Abstract
Defects in chloroplast development are ‘retrograde-signalled’ to the nucleus, reducing synthesis of photosynthetic or related proteins. The Arabidopsis cue8 mutant manifests virescence, a slow-greening phenotype, and is defective at an early stage in plastid development. Greening cotyledons or early leaf cells of cue8 exhibit immature chloroplasts which fail to fill the available cellular space. Such chloroplasts show reduced expression of genes of photosynthetic function, dependent on the plastid-encoded polymerase (PEP), while the expression of genes of housekeeping function driven by the nucleus-encoded polymerase (NEP) is elevated, a phenotype shared with mutants in plastid genetic functions. We attribute this phenotype to reduced expression of specific PEP-controlling sigma factors, elevated expression of RPOT (NEP) genes and maintained replication of plastid genomes (resulting in densely coalesced nucleoids in the mutant), i.e. it is due to an anterograde nucleus-to-chloroplast correction, analogous to retention of a juvenile plastid state. Mutants in plastid protein import components, particularly those involved in housekeeping protein import, also show this ‘retro-anterograde’ correction. Loss of CUE8 also causes changes in mRNA editing. The overall response has strong fitness value: loss of GUN1, an integrator of retrograde signalling, abolishes elements of it (albeit not others, including editing changes), causing bleaching and eventual seedling lethality upon cue8 gun1. This highlights the adaptive significance of virescence and retrograde signalling.This article is part of the theme issue ‘Retrograde signalling from endosymbiotic organelles’.
Highlights
Four decades ago plastid-to-nucleus communication was first observed as a reduction in synthesis rate of a nuclear-encoded chloroplast protein in a chloroplast ribosomes-deficient mutant [1]
It is distinct from the responses caused by later, ‘operational retrograde signals’, which occur when functional chloroplasts operate under stress [4]
A genetic effort to identify components involved in light signalling on the basis of its control of chloroplast development [10] led to the identification of a number of cab-underexpressed mutants, several among which exhibited a virescent phenotype [11]
Summary
Four decades ago plastid-to-nucleus communication was first observed as a reduction in synthesis rate of a nuclear-encoded chloroplast protein in a chloroplast ribosomes-deficient mutant [1]. A genetic effort to identify components involved in light signalling on the basis of its control of chloroplast development [10] led to the identification of a number of cab-underexpressed (cue) mutants, several among which exhibited a virescent phenotype [11]. In one of those mutants, the ultrastructure of plastids showed a transition from proplastid to fully differentiated chloroplast which is difficult to capture in wild-type (WT) plants. Average nuclear DNA content per cell of the developing seedlings was measured using flow cytometry (Sysmex CyFlow® Space, Sysmex, UK), broadly according to Mohammed et al [22], by counting a minimum of 16 000 nuclei per biological replicate (6–7 replicates per time point)
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