Sequence and comparative analysis of the maize NB mitochondrial genome.
Journal: 2005/January - Plant Physiology
ISSN: 0032-0889
Abstract:
The NB mitochondrial genome found in most fertile varieties of commercial maize (Zea mays subsp. mays) was sequenced. The 569,630-bp genome maps as a circle containing 58 identified genes encoding 33 known proteins, 3 ribosomal RNAs, and 21 tRNAs that recognize 14 amino acids. Among the 22 group II introns identified, 7 are trans-spliced. There are 121 open reading frames (ORFs) of at least 300 bp, only 3 of which exist in the mitochondrial genome of rice (Oryza sativa). In total, the identified mitochondrial genes, pseudogenes, ORFs, and cis-spliced introns extend over 127,555 bp (22.39%) of the genome. Integrated plastid DNA accounts for an additional 25,281 bp (4.44%) of the mitochondrial DNA, and phylogenetic analyses raise the possibility that copy correction with DNA from the plastid is an ongoing process. Although the genome contains six pairs of large repeats that cover 17.35% of the genome, small repeats (20-500 bp) account for only 5.59%, and transposable element sequences are extremely rare. MultiPip alignments show that maize mitochondrial DNA has little sequence similarity with other plant mitochondrial genomes, including that of rice, outside of the known functional genes. After eliminating genes, introns, ORFs, and plastid-derived DNA, nearly three-fourths of the maize NB mitochondrial genome is still of unknown origin and function.
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Plant Physiol 136(3): 3486-3503

Sequence and Comparative Analysis of the Maize NB Mitochondrial Genome<sup><a href="#fn1" rid="fn1" class=" fn">1</a>,</sup><sup><a href="#fn4" rid="fn4" class=" fn">[w]</a></sup>

+4 authors
Genome Sequencing Center, Washington University School of Medicine, St. Louis, Missouri 63108 (S.W.C., P.M., H.S., R.K.W.); University of Utah, Eccles Institute of Genetics, Salt Lake City, Utah 84112 (C.M.-R.F., M.G.); Division of Biological Sciences, University of Missouri, Columbia, Missouri 65211 (J.O.A., M.T., S.K., C.T., L.M., K.J.N.); and Donald Danforth Plant Science Center, St. Louis, Missouri 63132 (B.B.)
Corresponding author; e-mail ude.ltsuw.nostaw@notfilcs; fax 314–286–1810.
Present address: Magpie Systems, 4085 South 300 West, Salt Lake City, UT 84107.
Present address: Genome Science and Technology Program, University of Tennessee, Knoxville, TN 37996.
Received 2004 Apr 16; Revised 2004 Aug 25; Accepted 2004 Aug 25.

Abstract

The NB mitochondrial genome found in most fertile varieties of commercial maize (Zea mays subsp. mays) was sequenced. The 569,630-bp genome maps as a circle containing 58 identified genes encoding 33 known proteins, 3 ribosomal RNAs, and 21 tRNAs that recognize 14 amino acids. Among the 22 group II introns identified, 7 are trans-spliced. There are 121 open reading frames (ORFs) of at least 300 bp, only 3 of which exist in the mitochondrial genome of rice (Oryza sativa). In total, the identified mitochondrial genes, pseudogenes, ORFs, and cis-spliced introns extend over 127,555 bp (22.39%) of the genome. Integrated plastid DNA accounts for an additional 25,281 bp (4.44%) of the mitochondrial DNA, and phylogenetic analyses raise the possibility that copy correction with DNA from the plastid is an ongoing process. Although the genome contains six pairs of large repeats that cover 17.35% of the genome, small repeats (20–500 bp) account for only 5.59%, and transposable element sequences are extremely rare. MultiPip alignments show that maize mitochondrial DNA has little sequence similarity with other plant mitochondrial genomes, including that of rice, outside of the known functional genes. After eliminating genes, introns, ORFs, and plastid-derived DNA, nearly three-fourths of the maize NB mitochondrial genome is still of unknown origin and function.

Abstract

Mitochondrial genomes have been sequenced from a large number of protists, algae, fungi, and animals, but from few plants (for review, see Burger et al., 2003). To date, complete mitochondrial DNA (mtDNA) sequences from only five plants have been published: one nonvascular plant (Marchantia polymorpha; Oda et al., 1992), three eudicots (Arabidopsis [Arabidopsis thaliana]: Unseld et al., 1997; sugar beet [Beta vulgaris]: Kubo et al., 2000; rapeseed [Brassica napus]: Handa, 2003), and one monocot (rice [Oryza sativa]; Notsu et al., 2002). Plant mitochondria have a number of distinctive features, including considerable variation in genome size and organization, which can occur even within a single species (Fauron et al., 1995).

Although angiosperm mitochondrial genomes are at least 10 times larger than those of mammals, the total number of known genes they encode is fewer than twice as many as their mammalian counterparts. The mtDNAs of both plants and animals include genes for ribosomal RNAs, tRNAs, and several subunits of the oxidative phosphorylation complexes. The greatest difference is that some of the ribosomal proteins and some of the proteins involved in the biogenesis of cytochrome c are coded for by mtDNA in plants, whereas they are coded for by nuclear DNA in animals. In several angiosperm genera, two subunits of the succinate dehydrogenase complex are also coded for by mtDNA (Adams et al., 2001). Unlike their animal counterparts, a few of the plant mitochondrial tRNAs are encoded in the nucleus and imported into the mitochondrion (for review, see Maréchal-Drouard et al., 1993). Furthermore, some of the transcribed and functional mitochondrial tRNAs are originally of plastid origin, present on fragments of chloroplast DNA (ctDNA) that have become incorporated into the mtDNA. This movement of DNA between cellular compartments is responsible for some of the variation in the known gene sets of different plants and appears to be an ongoing evolutionary process in plants (for review, see Palmer et al., 2000). An additional curiosity is that, although plant mitochondrial genes are translated according to the universal code, transcripts of many genes require editing in order for that to occur (for review, see Brennicke et al., 1999).

One inference from the small number of sequenced plant mitochondrial genomes is that their sizes vary independently of the number of functional genes. The mitochondrial genome of the liverwort, M. polymorpha, was reported to be 184 kb and to encode 66 identified genes, including ribosomal and tRNAs (Oda et al., 1992). The 367-kb Arabidopsis mitochondrial genome was reported to include only 59 identified genes (Unseld et al., 1997). Although 84 unidentified open reading frames (ORFs) larger than 100 codons were also reported, it is unknown if any of them are actually expressed (Marienfeld et al., 1999). The recently sequenced mitochondrial genome of rapeseed, a member of the same family as Arabidopsis, contains a nearly identical set of identified genes, despite being only 222 kb in length (Handa, 2003). Indeed, the only difference in protein-gene content between the Arabidopsis and rapeseed mitochondrial genomes is that rps14 is intact in rapeseed, whereas it is a pseudogene in Arabidopsis. The 369-kb sugar beet mitochondrial genome is similar in size to that of Arabidopsis and contains a similar set of genes (29 protein coding, 5 rRNA, and 25 tRNA; Kubo et al., 2000). Although the mitochondrial genome of rice is quite a bit larger at 491 kb, the number of functional genes is comparable (Notsu et al., 2002). The major variation among all plant mitochondrial genomes characterized so far is in the ribosomal protein and tRNA gene content.

Comparative analyses of mitochondrial genes have shown that, with rare exceptions (Palmer et al., 2000), the sequences of protein-coding genes are highly conserved. Indeed, the rates of nucleotide substitution in plant mitochondrial protein-coding genes are usually lower than those of chloroplast genes or of plant or animal nuclear genes (for review, see Palmer, 1990). However, comparisons among plant mitochondrial genomes show that the sequences that occur between genes can be highly variable. Although these intergenic regions can include retrotransposons of nuclear origin and integrated chloroplast sequences, approximately 50% of each of the previously sequenced angiosperm mtDNAs could not be found in the extant databases (Unseld et al., 1997; Marienfeld et al., 1999; Kubo et al., 2000; Handa, 2003). Furthermore, there are no obvious similarities among the mtDNA sequences of the eudicots (Arabidopsis, rapeseed, and sugar beet) in these “unknown” regions. Within cucurbits, where mitochondrial genome size variation is extreme, an expansion of short, dispersed repeats (SDRs) has been proposed to account for some of the size increase (Lilly and Havey, 2001).

It is not clear why plant mitochondrial genomes rearrange so readily, or how their genomes expand and contract over such short evolutionary times. Complete mitochondrial sequence data are needed for many more plants, including closely related taxa, to address the question of how rapid changes in their intergenic regions occur. Relationships among grasses have been extensively studied (e.g. Freeling, 2001), and the rice mitochondrial genome sequence has been published (Notsu et al., 2002). We now report the complete sequence and comparative analysis of a second monocot mitochondrial genome, the maize (Zea mays subsp. mays) NB cytotype, which is present in most commercial hybrid maize lines.

Maize plastid sequences found in maize NB mitochondrial DNA. Sequences present in two locations in the mtDNA are parts of large repeats. IR indicates plastid inverted repeat sequence; coordinates are given only for the first IR. Brackets indicate truncation at the 5′ or 3′ end of genes. *, Part of 4.1-kb chimeric region in mtDNA (see text). **, Plastid sequences are identical, so the exact progenitor is uncertain.

The numbers of repeats and the numbers of bases in each size class of repeats, in roughly log-incremental size classes. All copies of repeats are included. Percents of genomes are calculated from total genome sizes. Sequence-identity criterion is 90%.

Total nucleotides within the maize and rice genomes that are parts of SDRs (20–499 bp). Nucleotides that are parts of overlapping repeats are counted only once; thus the maize 90% number is slightly less than the sum of the maize components in Table III (31,916). Percent is percentage of total genome.

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Acknowledgments

We thank John Spieth, Brandi Chiapelli, Warren Gish, William Nash, Jill Cifrese, and Leah Westgate for their contributions to this project. We thank Laurence Maréchal-Drouard, Jeffrey Palmer, David Stern, and Pankaj Jaiswal for helpful comments on the data and Makedonka Mitreva for help with final formatting and submission. We are grateful to our educational partners at Truman State University, Diane Janick-Buckner, Brent Buckner, and their students, particularly Anup Parikh, for input to the project.

Acknowledgments

Notes

This work was supported by the National Science Foundation Plant Genome Research Program (grant no. DBI–0110168).

The online version of this article contains Web-only data.

www.plantphysiol.org/cgi/doi/10.1104/pp.104.044602.

Notes
www.plantphysiol.org/cgi/doi/10.1104/pp.104.044602.
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