The colonization of land was a likely driving force for the evolution of mitochondrial retrograde signalling in plants

Abstract

Most retrograde signalling research in plants was performed using Arabidopsis, so an evolutionary perspective on mitochondrial retrograde regulation (MRR) is largely missing. Here, we used phylogenetics to track the evolutionary origins of plant MRR-regulators. In all cases, the gene families can be traced to ancestral green algae or earlier. However, the specific subfamilies containing plant MRR-regulators in many cases arose during the transition to land. NAC transcription factors with C-terminal transmembrane domains, as observed in key MRR-regulator ANAC017, can first be observed in non-vascular mosses, and close homologs to ANAC017 can be found in seed plants. Cyclin-dependent kinases (CDKs) are common to eukaryotes, but E-type CDKs that regulate MRR also diverged in conjunction with plant colonization of land. AtWRKY15 can be traced to the earliest land plants, while AtWRKY40 only arose in Angiosperms and AtWRKY63 even more recently in Brassicaceae. Apetala 2 (AP2) transcription factors are traceable to algae, but the ABI4-type again only appeared in seed plants. This strongly suggests that the transition to land was a major driver for developing plant MRR pathways, while additional fine-tunings have appeared in seed plants or later. Finally, we discuss how MRR may have contributed to facing the specific challenges that early land plants faced during terrestrialization.

A molecular atlas of plastid and mitochondrial proteins reveals organellar remodeling during plant evolutionary transitions from algae to angiosperms

“…A notable example of preadaptation includes malate decarboxylation in the C4 photosynthetic pathway [ 24 ]—a trait of the green lineage [ 25 ] that improves plant photosynthetic efficiency in warm and dry habitats [ 26 ]. Similarly, some components of mitochondrial retrograde signaling also evolved in the land plants and likely contributed to its ROS and draught tolerance [ 27 ].…”

Plant organellar signalling—back and forth and intertwined with cellular signalling

“…Over the past years, these connections were further elaborated, and the articles assembled in this Special Issue highlight various aspects of this integration of different signalling pathways. Starting with the fundamental question of ‘how it all began’, Khan and Van Aken (2022) performed a phylogenetic analysis and propose that the colonization of land was a likely driving force for the evolution of mitochondrial retrograde signalling in plants, while additional fine-tuning appeared in seed plants or even later. Such mechanisms for regulating chloroplast development are then reviewed by Liebers et al (2022) , hinting at functional feedback between plastid and cytosolic protein homeostasis in plastid retrograde signalling during chloroplast biogenesis.…”