Molecular Cytogenetics Laboratory, Clemson University
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Abstract |
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Introduction |
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Plant RLKs are classified into three major groups (Braun and Walker 1996
). The first group includes RLKs with an extracellular S-domain, characteristic of the S-locus receptor kinases (SRKs) and the S-locus glycoproteins (SLGs) from Brassica (Nasrallah and Nasrallah 1993
). SRKs and SLGs are expressed in the stigma and have been implicated in inhibition of self-pollination (Nasrallah and Nasrallah 1993
; Takasaki et al. 2000
).
The second group includes RLKs with novel extracellular domains. A unique extracellular domain was identified in Catharanthus roseus CrRLK1 (Schulze-Muth et al. 1996
). In contrast to other plant RLKs, CrRLK1 uses an intramolecular rather than an intermolecular phosphorylation mechanism (Schulze-Muth et al. 1996
). In Arabidopsis thaliana RLK Wak1, an extracellular domain with several epidermal growth factor repeats and a region similar to a viral movement protein was identified (He, Fujiki, and Kohorn 1996
). Wak1 is expressed in vegetative tissues, and its expression is induced by pathogen and salicylic acid (He, He, and Kohorn 1998
).
The third group of RLKs belongs to the leucine-rich repeat (LRR) protein superfamily (Kobe and Deisenhofer 1994
; Jiang et al. 1995
). Plant LRR-RLKs play major roles in cellular functions, including regulation of endosperm and pollen development (Li and Wurtzel 1998
; Muschietti, Eyal, and McCormick 1998
), regulation of meristem and flower development (Torii et al. 1996
; Clark, Williams, and Meyerowitz 1997
; Kim, Jeong, and An 2000
), floral organ abscission (Jinn, Stone, and Walker 2000)
, gibberellin-induced stem elongation (van der Knaap et al. 1999
), brassinosteroid signal transduction (Li and Chory 1997
), environmental stress responses (Hong et al. 1997
), and disease resistance (Song et al. 1995
). Thus, plant LRR-RLKs respond to a wide range of extracellular signals and transduce intracellular responses depending on the nature of the signal and cellular localization.
In A. thaliana, a putative membrane-bound LRR-RLK, AtCLV1, is involved in shoot and floral meristem development (Clark, Running, and Meyerowitz 1993
; Clark, Williams, and Meyerowitz 1997
). A GenBank search identified several putative A. thaliana LRR-RLKs that were similar in sequence to AtCLV1. One of these LRR-RLKs was characterized. The deduced amino acid sequence of the AtRLK gene (GenBank accession number CAA16688) contains characteristics of a membrane-bound LRR-RLK: an N-terminal signal peptide, an extracellular LRR domain, a transmembrane region, and a cytoplasmic serine/threonine kinase domain (Braun and Walker 1996
). The sequence identity of AtRLK and AtCLV1 is 48% in regions containing potential signal peptides, LRR domains, and transmembrane regions, while it is 81% in regions containing potential kinase domains.
We previously isolated and characterized two soybean (Glycine max) LRR-RLK genes, GmCLV1A and GmCLV1B (Yamamoto, Karakaya, and Knap 2000)
, homologs of AtCLV1. In this study, we isolated and characterized three other LRR-RLK family members, GmRLK1, GmRLK2, and GmRLK3, orthologs of AtRLK. A phylogenetic analysis of the deduced amino acid sequences of these soybean RLKs together with RLKs of several other plant species suggests that AtCLV1 orthologs may have developed later in the evolution of the plant RLK multigene families.
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Materials and Methods |
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Complementary DNA Isolation, Reverse TranscriptasePolymerase Chain Reaction, and Rapid Amplification of cDNA Ends
cDNA was synthesized from mRNA by Maloney murine leukemia virus reverse transcriptase (RT). Polymerase chain reaction (PCR) was performed using degenerate forward (RLKF) and reverse (RLKR) primers (table 1
) designed from the conserved kinase domains of AtRLK, AtCLV1, and Oryza sativa (GenBank accession numbers CAA16688, U96879, and X89226, respectively). PCR-amplified fragments were gel-purified, cloned into pCR2.1 (Invitrogen) or pGEM-T Easy (Promega, Madison, Wis.) vector, and sequenced with an ABI 373 automated sequencer using the ABI PRISM Dye Terminator Cycle Sequencing Ready Reaction kit (PE Biosystems, Foster City, Calif.). The regions of the open reading frame (ORF) were resequenced by direct-sequencing of RT-PCR products. Rapid amplification of cDNA ends (RACE) was performed using the SMART RACE amplification kit (Clontech, Palo Alto, Calif.). Gene-specific primers for 3' RACE were IF3', IIF3', and IIIF3' (table 1
), and gene-specific primers for 5' RACE were IR5', IIR5', and IIIR5' (table 1
).
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DNA Blot Analysis
Genomic DNA (10 µg) from genotypes BARC-11-11-ff and Clark 63 was digested with XbaI and EcoRV and loaded on a 0.8% agarose gel. The gel was depurinated, denatured, and blotted onto a Hybond N+ membrane (Amersham, Piscataway, N.J.). The membrane was prehybridized in a solution of 6 x SSC, 5 x Denhardt's reagent, 0.5% SDS, and 100 µg/ml salmon sperm DNA at 65°C for 2 h and hybridized with a probe derived from the 3' untranslated regions (UTRs) of GmRLK1 (IF-IR, 262 bp), GmRLK2 (IIF-IIR, 215 bp), or GmRLK3 (IIIF'-IIIR', 193 bp) (table 1
) at 65°C for 16 h. PCR conditions were as follows: denaturation at 95°C for 1 min; five cycles of 95°C for 30 s, 65°C for 30 s, and 72°C for 30 s; 25 cycles of 95°C for 30 s, 60°C for 30 s, and 72°C for 30 s; and extension at 72°C for 3 min. PCR products were gel-purified and resuspended in 50 µl of H2O. Two milliliters of the resuspended DNA was used for PCR labeling with 50 µCi 32P dCTP in a 20-µl reaction volume. PCR conditions were the same as previously stated. The membrane was washed in 2 x, twice in 1 x, and once in 0.1 x SSC containing 0.1% SDS at 65°C for 45 min and exposed to X-ray film at -70°C.
Screening of Soybean BAC Clones by DNA Fingerprinting and PCR
A soybean BAC library that covers nine genome equivalents (Tomkins et al. 1999
) was screened independently with GmRLK1, GmRLK2, and GmRLK3 probes. BAC clones in the microtiter plates were identified from the autoradiograph. BAC DNA was isolated using the Qiagen Plasmid Mini kit (Qiagen, Valencia, Calif.). For BAC DNA fingerprinting, DNA was digested with HindIII, fractionated on a 1% agarose gel, and analyzed using FPC V4.6.1 (Sanger Center, Cambridge, U.K.). Parameters for contig assignment were a tolerance value seven and cutoff scores of 10-410-12. The presence of GmRLK1, GmRLK2, and GmRLK3 in the BAC clones was examined by PCR using gene-specific primers. Gene-specific primers were GmRLK1 (IF and IR), GmRLK2 (IIF and IIR), and GmRLK3 (IIIF and IIIR) (table 1
) or GmCLV1A (1A3'5F and 1A3'6R) and GmCLV1B (1B3'7F and 1B3'8R) (Yamamoto, Karakaya, and Knap 2000)
. PCR conditions for primary screening were as follows: denaturation at 95°C for 1 min and 30 s; two cycles of 95°C for 30 s, 65°C for 30 s, and 72°C for 30 s; three cycles of 95°C for 30 s, 63°C for 30 s, and 72°C for 30 s; 25 cycles of 95°C for 30 s, 60°C for 30 s, and 72°C for 30 s; and extension at 72°C for 3 min. PCR conditions for secondary screening were as follows: denaturation at 95°C for 1 min and 30 s; 20 cycles of 95°C for 30 s, 65°C for 30 s, and 72°C for 30 s; and extension at 72°C for 3 min. PCR conditions for tertiary screening were as follows: denaturation at 95°C for 1 min and 30 s; two cycles of 95°C for 30 s, 62°C for 30 s, and 72°C for 30 s; 22 cycles of 95°C for 30 s, 60°C for 30 s, and 72°C for 30 s; and extension at 72°C for 3 min. PCR products were fractionated on a 1% agarose gel.
Relative Multiplex Quantitative RT-PCR
Expression of GmRLK1, GmRLK2, and GmRLK3 was examined by relative multiplex quantitative RT-PCR using the soybean proteasomal IOTA subunit gene as the internal control (Boissonneault and Lau 1993
; Spencer and Christensen 1999
; Yamamoto, Karakaya, and Knap 2000
). The soybean IOTA subunit gene is expressed constitutively and ubiquitously in soybean (Tang 1999
). The IOTA fragments (303 bp) were amplified using IO5' and IO3' primers (Tang 1999
), and GmRLK fragments were amplified using gene-specific GmRLK1 (IF-IR), GmRLK2 (IIF-IIR), GmRLK3 (IIIF'-IIIR'), and GmRLK4 (IVF-IVR) primers (table 1
). GmRLK4, a gene expressed only in root that was isolated at our laboratory (unpublished data), was included to show that there was no DNA contamination in the starting mRNA. GmRLK4 primers amplify 382-bp fragments. PCR conditions were as follows: denaturation at 95°C for 1 min; one cycle of 95°C for 30 s, 66°C for 30 s, and 72°C for 40 s; two cycles of 95°C for 30 s, 64°C for 30 s, and 72°C for 40 s; two cycles of 95°C for 30 s, 62°C for 30 s, and 72°C for 40 s; 20 cycles of 95°C for 30 s, 60°C for 30 s, and 72°C for 40 s; and extension at 72°C for 3 min. PCR products were fractionated on a 4% (w/v) Nusieve 3:1 agarose gel (FMC, Rockland, Maine), stained with ethidium bromide, and photographed. The relative intensities of the bands in each lane were quantitated by scanning the gel with the fluorescent image analyzer (Fuji Photo Film, Tokyo, Japan), and the areas of the peaks were compared with that of GmIOTA as the relative control.
Phylogenetic Analysis of Plant RLKs
Phylogenetic analysis of GmRLK1, GmRLK2, GmRLK3, GmCLV1A, GmCLV1B, AtRLK, and AtCLV1 (GenBank accession numbers AF244888, AF244889, AF244890, AAF59905, AAF59906, CAA16688, and AAB58929, respectively), together with other plant RLKs (A. thaliana AtHAESA, AtER, AtBR1, AtWak1, and AtRPK1, rice OsTMK and OsXa21, Brassica BoSRK3, maize ZmRLK2, tomato LePRK1 [GenBank accession numbers P47735, U47029, AF017056, AJ009696, U55875, Y07748, U72724, X79432, AF023165, and U58474, respectively], and rice OsLRK1 [Kim, Jeong, and An 2000]), was conducted with GeneBee (http://www.genebee.msu.ru/services/malign_full.html) using the Dayhoff amino acids distance matrix (Brodsky et al. 1993
). Phylogenetic trees were generated by cluster and topological algorithms using GeneBee-Net v.2.0 (http://www.genebee.msu.ru/services/phtree_reduced.html), and the branch lengths were adjusted by the Fitch-Margoliash method with contemporary tips, version 3.572c (http://sdmc.krdl.org.sg:8080/
lxzhang/phylip/).
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Results |
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Genomic Organization of the Soybean RLK Genes
DNA gel blot analysis was conducted to identify potential restriction fragment length polymorphisms (RFLPs) for GmRLK1, GmRLK2, and GmRLK3 using the gene-specific 3' UTR probes. No RFLPs were found between seven genotypes (two primitive genotypes, PI 209332 and PI 437654; five advanced cultivars, BARC-11-11-ff, Clark, Essex, Faribault, and Williams 82) with 10 restriction enzymes, implying that restriction sites are not rearranged within the genes or at the flanking regions of the GmRLK genes. The presence of one or two bands in each restriction digestion indicates that GmRLK1, GmRLK2, and GmRLK3 are transcribed from low-copy-number genes (restriction patterns of two genotypes digested with XbaI and EcoRV are shown in figure 3
). The GmRLK1 probe detects one major band (fig. 3
, lanes 1, 2, 7, and 8). The GmRLK2 probe detects two restriction bands (fig. 3
, lanes 3, 4, 9, and 10). The GmRLK3 probe (IIIF' and IIIR', 193 bp; table 1
) detects the lower-molecular-weight band of the GmRLK2 bands (fig. 3
, lanes 5, 6, 11, and 12). This result shows that the GmRLK2 and GmRLK3 genes, despite high sequence similarities in the ORFs (95%), could be distinguished by gene-specific primers which were designed from the divergent 3' UTRs of individual family members. Thus, the higher-molecular-weight band contains the GmRLK2 gene (fig. 3
, lanes 3, 4, 9, and 10), and the lower-molecular-weight band contains the GmRLK2 and GmRLK3 genes (fig. 3
, lanes 36 and 912).
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Expression Analyses of the GmRLK Genes
Expression analysis of GmRLK1, GmRLK2, and GmRLK3 was performed by relative multiplex quantitative RT-PCR using poly(A)+RNA as templates (Boissonneault and Lau 1993
; Spencer and Christensen 1999
; Yamamoto, Karakaya, and Knap 2000
). GmRLK4, an RLK with root-specific expression, was included in the experiment. GmRLK4 is a cDNA fragment (571 bp) that shares sequence similarity with common bean RLK PvRK20-1 (51% identity in 137 aa) (Lange et al. 1999
). PvRK201 is expressed in roots, and its expression is induced by pathogens and nodulin factors. Gene-specific GmRLK4 primers (table 1
) amplify a 382-bp-long fragment, which preferentially accumulates in soybean roots (fig 4
, lane 6). No transcript detection with GmRLK4 primers in leaves and shoot apices (fig. 4
, lanes 2 and 3) indicates no DNA contamination in the mRNA. Visible amplification of GmRLK1, GmRLK2, and GmRLK3 transcripts in roots, leaves, and vegetative-shoot and reproductive-floral apices implies that the GmRLK1, GmRLK2, and GmRLK3 genes are expressed in all organs in soybean (fig. 4
). The significant finding is that expression of GmRLK1 is most prominent in vegetative-shoot apices (fig. 4
, lanes 3 and 4). Expression of GmRLK1 in vegetative-shoot apices is 30%40% more extensive than that of leaves, reproductive-floral apices, and roots (fig. 4
, lanes 2, 5, and 6). Despite the high sequence similarities of GmRLK2 and GmRLK3 (96% identity; fig. 1
), there are small differences in the expression patterns of GmRLK2 and GmRLK3 (fig. 4
).
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Discussion |
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In genomic analysis using a nine-genome-coverage BAC library, GmRLK1, GmRLK2, and GmRLK3 were localized in five regions (contigs IV). The GmRLK regions could be easily distinguished based on DNA fingerprinting patterns. We do not know the genetic map positions of the five GmRLK regions at this time. We investigated two primitive and five advanced genotypes with 10 restriction enzymes and found no RFLPs for the GmRLK1, GmRLK2, and GmRLK3 genes. This low degree of molecular marker polymorphisms could be due to the limited genetic sources used in cultivar development in G. max species (Morgante et al. 1994
; Kisha et al. 1998
). The conventional RFLP method does not allow recognition of restriction fragments over 20 kb, and thus high-molecular-weight polymorphisms cannot be revealed. Our results show that genome analysis can be enhanced by BAC DNA fingerprinting, which detects segmental reorganization of restriction sites involving large fragments in the vicinities of paralogous genes.
We identified one cluster of paralogous genes, GmRLK2 and GmRLK3 in contig IV. This cluster could have evolved similarly to the RLK cluster (Lrk and Tak) in the grass family (Feuillet and Keller 1999
). Lrk and Tak have arisen from a common ancestral gene by duplication followed by structural chromosomal rearrangements. While searching the sequence similarities of GmRLKs in GenBank, we identified four A. thaliana BAC clones that contain two RLK genes in each clone. The four A. thaliana BAC clones are scattered on three chromosomes: two (GenBank accession numbers AL132955 and AL133292) on chromosome III, one (GenBank accession number AL022224) on chromosome IV, and one (GenBank accession number AL021684) on chromosome V. The BAC clone containing AtRLK (GenBank accession number CAA16688), the ortholog of GmRLK1, GmRLK2, and GmRLK3, is mapped at 131.1 cM on chromosome V, close to marker mi335 (http://genome-www3.stanford.edu). Grant, Cregan, and Shoemaker (2000)
identified substantial synteny between A. thaliana and soybean chromosomes using conceptual translations of DNA sequences; the sequences of soybean RFLPs on linkage group soy2A had strong homologies to three A. thaliana BAC sequences from chromosomes I, IV, and V. However, GmRLK1, GmRLK2, and GmRLK3 did not localize at these syntenic regions. Previously, we mapped one of the soybean RLKs (GmCLV1); an EcoRI RFLP of GmCLV1 was assigned on linkage group H of the soybean molecular map (Yamamoto, Karakaya, and Knap 2000)
. In A. thaliana, AtCLV1 is mapped at 117.8 cM, close to marker m532 (1.5 kb from orf1-1) on chromosome I (Williams, Clark, and Meyerowitz 1999
), suggesting that homeologous regions might also be present in linkage group H in soybean and chromosome I in A. thaliana.
Phylogenetic analysis indicates that a common ancestral GmRLK gene may have duplicated to give rise to GmRLK1, GmRLK2, and GmRLK3; GmRLK1 may have developed earlier than GmRLK2 and GmRLK3. The BAC contig analysis suggests that gene duplication was accompanied by genome rearrangement at the submegabase level. Evolutionary analysis of soybean RLK genes together with several other plant species indicates that CLV1 and RLK genes may have been generated by gene duplication from a common ancestral gene before the divergence of soybean, A. thaliana, and rice. AtCLV1- and AtRLK-related genes may have evolved later than the other plant RLKs involved in developmental, biotic, and abiotic responses. AtCLV1 is associated with shoot and floral meristem development (Clark, Williams, and Meyerowitz 1997
). Thus, AtCLV1-related genes including GmRLKs and GmCLV1s might have acquired in the course of evolution more specialized functions in plant ontogeny. The presence of isotype genes in a multigene family may allow species plasticity and confer selective advantage to an organism.
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Acknowledgements |
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Footnotes |
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1 Keywords: soybean
receptor-like protein kinase
gene duplication
paralogous
CLAVATA1
Arabidopsis thaliana.
2 Address for correspondence and reprints: Halina T. Knap, Clemson
University, 272 Poole, 50 New Cherry Road, Clemson, South Carolina
29634-0359. hskrpsk{at}clemson.edu
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References |
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