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

Alexander I Macleod,Simon Stockhorst,Sven B Gould,Parth K Raval,Eftychios Frangedakis,Michael R Knopp

doi:10.3389/fpls.2022.863076

Alexander I Macleod, Simon Stockhorst + Show 4 more

Open Access

https://doi.org/10.3389/fpls.2022.863076

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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.

Highlights

Hornworts are a unique group of bryophytes, the monophyletic non-vascular sister lineage to all vascular land plants (Harris et al, 2020)
We argue that the major changes in plastid biology, that coincided with major checkpoints in the evolutionary history of hornworts and facilitated them, are a consequence of multiple instances of gene loss observed in this unique group of embryophytes
We found that the gene content of hornworts is significantly lower than tracheophytes and other bryophytes (ANOVA; F = 129.5; d.f. = 2,30; p < 0.001), thereby suggesting that hornwort diversification and speciation were accompanied by significant instances of gene loss (Supplementary Figure 2), even more than what is observed for bryophytes in general (Harris et al, 2021)

Summary

INTRODUCTION

Hornworts are a unique group of bryophytes, the monophyletic non-vascular sister lineage to all vascular land plants (Harris et al, 2020). We screened the genomes and annotated transcriptomes of ten hornwort species to identify the presence/absence of genes that play key roles in regulating plastid development, such as those involved in protein import into the chloroplast, thylakoid biogenesis, and chloroplast division (Jarvis and López-Juez, 2013). We analyzed the genomes and transcriptomes of ten hornworts, along with the genomes of Arabidopsis thaliana and Marchantia polymorpha, to determine the presence of various components involved in plastid development (Lamesch et al, 2012; Bowman et al, 2017; Leebens-Mack et al, 2019; Li et al, 2020; Zhang et al, 2020; Supplementary Table 2) These orthology clusters (orthogroups) were identified using the OrthoFinder version 2.5.4 software (Emms and Kelly, 2015, 2019; Supplementary Table 2). ARC3 is part of the FtsZ family and unites an FtsZ domain with a C-terminal MORN domain (Zhang et al, 2013)

DISCUSSION

Findings

CONCLUSION AND OUTLOOK

DATA AVAILABILITY STATEMENT