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The Journal of Heredity 2002:93(3)
© 2002 The American Genetic Association 93:174-178

Inheritance of Organelle DNA Sequences in a Citrus–Poncirus Intergeneric Cross

C. D. Moreira, F. G. Gmitter, Jr., J. W. Grosser, S. Huang, V. M. Ortega, and C. D. Chase

From the University of Florida, Horticultural Sciences Department, Institute of Food and Agricultural Sciences, Gainesville, FL 32611-0690 (Moreira, Ortega, and Chase), and CREC, P.O. Box 1088, Lake Alfred, FL 33850 (Gmitter, Grosser, and Huang).

Address correspondence to C. D. Chase at the address above or e-mail: ctdc{at}mail.ifas.ufl.edu.


   Abstract
Top
 Abstract
Introduction
 Materials and Methods
 Results and Discussion
 References
 
Many land plants deviate from the maternal pattern of organelle inheritance. In this study, heterologous mitochondrial and chloroplast probes were used to investigate the inheritance of organelle genomes in the progeny of an intergeneric cross. The seed parent was LB 1–18 (a hybrid of Citrus reticulata Blanco cv. Clementine x C. paradisi Macf. cv. Duncan) and the pollen parent was the cross-compatible species Poncirus trifoliata (L.) Raf. All 26 progeny examined exhibited maternal inheritance of plastid petA and petD loci. However, 17 of the 26 progeny exhibited an apparent biparental inheritance of mitochondrial atpA, cob, coxII, and coxIII restriction fragment length polymorphisms (RFLPs) and maternal inheritance of mitochondrial rrn26 and coxI RFLPs. The remaining nine progeny inherited only maternal mitochondrial DNA (mtDNA) configurations. Investigations of plant mitochondrial genome inheritance are complicated by the multipartite structure of this genome, nuclear gene control over mitochondrial genome organization, and transfer of mitochondrial sequences to the nucleus. In this study, paternal mtDNA configurations were not detected in purified mtDNA of progeny plants, but were present in progeny DNA preparations enriched for nuclear genome sequences. MtDNA sequences in the nuclear genome therefore produced an inheritance pattern that mimics biparental inheritance of mtDNA.


   Introduction
Top
 Abstract
 Introduction
Materials and Methods
 Results and Discussion
 References
 
Many land plants deviate from the maternal pattern of plastid and mitochondrial genome inheritance, with some species demonstrating biparental or even paternal transmission of one or both genomes (reviewed by Harrison and Doyle 1990; Mogensen 1996; Reboud and Zeyl 1994). Studies of plant mitochondrial genome inheritance are further complicated by the complex, multipartite organization of this genome. Although the entire complexity of a plant mitochondrial genome can be physically mapped as a "master circle," recombination across direct repeats results in subgenomic molecules (reviewed by Backert et al. 1997; Fauron et al. 1995). Many plant (mitochondrial DNA [mtDNA]) configurations exist as low-abundance copies termed sublimons (Small et al. 1987). The relative abundance of a particular mtDNA configuration can vary in different plant lineages, such that a sublimon in one lineage is the predominant configuration in another lineage (Small et al. 1987, 1989). Furthermore, nuclear genes regulate mitochondrial genome organization and influence the relative abundance of the various mitochondrial subgenomes (Mackenzie and Chase 1990; Sakamoto et al. 1996; Small et al. 1989).

An additional complication in studies of organelle genome inheritance is the presence of organelle DNA sequences in the nuclear genome. Insertions of organelle DNA into the nuclear genome of plants and animals have occurred frequently over the course of evolution (reviewed by Blanchard and Lynch 2000; Blanchard and Schmidt 1995; Henze and Martin 2001; Martin and Herrmann 1998). In the land plants there are many examples of functional gene transfer from mitochondria to nucleus. These most likely occur via RNA intermediates with the subsequent gain of nuclear promoters and mitochondrial targeting signals (reviewed by Gray 2000; Palmer et al. 2000). In animals, such functional gene transfers were precluded once mitochondria evolved a unique genetic code (Gray 2000). However, nonfunctional mtDNA sequences are common in animal nuclear genomes (reviewed by Blanchard and Schmidt 1996; Henze and Martin 2001; Shay and Werbin 1992). A notable example of nonfunctional mtDNA in a plant nuclear genome is the complete mitochondrial genome copy on chromosome 2 of Arabidopsis thaliana (Lin et al. 1999; Stupar et al. 2001). This insertion is much larger than any of the previously reported organelle-nuclear transfers. High levels of sequence identity between the mitochondrial genome and nuclear copy suggest a very recent transfer event (Lin et al. 1999).

The present investigation of organelle DNA inheritance in a Citrus–Poncirus intergeneric cross revealed an unusual pattern of mtDNA transmission resulting from the presence of mtDNA in the nuclear genome.


   Materials and Methods
Top
 Abstract
 Introduction
 Materials and Methods
Results and Discussion
 References
 
The intergeneric sexual hybrid family analyzed in this work was developed at the Citrus Research and Education Center, University of Florida, Lake Alfred, FL. The seed parent was LB 1–18, a hybrid of Citrus reticulata Blanco cv. Clementine x C. paradisi Macf. Duncan grapefruit. Seeds produced by LB 1–18 are monoembryonic, containing sexually derived zygotic embryos. The sexually compatible pollen parent was a seed-derived tree of Poncirus trifoliata (L.) Raf. The paternal tree is no longer extant and its cultivar is unknown. Organelle DNA restriction patterns of two different P. trifoliata varieties (Gainesville and Rubidoux) were compared and no differences were observed when DNA from these two varieties was restricted with six different enzymes and hybridized with two plastid and two mitochondrial probes. In subsequent studies, DNA of the cultivar Rubidoux was used to identify P. trifoliata-unique organelle DNA configurations. We do not know if the paternal tree was identical to Rubidoux in all mtDNA configurations, but the maternal tree was available for analysis. Therefore progeny mtDNA configurations matching P. trifoliata cultivar Rubidoux and absent from the maternal tree could be identified as paternally derived. Seven-year-old progeny trees from the intergeneric cross were screened for the inheritance of mitochondria and chloroplast DNA polymorphisms (F1 hybrids 3, 4, 6, 7, 9, 10, 12–16, 18, 19, 21–24, 27, 28, 30, 33, 35, 36, 44, 48, and 55). Leaf material from each tree was collected at different times of the year, but always at about 50% leaf expansion.

F1 33 and F1 44 were open-pollinated, and the resulting progeny were examined for inheritance of mtDNA configurations. Nuclear embryony reviewed by Koltunow (1993) is common in citrus, so random amplified polymorphic DNA (RAPD) markers (developed as described by Gmitter et al. 1996) were used to verify the zygotic nature of the progeny plants. The primer that best demonstrated the zygotic nature of these progeny was H01 (5'GGTCGGAGAA3') purchased from Operon Technologies (Alameda, CA). All progeny carried either nonparental RAPD markers, indicating progeny resulting from outcrossing, or a subset of the seed parent's RAPD markers, indicating progeny resulting from either self-pollination or outcrossing.

Total cellular DNA was isolated from 1 g frozen leaf samples by the phenol-chloroform extraction method of Durham et al. (1992). MtDNA was recovered from 50 g of freshly collected leaves as described by Hsu and Mullin (1988). To prepare DNA enriched for nuclear genome sequences, nuclei were prepared by the Triton washing procedure of Jofuku and Goldberg (1998). DNA was extracted from Triton-washed nuclei by the procedure of Dellaporta et al. (1983). DNA was digested by restriction enzymes having six-base recognition sequences (EcoRI, HindIII, PstI, EcoRV, BamHI, SmaI, DraI, or XbaI) according to the manufacturer's instructions (Life Technologies Inc.). Restriction fragments were separated by electrophoresis through 0.8% agarose gels in TPE buffer (30 mM NaH2PO4, 36 mM Trizma base, and 1 mM Na2EDTA·2H2O) at 800 V-h.

DNA fragments were transferred to nylon supports and hybridized with radiolabeled mitochondrial and chloroplast probes. The blots were prehybridized for at least 1 h in 10x SSPE (1x 0.18 M NaCl, 0.01 M NaH2PO4, 0.001 M Na2EDTA), 50x Denhardts (1x 0.02% w/v bovine serum albumin, 0.02% w/v Ficoll, 0.02% w/v PVP 360), 10% w/v SDS, and 20 µg/ml herring sperm DNA. The source, amplification, recovery, and radiolabeling of plastid petA and petD; mitochondrial atpA, atp9, cob, and coxI; and nuclear lycopene cyclase (lyc) probes were described previously (Moreira et al. 2000; Wen and Chase 1999). Primers 5'GTAGATCCAAGTCCATGG and 5'GCATGATGGGCCCAAGTT (Malek et al. 1996) were used to amplify coxIII coding sequences from maize mtDNA. Primers 5'GCGGAACCATGGCAATTA and 5'GGCATGATTAGTTCCACT (Moon et al. 1985) were used to amplify coxII coding sequences from maize mtDNA, and universal primers (5'CAGGAAACAGCTATGACC and 5'GTAAAACGACGGCCAGT) were used to amplify rrn26 coding sequences from a Phaseolus vulgaris mitochondrial cDNA clone. Following denaturation, radiolabeled probes were added directly to the prehybridization solution and the blots were hybridized for a minimum of 16 h at 60°C. Following hybridization, the blots were washed in 2x SSPE, 0.1% SDS at room temperature for 10 min. Following a second identical wash, the blots were washed in 1x SSPE, 0.1% SDS at 60°C for 15 min and then in 0.1x SSPE, 0.1% SDS at 60°C for 10 min. Membranes were exposed to Kodak (X-Omat RP XRP-5) film for 7–14 days.


   Results and Discussion
Top
 Abstract
 Introduction
 Materials and Methods
 Results and Discussion
References
 
To identify DNA polymorphisms between LB 1–18 and P. trifoliata, total cellular DNA samples were digested and hybridized with two chloroplast probes (petA and petD) and seven mitochondrial probes (atpA, cob, coxI, coxII, coxIII, rrn26, and atp9). Most hybridization profiles revealed polymorphisms, and seven probes were selected for use in inheritance analysis.

Plastid DNA appeared to exhibit strict maternal inheritance in the intergeneric hybrids. The petA probe detected the maternal 13 kb BamHI fragment in all the 26 F1 progeny, and no P. trifoliata (10 kb) fragments were observed in any of the progeny. DNAs from 14 of the analyzed progeny are shown in Figure 1A. Furthermore, only maternal configurations were observed in the hybrids analyzed with the chloroplast petD clone (not shown). Although the lack of polymorphisms limited the number of loci that could be tested, the results indicated a maternal inheritance of the chloroplast genome.



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  		Figure 1.. Mitochondrial and plastid DNA configurations in the progeny of a Citrus x Poncirus cross. Autoradiographs of Southern blots containing total DNA from LB 1–18 (maternal parent), P. trifoliata cultivar Rubidoux, and 14 F1 hybrids are shown. DNA samples (5 µg/lane) were loaded as follows: 1, P. trifoliata; 2, LB 1–18; 3–16, F1 hybrids 3, 6, 7, 10, 15, 16, 19, 21, 27, 33, 35, 44, 48, and 55, respectively. Enzyme-probe combinations used in the hybridizations were: panel A, BamHI-petA; panel B, HindIII-atpA; panel C, HindIII-coxIII; panel D, BamHI-cob; panel E, EcoRI-coxII, panel F, PstI-coxI. PetA is a plastid gene probe; all others are mitochondrial gene probes.

 
All intergeneric hybrid progeny carried abundant maternal mtDNA configurations for all loci examined (Figure 1B–F). Hybridization of the atpA mtDNA probe to HindIII-digested DNAs of 26 progeny trees revealed an intense 3.4 kb maternal fragment in all 26. However, 17 progeny (progeny 6, 7, 9, 10, 12–16, 18, 23, 27, 28, 30, 33, 36, and 44) also carried a faint 4.3 kb fragment characteristic of P. trifoliata. (Eight progeny DNAs of this type are included in Figure 1B.) The coxIII probe identified a 4.5 kb maternal fragment in HindIII-digested DNA from all progeny, and those progeny carrying P. trifoliata atpA configurations also carried a faint 6 kb P. trifoliata coxIII fragment (Figure 1C). All progeny carried a 10.5 kb maternal cob gene configuration, and those progeny with P. trifoliata atpA and coxIII configurations also carried a 2.1 kb P. trifoliata cob configuration (Figure 1D). This same subset of progeny also carried a faint 16.0 kb P. trifoliata coxII configuration in addition to the 9.0 kb maternal configuration (Figure 1E). The atpA, cob, coxII, and coxIII loci appeared to be "linked," in that the same 17 individuals carried all four P. trifoliata configurations, whereas the other 9 progeny carried none of the P. trifoliata configurations. The intergeneric hybrids were therefore segregating for the presence or absence of the P. trifoliata mtDNA configurations. This pattern of inheritance was not observed for all mitochondrial loci. The rrn26 (not shown) and coxI (Figure 1F) probes identified only maternal fragments in all progeny.

Although the P. trifoliata mtDNA configurations were of low abundance in the progeny, these configurations were not likely the result of partial digestion. P. trifoliata configurations were always reproducible in different DNA preparations from the same plant, and one of the substoichiometric P. trifoliata configurations, the 2.1 kb cob fragment (Figure 1D), was of smaller size than the abundant 10.5 kb maternal fragment. Furthermore, it is improbable that partial digestion products at the atpA, coxII, and coxIII loci would each comigrate with the major corresponding P. trifoliata mtDNA configuration.

The apparent segregation of the intergeneric F1 progeny with respect to the P. trifoliata mtDNA configurations suggested that these configurations resulted from influence of the nuclear genome. Nuclear alleles might alter mtDNA organization in the progeny, producing P. trifoliata configurations. Alternatively, the P. trifoliata mtDNA configurations observed in the progeny might result from nuclear copies of these mitochondrial genes in the paternal parent, and consequently in the progeny plants. To distinguish between these two hypotheses, we analyzed mtDNA purified from two of the progeny (progeny 7 and 33) for the presence of P. trifoliata and LB 1–18 atpA configurations. The 4.3 kb P. trifoliata atpA configuration was not detected in the purified mtDNA samples (Figure 2A, lanes 4 and 6). To determine whether this configuration was present in the nuclear genome of the F1 progeny, we compared total DNA preparations with DNA preparations enriched for nuclear sequences from progeny tree 33 (Figure 2B–D). The nuclear-enriched sample was contaminated by organelle DNA, as evidenced by hybridization to the plastid petD probe (Figure 2D, lane 4). However, the abundance of single-copy, nuclear lycopene cyclase (lyc) sequences was increased relative to the plastid petD sequences in this sample (Figure 2C and D, lanes 3 and 4). The abundance of the P. trifoliata atpA configuration relative to the maternal (LB 1–18) atpA configuration was also increased in the nuclear-enriched DNA sample (Figure 2B, lanes 3 and 4).



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  		Figure 2.. Location of P. trifoliata mtDNA configurations in Citrus x Poncirus hybrids. Autoradiographs of Southern blots containing DNA from LB 1–18 (maternal parent), P. trifoliata cultivar Rubidoux, and F1 hybrids 7 and 33 are shown. Panel A DNA samples were loaded as follows: 1, P. trifoliata total DNA; 2, LB 1–18 total DNA; 3, F1 hybrid 33 total DNA; 4, F1 hybrid 33 mtDNA; 5, F1 hybrid 7 total DNA; 6, F1 hybrid 7 mtDNA. DNA samples (15 µg of total DNA or 1.5 µg of mtDNA) were digested with HindIII and hybridized with the atpA probe. Autoradiographs shown in panels B, C, and D resulted from the hybridization of a single blot with mitochondrial atpA, nuclear lyc, and plastid petD probes, respectively. HindIII-digested DNA samples of 15 µg/lane were loaded as follows: 1, P. trifoliata total DNA; 2, LB 1–18 total DNA; 3, F1 hybrid 33 total DNA; 4, F1 hybrid 33 DNA enriched for nuclear genome sequences.

 
These observations are consistent with the hypothesis that low-abundance P. trifoliata atpA, cob, coxII, and coxIII configurations present in the F1 progeny were inherited from a paternal plant hemizygous for a relatively large mtDNA segment inserted into the nuclear genome. Seventeen of 26 hybrids carried the P. trifoliata configurations. The Yates-corrected chi-squared test (Yates 1934) for a 1:1 segregation in this population was 1.9 (P > .1). This hypothesis cannot be confirmed directly because the paternal tree is no longer living. Given that P. trifoliata trees are naturally outcrossing and highly heterozygous (Durham et al. 1992; Torres et al. 1985), mtDNA transfer into one member of a chromosome pair would be expected to remain hemizygous in some individuals.

The fate of P. trifoliata mtDNA configurations in subsequent plant generations provided additional genetic evidence for nuclear hemizygosity. Zygotic progeny resulting from the open pollination of intergeneric hybrids 33 and 44 (both of which carried the P. trifoliata configurations) were analyzed for atpA configurations. Six of 12 progeny recovered from hybrid 33 and 9 of 12 progeny recovered from hybrid 44 carried the 4.3 kb P. trifoliata configuration in addition to the LB 1–18 configuration, and the relative abundance of the two atpA configurations was similar between the F1 intergeneric hybrids and this subsequent generation of progeny (not shown). Because paternal parents of open-pollination progeny are unknown, a specific model for segregation of the P. trifoliata atpA configuration could not be tested. However, the segregation of both progenies for the presence or absence of this configuration was consistent with a single nuclear copy in the seed parent.

The nuclear copies of the atpA, cob, coxII, and coxIII genes appear to be linked, as no recombinant progeny carrying a subset of these configurations were observed. Whether these genes are, or were at any time, contiguous in the P. trifoliata mitochondrial genome is unknown. The mitochondrial genes transferred as large multigene segments are unlikely to function in the nucleus due to requirements for a nuclear promoter, RNA editing, and a mitochondrial targeting sequence. This is in contrast to the functional transfer of single plant mitochondrial genes to the nucleus. Functional transfer involves edited RNA intermediates and the acquisition of nuclear promoters and mitochondrial targeting sequences (Adams et al. 2000).

The occurrence of mitochondrial sequences in the nucleus complicates the study of mtDNA inheritance. The purification of mtDNA is needed to distinguish nuclear copies from low-abundance mitochondrial configurations. While some researchers have utilized mtDNA purification to demonstrate maternal (Conde et al. 1979) or biparental (Erickson and Kemble 1990) inheritance of mtDNA, other reports of mtDNA inheritance (reviewed by Reboud and Zeyl 1994) have not employed this technique.

MtDNA sequences in the nucleus also complicate the use of mtDNA as a molecular marker in natural populations. Our observations in Citrus, together with those in Arabidopsis (Lin 1999; Stupar 2000), indicate that the insertion of large mtDNA segments into the nuclear genome may be a relatively frequent event in plant genome evolution. An extensive survey of angiosperms revealed a high frequency of functional, single-gene transfers from mitochondrial to nuclear genomes (Adams et al. 2000; Gray 2000). Computer database searches estimated 3–7% of plant nuclear genome sequence files contain short (38–785 nucleotide) segments of organelle DNA randomly integrated by nonhomologous end joining (Blanchard and Schmidt 1995). The mechanism for transfer of large multigene segments from mitochondria to nucleus is unknown, and no published surveys address the frequency of such transfers. The study of mtDNA sequences in the nucleus is of considerable evolutionary interest, providing insight into the dynamics of genome evolution and intergenomic interactions, as well as a potentially important mechanism for generating genomic diversity (Benasson et al. 2000).


   Acknowledgments
 
We thank Drs. K. Cline, W. Gruissem, D. Pring, and G. Moore for providing the petA, petD, atp9, and lycopene cyclase clones, respectively. The Phaseolus vulgaris mitochondrial rrn26 cDNA clone was constructed by Dr. B. O. Kim. This work was supported in part by grant no. 942-27 (to F.G.G. and J.W.G.) by the Florida Citrus Production Research Advisory Council—Florida Department of Agriculture and Consumer Services. C.D.M. was supported by Conselho Nacional de Desenvolvimento Cientifico e Tecnologico/Brasilia-DF/Brazil (CNPq). This research was approved for publication as Florida Agriculture Experiment Station Journal Series no. R-06487.


   Footnotes
 
Corresponding Editor: David Wagner

Received August 24, 2001
Accepted March 5, 2002


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 Materials and Methods
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