Abstract
A new member of the S gene family,SLR3 (S-Locus Related 3), was identified inBrassica oleracea. This gene had a novel pattern of expression compared with previously described members of the family, being expressed in petals, sepals and vegetative apices, in addition to stigmas and anthers. Moreover, use ofSLR3-derived probes in RNA blot and RACE-PCR (rapid amplification of cDNA ends-polymerase chain reaction) experiments has identified transcripts of genes closely related toSLR3 in leaves, cotyledons and, at high levels in developing anthers.SLR3 is not linked to theS locus but is linked to two or three closely related genes. Sequence analysis of theSLR3 gene indicates that it is derived from an ancestral receptor kinase gene that has been modified by a series of deletion events. As a result of these modifications,SLR3 is predicted to encode a secreted glycoprotein lacking both transmembrane and kinase domains. The putativeSLR3 protein differs from the products of most other S gene family members in that several of the highly conserved cysteines have been lost. Within theS gene family, modification of receptor kinase genes by deletion may represent a general mechanism for the generation of genes encoding secreted glycoproteins.
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References
Bateman AJ (1955) Self-incompatibility systems in angiosperms. III. Cruciferae. Heredity 9:53–68
Boyes DC, Chen CH, Tantikanjana T, Esch JJ, Nasrallah JB (1991) Isolation of a secondS-locus-related cDNA fromBrassica oleracea: Genetic relationships between the S-locus and two related loci. Genetics 127:221–228
Chen C-H, Nasrallah JB (1990) A new class of S sequences defined by a pollen recessive self-incompatibility allele ofBrassica oleracea. Mol Gen Genet 222:241–248
Childs SR, Wrana JL, Arora K, Attisano L, O'Connor MB, Massagué J (1993) Identification of aDrosophila activin receptor. Proc Natl Acad Sci USA 90:9475–9479
Choumane W, Heizmann P (1988) Structure and variability of nuclear ribosomal genes in the genusHelianthus. Theor Appl Genet 76:481–489
Dickinson H (1994) Simply a social disease? Nature 367:517–518
Duan D-SR, Pazin MJ, Fretto LJ, Williams LT (1991) A functional soluble extracellular region of the platelet-derived growth factor (PDGF) receptor antagonizes PDGF-stimulated responses. J Biol Chem 266:413–418
Dwyer KG, Choa A, Cheng B, Chen C-H, Nasrallah JB (1989) TheBrassica self-incompatibility multigene family. Genome 31:969–972
Dwyer KG, Lalonde BA, Nasrallah JB, Nasrallah ME (1992) Structure and expression ofAtS1, anArabidopsis thaliana gene homologous to the S-locus related genes ofBrassica. Mol Gen Genet 231:442–448
Dzelzkalns VA, Thorsness MK, Dwyer KG, Baxter JS, Balent MA, Nasrallah ME, Nasrallah JB (1993) Distinctcis-acting elements direct pistil-specific and pollen-specific activity of theBrassica S locus glycoprotein gene promoter. Plant Cell 5:855–863
Flickinger TW, Maihle NJ, Kung H-J (1992) An alternatively processed mRNA from the avian c-erbB gene encodes a soluble truncated form of the receptor that can be black ligand dependent transformation. Mol Cell Biol 12:883–893
Frohman MA, Dush MK, Martin GR (1988) Rapid production of full-length cDNAs from rare transcripts: Amplification using a single gene-specific oligonucleotide primer. Proc Natl Acad Sci USA 85:8998–9002
Gaude T, Friry A, Heizmann P, Mariac C, Rougier M, Fobis I, Dumas C (1993) Expression of a self-incompatibility gene in a self-compatible line ofBrassica oleracea. Plant Cell 5:75–86
Goring DR, Rothstein SJ (1992) TheS-locus receptor kinase gene in a self-incompatibleBrassica napus line encodes a functional serine threonine kinase. Plant Cell 4:1273–1281
Guilluy C-M, Trick M, Heizmann P, Dumas C (1991) PCR detection of transcripts homologous to the self-incompatibility gene in anthers ofBrassica. Theor Appl Genet 82:466–472
Hackett RM, Lawrence MJ, Franklin FCH (1992) ABrassica S-locus related gene promoter directs expression in both pollen and pistil of tobacco. Plant J 2:613–617
Jackson AO, Larkins BA (1976) Influence of ionic strength, pH and chelation of different metals on isolation of polyribosomes from tobacco leaves. Plant physiol 57:5–10
Kumar V, Trick M (1993) Sequence complexity of the S receptor kinase gene family inBrassica. Mol Gen Genet 241:440–446
Lalonde BA, Nasrallah ME, Dwyer KG, Chen C-H, Barlow B, Nasrallah JB (1989) A highly conservedBrassica gene with homology to theS-locus-specific glycoprotein structural gene. Plant Cell 1:249–258
Nasrallah JB, Nasrallah ME (1993) Pollen-stigma signalling in the sporophytic self-incompatibility response. Plant Cell 5:1325–1335
Nasrallah JB, Kao TH, Chen CH, Goldberg ML, Nasrallah ME (1987) Amino-acid sequence of glycoproteins encoded by three alleles of theS-locus ofBrassica oleracea. Nature 326:617–619
Nasrallah JB, Rundle SJ, Nasrallah ME (1994) Genetic evidence for the requirement of theBrassica S-locus receptor kinase gene in the self-incompatibility response. Plant J 5:373–384
Ockendon DJ (1974) Distribution of self-incompatibility alleles and breeding structure of open pollinated cultivars of Brussel sprouts. Heredity 33:159–171
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning: a laboratory manual. Cold Spring Harbour Laboratory Press, Cold Spring Harbor, New York
Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain termination inhibitors. Proc Natl Acad Sci USA 74:5463–5467
Sato T, Thorness MK, Kandasamy MK, Nishio T, Hirai M, Nasrallah JB, Nasrallah ME (1991) Activity of anS-locus gene promoter in pistils and anthers of transgenicBrassica. Plant Cell 3:867–876
Stein JC, Howlett B, Boyes DC, Nasrallah ME, Nasrallah JB (1991) Molecular cloning of a putative receptor protein kinase gene encoded at the self-incompatibility locus ofBrassica oleracea. Proc Natl Acad Sci USA 88:8816–8820
Tantikanjana T, Nasrallah ME, Stein JC, Chen CH, Nasrallah JB (1993) An alternative transcript of theS-locus glycoprotein gene in a class-II pollen-recessive self-incompatibility haplotype ofBrassica oleracea encodes a membrane-anchored protein. Plant Cell 5:657–666
Tobias CM, Howlett B, Nasrallah JB (1992) AnArabidopsis thaliana gene with sequence similarity to theS-locus receptor kinase ofBrassica oleracea: sequence and expression. Plant Physiol 99:284–290
Trick M, Flavell RB (1989) A homozygous S genotype ofBrassica oleracea expresses twoS-like genes. Mol Gen Genet 218:112–117
Ullrich A, Schlessinger J (1990) Signal transduction by receptors with tyrosine kinase activity. Cell 61:203–212
van Engelen FA, Hartog MV, Thomas TL, Taylor B, Sturm A, van Kammen A, de Vries SC (1993) The carrot secreted glycoprotein geneEP1 is expressed in the epidermis and has sequence homology to theBrassica S-locus glycoproteins. Plant J 4:855–862
Walker JC (1993) Receptor-like protein kinase genes ofArabidopsis thaliana. Plant J 3:451–456
Walker JC, Zhang R (1990) Relationship of a putative receptor kinase from maize to theS-locus glycoproteins ofBrassica. Nature 345:743–746
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Cock, J.M., Stanchev, B., Delorme, V. et al. SLR3: A modified receptor kinase gene that has been adapted to encode a putative secreted glycoprotein similar to theS locus glycoprotein. Molec. Gen. Genet. 248, 151–161 (1995). https://doi.org/10.1007/BF02190796
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DOI: https://doi.org/10.1007/BF02190796