mechanisms of maternal inheritance of plastids and mitochondria: developmental and ultrastructural...

PLANT MOLECUI.AR BIOLOGY REPORTER Volume 4, Number 4, 1987 Pages 92,-205

G E N E T I C R E S O U R C E S

Mechanisms of Maternal Inheritance of

Plastids and Mitochondria: Developmental and

Ultrastructural Evidence Marie B. C o n n e t t

Section of Geneticr anal Development, BradJie/d Hall. Cornel/University, Ithaca. N Y 14853

S u m m a r y A number of maternally inherited characters are now known to be associated with mitochondria or chloroplasts, which contain small genomes segregating separately from that of the nucleus. The reason often given for maternal inheritance of plastid-associated characters in plants is the absence of plastids in the generative cell of pollen following an unequal mitosis (Vaughn, 1980). However, fine ultrastructural studies have not established "exclusion" as the sole mechanism for maternal inheritance; in many cases, other mechanisms may be operating. Three lines of evidence concerning the mechanism of maternal inheritance will be discussed:

First, while it is true that thorough fine ultrastructural studies have failed to find plastids in generative cells of many seed plants (Cass and Karas, 1975), similar studies in some seed plants have found plastids or structures taken to be plastids in generative cells, and a few studies using serial section electron microscopy to re-examine some plants in the first group have found

Inquiries to." Marie B. Connett, Section of Genetics and Development, Bradfield Hall, Cornell University, Ithaca, NY 14853

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194 Plant Molecular Biology Reporter

plastids in generative cells and even in the sperm. Also, the exclusion model fails to account at all for maternal inheritance of mitochondria, which are found nearly universally in the generative cells and sperm which have been studied ultrastructurally.

Second, maternal inheritance of plastid characters is seen in many lower plants and algae, despite the presence of plastids and mitochondria in the male gametes and their reported deposition in the zygote.

Third, there is evidence for an alternative or additional mechanism which may occur in many plants: mitochondria and plastids in male gametes may be altered during development or syngamy so that, although not excluded, they are genetically and perhaps functionally debilitated, which would result in maternal inheritance. This evidence derives both from ultrastructural studies of pollen and fertilization, and from genetic and developmental analysis of algal zygotes and of embryos derived from pollen tissue culture. This mechanism is logically attractive in that it allows for the observed continuum of variation from strict uniparental inheritance in a number of plants, which cannot be explained by the "all-or-nothing" exclusion hypothesis.

Indeed, it may be appropriate to think of both mechanisms as part of a continuum ranging from destruction within the zygote, to exclusion during syngamy, to pre-fertilization debilitation, to absence from male gametes and generative ceils (Russell and Cass, 198 t).

O r g a n e l l e s in G e n e r a t i v e Cells and S p e r m o f H i g h e r P l an t s A number of studies claim to show that maternal inheritance of plastids in a given taxon must be the result of plastids being entirely absent from the generative cells (e.g., Schroeder, 1985; Angold, 1968). Hagemann, in a 1979 review of plastid inheritance, summarized a number of ultrastructural studies prior to that time and classified the plants investigated into three categories: (1) plants in which no plastids are found in the generative cell (the maiority in his review) and which therefore show maternal inheritance of plastid-associated characters; (2) plants in which plastids are found in the generative cell but which pass them only rarely into the sperm cells, and which are assumed to show maternal inheritance except for rare instances reflecting this rare inclusion ofplastids; (3) plants in which normal, abundant plastids are present in generative cells and sperm, and which therefore show biparental inheritance.

However, many of the studies reviewed were performed without the benefit of glutaraldehyde-osmium fixation (e.g., Bopp-Hassenkamp, 1960; Sassen, 1964; Larson, 1965), rendering their identification of organelles somewhat tentative (Sanger and Jackson, 1971); mitochondria and plastids were ad- mittedly difficult to positively identify and differentiate from one another

Mechanisms of Maternal Inheritance of Plastids and Mitochondria 195

(Sassen, 1964; Larson, 1965; Lombardo and Gerola, 1966; Jensen, 1968, Jensen et al., 1968; Mepham and Lane, 1970). For example, Jensen (1968) cautiously chose to identify double all membrane-bounded organelles in the sperm as mitochondria because they were close in size to mitochondria in the vegetative cell and because plastids were usually reported to be absent from the sperm. However, Jensen left the possibility open that some of them might be proplastids. More recently, serial ultrathin sectioning techniques used to examine pollen tubes have shown that plastids can be present as clusters in small numbers in generative cells and sperm, such that the probability of missing them in a given single section would be high (Sanger and Jackson, 1971; Russell and Cass, 1981). This may account for some of the earlier reports of the absence of plastids in generative cells of taxa which nonetheless occasionally deviate from strict maternal inheritance.

A second problem with Hagemann's classification is that presence or absence of plastids in the generative cell or sperm is taken to be the single factor which determines biparental vs. maternal inheritance, but genetic evidence of the inheritance pattern is unavailable for most of the plants reviewed (Sears, 1980). In the great majority of species uniparental inheritance simply has not been shown because of the lack of defined organellar markers (Russell, 1980; Russell and Cass, 1981), so they could not be used to exemplify a putative causal relationship between exclusion and maternal inheritance. Also, in rigorous studies using large numbers of crosses with combinations of well-defined organellar markers (necessary to define the actual extent of uniparental inheritance and to rule out apparent departures from strict maternal inheritance of a certain character due to mutations or to contamination of the examined progeny by seeds of different genotypes), some of the taxa listed have been shown to differ from the predicted pattern, giving a certain frequency of progeny with the paternal organellar genotype when many crosses are analyzed (e.g., Medgyesy et al., 1986). It is not known whether this "leakiness" is due to a low frequency of plastid inclusion in the sperm, or to some other cause. It may be possible to isolate specific paternal transmission mutants from among such progeny to see how the developmental pattern of the gametes might be altered to allow paternal transmission of organelles.

The exclusion model also fails to explain completely the non-Mendelian inheritance pattern of plants in Hagemann's third classification, i.e., those which contain plastids in the generative cells and show biparental inheritance such as the variegated Oenothera and Pelargonium zonale. Although paternal plastids are not excluded from the zygote, their genomes do not recombine with those of the maternal plastids. Instead, the parental plastid genomes segregate into different cell lines as soon as cleavage of the heteroplasmic zygote commences, and the degree of biparental inheritance is correlated sig-


nificantly better to the female nuclear genotype than to the fraction of plastids contributed to the zygote by the male gamete (Tilney-Bassett, 1975). Clearly then, during syngamy, there must be some factor operating to sort genetically different plastids into different cells and maintain differential rates of plastid replication even when the plastids of the male parent are not excluded from the sperm or the zygote.

lforganelles from both parents are present in the zygote but cannot recombine (Sears, 1980), random segregation of organelles between daughter cells may be able to account for the sorting of the different genomes into different homoplastic cell lines (Birky, 1983). Russell (1980) has suggested that di- rected sorting might also be a possible mechanism for maternal inheritance in some cases: paternal plastids may be sorted into cell lines not contributing to the mature progeny, e.g., the suspensor.

Although mitochondria are uniparentally inherited in all cases that have been examined, incidence of biparental or partial paternal inheritance could remain undetected due to the lack of phenotypic or selectable markers for detecting the inheritance pattern. A low frequency of leakage could also easily escape detection, as in crosses involving mitochondrially-associated cytoplasmic male sterility. Restriction fragment length polymorphisms may be more useful markers for analysis of transmission of organellar genomes when phenotypic markers are not available. An extensive study of sexual crosses using parents differing in mitochondrial restriction fragment pattern did not show any incidence of paternal inheritance (Medgyesy et al., 1986). However, nearly every ultrastructural study of sperm and generative cells of higher plants, with the single exception of those in the orchid family (Chadard, 1969, Cocucci and Jensen, 1969), identify mitochondria as present, and in some studies where fertilization was examined, as entering the egg with the sperm nucleus (e.g., Camefort, 1968; Scott and Russell, 1980). Thus, the theory that exclusion from the generative cell or sperm is generally responsible for maternal inheritance may seem plausible for plastids, but it cannot explain uniparental inheritance for mitochondria. In addition, when somatic hybrids are formed, recombination of mitochondrial genomes seems to be usual (Hanson, 1984; Clark et al., 1986), although it occurs only at a very low frequency in plastomes (Medgyesy et al., 1985). Hence, if both paternal and maternal mitochondria are present in the following syngamy, some other mechanism must be operating to prevent them from recombining in the zygote as they might in a somatic hybrid.

Several possibilities exist which could preclude transmission of male plastids and mitochondria despite their presence in the generative cell and sperm. For example, they may become degenerated before or after syngamy, or they may fail to enter the egg during syngamy. Mogensen and Rusche (1985)

Mechanisms of Maternal Inheritance of Plastids and M itochondria 197

report that mitochondria are present in large numbers in barley sperm just after mitosis, but that the numbers are reduced by 50% in mature sperm and may become further reduced by time of syngamy. Clauhs and Grun (1977) and Schroeder (1986) report the same trend for plastids in generative cells of Solanum and Com,allaria vmjalis, respectively. Few studies, have been made of the actual events of fertilization in higher plants because this presents so many practical difficulties (Jensen, 1973): timing of observation is difficult, as the time of arrival of the pollen tube at the embryo sac is not predictable to within minutes or even hours, but discharge of the pollen tube and fertilization proceed rapidly after that. Another major difficulty is that light microscope studies are virtually non-existent since the whole cytoplasmic mass stains so darkly with commonly used histological dyes that it is difficult to differentiate ooplasm from pollen tube, sperm cells, or synergids. However, in the electron micrographic studies that have been done, it appears that the intact sperm cells, as well as cytoplasm from the pollen tube tip (which, incidentally, usually contains abundant mitochondria and amyloplasts) are discharged into a synergid (Jensen and Fisher, 1968; Cass and Jensen, 1970; Wilms, 1981). The sloughing offof the tube cytoplasm with its many organelles is presumed to take place in the synergid before the sperm cell fuses with the egg (Jensen and Fisher, 1968); it may be that any remaining organelles in the sperm cell itself are also stripped from it at the same point (Van Went, 1970; Wilms, 1981), so that the sperm nucleus entering the egg is devoid of them. On the other hand, if syngamy occurs by fusion of the sperm cell membranes with those of the egg cell, inclusions in the sperm cytoplasm would enter the egg (Russell, 1983). Plastids and mitochondria of the sperm have been seen intact in the newly-fertilized egg of Plumbago zey/anica; whether or not they remain intact and contribute to the genotype of the progeny or are debilitated or degenerated is not known due to the lack of organellar markers (Russell, 1980).

Maternal Inheritance in Lower Plants and Algae The male gametes of investigated lower plants and green algae generally contain plastids and mitochondria (Paolillo, 1974); what happens to them during fertilization? There are not many studies of fertilization ultrastructure in lower plants, and the results of these have occasionally been contradictory. For example, Yuasa (1952) observed with the light microscope that in the liverwort Marchantia and other liverworts, the single prominent sperm plastid enters the ooplasm at syngamy; but in the liverwort Sphaerocarpus, sperms are reported to lose their cytoplasmic inclusions, except for the apical body, while transversing the archegonial neck (Diets, 1967). Tourte (1971) and Kuligowski-Andres and Tourte (1978) reported that the spermatozoid of Pter-

198 Plant Molecular Biology R@orter

idium aquilinum contains both mitochondria and plastids and that these can be shown by autoradiographic labeling to enter the egg at syngamy and per- sist in integral forms at least until after the onset of cleavage, but Duckett and Bell (1971, 1972) reported for tile same species that the plastids are observed to be lost in the archegonial neck. As for the fate of the sperm apical body, which contains a mitochondrion, it is reported for the fern ll,la~:ri/m vest#a that while the plastids are "stripped" during syngamy and remain outside the ooplasm (Myles and Bell, 1975), the mitochondrion associated with the nucleus does enter the ooplasm, where it appears to "degenerate" before the onset of mitosis in the zygote, losing its outer membrane and showing progressive flattening of the cristae until tile structures are no longer recog- nizable (Myles, 1978).

Unfortunately, genetic information about the inheritance pattern of orga- helle-associated characters is lacking for these lower plants. Since tile entire sequence of chloroplast D N A for Marchantia is now available (Ohyama et al., 1986), DNA-level analysis of crosses between the sequenced type and variants or mutants may aid in correlating ttle ultrastructural observations with the plastid inheritance pattern that is found.

Ultrastructural evidence for post-fertilization destruction of a paternal organelle has been supplemented with autoradiographic evidence in Ull'a muta- bills, a chlorophytic alga whose gametes each contain a single chloroplast. Radioactive carbohydrate in the paternal plastid was found to become redis- tributed throughout the zygote in a time course parallel with ultrastructural observations of"disintegration" of the paternal plastid (Braten 1971, 1973).

Post-fertilization debilitation of the organellar genome has been invoked to account for uniparental inheritance in Chlam),domonas. an isogamous chlorophytic alga with two mating types controlled by the mt locus, since the paternally-derived chloroplast can be clearly seen intact in the zygote until it physically fuses with the maternal chloroplast about six hours after syngamy. Labeling experiments with l~C-adenine showed that chloroplast DNA from ,he male ( m r ) parent was no longer present in CsCI gradients of DNA isolated from zygotes over a time course within six hours of syngamy, before chloroplast fusion occurs (Schlanger & Sager, 1974). Fluorescence labeling of the parental plastomes with 4'-6-diamidino-2-phenylindole (DAPI) has confirmed ultrastructurally that the nucleoids disappear from tile paternal plastid before plastid fusion in Chlamydomonas reinharattii (Kuroiwa et al., 1982) and C. moeu,usii (Coleman and Maguire, 1983). It has been proposed that a gene product of mt+ or a locus tightly linked to it causes the active destruction of plastid D N A from the mr- cells (Sager and Ramanis, 1973). Transmission of the paternal chloroplast genome is infrequent but may be increased by mutations in the nuclear genotype of the female (mr § parent

Mechanisms of Maternal Inheritance of Plastidr and Mitochondrm I99

(Gillham et al., 1974), and mutations in the rot- nuclear genotype or nutri- tional stress may decrease the ability of the paternal parent to transmit its chloroplast D N A (Sears et al., 1980) at even the normal low frequency (Adams, 1978). Furthermore, separate organelle inheritance mechanisms must be operating in Chlamydomonas. since the mitochondrial genome is inherited from the rot- parent, opposite to the transmission pattern of the plas- tome (Boynton et al., 1984).

E v i d e n c e F o r P r e - F e r t i l i z a t i o n D e b i l i t a t i o n o f P a t e r n a l

Organelles in Higher Plants Is post-syngamic destruction of organellar genomes a mechanism of maternal inheritance in other plant taxa? In plants where the chloroplasts or mitochondria from both parents are present in the zygote, such a mechanism would ensure that the paternally-derived organelles would be unable to replicate their D N A or maintain protein synthesis, so that they would rapidly degenerate and not contribute to the progeny phenotype. Vaughn et al. (1980) have suggested such an alternative hypothesis to the exclusion model in higher plants: that plastids and mitochondria of pollen are physically altered or debilitated during microporogenesis, so that they are unable to contribute to the progeny.

Plastids and mitochondria which have been observed in generative cells or sperm of higher plants are often described as being smaller than those in vegetative cytoplasm and "rudimentary" in appearance (Clauhs and Grun, 1977). As mentioned before, the lack of specialization and small size makes it difficult to distinguish plastids from mitochondria, but the presence of phytoferritin crystals or starch grains in plastids have allowed positive identification in some cases (Vaughn, 1981). In these cells, plastids are seen as electron dense with few lamellae (if any) (Jensen and Fisher, 1970; Clauhs and Grun, 1977, Russell and Cass, 1981; Vaughn, 1981) and sometimes contain the paracrystalline structures seen in vegetative etioplasts and senes- cent plastids (Russell and Cass, 1981). Mitochondria are often seen to be aggregated (Vaughn et al., 1980; Vaughn, 198 l), to show membrane altera- tions (Clauhs and Grun, 1977; Vaughn et al., 1980), and to "exhibit myelin- like figures" (Hagemann, 1979; Vaughn, 1981; Vaughn et al., 1981) and an "abnormal" cristae system (Jensen and Fisher, 1970; Vaughn, 198 l).

While such observations may be supportive of Vaughn's debilitation hypothesis, we must be careful to ask in each case whether such observations really represent debilitation, and not just transient &differentiation or reduction (perhaps due to a lack of significant current contribution to the metabo- lism of the cells) which may, however, leave the genomes intact (Thomas and Rose, 1983). A similar transient &differentiation of organelles is seen during


meiosis in both male (e.g., Bird et al., 1983) and female (e.g., Medina et al., 1981) meiocytes; micrographs of these dedifferentiated organelles bear a resemblance to those which have been called "degenerating" in studies of mature pollen. It may also be important to examine carefully whether "degenerating" organelles might in some of these studies be an artifact of prepar- ing pollen tubes outside their normal growth medium, the style (Jensen and Fisher, 1970).

The best evidence for pre-fertilization disabling of organellar genomes in higher plants comes from studies of cytoplasmic mutants in pollen-derived embryos. Plantlets derived from binucleate pollen and even from uninucleate pollen of some taxa display a high frequency of abnormalities such as albin- ism. Vaughn et al. (1980) investigated albino plantlets derived from pollen cultures of rice and found that the thylakoids were abnormal in appearance. Sun et al. (1979) investigated the biochemistry of such rice plantlets and discovered that they lacked the 23S and 16S ribosomal RNAs and the large subunit of ribulose bisphosphate carboxylase/oxygenase, all of which are products of the normal plastid genome. Similar aberrations in wheat plantlets regenerated from pollen were conclusively shown to be correlated with large deletion mutations in the plastid genome (Day and Ellis, 1984).

Mitochondrial aberrations have not been specifically reported in pollen- derived embryos, but this may be because non-lethal phenotypes for mitochondrial mutations are not well understood. As our comprehension of the coding functions of organellar genomes broadens, it may be that more organellar deletion mutants will be detected in pollen-derived embryos.

A C o n t i n u u m o f Var ia t ion F r o m St r ic t M a t e r n a l I n h e r i t a n c e Any mechanism proposed to account for maternal inheritance would have be able to account for the continuum of variation from this absolute (Sears, 1980); i.e., although the great majority of examined taxa do seem to show maternal inheritance in all cases, screening of high enough numbers of progeny of parents with suitable plastid or mitochondrial genetic markers might lead to the finding of more examples of paternal contribution at a low frequency (e.g., Medgyesy et al., 1986). Also, as mentioned before, some plants are generally biparental in cytoplasmic inheritance, and some are even paternal in inheritance pattern, with the maternal cytoplasmic contribution being masked or destroyed (Favre-Duchartre, 1957; Chesnoy, 1977). One of the most appealing aspects of the debilitation theory is that it gives a developmental mechanism for this departure from the norm: the system responsible for debilitation of male cytoplasmic components is controlled by products of genes expressed during reproductive maturation and may fail to operate if conditions occur during maturation (Van Winkle-Swift, 1978; Diets, 1971)

Mechanisms of Maternal Inheritance of Plastids and Mitochondria 201

which can destroy or inactivate their products, or if stochastic mutations occur to these genes which are favored by or at least not eliminated by selec- tion within certain taxa. It may be that "leaky" mutants can be isolated from among the paternally-inheriting progeny of plants with a low frequency of paternal transmission in order to examine regulation of this phenomenon.

In summary, it seems most appropriate to acknowledge that there may be many mechanisms explaining maternal inheritance, which may be derived from each other or which may arise independently in different taxa in response to the same or differing selectional forces and histories (Sears, 1980). One end of the continuum may be represented by species such as Pelargonium zonale, in which paternal plastids survive in the zygote but, instead of recombining, are sorted into homoplastic cell lines by an unknown mechanism correlated to the maternal genotype; another point may be represented by Chlamydomonas, where the paternal plastid survives but its genome is destroyed so that it cannot replicate; another is represented by Ulva mutabilis, where the plastid is destroyed following syngamy; yet another point would be presyngamic debilitation of the organelles, as evidenced by cytoplasmic mutants derived from pollen culture; and the other extreme in the continuum would be exclusion from the male gametes and ultimately from the generative cell. The same mechanism evidently may not always operate for both mitochondria and plas- rids in a given taxon (Vaughn et al., 1981; Boynton et al., 1984), lending further credence to the idea that these mechanisms may occur independently in response to different genetic constraints and selectional forces.

A c k n o w l e d g e m e n t s The author was supported by a training grant in Plant Reproductive Biology from the McKnight Foundation.

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