Loss of plastid developmental genes coincides with a reversion to monoplastidy in hornworts

The first plastid evolved from an endosymbiotic cyanobacterium in the common ancestor of the Archaeplastida. The transformative steps from cyanobacterium to organelle included the transfer of control over developmental processes; a necessity for the host to orchestrate, for example, the fission of the organelle. The plastids of almost all embryophytes divide independent from nuclear division, leading to cells housing multiple plastids. Hornworts, however, are monoplastidic (or near-monoplastidic) and their photosynthetic organelles are a curious exception among embryophytes for reasons such as the occasional presence of pyrenoids. Here we screened genomic and transcriptomic data of eleven hornworts for components of plastid developmental pathways. We find intriguing differences among hornworts and specifically highlight that pathway components involved in regulating plastid development and biogenesis were differentially lost in this group of bryophytes. In combination with ancestral state reconstruction, our data suggest that hornworts have reverted back to a monoplastidic phenotype due to the combined loss of two plastid division-associated genes: ARC3 and FtsZ2.

TIC236 gain-of-function mutations unveil the link between plastid division and plastid protein import

The chloroplast translocons TOC75 and TIC236 are homologs of the bacterial translocation and assembly module (Tam) A and TamB involved in protein export. Here, we unveil a TIC236-allied component, the chloroplast outer membrane protein CRUMPLED LEAF (CRL), absence of which impairs plastid division and induces autoimmune responses in Arabidopsis thaliana. A forward genetic screen aimed at finding crl suppressors revealed multiple TIC236 gain-of-function mutations (TIC236GFs). Despite the low sequence identity between TIC236 and bacterial TamB, each mutated TIC236GF residue is conserved in TamB. Consistently, a tic236-knockdown mutant exhibited multiple lesion phenotypes similar to crl, indicating a shared functionality of CRL and TIC236. Ensuing reverse genetic analyses revealed genetic interaction between CRL and SP1, a RING-type ubiquitin E3 ligase, as well as with the plastid protease FTSH11, which function in TOC and TIC protein turnover, respectively. Loss of either SP1 or FTSH11 rescued crl mutant phenotypes to varying degrees due to increased translocon levels. Consistent with impaired plastid division exhibited by both crl and tic236-knockdown mutants, CRL interacts with the transit peptides of proteins essential in plastid division, and TIC236GF mutant proteins reinforce their import via increased TIC236 stability. Overall, our data shed new light on the links between plastid division, plant stress response and plastid protein import. We have also isolated and characterized the first GF mutants exhibiting increased protein import efficiency, which may inspire chloroplast engineering for agricultural advancement.

The Ringleaders: Understanding the Apicomplexan Basal Complex Through Comparison to Established Contractile Ring Systems

The actomyosin contractile ring is a key feature of eukaryotic cytokinesis, conserved across many eukaryotic kingdoms. Recent research into the cell biology of the divergent eukaryotic clade Apicomplexa has revealed a contractile ring structure required for asexual division in the medically relevant genera Toxoplasma and Plasmodium; however, the structure of the contractile ring, known as the basal complex in these parasites, remains poorly characterized and in the absence of a myosin II homolog, it is unclear how the force required of a cytokinetic contractile ring is generated. Here, we review the literature on the basal complex in Apicomplexans, summarizing what is known about its formation and function, and attempt to provide possible answers to this question and suggest new avenues of study by comparing the Apicomplexan basal complex to well-studied, established cytokinetic contractile rings and their mechanisms in organisms such as S. cerevisiae and D. melanogaster. We also compare the basal complex to structures formed during mitochondrial and plastid division and cytokinetic mechanisms of organisms beyond the Opisthokonts, considering Apicomplexan diversity and divergence.

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.