Retrograde signals from endosymbiotic organelles: a common control principle in eukaryotic cells

Abstract

Endosymbiotic organelles of eukaryotic cells, the plastids, including chloroplasts and mitochondria, are highly integrated into cellular signalling networks. In both heterotrophic and autotrophic organisms, plastids and/or mitochondria require extensive organelle-to-nucleus communication in order to establish a coordinated expression of their own genomes with the nuclear genome, which encodes the majority of the components of these organelles. This goal is achieved by the use of a variety of signals that inform the cell nucleus about the number and developmental status of the organelles and their reaction to changing external environments. Such signals have been identified in both photosynthetic and non-photosynthetic eukaryotes (known as retrograde signalling and retrograde response, respectively) and, therefore, appear to be universal mechanisms acting in eukaryotes of all kingdoms. In particular, chloroplasts and mitochondria both harbour crucial redox reactions that are the basis of eukaryotic life and are, therefore, especially susceptible to stress from the environment, which they signal to the rest of the cell. These signals are crucial for cell survival, lifespan and environmental adjustment, and regulate quality control and targeted degradation of dysfunctional organelles, metabolic adjustments, and developmental signalling, as well as induction of apoptosis. The functional similarities between retrograde signalling pathways in autotrophic and non-autotrophic organisms are striking, suggesting the existence of common principles in signalling mechanisms or similarities in their evolution. Here, we provide a survey for the newcomers to this field of research and discuss the importance of retrograde signalling in the context of eukaryotic evolution. Furthermore, we discuss commonalities and differences in retrograde signalling mechanisms and propose retrograde signalling as a general signalling mechanism in eukaryotic cells that will be also of interest for the specialist. This article is part of the theme issue ‘Retrograde signalling from endosymbiotic organelles’.

A Core Module of Nuclear Genes Regulated by Biogenic Retrograde Signals from Plastids

“…Proper timely and spatial expression of genes essential for chloroplast biogenesis, therefore, requires a high coordination between the two genetic compartments. This is achieved by a mutual information exchange called anterograde signaling (nucleus-to-plastid signaling) and retrograde signaling (plastid-to nucleus signaling) [ 12 , 13 , 14 , 15 , 16 , 17 ].…”

Translocation of chloroplast NPR1 to the nucleus in retrograde signaling for adaptive response to salt stress in tobacco

“…How organelles communicate with the nucleus to coordinate genetic programs and cellular functions is a fundamental question of plant physiology and cell biology (Pfannschmidt et al, 2020). Reduction/oxidation (redox)-associated signaling is an essential component of responses to environmental stresses and pathogen attack in all organisms, including plants (Munné-Bosch et al, 2013), in which stress-related reactive oxygen species (ROS) and redox information are principally accumulated in chloroplasts.…”

Oxylipins in plastidial retrograde signaling

“…Since plastids, in particular chloroplasts, are site sensors of environmental and developmental changes, communication from these organelles to the nucleus is essential to grant plant acclimation and metabolic adjustments. This form of signal transduction is known as retrograde signaling, opposite to anterograde signaling that refers to signals emanating from the nucleus to other organelles, and was firstly evidenced by studies on plastid ribosome deficient mutants of barley in the early 1970s [ 2 , 3 ]. From this pioneer work, much information is now available on retrograde signals, which can be divided into two classes: (i) those related to plastid biogenesis or differentiation (either of chloroplasts, gerontoplasts, amyloplasts, elaioplasts or chromoplasts) and the consequent development of specific morphological and functional characteristics (biogenic control), and (ii) those related to the function of the corresponding plastids in the plant response to environmental stimuli (operational control) [ 3 ].…”

“…This form of signal transduction is known as retrograde signaling, opposite to anterograde signaling that refers to signals emanating from the nucleus to other organelles, and was firstly evidenced by studies on plastid ribosome deficient mutants of barley in the early 1970s [ 2 , 3 ]. From this pioneer work, much information is now available on retrograde signals, which can be divided into two classes: (i) those related to plastid biogenesis or differentiation (either of chloroplasts, gerontoplasts, amyloplasts, elaioplasts or chromoplasts) and the consequent development of specific morphological and functional characteristics (biogenic control), and (ii) those related to the function of the corresponding plastids in the plant response to environmental stimuli (operational control) [ 3 ]. Although lipid peroxidation has been studied in detail in plants and recently reviewed [ 4 , 5 ] and the differentiation of chloroplasts to either gerontoplasts (in senescing leaves) or chromoplasts (during fruit ripening) has been characterized in some detail [ 6 ], less attention has been paid on the focus on how signals emanating from chloroplasts modulate plastid interconversion.…”