Loss of Plastid Developmental Genes Coincides With a Reversion to Monoplastidy in Hornworts

Abstract

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 independently 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. In this study, we screened genomic and transcriptomic data of eleven hornworts for components of plastid developmental pathways. We found 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. Our results also confirmed that hornworts underwent significant instances of gene loss, underpinning that the gene content of this group is significantly lower than other bryophytes and tracheophytes. 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, namely, ARC3 and FtsZ2.

A Comparative Physiological Perspective on UV RESISTANCE LOCUS 8 Signalling in Green Plants

“…HY5's absence in these two species could be the result of a genome/transcriptome annotation error (Cheon et al, 2020). However, hornwort emergence and diversification were accompanied by major instances of gene loss (MacLeod et al, 2022), so HY5's absence in A. punctatus and L. dussii could be explained by this phenomenon.…”

“…However, whether UVR8 signalling is conserved in hornworts is unknown as the lack of experimental data prevent this question from being answered. However, data from phylogenomic analyses (MacLeod et al, 2022) indicate that orthologues for core UVR8 components are found in most hornworts; with the exception of Anthoceros punctatus (Bonn ecotype) and Leiosporoceros dussii, which appear to have differentially lost HY5. HY5's absence in these two species could be the result of a genome/transcriptome annotation error (Cheon et al, 2020).…”

What can hornworts teach us?

“…Interestingly, some of the unique hornwort characters vary even between different families. For example, the number of chloroplasts per cell or the presence of pyrenoids, stomata and arbuscular mycorrhizal symbiosis ( Villarreal and Renner, 2012 ; Desiro et al., 2013 ; Frangedakis et al., 2021a ; MacLeod et al., 2022 ) ( Figure 3B ). Thus, comparative studies within hornworts can help identify the genetic mechanisms that control these characters.…”

“…This smaller gene repertoire, together with lineage-specific gene losses, provides a useful avenue to investigate their role in polyplastidy evolution. There have also been losses of plastid-related genes specifically within hornworts ( MacLeod et al., 2022 ). Most notable in this regard are the distributions of Accumulation and Replication of Chloroplasts 3 ( ARC3 ) and the Filamentous Temperature Sensitive Z (FtsZ) gene family ( FtsZ 1, 2 and 3 ) in hornworts.…”

“…P. patens (though this may be compensated for by a MinC -like gene) ( Miyagishima et al., 2011 ; Osteryoung and Pyke, 2014 ). Crucially, all hornworts analyzed thus far only possess a copy of FtsZ1 and FtsZ3 , that is, they lack FtsZ2 , and have lost ARC3 ( MacLeod et al., 2022 ). ftsZ2 and arc3 mutants in A. thaliana and P. patens have impaired chloroplast division dynamics, displaying extreme phenotypes of large, misshapen chloroplasts ( Martin et al., 2009 ; Schmitz et al., 2009 ; Zhang et al., 2013 ).…”