Molecular basis of plastid inheritance

“How is genetic material inherited?” This is one of the fundamental questions in biology. Although the inheritance of nuclear genes is nicely described by Mendelian laws, the underlying mechanisms that regulate the transmission of plastid and mitochondrial genomes are still poorly understood.
Molecular basis of plastid inheritance

Plastid: A Multifunctional Entity in Plant Cells

Plastids stand out as one of the most intriguing organelles within plant cells. These versatile entities can transform into various specialized forms, each serving a specific function. For instance, plastids can differentiate into amyloplasts, specialized compartments responsible for storing starch and sensing gravity or undergo conversion into chromoplasts, which impart the red color to tomato fruits. Perhaps the most familiar form of plastid is the chloroplast, containing chlorophyll crucial for photosynthesis. Given these diverse functions, research on plastids remains a focal point in plant biology.

Remarkably, plastids were initially alien entities within early eukaryotic cells. According to the endosymbiosis theory, plastids were once free-living cyanobacteria captured by eukaryotes.  Over millions of years of evolution, most plastid genes were lost or transferred to the nuclear genome, yet certain genes essential for photosynthesis and metabolism are retained in plastids. Consequently, plastid genomes exert a significant impact on plant growth and development.

Non-Mendelian Inheritance of Plastid Genomes

While both the nuclear and plastid genomes are essential for plant survival, the inheritance of these genomes is subject to different sets of rules. In sexual reproduction, nuclear genes are inherited from both parents. Strikingly, plastid genomes are almost exclusively transmitted from the mother in most flowering plants. There are exceptions to the predominant maternal inheritance pattern; for instance, in gymnosperms like the Douglas fir, plastids are inherited from the father. In the case of evening primrose, plastids are passed down from both the mother and the father. 

Mechanisms of Plastid Inheritance

In 1909, Erwin Baur and Carl Correns reported the very first cases of non-Mendelian inheritance and laid the foundation for plastid inheritance research. Despite its long-standing recognition, the underlying mechanisms governing plastid inheritance have remained elusive. The challenge in plastid inheritance research stems from the lack of established research methodologies. Only with recent breakthroughs in genome editing do we now have the opportunity to re-examine this significant yet understudied topic.

In our group, we study plastid inheritance in the model plant species Nicotiana tabacum, commonly known as tobacco. Previous studies on tobacco pollen development have indicated that plastids are predominantly excluded from male gametes, thereby preventing the transmission of paternal plastids. We hypothesized that environmental stresses during pollen development might compromise this plastid exclusion mechanism, potentially resulting in altered plastid inheritance patterns. Through extensive screening efforts involving millions of plants conducted by both former and current lab members, we successfully identified an abiotic factor (temperature) that governs the mode of plastid inheritance. Specifically, when the pollen is developed under cold conditions, we observed a higher proportion of plastids being included in male gametes (Video 1). Consequently, this increased the likelihood of transmitting paternal plastids to the progeny.

Video 1. Time-lapse confocal imaging of a germinating pollen tube derived from cold-stressed transplastomic plants. Mature pollen was harvested from the cold-stressed transplastomic plants expressing fluorescent protein DsRed in plastids, followed by in vitro pollen germination and staining with SYTO11, a nucleic acid-binding dye. The generative cell nucleus (GCN) within the growing pollen tube is visualized by green SYTO11 fluorescence. Paternal plastids (arrowhead, magenta) are closely associated with the GCN and enclosed by the generative cell membrane. Consequently, these plastids display similar movement dynamics as the GCN. By contrast, plastids outside of the generative cell (asterisk) display a much more rapid movement due to intense cytoplasmic streaming in the growing tube. 

The initial success of our experiments has motivated us to expand our investigation, with the objective of identifying additional mechanisms that govern plastid inheritance. One notable cellular process we are exploring is the degradation of cytoplasmic genomes in male gametes. In tobacco, we have observed the active elimination of plastid genomes in mature pollen, rendering the transmission of paternal plastid genomes impossible.

Inspired by a study conducted in Arabidopsis thaliana (Matsushima et al. 2011), we explored the potential role of the exonuclease DPD1 in plastid inheritance. DPD1 exhibits specific expression in male gametes and is responsible for degrading plastid DNA in maturing pollen. Our hypothesis posited that a retention of plastid DNA would occur in dpd1 mutant pollen, facilitating the transmission of paternal plastid genomes. To test this hypothesis, we generated a tobacco dpd1 knock-out mutant and assessed its impact on plastid inheritance (Fig. 1). Excitingly, we observed an elevated rate of paternal plastid transmission when dpd1 mutants were used as pollen donors, affirming that DPD1 indeed plays a regulatory role in plastid inheritance.

Fig. 1. Confocal image of a dpd1 mature pollen. DAPI staining was performed to visualize both nuclear and cytoplasmic DNA. The arrowheads indicate the vegetative (hollow) and generative (filled) nucleus respectively. Numerous DAPI punctate signals are observed in the cytosol (arrow), suggesting the retention of cytoplasmic DNA in dpd1 mature pollen. Scale bar = 10 μm.

Broader Implications

Through our study, we discovered that plastids are passed from father plants more frequently than previously assumed. The inheritance mode of plastid can be altered by manipulating the growth conditions or the genetic background of the father plants. Our research thus supports the emerging notion that plastid inheritance should be described as a quantitative trait rather than a categorical one. Moreover, we have revealed the impact of temperature on the inheritance mode, providing insights into how climate change might influence plastid inheritance. Specifically, our findings indicate that low temperatures enhance the transmission of plastid genomes through pollen. This prompts a re-evaluation of the environmental risk assessment of genetically modified organisms, as the containment of transgenes through maternal inheritance may not be as stringent as previously believed.

Additionally, an increasing number of studies have acknowledged the potential of cytoplasmic genomes in improving crop traits. Our fundamental research in plastid inheritance serves to advance our understanding of cytoplasmic genetics. This knowledge will enable the deliberate manipulation of cytoplasmic inheritance, with the overarching goal of contributing to the development of innovative approaches in crop breeding.

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Plant Genetics
Life Sciences > Biological Sciences > Plant Science > Plant Genetics
Life Sciences > Biological Sciences > Cell Biology > Organelles
Life Sciences > Biological Sciences > Cell Biology > Organelles > Chloroplasts
Plant Breeding
Life Sciences > Biological Sciences > Genetics and Genomics > Agricultural Genetics > Plant Breeding
Plant Science
Life Sciences > Biological Sciences > Plant Science
Genome Evolution
Life Sciences > Biological Sciences > Genetics and Genomics > Genomics > Genome > Genome Evolution