Fig. 4.

The appearance of mitochondrial retrograde regulators during the evolution of land plants. Eukaryotes are thought to have evolved by endosymbiosis between a host archaeon and an aerobic prokaryotic cell (related to α-proteobacteria), which gradually resulted in a mitochondrion (Dyall et al., 2004; Embley and Martin, 2006; Khachane et al., 2007; Martin et al., 2015). In photosynthetic eukaryotes, this was followed by acquisition of free-living photosynthetic cyanobacteria, which led to evolution of specialized plastids (Nisbet and Sleep, 2001; Martin and Russell, 2003; Dyall et al., 2004; Pereira-Santana et al., 2015). These events of endosymbiosis gave rise to the group of glaucophytes, rhodophytes, and chlorophytes. The chlorophyte subgroup of charophytes (photosynthetic freshwater green algae) probably contained the ancestor that diversified into the land plants. Major environmental pressures including drought, salinity, desiccation, UV irradiation, drastic temperature shifts, variable oxygen levels, mechanical stimuli, and submergence were associated with their movement from the aquatic environment to land. These ancestral streptophytes possessed various biochemical/physiological/genetic traits such as basic gene families of present-day regulators of retrograde signalling (green boxes shown at the bottom). During the course of evolution, these emerging early plants evolved traits adaptive to land, resulting in non-vascular plants (mosses), and later on tracheophytes and seed plants. This explosion of land plants further increased the oxygen levels to current levels. One part of the adaptations was probably the improved communication and interaction between mitochondria and nuclear gene expression via retrograde signalling, with more complex regulatory networks arising as vascular and eventually flowering plants developed. Green boxes at the bottom represent the evolution of gene families (AP2/ABI4, WRKY; CDKs/CDKE1: cyclin-dependent kinases, and NAC gene families), containing known regulators of mitochondrial retrograde signalling in modern plants. In all cases, the basic gene families were present in ancestral green algae, but large expansions occurred together with the transition to land, including formation of C-terminal transmembrane NAC genes (TMM NACs), formation of the CDKE land plant group, and WRKY15-type proteins. With seed plants, came the development of the ANAC017-type proteins and ABI4-like proteins. WRKY40/18/60-type genes appeared relatively late in the angiosperms, and WRKY63-type genes are even more recent, apparently having evolved in Brassicaceae. These observations suggest that the transition to land was a major driver for development of mitochondrial signalling in plants, and that further fine-tuning of the regulatory network developed during the more recent evolution of land plants and is likely to be still ongoing.