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• W2798589457 abstract "Mark Marchionni and Walter Gilbert Department of Cellular and Developmental Biology Harvard University Biological Laboratories 16 Divinity Avenue Cambridge, Massachusetts 02138 Summary We have cloned and characterized a cDNA and genomic DNA for the triosephosphate isomerase ex- pressed in maize roots. The gene is interrupted by eight introns. If we compare this gene with that for the protein in chicken, which has six intmns, we see that five of the introns are at identical places, one has shifted by three codons, and two are totally new. This great matching leads us to conclude that the introns were in place before the plant-animal divergence, and that the parental gene had at least eight introns, two of which were lost in the line that leads to animals. Introduction Genes of higher eukaryotes are discontinuous: regions of noncoding DNA (introns) separate the coding sequence into discrete segments (exons). Gilbert (1978) proposed that introns are vestigial DNA sequence, remnants of a recombination process that accelerated molecular evolu- tion by assembling new linkage groups from the exons, creating novel gene products. That hypothesis of exon shuffling predicts that positions of introns should portray the evolutionary history of a gene; the exons themselves would encode distinct functional elements (Gilbert, 1978, 1979), stably folding peptides (Blake, 1978) or compact modules (Go, 1981, 1983). Evidence in support of these ideas derives from molecular studies on genes and pro- teins as diverse as immunoglobulins (reviewed by Tone- gawa, 1983, and Honjo, 1983) collagen (Yamada et al., 1980) serum albumin-a-fetoprotein (Sargent et al., 1981; Eiferman et al., 1981) ovomucoid (Stein et al., 1980), glo- bins (Go, 1981) intermediate filaments (Marchuk et al., 1984; Balcarek and Cowan, 1985), lysozyme (Jung et al., 1980) and crystallins (Moormann et al,, 1983). Moreover, recent studies (Siidhof et al., 1985a, 1985b) comparing the gene structure of low density lipoprotein receptor with those of epidermal growth factor and blood coagulation factors 9 and 10 provide a dramatic example of exon shuf- fling in recent evolutionary history. Although there are a few exceptions (Kaine et al., 1983; Chu et al., 1984; Nellen et al., 1981; Miller, 1984), the con- spicuous absence of introns in bacteria and yeast poses questions as to their age and origins. Were introns present as the first genes formed? Or have they more recently taken up residence in genomic DNA by invading continu- ous gene sequences? Doolittle (1978) suggested that the genomes of primitive cells contained introns but that rap- idly dividing organisms lost them by streamlining in re- sponse to the selection pressure of rapid reproduction. The highly conserved, ubiquitous glycolytic enzymes most likely evolved completely before the archaebacteria-pro- karyotic-eukaryotic division and thus represent extremely ancient genes. In vertebrates, introns punctuate nonran- domly the sequences encoding chicken pyruvate kinase (Lonberg and Gilbert, 1985), chicken glyceraldehyde phosphate dehydrogenase (Stone et al., 1985) chicken triosephosphate isomerase (Straus and Gilbert, 1985b), as well human phosphoglycerate kinase (Michelson et al., 1985), suggesting that the introns were not inserted into preexisting genes. To push our view of one these glycolytic enzyme genes back in time, we have character- ized a gene encoding triosephosphate isomerase (EC 5.3.1.1, TIM) in maize in order to compare its structure to the chicken gene. A remarkable conservation of intron po- sitions between these distant relatives indicates that the introns were in place before the plant-animal divergence, more than one billion years ago. Results Cloning and Structure of Maize TIM cDNA During glycolysis, triosephosphate isomerase (TIM) cata- lyzes the interconversion of dihydroxyacetone phosphate and glyceraldehyde 3-phosphate. In addition to a cytosolic TIM, plant cells active in photosynthesis express a plastid enzyme encoded in the nucleus (Pichersky and Gottlieb, 1982). That isozyme functions in the dark reactions that fix carbon dioxide into sugars. As is true for other pho- tosynthetic proteins, the chloroplast-specific TIM is light inducible (e.g., Nelson et al., 1984; Berry-Lowe et al., 1982). Hence, mRNA from roots grown in the dark should be enriched in the cytosolic form, which ought to cog- nate to the chicken enzyme. Because TIM is less than 60% diverged across the most distant species (Pichersky et al., 1984; Straus and Gilbert, 1985b), cross-hybridiza- tion from chicken to maize root cDNA was a plausible ap- proach to cloning the maize gene. Using a chicken probe (Straus et al., 1985a), we screened 80,000 phage cDNA recombinants that repre- sented mRNA extracted from maize root seedlings grown in the dark for 7 days. We chose hybridization and wash- ing conditions of medium stringency (see Experimental Procedures) and detected 18 potential TIM clones. After partially mapping all of the inserts, we focused on two large (>800 bp) overlapping clones, subcloned each of these into the EcoRl site of pUC8 (Vieira and Messing, 1982), and sequenced (Maxam Gilbert, 1980) both strands of the DNA. Figure 1 displays a partial restriction map and the com- plete nucleotide sequence of a full-length maize root TIM cDNA clone, designated pMRT1. Within the 123 bases of 5’ untranslated sequence is a 37 base pyrimidine tract, which is flanked by two overlapping, imperfect, direct repeats of 20 bases each. A similar alternating pyrimidine" @default.
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• W2798589457 date "1986-01-01" @default.
• W2798589457 modified "2023-09-27" @default.
• W2798589457 title "The Triosephosphate lsomerase Gene from Maize: lntrons Antedate the Plant-Animal Divergence" @default.
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