Biparental plastid inheritance and its implications in plastid genome engineering

This review discusses the mechanism of the inherirance of plastids (and other organelles), where maternal inhertiance is predominat. This inheritance can be shifted to be biparental by modulating genetic and environmental factors, which can have implications in plant fitness and plastid genome engneering to attain homoplastomic plants in fewer generations. In most plant species, plastids (and mitochondria) are inherited maternally, a mode of transmission that ensures cytoplasmic and genetic compatibility, thereby supporting plant fitness. However, in certain species, plastids (and mitochondria) can be inherited from both parents, a phenomenon known as biparental plastid inheritance (BPI), which occurs in approximately 20% of angiosperms. In maternal inheritance, these organelles are excluded during male gametogenesis, probably through genetically regulated selective degradation of the organelle genome and other cytoplasmic components from the generative cell (GC) of pollen grains. Environmental factors like temperature also influence this process. While maternal plastid inheritance has been studied extensively, the mechanisms and significance of BPI remain comparatively underexplored. Recent studies showed that modulation of either of the genes involved or temperature conditions during pollen development results in the inheritance of cytoplasm, including plastids from pollen cells, promoting biparental inheritance of plastids (and likely of mitochondria) in plants. Our review discusses the role and evolutionary relevance of BPI, addressing why it is an uncommon yet vital mechanism in plants. An emphasis is given on the mechanisms of maternal inheritance, and on how modulation of genetic and environmental factors can achieve BPI. Furthermore, we underscore the significance of BPI, particularly in producing homoplasmic transplastomic plants with broad applications in agriculture and synthetic biology.