Organelle inheritance in plants

Received 1 June 1993 Heredity72 (1994)132—140 Genetical Society of Great Britain Organelle inheritance in plants XAVIER REBOUDI & CLIFFORD ZEYL* Laboratofre d'Evolution et Systematique des Végétaux, Sâtiment 362, Université Paris Süd, 91405 Orsay CEDEX, France and [Department of Biology, McGill University, 1205 A venue Docteur Pen field, Montréal, Québec, Canada H3A 1B1 Most angiosperms are thought to share strict maternal inheritance of both plastids and mitochondria. Exceptions have been described and analysed, especially for plastids. However, the lack of phenotypic markers and the use of RFLPs on small samples may have biased the prevailing view of organelle inheritance by underestimating the occurrence of low-frequency paternal transmission of organelles. According to Muller's Ratchet, some recombination among organelle genomes is required, which would necessitate at least occasional biparental transmission. Uniparental inheritance can reduce the spread of selfish genetic elements and maintain good combinations of alleles. However, this does not explain why organelles transmitted by both parents have not invaded populations with uniparental inheritance. A link between outcrossing reproductive systems and the occurrence of biparental transmission suggests that plastids may play more of a genetic role in their inheritance than is usually assumed. Their prevailing non-Mendelian mode of inheritance thus remains to be convincingly explained. Keywords: chloroplasts, intracellular conflict, non-Mendelian inheritance, organelle transmission, reproductive systems. Introduction Organelle inheritance in most plants is purely maternal, with just enough exceptions to produce a substantial body of literature on the topic. Our view of organelle inheritance patterns has changed in response to ad- cal approaches. The advantages and disadvantages of these three approaches are summarized in Table 1. Because the disadvantages of one technique can often be overcome by the use of another, recent studies often combine approaches. However, we think that technical limitations have influenced prevailing views of organ- vances in research techniques. However, the predominance of uniparental organelle inheritance has yet to be convincingly explained. In this paper, we summarize the impact of methodology on present knowledge of organelle inheritance. We then review known mechanisms of organelle inheritance and discuss evolutionary explanations of inherit- elle inheritance in at least four ways. ance patterns which suggest new experimental described. This may reflect either inherent differences between these organelles or the lack of mitochondrial phenotypic markers. approaches. Impact of methodology on present knowledge Interest in organelle inheritance was aroused only 10 1 The inheritance of mitochondria is an almost untouched topic and is still too often ignored. Only six cases in which mitochondrial inheritance is not strictly maternal have been discovered, two of these by the use of interspecific crosses (Table 2), in contrast to plastids for which more than 40 such cases have been 2 Crop and ornamental plant species are overrepresented relative to wild species (see Table 3). This impedes attempts to understand the evolutionary reasons for inheritance patterns as changes in these 1909). The study of organelle inheritance began patterns may be by-products of domestication, such as selection on reproductive systems (e.g. male sterility) or popular of which remains chlorophyll deficiency) and has recently been extended by molecular and cytologi- changes in plastome—genome interaction resulting from hybridization. This is particularly unfortunate as the DNA polymorphisms required by molecular tech- *Correspondence. niques are probably more abundant in wild plants than in cultivated plants. years after the rediscovery of Mendel's laws (Correns, with the use of phenotypic markers (the most ORGANELLE INHERITANCE IN PLANTS 133 Table 1 Advantages and disadvantages of three major approaches to the study of organelle inheritance in plants Method Advantages Disadvantages Phenotypic markers Very large samples can be screened Few markers exist Selective screening sometimes possible (e.g. resistance to herbicides (Gasquez et a!., 1981) or to antibiotics (Medgyesy etL 1986)) Restricted to plastids Requires minimal equipment or materials and thus accessible to most labs Spontaneous mutations, alteration in chimeral shoots, and restitution of mutant plastids may affect estimated transmission frequencies Greatly increases number of potential markers Expensive and laborious, thus restricting sample sizes and possibly preventing detection of low frequency paternal inheritance; also, biased towards species of economic interest Molecular techniques Permits analysis of mitochondrial as well as chloroplast inheritance Origin of organelle DNA can be indisputably determined, so alternative explanations for apparent paternal transmission can be eliminated Markers may not be neutral, affecting inferred inheritance patterns Requires DNA polymorphism; where intraspecific polymorphism is absent, interspecific crosses are required and novel plastome—genome interactions may induce atypical inheritance (Sundberg & Glimelius, 1991; Chiu & Sears, 1993) RFLP techniques insensitive to minute amounts of DNA, precluding analysis of heteroplasmy, which requires PCR Cytology Restricted to few individuals or genotypes, so may be misleading when generalized Easily mastered Applicable to a large range of species Informative regarding mechanisms and stages of organelle exclusion Presence of plastids in sperm cells does not indicate their inclusion in the zygote, which is usually the question of interest Requires no markers Table 2 Species in which inheritance of mitochondria is not strictly maternal. In such species, plastid inheritance is also frequently not strictly maternal. References include methods of analysis (M;R), abbreviated as in Table 3 except for Brassica napus, in which maternal inheritance of the mitochondrial genome was inferred from the inheritance of a mitochondrial plasmid Species Reference Brassica napus Calocedrus decurrens Hordeum vulgare X Secale cereale Petunia hybrida Erickson eta!. (1989) Neale eta!. (1991) Soliman eta!. (1987) Derepas (1991) (M;R) Wagner eta!. (1991) (R) Neale eta!. (1989) (R) Pinus banksiana x contorta Sequoia sempervirens Acacia decurrens (C) Acacia mearnsii (C) Antirrhinum majus (M) Borago officinalis (M) Browallia speciosa(M) Chenopodium album (M) Chiorophytum comosum (M) Chiorophytum datum (M) Epilobium angustifolium (M, R) Impatiensglandulifera (C) Ipomoea nil(C) Melilotus alba (C) Melilotus officinalis (C) Oiyzasativa (malesterile) (R) Petunia hybrida (M, R) I'lumbago zeylanica(C) Poa annua (M) Rhododendron (11 spp,) Silenepseudotites Beta vulgaris (C, M) Helianthus annus (M) Lolium perenne (C) Phleum pralense (C) Prunus (...truncated)