Large-scale comparison of intron positions among animal, plant, and fungal genes

Abstract

We purge large databases of animal, plant, and fungal introncontaining genes to a 20% similarity level and then identify the most similar animal-plant, animal-fungal, and plant-fungal protein pairs. We identify the introns in each BLAST 2.0 alignment and score matched intron positions and slid (near-matched, within six nucleotides) intron positions automatically. Overall we find that 10% of the animal introns match plant positions, and a further 7% are ''slides.'' Fifteen percent of fungal introns match animal positions, and 13% match plant positions. Furthermore, the number of alignments with high numbers of matches deviates greatly from the Poisson expectation. The 30 animal-plant alignments with the highest matches (for which 44% of animal introns match plant positions) when aligned with fungal genes are also highly enriched for triple matches: 39% of the fungal introns match both animal and plant positions. This is strong evidence for ancestral introns predating the animal-plant-fungal divergence, and in complete opposition to any expectations based on random insertion. In examining the slid introns, we show that at least half are caused by imperfections in the alignments, and are most likely to be actual matches at common positions. Thus, our final estimates are that Ϸ14% of animal introns match plant positions, and that Ϸ17-18% of fungal introns match animal or plant positions, all of these being likely to be ancestral in the eukaryotes.exon ͉ phase distribution ͉ evolution ͉ eukaryote ͉ prokaryote I ntrons are prevalent in the complex eukaryotes but rare in the simple ones. Are these introns ancestral in all of the eukaryotes or do they arise as the organisms become more complex? Introns can be acquired by or eliminated from a gene during evolution, but what is the balance?An introns-late view argues that introns arise as ''selfish'' elements that play no constructive role in evolution. On this picture, introns appear relatively late in the evolution of eukaryotes (1-3) and spread as mobile elements that invade genes by insertion into short Ϸ4-to 5-nt-long ''proto-splice sites'' (4) (although the notion of proto-splice sites has been challenged; refs. 5 and 6).An introns-early theory suggests that introns made an essential contribution to the evolution of genes via ''exon shuffling,'' which created genes from exon ''pieces'' by recombination within the introns (7-12). In this view, introns existed before any eukaryote-prokaryote divergence, and since that time, the prokaryotic lineage completely lost its introns, whereas they were retained in the eukaryotes.The sequences within the introns change during evolution, far more rapidly than those of the exons. The only conserved elements are the short sequences at the 5Ј and 3Ј termini, which are very similar for all introns. The rest of the intron sequence appears neutral to selection, and the length of the intron sequence can change by orders of magnitude. However, the position of an intron in a gene's coding sequence is well conserved. If one compares the e...

A Single-Electron Reducing Quinone Oxidoreductase Is Necessary to Induce Haustorium Development in the Root Parasitic Plant Triphysaria

“…These best hit genes had the same intron-exon structure as QR1, with some variation in intron size, though positioned at nearly identical locations 1.8 6 0.4 1.6 6 0.3 1.7 6 0.2 1.6 6 0.1 0.83 n = 352 n = 378 n = 339 n = 323 Root length (cm) c 3.5 6 1.8 3.4 6 1.7 3.2 6 1.6 3 6 1.5 0.18 n = 49 n = 50 n = 49 n = 51 Lateral roots per YFP root c 0.1 6 0.3 0.1 6 0.4 0.1 6 0.3 0.1 6 0.4 0.82 n = 49 n = 50 n = 49 n = 51 Root growth no DMBQ (mm/24 h) c 2.6 6 0.4 2.7 6 0.5 2.6 6 0.4 2.6 6 0.3 0.72 n = 40 n = 40 n = 40 n = 40 Root growth with DMBQ (mm/24 h) c 2.7 6 0.5 2.6 6 0.4 2.7 6 0.5 2.6 6 0. within the homologs. The conservation of intron position, but not size, is typical of homologous genes across taxonomic boundaries (Fedorov et al, 2002). To examine expression of the Arabidopsis homolog of QR1, we treated Arabidopsis roots with DMBQ or water and then probed the RNA gel blot with the T. versicolor QR1 cDNA.…”

Resolution of a deep animal divergence by the pattern of intron conservation

“…Introns have a very slow rate of insertion and loss with intron turnover estimates ranging from around 10 Ϫ9 per year for flies (20,21) and worms (21,22) to 10 Ϫ11 per year for mammals (23) and with a large fraction of introns persisting for very long periods (18,24,25), presumably allowing them to retain phylogenetic signal long after nucleic acid and many protein sequences have saturated. In addition, intron loss is presumably virtually irreversible (once lost, an intron is quite unlikely to be subsequently gained at the exact site), thus evading the problems of back mutation endemic to sequence-based methods.…”

A new Drosophila spliceosomal intron position is common in plants

“…Once released from the constraints of self-splicing, spliceosomal introns may have been instrumental in creating a profusion of new eukaryotic genes by exon shuffling (6). IE supporters now admit that intron insertion is an important process in the evolution of eukaryotic genes, although they persist in asserting that deletion of ancestral introns is the main factor responsible for present-day phylogenetic distributions of introns (7,8). On their part, IL theorists accept regularities in intron phases and intron genomic distributions, but they explain them, as well as present-day intron phylogenetic distributions, using parsimonious population-genetic arguments that do not demand special evolutionary scenarios (refs.…”

“…In addition, IL advocates now acknowledge intron sliding as a real evolutionary phenomenon even though it is uncommon (10, 11) and, in most cases, implicates just one nucleotide base-pair slide (12-14). IL supporters now tend to view spliceosomal introns as genomic parasites that have been co-opted into many essential functions such that few, if any, eukaryotes could survive without them (2).In this emerging scenario, IE upholders claim that the last common ancestor to all eukaryotes had a genome densely populated with introns, a significant fraction (up to 40%) of which are still conserved in present-day, typically intron-rich multicellular eukaryotes (7,8). IE theorists base their claim on the observed numbers of intron positions in highly conserved genes, which are identical across animals, fungi, and plants, by assuming that the introns at those sites are all orthologous (and therefore ancestral; ref.…”

“…In this emerging scenario, IE upholders claim that the last common ancestor to all eukaryotes had a genome densely populated with introns, a significant fraction (up to 40%) of which are still conserved in present-day, typically intron-rich multicellular eukaryotes (7,8). IE theorists base their claim on the observed numbers of intron positions in highly conserved genes, which are identical across animals, fungi, and plants, by assuming that the introns at those sites are all orthologous (and therefore ancestral; ref.…”