University of Maryland

Further evidence for the maternal inheritance of plastids

--Joseph L. Corriveau

Geneticists seeking to manipulate plastid genome-encoded traits need to know the mode of plastid inheritance for their respective plant species of interest. Genetic evidence is available describing the mode of plastid transmission for only about 60 genera of angiosperms (see reviews by Sears, Plasmid, 4:233, 1980; Smith, Plant Breed. Rev. 6:361, 1988). For the majority of these species, including maize, plastids appear to be maternally inherited.

Recently, further evidence for the maternal inheritance of plastids in maize was reported by Corriveau and Coleman (Amer. J. Bot. 75:1443, 1988). Using the DNA fluorochrome DAPI in conjunction with epifluorescence microscopy, Corriveau and Coleman examined the generative and/or sperm cells of pollen from 235 plant species, including maize, for the presence or absence of detectable plastid DAPI-DNA aggregates. Species were scored as potentially capable of biparental plastid transmission if plastid DNA was detected in the male reproductive cells. Conversely, species were scored as being maternal for plastid transmission if no plastid DNA was detected. There was a striking correlation between the known genetic and new cytological evidence for the mode of plastid transmission for 42 of the species examined. Plastid DNA was detected in the cytoplasm of generative and/or sperm cells of pollen from 13 species known genetically to be biparental for plastid transmission, but no plastid DNA was detected in the male reproductive cells of pollen from 29 species known genetically to display maternal inheritance. Plastid DNA was not detected in the sperm cells of over 500 mature pollen grains of maize inbred line B37 examined using this novel cytological methodology.

Although there is now genetic (Anderson, Bot. Gaz. 76:411, 1923), molecular genetic (Conde et al., J. Hered. 70:2, 1979), and cytological (Corriveau and Coleman, 1988) evidence for maternal inheritance of plastids in maize, there is precedent for the possibility that trace biparentalism may still be detected in the genus Zea. For example, there is now evidence for trace biparental transmission of plastids for petunia (Cornu and Dulieu, J. Hered. 67:40, 1988), tobacco (Medgyesy et al., Mol. Gen. Genet. 204:195, 1986), Epilobium (Schmitz and Kowallik, Curr. Genet. 11:1, 1985), and Pisum (Corriveau et al., Pisum Newsl. 20:5, 1988), genera previously thought to be maternal for plastid transmission. Perhaps previous analyses of plastid inheritance in maize did not take into consideration the possibility of paternal plastids being contributed to progeny at a very low frequency. An additional consideration is the possibility of genetic variability for plastid transmission patterns within the genus Zea. Such genetic variability is known to exist and has been genetically analyzed in Oenothera (Chiu et al., Curr. Genet. 13:181, 1988) and Pelargonium (Tilney-Bassett and Birky, Theor. Appl. Genet. 60:43, 1981). The novel DNA fluorochrome/epifluorescence microscopy protocol used by Corriveau and Coleman to screen pollen from 235 plant species could be used to screen pollen samples rapidly from maize accessions for potential biparental plastid in-heritance. If biparentalism is to be detected within the genus Zea, one may expect to find it amongst uncultivated accessions because early maize breeders may have unknowingly selected for maternal inheritance of plastids.

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