Retrograde signalling in a virescent mutant triggers an anterograde delay of chloroplast biogenesis that requires GUN1 and is essential for survival

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 nucleusencoded 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’.