLSYMLHLFCVYSRVGA---------------------------------IRIFPETPASGKRQ-EEDLMKKYFGAGK L L LIL LLL S
STEEAREG------------------VMVAPRPVPSGPNPIHHFPAPAPQPHHHHRCHDLPPASTEEACEGDIVAPRPVPFGSHPIHNHPAPVPQPNQQRRRKAHRLHL STRRSRTS------RRRE--------FGNDAHEVPSGPNPISN-----------------------------------------------------------------KQPLLSPPPP---EIDPR--------YGVDKRLVPSGPNPLHN------------------------------------------------------------------QPLFSPPPPPT-EIDQR--------YGVEKRLVPSGPNPLHN-----------------------------------------------------------------HRKALPAGGS---EIDPR--------YGVEKRLVPSGPNPLHH-----------------------------------------------------------------NHRSGEQYDGD--EIDPR--------YGVEKRRVPSGPNPLHH-----------------------------------------------------------------RQRQSPSLTVK--ENGFW--------YNDEERVVPSGPNPLHH-----------------------------------------------------------------NGEAEKAKTKG-----LG--------LHEELRTVPSGPDPLHHHVNPPRQPRNNFQLP--------------------------------------------------AQFEKGAATRVEKMRAQLRELAEKMTDKDPKRLSPSGPDPHHH-----------------------------------------------------------------GEETILGN------------------TLDSKRLSPGGPDPRHH-----------------------------------------------------------------DGQTVLG-------------------TLDSKRLSPGGPDPRHH-----------------------------------------------------------------KGQDERRF------------------LVDSERVSPGGPDPQHH-----------------------------------------------------------------KGHNERRF------------------LVSSDRVSPGGPDPQHH-----------------------------------------------------------------EKLMERG-------------------FNESMRLSPGGPDPRHH-----------------------------------------------------------------DDQAAGSHG------------------KSPERLSPGGPDPQHH------------------------------------------------------------------ELSVQN---------------------EVDRFSPGGPDPQHHSYPLSSKPRI----------------------------------------------------------GTAN--------------------EVEERQVPTGSDPLHHKHIPFTP------------------------------------------------------------------------------IREDPSLIGVDRQIPTGPDPLHNPPQPSPKHHHWIGVEENNIDRSWNYVDYESHHAHSPIHNSPEPAPLYRHLIGV------------RRKTDGDE------------------EEEEKRSIPTGPNPLHNK----------------------------------------------------------------NNGSYEEEEQVLKYDSMG--TIANSSALDSKRVIPTGPNPLHNR----------------------------------------------------------------AKPHLPN-------------------LFRTMRRVPTGPNPLHHISPPQPGSLNYARN---------------------------------------------------RGPLSRDD-----------------IYGDDKRVVHTGPNPLHN-----------------------------------------------------------------REEENRDE-----------------VYKDDKRLVHTGPNPLHN-----------------------------------------------------------------TNYEGGGED----------------VFEDGKRRVFTGPNPLHNR----------------------------------------------------------------AGEILPD-----------------------KRKVKTGSNPLHNKR---------------------------------------------------------------ADKKYDR------------------IYGASARLVPKGPNPLHNK----------------------------------------------------------------FSGKDVN------------------LFHVSKRKVPNGPDPIHNRFLSLLSRIFNLLLLLL------------------------------------------------DGSRNDDLS-----------------YVASKRKVPRGPDPIHNRFLLLSRFILSLLTNPYPYLHICVLDVSV------------------------------------FPPVDSFVGKG---------------ISESKRIVPSCPDPLHN-----------------------------------------------------------------KRLVPSGPNPLHH TRENDS in Plant Science
Fig. 1. Alignment of the esophageal gland cell polypeptide from Heterodera glycines (GenBank Accession number: AAG21331, here referred to as HgCLE) with CLAVATA3 and Arabidopsis CLE sequences. Also included in the alignment is the sequence encoded by wheat EST clone BE401912, exemplifying a sequence encoding multiple CLE motifs. CLE1 –CLE27 were identified by J. Mark Cock and Sheila McCormick [2]. CLE40 and CLE41 are included in the annotation of the Arabidopsis genome performed by The Institute for Genomic Research, Rockville, MD, USA (http://www.tigr.org); the sequences are encoded by loci At5g12990 and At3g24770, respectively. Residues highlighted in red are common to at least half of the sequences, and residues highlighted in blue are chemically similar in more than half of the sequences or similar to the dominating residue. The last line shows the consensus residues. Predicted signal peptides are underlined. CLE16, CLE25, CLE26 and CLE27 are predicted to contain an N-terminal signal anchor instead of a signal peptide [2]. The three occurrences of the conserved motif in the sequence encoded by EST clone BE401912 are highlighted in gray.
plant cells. HgCLE might thus function as a ligand for a host LRR receptor kinase, possibly imitating or inhibiting the function of an endogenous peptide ligand. This hypothesis concurs with a model proposed by David McKenzie Bird [9] to explain the development of nematode-induced feeding sites. Moreover, it has been demonstrated that a low-molecular-weight peptide component of potato cyst nematode secretions can costimulate the proliferation of tobacco protoplasts in the http://plants.trends.com
presence of phytohormones [10]. It would be interesting to determine the effects of HgCLE in a plant protoplast proliferation assay. Furthermore, doublestranded RNA-mediated interference of HgCLE gene expression could be applied to investigate the role of HgCLE in the plant – parasite interaction [11]. Database searches revealed no sequences from Caenorhabditis elegans or other non-plant organisms with the characteristics of HgCLE or of the plant CLE sequences.
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TRENDS in Plant Science
The intriguing similarity between host and parasite sequences could be an example of adaptive molecular mimicry, defined by Roger Hall [12] as ‘a parasite molecule mimics a host molecule for a biological reason’. Although lateral gene transfer influences the evolution of archeal and bacterial genomes, the transfer of genes between two multicellular eukaryotes is not expected to be common [13]. Considering the simplicity of the features shared by HgCLE and the CLE sequences, a more likely explanation of the sequence similarity is convergent evolution. If indeed this is an example of ligand mimicry, it emphasizes the importance of peptide ligands in plant biology and constitutes a convergence of research in nematode parasitism and peptide signaling. References 1 DeYoung, B.J. and Clark, S.E. (2001) Signaling through the CLAVATA1 receptor complex. Plant Mol. Biol. 46, 505 – 513 2 Cock, J.M. and McCormick, S. (2001) A large family of genes that share homology with CLAVATA3. Plant Physiol. 126, 939 – 942 3 Altschul, S.F. et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389 – 3402 4 Bailey, T.L. and Elkan, C. (1994) Fitting a mixture model by expectation maximization to discover motifs in biopolymers. Proc. Int. Conf. Intell. Syst. Mol. Biol. 2, 28– 36
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5 Bailey, T.L. and Gribskov, M. (1998) Combining evidence using p-values: application to sequence homology searches. Bioinformatics 14, 48 – 54 6 Davis, E.L. et al. (2000) Nematode parasitism genes. Annu. Rev. Phytopathol. 38, 365 – 396 7 Wang, X. et al. (2001) Signal peptide-selection of cDNA cloned directly from the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol. Plant – Microbe Interact. 14, 536 – 544 8 Gao, B. et al. (2001) Identification of putative parasitism genes expressed in the esophageal gland cells of the soybean cyst nematode Heterodera glycines. Mol. Plant – Microbe Interact. 14, 1247 – 1254 9 Bird, D.M. (1996) Manipulation of host gene expression by root-knot nematodes. J. Parasitol. 82, 881– 888 10 Goverse, A. et al. (1999) Naturally induced secretions of the potato cyst nematode co-stimulate the proliferation of both tobacco leaf protoplasts and human peripheral blood mononuclear cells. Mol. Plant – Microbe Interact. 12, 872 – 881 11 Urwin, P.E. et al. (2002) Ingestion of double-stranded RNA by preparasitic juvenile cyst nematodes leads to RNA interference. Mol. Plant –Microbe Interact. 15, 747 – 752 12 Hall, R. (1994) Molecular mimicry. Adv. Parasitol. 34, 81 – 132 13 Doolittle, W.F. (1999) Phylogenetic classification and the universal tree. Science 284, 2124 – 2128 1360-1385/03/$ - see front matter q 2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S1360-1385(03)00003-7
Articles of interest in other Trends journals 21st century wheat breeding: plot selection or plate detection? Robert M.D. Koebner and Richard W. Summers. Trends in Biotechnology (19 December 2002) DOI: 10.1016/S0167-7799(02)00036-7 Inducible systems see the light William M. Keyes and Alea A. Mills. Trends in Biotechnology (2 December 2002) DOI: 10.1016/S0167-7799(02)00022-7 Progress towards commercialization of plastid transformation technology Pal Maliga. Trends in Biotechnology (2003) 21, 20 – 28 The genes of the Green Revolution Peter Hedden. Trends in Genetics (2003) 19, 5– 9 Macro effects of microRNAs in plants Catherine A. Kidner and Robert A. Martienssen. Trends in Genetics (2003) 19, 13 –16 Chloroplast research in the genomic age Dario Leister. Trends in Genetics (2003) 19, 47 –56 Pharmacological effects of garlic extract Ruomei Qi and Zhengang Wang. Trends in Pharmacological Sciences (14 December 2002) DOI: 10.1016/S0165-6147(02)00014-7 http://plants.trends.com
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