Trans-splicing Group II Introns in Plant Mitochondria: the Complete Set of Cis-arranged Homologs in Ferns, Fern Allies, and a Hornwort

Overview

Journal RNA

Specialty Molecular Biology

Date 1998 Dec 16

PMID 9848656

Citations 42

Authors

O Malek

V Knoop

Affiliations

Soon will be listed here.

Abstract

The fragmentation of group II introns without concomitant loss of splicing competence is illustrated by extraordinary gene arrangements in plant mitochondrial genomes. The mitochondrial genes nad1, nad2, and nad5, all encoding subunits of the NADH dehydrogenase, require trans-splicing for functional assembly of their mRNAs in flowering plants. Tracing the origins of trans-splicing group II introns shows that they have evolved from formerly cis-arranged homologs whose descendants can still be identified in lineages of early branching land plants. In this contribution we present the full set of ancestor introns for all five conserved mitochondrial trans-splicing positions. These introns are strikingly small in the quillwort Isoetes lacustris, the continuous nad2 gene intron in this species representing the smallest (389 nt) land plant group II intron yet identified. cDNA analysis shows correct splicing of the introns in vivo and also identifies frequent RNA editing events in the flanking nad gene exons. Other representatives of the ancestral cis-arranged introns are identified in the fern Osmunda regalis, the horsetail Equisetum telmateia, and the hornwort Anthoceros crispulus. Only the now identified intron in Osmunda carries significant traces of a former maturase reading frame. The identification of a continuous homolog in Anthoceros demonstrates that intron invasion into the affected genes in some cases predated the split of vascular and nonvascular plants more than 400 million years ago. As an alternative to disruption after size increase, the respective introns can get secondarily lost in certain lineages.

Citing Articles

PPR596 Is Required for Intron Splicing and Complex I Biogenesis in Arabidopsis.

Sayyed A, Chen B, Wang Y, Cao S, Tan B Int J Mol Sci. 2024; 25(6).

PMID: 38542518 PMC: 10971677. DOI: 10.3390/ijms25063542.

Mitochondrial Genome Sequence of (Lamiales: Lamiaceae) Suggests Diverse Genome Structures in Cogeneric Species and Finds the Stop Gain of Genes through RNA Editing Events.

Yang H, Chen H, Ni Y, Li J, Cai Y, Wang J Int J Mol Sci. 2023; 24(6).

PMID: 36982448 PMC: 10048906. DOI: 10.3390/ijms24065372.

Rickettsial DNA and a trans-splicing rRNA group I intron in the unorthodox mitogenome of the fern Haplopteris ensiformis.

Zumkeller S, Polsakiewicz M, Knoop V Commun Biol. 2023; 6(1):296.

PMID: 36941328 PMC: 10027690. DOI: 10.1038/s42003-023-04659-8.

Categorizing 161 plant (streptophyte) mitochondrial group II introns into 29 families of related paralogues finds only limited links between intron mobility and intron-borne maturases.

Zumkeller S, Knoop V BMC Ecol Evol. 2023; 23(1):5.

PMID: 36915058 PMC: 10012718. DOI: 10.1186/s12862-023-02108-y.

Development of DNA methylation-based epigenetic age predictors in loblolly pine (Pinus taeda).

Gardner S, Bertucci E, Sutton R, Horcher A, Aubrey D, Parrott B Mol Ecol Resour. 2022; 23(1):131-144.

PMID: 35957540 PMC: 10087248. DOI: 10.1111/1755-0998.13698.

References

Thompson M, Zhang L, Hong L, Hallick R . Extensive structural conservation exists among several homologs of two Euglena chloroplast group II introns. Mol Gen Genet. 1998; 257(1):45-54. DOI: 10.1007/s004380050622. View

Grivell L . Transposition: mobile introns get into line. Curr Biol. 1996; 6(1):48-51. DOI: 10.1016/s0960-9822(02)00420-7. View

Michel F, Ferat J . Structure and activities of group II introns. Annu Rev Biochem. 1995; 64:435-61. DOI: 10.1146/annurev.bi.64.070195.002251. View

Conklin P, Wilson R, Hanson M . Multiple trans-splicing events are required to produce a mature nad1 transcript in a plant mitochondrion. Genes Dev. 1991; 5(8):1407-15. DOI: 10.1101/gad.5.8.1407. View

Malek O, Brennicke A, Knoop V . Evolution of trans-splicing plant mitochondrial introns in pre-Permian times. Proc Natl Acad Sci U S A. 1997; 94(2):553-8. PMC: 19551. DOI: 10.1073/pnas.94.2.553. View

Knoop V, Schuster W, Wissinger B, Brennicke A . Trans splicing integrates an exon of 22 nucleotides into the nad5 mRNA in higher plant mitochondria. EMBO J. 1991; 10(11):3483-93. PMC: 453077. DOI: 10.1002/j.1460-2075.1991.tb04912.x. View

Unseld M, Marienfeld J, Brandt P, Brennicke A . The mitochondrial genome of Arabidopsis thaliana contains 57 genes in 366,924 nucleotides. Nat Genet. 1997; 15(1):57-61. DOI: 10.1038/ng0197-57. View

Kuck U, Choquet Y, Schneider M, Dron M, Bennoun P . Structural and transcription analysis of two homologous genes for the P700 chlorophyll a-apoproteins in Chlamydomonas reinhardii: evidence for in vivo trans-splicing. EMBO J. 1987; 6(8):2185-95. PMC: 553617. DOI: 10.1002/j.1460-2075.1987.tb02489.x. View

Malek O, Lattig K, Hiesel R, Brennicke A, Knoop V . RNA editing in bryophytes and a molecular phylogeny of land plants. EMBO J. 1996; 15(6):1403-11. PMC: 450045. View

10.

Goldschmidt-Clermont M, Choquet Y, Girard-Bascou J, Michel F, Schirmer-Rahire M, Rochaix J . A small chloroplast RNA may be required for trans-splicing in Chlamydomonas reinhardtii. Cell. 1991; 65(1):135-43. DOI: 10.1016/0092-8674(91)90415-u. View

11.

Weiner A . mRNA splicing and autocatalytic introns: distant cousins or the products of chemical determinism?. Cell. 1993; 72(2):161-4. DOI: 10.1016/0092-8674(93)90654-9. View

12.

Jacquier A . Self-splicing group II and nuclear pre-mRNA introns: how similar are they?. Trends Biochem Sci. 1990; 15(9):351-4. DOI: 10.1016/0968-0004(90)90075-m. View

13.

Handa H, Pinyarat W . The rapeseed mitochondrial gene for subunit 2 of the NADH dehydrogenase complex: a trans-spliced structure is conserved in one of the smallest plant mitochondrial genomes. Curr Genet. 1997; 31(4):336-42. DOI: 10.1007/s002940050213. View

14.

Chapdelaine Y, Bonen L . The wheat mitochondrial gene for subunit I of the NADH dehydrogenase complex: a trans-splicing model for this gene-in-pieces. Cell. 1991; 65(3):465-72. DOI: 10.1016/0092-8674(91)90464-a. View

15.

Hetzer M, Wurzer G, Schweyen R, Mueller M . Trans-activation of group II intron splicing by nuclear U5 snRNA. Nature. 1997; 386(6623):417-20. DOI: 10.1038/386417a0. View

16.

Wissinger B, Schuster W, Brennicke A . Trans splicing in Oenothera mitochondria: nad1 mRNAs are edited in exon and trans-splicing group II intron sequences. Cell. 1991; 65(3):473-82. DOI: 10.1016/0092-8674(91)90465-b. View

17.

Doetsch N, Thompson M, Hallick R . A maturase-encoding group III twintron is conserved in deeply rooted euglenoid species: are group III introns the chicken or the egg?. Mol Biol Evol. 1998; 15(1):76-86. DOI: 10.1093/oxfordjournals.molbev.a025850. View

18.

Knoop V, Altwasser M, Brennicke A . A tripartite group II intron in mitochondria of an angiosperm plant. Mol Gen Genet. 1997; 255(3):269-76. DOI: 10.1007/s004380050497. View

19.

Pereira de Souza A, Jubier M, Delcher E, Lancelin D, Lejeune B . A trans-splicing model for the expression of the tripartite nad5 gene in wheat and maize mitochondria. Plant Cell. 1991; 3(12):1363-78. PMC: 160098. DOI: 10.1105/tpc.3.12.1363. View

20.

Devereux J, Haeberli P, SMITHIES O . A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984; 12(1 Pt 1):387-95. PMC: 321012. DOI: 10.1093/nar/12.1part1.387. View