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(American Journal of Botany. 2000;87:1452-1458.)
© 2000 Botanical Society of America, Inc.

Paternal inheritance of chloroplast DNA in interspecific hybrids in the genus Larrea (Zygophyllaceae)1

Tien Wei Yang2, Yoko A. Yang5,3 and Zhongguo Xiong4

2 Instituto de Botanica Darwinion, San Isidro, Buenos Aires, Argentina; 3 Larrea Research, 111 South La Creciente, Tucson, Arizona 85711 USA; and 4 Department of Plant Pathology, University of Arizona, Tucson, Arizona 85721 USA

Received for publication June 4, 1999. Accepted for publication December 14, 1999.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
The mode of chloroplast DNA (cpDNA) inheritance was investigated in the genus Larrea (Zygophyllaceae) by polymerase chain reaction (PCR) amplification of cpDNA fragments using three pairs of chloroplast universal primers. A total of 20 F1s from interspecific crosses among five different taxa in the section Bifolium was examined. Twelve F1s were from six crosses between L. cuneifolia (4x) and L. divaricata (2x) (Peru or Argentina) or L. tridentata (2x or 4x). Eight F1s were from two sets of reciprocal crosses between L. divaricata (2x) (Argentina) and L. tridentata (2x). Length polymorphism was observed in all three regions of cpDNA that separated L. cuneifolia parents from L. divaricata and L. tridentata parents and in one of the three cpDNA regions that differentiated L. divaricata (Argentina) parents from L. tridentata (2x) parents. In each case, it was the paternal cpDNA marker that appeared in the F1 individuals. This was further confirmed by restriction fragment length polymorphism (RFLP) analysis of the amplified cpDNA fragments. Larrea may be the fifth genus reported in angiosperms with a paternal bias in cpDNA transmission. Possible mechanisms that may result in paternal cpDNA inheritance were briefly reviewed. Based on the observed uniparental paternal inheritance of cpDNA, restriction analysis of the three cpDNA regions and previous cytogenetic studies, L. divaricata was probably the maternal progenitor of L. cuneifolia.

Key Words: chloroplast DNA • interspecific hybrids • Larrea • paternal inheritance • Zygophyllaceae


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 LITERATURE CITED
 
Chloroplast DNA (cpDNA) is inherited maternally in the majority of angiosperms studied, while among gymnosperms the inheritance is predominantly paternal in the conifers (Sears, 1980 ; Corriveau and Coleman, 1988 ; Smith, 1989a ; Harris and Ingram, 1991 ; Hagemann, 1992 ; Reboud and Zeyl, 1994 ; Owens et al., 1995 ; Mogensen, 1996 ).

In angiosperms, exceptions have been found in many taxa that showed predominantly maternal but with a trace to varying degrees of paternal cpDNA transmission (Cruzan et al., 1993 ; Sewell et al., 1993 ; Chong, Chinnappa, and Yeh, 1994 ; Yao, Cohen, and Rowland, 1994 ; Rajora and Mahon, 1995 ). In these cases, individual progeny may have maternal, paternal, or both types of cpDNA. The outcome, in some of the taxa, depends on the type of crosses involved. In certain crosses in zonal pelargonium the paternal contribution of plastids among the progeny even exceeds the maternal contribution, although maternal inheritance predominates among all crosses studied (Tilney-Bassett and Almouslem, 1989 ).

In contrast to gymnosperms, the predominantly paternal inheritance of cpDNA has been reported so far only in a few taxa in angiosperms. In Medicago, following findings of a strong paternal bias in plastid transmission in alfalfa that used chlorophyll-deficient mutants (Smith, Bingham, and Fulton, 1986 ; Smith, 1989b ), Schumann and Hancock (1989) reported the presence of predominantly paternal transmission of normal green plastids in alfalfa. In their restriction fragment length polymorphism (RFLP) analysis, all 16 F1s showed the paternal cpDNA in the cross between M. sativa ssp. falcata (maternal) and M. sativa ssp. sativa (paternal), while 12 of 14 F1s in the reciprocal cross had paternal, one maternal and one with both types of cpDNA. Also using RFLP analysis in normal alfalfa plants, Masoud, Johnson, and Sorensen (1990) found 173 paternal, five maternal, and 34 biparental cpDNA from 212 progeny that were the result of 16 different inter- and intrasubspecific crosses among M. sativa ssp. sativa and M. sativa ssp. falcata. These studies in alfalfa also found that the ratio of paternal to maternal plastids in the progeny varies according to the genotypes of the parents, although a paternal bias is consistently present (Rusche et al., 1995 ).

In a study of the Turnera ulmifolia complex, from the cross var. angustifolia (maternal) x var. velutina (paternal), all 23 F1s received the paternal cpDNA based on RFLP analysis in polymerase chain reaction (PCR) amplification of the rbcL gene. In the reciprocal cross, however, six paternal, six maternal, and four biparental cpDNA were found in the 16 F1s (Shore, McQueen, and Little, 1994 ). Moreover, a subsequent study (Shore and Triassi, 1998 ) further documented the paternally biased cpDNA inheritance within T. ulmifolia, without involving T. velutina (formerly T. ulmifolia var. velutina). Forty-five paternal, 13 maternal, and 12 biparental cpDNA were found among 70 progeny from 24 sets of reciprocal crosses.

In dioecious Actinidia, uniparental paternal inheritance of cpDNA was observed in a total of 119 progeny from eight different interspecific crosses among A. arguta, A. deliciosa, A. chinensis, A. kolomikta, A. eriantha, A. chrysantha, A. polygama, and A. valvata based on RFLP analysis of PCR-amplified fragments from the rbcL gene, the psbA gene, and the noncoding regions of cpDNA (Cipriani, Testolin, and Morgante, 1995 ; Testolin and Cipriani, 1997 ).

In Pharbitis, reciprocal crosses between P. nil and P. limbata found the paternal inheritance of plastid DNA based on RFLP analysis, although the possibility of biparental inheritance of plastid DNA could not be ruled out when P. limbata was the maternal parent and P. nil was the paternal parent (Hu, Hu, and Zhong, 1996 ).

In the case of Daucus where uniparental paternal inheritance of cpDNA was first reported (Boblenz, Nothnagel, and Metzlaff, 1990 ), subsequent investigations suggested uncertain identities of the parental plants in the earlier study and found maternal cpDNA inheritance in all ten crosses that involved seven species and subspecies of the genus (Steinborn et al., 1995 ).

The genus Larrea in the Zygophyllaceae is composed of evergreen woody shrubs of wide geographical and ecological distribution in the major warm deserts of the New World. Throughout most of its extensive range it is the dominant perennial of the desert community. The genus has two sections and five species (Palacios and Hunziker, 1972 ). Larrea nitida (2x) and L. ameghinoi (2x), both South American, belong to the multifoliolate section Larrea, which is considered to be the more primitive of the two sections. South American L. cuneifolia (4x) and L. divaricata (2x) and North American L. tridentata (2x, 4x, 6x) belong to the bifoliolate section Bifolium. Larrea divaricata is known as "jarilla" in South America, where the population in Peru is distinctly different from the populations in Argentina morphologically (T. W. Yang, unpublished data) and biochemically (Mabry et al., 1977 ). Larrea tridentata is known as "creosotebush" or "gobernadora" in North America, where there are three distinct cytotypes with diploid (Chihuahuan Desert), tetraploid (Sonoran Desert), and hexaploid (Mojave Desert) chromosome numbers (Yang, 1970 ). The basic chromosome number of Larrea species is x = 13. All members of Larrea outcross mainly by insect pollination with different degrees of self-pollination (Simpson, Neff, and Moldenke, 1977 ).

In our random amplified polymorphic DNA (RAPD) analysis of the genus Larrea, we found Primer 196 (University of British Columbia) to generate high-intensity bands at around 1 kb (kilobase) that separated L. cuneifolia from L divaricata and L. tridentata (Yang, Yang, and Xiong, unpublished data). The former showed a smaller band at ~1000 bp (base pair) and members of the latter group a larger band at ~1060 bp with a slight length variation, suggesting length polymorphism of a specific RAPD amplification region. We then used Primer 196 to determine the distribution of 1000 bp and 1060 bp bands among 12 F1s from six interspecific crosses. Larrea cuneifolia was one of the parents in each of the crosses with L. divaricata (Peru or Argentina) or L. tridentata (2x or 4x) as the other parent. Without exception it was the paternal band that appeared in the F1 individuals, whether L. cuneifolia was the maternal or the paternal parent. Since we used total DNA that contained both nuclear and cytoplasmic DNA and since these results showed uniparental inheritance, it led us to suspect the presence of paternal cytoplasmic inheritance in Larrea.

To test this hypothesis we decided to first examine the inheritance pattern of chloroplast DNA in Larrea, using the same 12 F1s examined with RAPD Primer 196 and eight additional F1s from two sets of reciprocal crosses between L. divaricata (Argentina) and L. tridentata (2x). We selected three pairs of universal chloroplast DNA primers for the amplification of mostly noncoding regions (Taberlet et al., 1991 ; Demesure, Sodzi, and Petit, 1995 ).


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 LITERATURE CITED
 
Hybridization experiments have been conducted since 1971 in Tucson, Pima County, Arizona. All parental Larrea plants, except one L. tridentata (4x) individual from a natural community in Tucson, were grown from seeds collected in North and South America. The two parents of each cross were planted side by side. Seeds were collected from each parental plant with the identities of both the seed (maternal) parent and the putative paternal parent carefully recorded and were grown to mature plants. Those F1s that showed intermediate morphological characteristics of the parental plants were determined as interspecific hybrids. The paternity of each F1 hybrid was confirmed with reasonable certainty by the results of RAPD banding patterns of both the parents and the F1s (Yang, Yang, and Xiong, unpublished data).

Table 1 lists the six crosses and the number of F1s between L. cuneifolia (Catamarca, Argentina) and L divaricata (Peru or Argentina) or L. tridentata (2x or 4x). Table 2 lists the reciprocal crosses between L. tridentata (2x) from Culberson County, Texas and L. divaricata from La Rioja, Argentina and their F1s. Table 3 lists the reciprocal crosses between L. divaricata from Tucuman, Argentina, and L. tridentata (2x) from Pecos County, Texas. Although both parents of the cross in Table 3 died prior to the current study, the F1s examined in this study were confirmed in an earlier study by Yang et al. (1977) .


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  		Table 1. Six interspecific crosses between L. cuneifolia and L. divaricata or L. tridentata (maternal x paternal) and their F1s

 

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  		Table 2. Interspecific reciprocal crosses between L. tridentata 2x from Texas and L. divaricata [Argentina] 2x from La Rioja (maternal x paternal) and their F1s

 

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  		Table 3. Interspecific reciprocal crosses between L. divaricata [Argentina] 2x from Tucuman and L. tridentata 2x from Texas (maternal x paternal) and their F1s

 
The three pairs of universal chloroplast primers are described in Table 4, in which primer pair 1–1' was designed by Demesure, Sodzi, and Petit (1995) and the primer pairs 2–2' and 3–3' by Taberlet et al. (1991) . The primers were synthesized by Life Technologies, Grand Island, New York, USA.


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  		Table 4. Description of the three pairs of universal cpDNA primers applied in this study. Primers 1,1' were designed by Demesure et al. (1995) and primers 2,2' and 3,3' by Taberlet et al. (1991)

 
Total DNA was extracted from each individual plant. One gram of fresh young leaves from each plant was ground in liquid nitrogen and transferred into 15 mL of the extraction buffer preheated to 60°C. The extraction buffer contained 0.1 mol/L Tris (pH 8), 0.5 mol/L NaCl, 40 mmol/L EDTA (pH 8), 1.5% (w/v) CTAB (hexadecyltrimethylammonium bromide) and 1% (w/v) Sarkosyl (lauroylsarcosin). Immediately before and after the transfer of leaf tissue, 200 µL of ß-mercaptoethanol were added to the extraction buffer, followed by incubation at 60°C for 1 h. The lysate was mixed with an equal volume of chloroform/isoamyl alcohol (24:1) and centrifuged at 5000x g for 10 min. This was repeated 4–7 times until the interphase was clean. The aqueous phase was mixed with 1/10 volume 3 mol/L sodium acetate and 2/3 volume cold isopropanol to precipitate DNA followed by centrifugation at 5000x g for 10 min. After washing with 70% ethanol 1–2 times, the DNA was resuspended in 1 mL of sterile distilled water and incubated with RNase A (final concentration of 30 µg/mL) at 37°C for 30 min. DNA concentration was measured by fluorescent spectroscopy using Hoefer TKO 100 (Hoefer Scientific Instruments, San Francisco, California, USA). Each DNA sample was diluted to 5 ng/µL concentration for the assay.

Amplification of cpDNA was carried out in a 25-µL reaction mixture containing 1x Taq polymerase buffer (Promega, Madison, Wisconsin, USA), 100 µmol/L of each dNTP, 3 mmol/L MgCl2, 0.2 µmol/L of each primer, 20 ng of DNA, and 0.5 units of Taq polymerase (Promega). The reaction mixture was overlaid with a drop of mineral oil. Amplification was performed in a Temp-tronic thermocycler (Thermoline, Dubuque, Iowa, USA) programmed as follows: an initial 5 min denaturation at 94°C; 35 cycles of denaturation at 94°C for 45 s, annealing at 54.5°C for 45 s, and polymerization at 72°C for 2 min; followed by a 10 min final extension at 72°C. Amplification products were electrophoresed on 1.5% agarose gel with ethidium bromide and TAE (Tris-acetate/EDTA) buffer and photographed under UV light. The size of each amplified cpDNA fragment was estimated by Bio Image Whole Band Analyzer version 3.2. For RFLP analysis of the amplified cpDNA fragments, PCR products were digested with seven restriction enzymes (AluI, DdeI, HaeIII, HinfI, MboI, RsaI, and TaqI) and analyzed in 1.5% or 2% agarose gel.


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 LITERATURE CITED
 
We first examined 12 F1s from the six crosses between L. cuneifolia and either L. divaricata (Peru or Argentina) or L. tridentata (2x or 4x) (Table 1). The primer pair 1–1' produced a high-intensity band of the cpDNA amplification product. In addition, a nonspecific, medium-intensity DNA band of ~250 bp was observed in all parental individuals studied. The primer pairs 2–2' and 3–3' produced a single high-intensity band in each sample. With all three pairs of primers, length polymorphism was observed that differentiated the parents in each cross.

The primer pair 1–1' produced a DNA band of ~1190 bp in L. cuneifolia and a slightly smaller DNA band of ~1160 bp in L. divaricata and L. tridentata. The primer pair 2–2' generated a DNA fragment of ~810 bp in L. cuneifolia and larger DNA fragments of ~870 bp in L. divaricata (Argentina) and of ~850 bp in L. divaricata (Peru) and in L. tridentata. The primer pair 3–3' separated L. cuneifolia from L. divaricata and L. tridentata by a slight length difference of ~10 bp (distinguishable with increase in electrophoresis time) in the amplified DNA fragments. Larrea cuneifolia displayed a DNA fragment of ~940 bp, while L. divaricata and L. tridentata showed a DNA fragment of ~950 bp. In each case, it was the paternal cpDNA marker that appeared in F1 individuals. Figure 1 shows PCR amplification of each cpDNA region within one of the crosses as an example.



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  		Fig. 1. PCR amplification of three cpDNA regions in a cross between L. divaricata as the maternal parent and L. cuneifolia as the paternal parent (Table 1 –Cross 5). Lanes 1 and 19: 1 kb DNA marker; lanes 2–6: primer pair 1–1' region; lanes 8–12: primer pair 2–2' region; lanes 14–18: primer pair 3–3' region. Lanes 2, 8, 14: maternal parent (L. divaricata); lanes 3, 9, 15: paternal parent (L. cuneifolia); lanes 4–6, 10–12 and 16–18: F1s

 
Since we have found that the primer pair 2–2' produced an 870-bp band in the L. divaricata (Argentina) parent and an 850-bp band in L. tridentata (2x) parents, we used this pair of primers to examine the cpDNA inheritance pattern in the eight F1s of two sets of reciprocal crosses between L. divaricata (Argentina) and L. tridentata (2x) (Tables 2, 3) based on the expected length polymorphism. The two parents in the reciprocal crosses between L. tridentata (2x) from Culberson County, Texas and L. divaricata from La Rioja, Argentina (Table 2) showed the expected length polymorphism. All F1s showed the paternal cpDNA marker.

Since both parents have died in the reciprocal crosses between L. divaricata (Argentina) from Tucuman and L. tridentata (2x) from Pecos County, Texas (Table 3), we examined other L. divaricata individuals grown from seeds collected from the original Tucuman site and other L. tridentata (2x) from the same Texas (Pecos) collection in order to assure ourselves with reasonable confidence that the L. divaricata parent had the 870-bp band and the L. tridentata parent had the 850-bp band. Of the five F1s examined we found the 850-bp band only in individuals in which the paternal parent was L. tridentata (2x) and the 870-bp band only in individuals in which the paternal parent was L. divaricata (Argentina). Thus, all eight F1s in the crosses between L. divaricata (Argentina) and L. tridentata (2x) also showed paternal cpDNA inheritance.

The initial observation of paternal cpDNA inheritance in Larrea spp. was further supported by RFLP analysis of the amplified cpDNA fragments. Because of the small size differences in the cpDNA fragments from various parents, restriction digestion was attempted to provide better distinctions among similarly sized DNA fragments. Of seven restriction enzymes screened, AluI, HinfI, MboI, and TaqI produced restriction fragment patterns in all three cpDNA regions. Restriction fragment patterns were produced by DdeI and RsaI in the cpDNA regions of the primer pairs 1–1' and 3–3' and by HaeIII in the cpDNA region of the primer pair 1–1'. We found distinct differences in restriction fragment pattern between L. cuneifolia parents on the one hand and L. divaricata and L. tridentata parents on the other in all three cpDNA regions, which were most prominently expressed by HinfI. Figure 2 shows the result of digestion with HinfI in each cpDNA region, within the same cross that was shown in Fig. 1. Larrea divaricata and L. tridentata parents showed similar restriction fragment patterns, except for differences in fragment length in the region of the primer pair 2–2' that differentiated L. divaricata (Argentina) parents from L. divaricata (Peru) and L. tridentata parents (Fig. 3). The RFLP data clearly demonstrated the paternal inheritance of cpDNA in the crosses we have examined.



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  		Fig. 2. Hinf I digestion of three cpDNA regions in a cross between L. divaricata as the maternal parent and L. cuneifolia as the paternal parent (Table 1 – Cross 5). Lanes 1, 7, 13: 1 kb DNA marker; lanes 2–6: primer pair 1–1' region; lanes 8–12: primer pair 2–2' region; lanes 14–18: primer pair 3–3' region. Lanes 2, 8, 14: maternal parent (L. divaricata); lanes 3, 9, 15: paternal parent (L. cuneifolia); lanes 4–6, 10–12 and 16–18: F1s. Note that the bands at ~ 250 bp in lanes 2–6 are from nonspecific amplification products that remained unrestricted by HinfI

 


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  		Fig. 3. Hinf I digestion of the cpDNA region amplified with primer pair 2–2' within a set of reciprocal crosses between L. tridentata (2x) and L. divaricata (Table 2 ). Lanes 1, 6: 1 kb DNA marker; lane 2: maternal parent (L tridentata); lane 3: paternal parent (L. divaricata); lanes 4,5: F1s; lane 7: maternal parent (L. divaricata); lane 8: paternal parent (L. tridentata); lane 9: F1

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
LITERATURE CITED
 
The observed pattern of uniparental paternal inheritance of cpDNA in Larrea is based entirely on the small sample of 20 F1s. As emphasized by Smith (1989a) , Hagemann (1992) , and Milligan (1992) , uniparental inheritance, whether maternal or paternal, cannot be reasonably assumed unless a large number of progeny is tested. In order to estimate the probability of possible maternal cpDNA transmission in Larrea based on our study of 20 F1s, we used a binomial model of organelle inheritance (Milligan, 1992 ). In this model, when all progeny in a given sample size have only paternal cpDNA, the probability of maternal cpDNA transmission, P, can be calculated using the equation of ß = 1- (1-P)N, where ß is the power of the test and N, the number of progeny examined. We obtained P = 0.14 at 95% confidence level (ß = 0.95) and P = 0.21 at 99% confidence level (ß = 0.99). These P values indicate predominantly, if not exclusively, paternal inheritance of cpDNA in Larrea. To the best of our knowledge, in addition to Medicago, Turnera, Actinidia, and Pharbitis, Larrea is the fifth genus reported in angiosperms that has a strong paternal bias in cpDNA transmission. There is a possibility that Larrea has strict paternal cpDNA inheritance.

All five Larrea taxa involved in this study belong to section Bifolium of the genus. It is, therefore, not known whether or not this mode of cpDNA inheritance is also the rule in section Larrea, in which L. nitida and L. ameghinoi are the members. Both species are likely to have high levels of self-pollination (Simpson, Neff, and Moldenke, 1977 ). Within section Bifolium our results suggest that the parental genotypes are not affecting the cpDNA inheritance pattern, since all F1s showed the paternal cpDNA regardless of the species or taxa involved or the direction of crosses. However, because of the small number of F1s examined in this study, a much larger sample size is needed to determine more conclusively this aspect of cpDNA inheritance in Larrea.

In addition, since all the F1s studied are the result of interspecific crosses, we have no data on the mode of cpDNA inheritance within a species or a taxon. Interspecific crosses may be misleading if novel plastome-genome interactions induce atypical cpDNA inheritance (Chiu and Sears, 1993 ; Reboud and Zeyl, 1994 ). However, as L. divaricata (Argentina) and L. tridentata (2x) are considered to be closely related "semispecies" based on morphology, regular meiotic behavior and partial fertility of their F1s, high homology of their proteins, and similarity of their phenolic compounds (Hunziker et al., 1977 ; Mabry et al., 1977 ; Yang et al., 1977 ), and since these two taxa so far appear to have similar cpDNA types, the same mode of cpDNA inheritance can be expected to occur intraspecifically in Larrea.

The mechanisms that may result in different modes of cytoplasmic inheritance have been studied and discussed by many investigators (Singh, 1978 ; Sears, 1980 ; Whatley, 1982 ; Chiu, Stubbe, and Sears, 1988 ; Tilney-Bassett and Almouslem, 1989 ; Kuroiwa, 1991 ; Hagemann, 1992 ; Russell, 1992 ; Birky, 1995 ; Owens et al., 1995 ; Mogensen, 1996 ). Larrea is apparently successful in circumventing different steps that lead to the exclusion or degeneration of paternal plastids or the degradation of paternal plastid DNA during the development of the male gamete and its passage to the egg cell, and further during or after fertilization. This would characterize Larrea as a member of the Pelargonium type in the classification of Hagemann and Schroder (1989) . The question, then, would be what happens to the maternal plastids (and their DNA) when the inheritance is predominantly or strictly paternal.

There may be a number of possible ways in which maternal plastids or their DNA may not be inherited by the offspring. First, plastids may be absent from the initial stage of egg cell development by unequal distribution of plastids during the formation of megaspores (Hagemann, 1992 ) or during the cellularization of the embryo sac that may result in the embryo sac or the egg cell having no plastids. Second, plastids may be present in the young egg cell but may be greatly deformed or degenerated during egg cell development, as in Taxaceae, Pinaceae, and Cephalotaxaceae of the conifers (Gianordoli, 1974 ; Willemse, 1974 ; Pennell and Bell, 1987 ; Owens and Morris, 1990 ). Third, plastids may be present without deformation or degeneration in the mature egg cell but may be positioned in or moved to the regions of the cell at fertilization that will not become a part of the functional embryo, as in Araucariaceae and Cupressaceae of the conifers (Singh, 1978 ; Owens et al., 1995 ; Mogensen, 1996 ). In alfalfa the genotype of the maternal parent seems to affect the distribution of plastids in the egg cell that may result in a larger number of paternal plastids than maternal plastids in the apical portion of the zygote and the two-celled proembryo, which gives rise to the functional embryo (Zhu, Mogensen, and Smith, 1993 ; Rusche et al., 1995 ). Fourth, maternal plastids may be present in the apical cell of the two-celled proembryo but may still be eliminated during early development of the offspring. If paternal plastids predominate, maternal plastids may be further sorted into a determinate cell lineage (Rusche et al., 1995 ) or diluted out (Schumann and Hancock, 1989 ). Preferential degeneration of maternal plastids may occur during embryogenesis as in alfalfa (Rusche et al., 1995 ). If maternal plastids develop into large amyloplasts, their DNA content may substantially decrease (Sodmergen et al., 1994 ). Maternal plastids may fail to replicate if they lack functional DNA. DNA degradation within seemingly structurally intact plastids (Morgensen, 1996) was indicated in alfalfa (Shi et al., 1991 ) and Pelargonium zonale (Nagata et al., 1997 ).

Through structural studies and analysis of DNA content of plastids, Larrea, in addition to Turnera, Actinidia, and Pharbitis, may offer new material to further elucidate what may be taking place in the predominantly and strictly paternal inheritance of cpDNA in angiosperms.

The effect of the mode of cpDNA inheritance observed in this study on the systematic and evolutionary relationships among members of the genus Larrea is difficult to assess, unless some confirmations are made on the pattern of cpDNA transmission within the entire genus. If we assume that the uniparental paternal inheritance of cpDNA is the general rule in this genus, a phylogenetic tree based on cpDNA data would present a paternal lineage in the intrageneric evolution of Larrea. Although we have not yet found the mode of mitochondrial DNA inheritance in Larrea, if it were found to be maternal, as is the case in most of the angiosperms so far studied (Reboud and Zeyl, 1994 ; Mogensen, 1996 ), the use of both paternal and maternal lineages from these organelles, combined with nuclear genetic data, would provide us with more insight in the evolutionary study of Larrea.

One of the subjects of interest in the study of Larrea has been the origin of L. cuneifolia, which was considered to be an allotetraploid based partly on the observed 26 bivalents at meiosis of this species in the cytogenetic studies of Larrea (Hunziker et al., 1977, 1978 ). These studies further suggested that L divaricata, or a species very closely related to it, was probably one of the two diploid progenitors of L. cuneifolia based on the chromosome pairing during meiosis of the triploid hybrids between L. cuneifolia and L. divaricata (13 bivalents and 13 univalents in nearly 50% of the cells). The present study has found length polymorphism between L. cuneifolia parents and L. divaricata parents in all three regions of cpDNA examined. Moreover, our preliminary restriction analysis of these cpDNA regions showed substantial differences in restriction fragment pattern between L. cuneifolia and L. divaricata parents (Fig. 2). The same results were obtained when we examined some of the other available individuals of these two species that were originated in different localities of South America. These results seem to suggest that L. divaricata was not likely the cpDNA donor species in the origin of L. cuneifolia. Furthermore, if we assume the uniparental paternal inheritance of cpDNA during the hybridization process between the progenitors, it may suggest that L. divaricata was the maternal progenitor.

In our preliminary examination of these three cpDNA regions with available samples of L. nitida and L. ameghinoi, we have found at least two types of cpDNA among different individuals of L. nitida, one of which so far appears to be identical (or extremely similar) both in length and restriction fragment pattern to the cpDNA of L. cuneifolia individuals so far examined (Yang, Yang, and Xiong, unpublished data). However, previous cytogenetic studies found highly irregular meiosis accompanied by cytomixis in a triploid hybrid individual between L. cuneifolia and L. nitida (and also in several triploid hybrid individuals between L. cuneifolia and L. ameghinoi) and suggested that the other genome of L. cuneifolia could have come from a species that is now extinct (Hunziker et al., 1977 ). Further studies on the subject of the other progenitor (possibly the paternal progenitor) of L. cuneifolia are currently being undertaken, first by analyzing the phylogenetic relationships among all cpDNA types that we have so far found within the genus.

As in the studies of phylogenetics and hybrid speciation, an understanding of the mode of cytoplasmic inheritance is an important element also in the studies of hybridization and introgression (Arnold, Buckner, and Robinson, 1991 ; Sutton et al., 1991 ; Cruzan et al., 1993 ; Watano, Imazu, and Shimizu, 1996 ) and population genetics (Asmussen and Schnabel, 1991 ; Schnabel and Asmussen, 1992 ; Petit, Kremer, and Wagner, 1993 ; Dong and Wagner, 1994 ; Ennos, 1994 ; Latta and Mitton, 1997 ). In Larrea there is ample evidence of natural hybridization among South American species (Hunziker et al., 1977, 1978 ) and indications of introgression between L. nitida and L. ameghinoi (Hunziker et al., 1977, 1978 ) and between cytotypes of L. tridentata (T. W. Yang, unpublished data). Population genetic studies have so far been reported with isozymes for populations of L. nitida, L. divaricata, and L. tridentata (Cortes and Hunziker, 1988, 1997 ; Duran et al., 1998 ) and with cpDNA haplotypes for populations of L. tridentata (Hunter and Riddle, 1995 ). Paternal cpDNA inheritance found in the present study may offer critical information in the interpretation of cytonuclear data, as one of the factors that affect cytoplasmic gene flow, in future molecular studies of hybrid populations and populations of each member of Larrea.


   FOOTNOTES
 
1 The authors thank Juan H. Hunziker, Juan C. Gamerro, Frank R. H. Katterman, William S. Bickel, Dan Martin, and Ziming Weng for their contributions in the extended course of our investigation; two anonymous reviewers, H. Lloyd Mogensen and Elizabeth Lawson for their valuable comments and suggestions on the manuscript; Caroline Spellman for special assistance; the Department of Plant Pathology, University of Arizona for space and facilities; the Laboratory of Molecular Systematics and Evolution, University of Arizona for consultation; the Instituto de Botanica Darwinion for institutional support; and Anthony T. Yeung, Erle E. Peacock, Jr., Sam Shellhorn, and Constance D. Mail for their gifts to our continuing research on creosotebush and jarilla. Back

5 Author for correspondence. Back


   LITERATURE CITED
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
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