Clade-Specific Plastid Inheritance Patterns Including Frequent Biparental Inheritance in Passiflora Interspecific Crosses

Plastid inheritance in angiosperms is presumed to be largely maternal, with the potential to inherit plastids biparentally estimated for about 20% of species. In Passiflora, maternal, paternal and biparental inheritance has been reported; however, these studies were limited in the number of crosses and progeny examined. To improve the understanding of plastid transmission in Passiflora, the progeny of 45 interspecific crosses were analyzed in the three subgenera: Passiflora, Decaloba and Astrophea. Plastid types were assessed following restriction digestion of PCR amplified plastid DNA in hybrid embryos, cotyledons and leaves at different developmental stages. Clade-specific patterns of inheritance were detected such that hybrid progeny from subgenera Passiflora and Astrophea predominantly inherited paternal plastids with occasional incidences of maternal inheritance, whereas subgenus Decaloba showed predominantly maternal and biparental inheritance. Biparental plastid inheritance was also detected in some hybrids from subgenus Passiflora. Heteroplasmy due to biparental inheritance was restricted to hybrid cotyledons and first leaves with a single parental plastid type detectable in mature plants. This indicates that in Passiflora, plastid retention at later stages of plant development may not reflect the plastid inheritance patterns in embryos. Passiflora exhibits diverse patterns of plastid inheritance, providing an excellent system to investigate underlying mechanisms in angiosperms.

The monoplastidic bottleneck in algae and plant evolution

Plant and algae plastids evolved from the endosymbiotic integration of a cyanobacterium by a heterotrophic eukaryote. A consequence of their ancestry is that new plastids can only emerge through fission and vital to organelle and host co-evolution was the early synchronization of bacterial division with the host’s eukaryotic cell cycle. Most of the sampled algae, including multicellular macroalgae, house a single plastid per cell — or nucleus in case of coenocytic cells — and basal branching relatives of polyplastidic lineages are all monoplastidic. The latter is also true regarding embryophytes, as some non-vascular plants are monoplastidic at least at some stage of their life cycle. Here we synthesize recent advances regarding plastid division and associated proteins, including those of the peptidoglycan wall biosynthesis, across the diversity of phototrophic eukaryotes. Through the comparison of the phenotype of 131 species harbouring plastids of primary or secondary origin, we uncover that one prerequisite for an algae or plant to house multiple plastids per nucleus appears the loss of the genes MinD and MinE from the plastid genome. Housing a single plastid whose division is coupled to host cytokinesis appears a prerequisite of plastid emergence; escaping that monoplastidic bottleneck succeeded rarely and appears tied to evolving a complex morphology. Considering how little we know about the mechanisms that guarantee proper organelle (and genome) inheritance raises the peculiar possibility that a quality control checkpoint of plastid transmission remains to be explored and which is tied to understanding the monoplastidic bottleneck.

Plastome-genome interactions affect plastid transmission in Oenothera.

Plastids of Oenothera, the evening primrose, can be transmitted to the progeny from both parents. In a constant nuclear background, the frequency of biparental plastid transmission is determined by the types of plastid genomes (plastomes) involved in the crosses. In this study, the impact of nuclear genomes on plastid inheritance was analyzed. In general, the transmission efficiency of each plastome correlated strongly with its compatibility with the nuclear genome of the progeny, suggesting that plastome-genome interactions can influence plastid transmission by affecting the efficiency of plastid multiplication after fertilization. Lower frequencies of plastid transmission from the paternal side were observed when the pollen had poor vigor due to an incompatible plastome-genome combination, indicating that plastome-genome interactions may also affect the input of plastids at fertilization. Parental traits that affect the process of fertilization can also have an impact on plastid transmission. Crosses using maternal parents with long styles or pollen with relatively low growth capacity resulted in reduced frequencies of paternal plastid transmission. These observations suggest that degeneration of pollen plastids may occur as the time interval between pollination and fertilization is lengthened.

Nuclear gene induced plastid alterations in Pennisetum americanum

A nonlethal stripe mutant (700430) of Pennisetum americanum was crossed reciprocally with other normal inbred lines to establish its inheritance pattern. A recessive nuclear gene, when homozygous, led to defective plastid development with variable penetrance and expressivity. Intraplant and interspikelet crosses revealed maternal plastid transmission. When stripe plants were crossed with pollen from normal inbreds, green and yellow progeny were obtained; selfing stripe plants or crossing with its green sib produced yellow, stripe, and green progeny. These results suggest that in egg cells with exclusively defective plastids, the plastids do not revert back inspite of acquiring a dominant allele from the pollen parent, while in egg cells with a mixture of green and yellow plastids, the yellow plastids could develop into functional plastids under the influence of a dominant allele.Key words: altered plastids, variable penetrance, plastid transmission, plastid reversion.

AN IRREVERSIBLE GENE-INDUCED PLASTID MUTATION

When plants of a variegated barley are self-pollinated, they produce few variegated and many albino offspring. In different years the proportion of albino plants has ranged from 80.2 to 93.1% of the total population. Seed from heads having much green tissue gave rise to a much larger proportion of variegated plants than did seed from heads with more white tissue. Maternal inheritance of plastids is probably the cause of this difference. In crosses F1 plants are green, variegated, or albino if the ♂ parent is variegated, but if the ♂ parent is green all the progeny are green. The albino plastids thus apparently do not mutate back to normal in the presence of the normal gene. In some F2 populations deviation from a ratio of 3 green: 1 others is insignificant, in other populations significant deviations, attributed to irregularities of plastid mutation and segregation, occur. F3 results support the hypothesis that a single pair of genes affecting plastids is segregating in hybrids. The normal (green) gene is dominant if "green" proplastids are present in the egg but not dominant if the proplastids are all "white". From cytological observations on sperms and eggs as well as from the genetic results, it is considered likely that direct plastid transmission to zygotes is exclusively from the female parent.