Control of plastid inheritance by environmental and genetic factors

Abstract

The genomes of cytoplasmic organelles (mitochondria and plastids) are maternally inherited in most eukaryotes, thus excluding organellar genomes from the benefits of sexual reproduction and recombination. The mechanisms underlying maternal inheritance are largely unknown. Here we demonstrate that two independently acting mechanisms ensure maternal inheritance of the plastid (chloroplast) genome. Conducting large-scale genetic screens for paternal plastid transmission, we discovered that mild chilling stress during male gametogenesis leads to increased entry of paternal plastids into sperm cells and strongly increased paternal plastid transmission. We further show that the inheritance of paternal plastid genomes is controlled by the activity of a genome-degrading exonuclease during pollen maturation. Our data reveal that (1) maternal inheritance breaks down under specific environmental conditions, (2) an organelle exclusion mechanism and a genome degradation mechanism act in concert to prevent paternal transmission of plastid genes and (3) plastid inheritance is determined by complex gene–environment interactions.

Unveiling the Mysteries of Non-Mendelian Heredity in Plant Breeding

“…Gene-environment interaction is one of the most important factors in plant breeding areas when the expression of a gene is influenced by the environment [ 11 , 12 ]. In plant breeding, environmental factors can play a role in the expression of complex traits such as yield [ 13 ].…”

“…For example, a plant grown in a hot and dry climate may have a different yield than the same plant grown in a cooler climate [ 14 ]. Gene–gene interaction is a phenomenon in which two or more genes interact with each other to produce a phenotype that is different from the effect of either gene alone [ 11 ]. In plant breeding, non-Mendelian traits can be transmitted through gene–gene interactions, either through epistatic (complex) interactions between genes, or through the action of regulators of gene expression [ 8 , 9 , 11 ].…”

“…Gene–gene interaction is a phenomenon in which two or more genes interact with each other to produce a phenotype that is different from the effect of either gene alone [ 11 ]. In plant breeding, non-Mendelian traits can be transmitted through gene–gene interactions, either through epistatic (complex) interactions between genes, or through the action of regulators of gene expression [ 8 , 9 , 11 ]. In addition, gene–gene interactions can play a role in the control of gene expression, allowing the expression of non-Mendelian traits to be modulated [ 11 ].…”

“…In plant breeding, non-Mendelian traits can be transmitted through gene–gene interactions, either through epistatic (complex) interactions between genes, or through the action of regulators of gene expression [ 8 , 9 , 11 ]. In addition, gene–gene interactions can play a role in the control of gene expression, allowing the expression of non-Mendelian traits to be modulated [ 11 ]. Epigenetics, which deals with the regulation of gene expression without changing the underlying DNA sequence, can affect the expression of traits, and may be inherited in the same way as non-Mendelian traits [ 11 , 15 ].…”

Characterizing conflict and congruence of molecular evolution across organellar genome sequences for phylogenetics in land plants

“…Indeed, there are many plant lineages in which biparental inheritance of at least one organelle is common and also those in which mitochondrial genomes and plastomes are usually inherited from different parents ( Mogensen, 1996 ; Camus et al., 2022 ). There has also been recent evidence that patterns of biparental inheritance may vary with environmental conditions in some taxa ( Chung et al., 2023 ).…”