Lose it or keep it: (how bivalves can provide) insights into mitochondrial inheritance mechanisms

Abstract

The strictly maternal inheritance (SMI) is a pattern of mitochondrial inheritance observed across the whole animal kingdom. However, some interesting exceptions are known for the class Bivalvia, in which several species show an unusual pattern called doubly uniparental inheritance (DUI) whose outcome is a heteroplasmic pool of mtDNA in males. Even if DUI has been studied for long, its molecular basis has not been established yet. The aim of this work is to select classes of proteins known to be involved in the maintenance of SMI and to compare their features in two clam species differing for their mitochondrial inheritance mechanism, that is, the SMI species Ruditapes decussatus and the DUI species Ruditapes philippinarum. Data have been obtained from the transcriptomes of male and female ripe gonads of both species. Our analysis focused on nucleases and polymerases, ubiquitination and ubiquitin-like modifier pathways, and proteins involved in autophagy and mitophagy. For each protein group of interest, transcription bias (male or female), annotation, and mitochondrial targeting (when appropriate) were assessed. We did not find evidence supporting a role of nucleases/polymerases or autophagic machinery in the enforcement of SMI in R. decussatus. On the other hand, ubiquitinating enzymes with the expected features have been retrieved, providing us with two alternative testable models for mitochondrial inheritance mechanisms at the molecular level.

Putative Mitochondrial Sex Determination in the Bivalvia: Insights From a Hybrid Transcriptome Assembly in Freshwater Mussels

“…Their analysis of gonad transcriptomes focused on nucleases and polymerases, ubiquitination, and proteins involved in autophagy/mitophagy. Their results provided no evidence for a role of nucleases/polymerases or autophagic machinery in the enforcement of SMI in R. decussatus , but transcripts of ubiquitinating enzymes were retrieved, providing additional support to previous transcriptomic studies (Punzi et al, 2018).…”

“…For example, paternal mtDNA can be eliminated by a nuclease-mediated mechanism either during spermatogenesis or after fertilization, or paternal mitochondria can be selectively degraded by autophagy after fertilization (Sato and Sato, 2017). To better understand the molecular basis of DUI, Punzi et al (2018) selected classes of proteins known to be involved in the maintenance of SMI and compared their features in two closely-related gonochoric clam species differing in their mitochondrial inheritance mechanism, that is, the SMI species Ruditapes decussatus and the DUI species R. philippinarum . Their analysis of gonad transcriptomes focused on nucleases and polymerases, ubiquitination, and proteins involved in autophagy/mitophagy.…”

Mitochondria and Their Role in Human Reproduction

“…In Caenorhabditis elegans, autophagy appears to contribute to paternal mitochondrial degradation after fertilization, and sperm-derived mitochondria cannot be detected after the 16-cell embryo stage Sato, 2011, 2018;Punzi et al, 2018). Within minutes of fertilization, autophagosomes triggered by the penetration of sperm components begin to accumulate around sperm mitochondria.…”

“…In cows, mice, and other mammals, ubiquitin also appears to be a major player in activating paternal mitochondrial elimination (Sato and Sato, 2013;Punzi et al, 2018). Membrane proteins carried by sperm mitochondria are ubiquitinated before fertilization and disappear by the 4-cell to 8-cell embryo stage (Sutovsky et al, 1999).…”

“…Moreover, ubiquitinated proteins on the inner membrane of sperm mitochondria migrate to the outer membrane where they are exposed to ubiquitination machinery after fertilization. Positive feedback promotes more ubiquitination, and, eventually, paternal mitochondria are destroyed by the collaborative actions of proteasomes and autophagous lysosomes (Punzi et al, 2018).…”