The chloroplast division mutant caa33 of Arabidopsis thaliana reveals the crucial impact of chloroplast homeostasis on stress acclimation and retrograde plastid‐to‐nucleus signaling

Abstract

SUMMARY Retrograde plastid-to-nucleus signaling tightly controls and coordinates nuclear and plastid gene expression that is required for plastid biogenesis and chloroplast activities. As chloroplasts act as sensors of environmental changes, plastid-derived signaling also modulates stress responses of plants by transferring stress-related signals and altering nuclear gene expression. Various mutant screens have been undertaken to identify constituents of plastid signaling pathways. Almost all mutations identified in these screens have in common that they target plastid-specific but not extra-plastidic functions. They have been suggested to define either genuine constituents of retrograde signaling pathways or components required for the synthesis of plastid signals. Here we report the characterization of the caa33 (constitutive activator of AAA-ATPase) mutant, which reveals another way of how mutations that affect plastid functions may modulate retrograde plastid signaling. caa33 disturbs a plastid-specific function by impeding plastid division thereby perturbing plastid homeostasis. This results in pre-conditioning plants by activating the expression of stress genes, enhancing pathogen resistance and attenuating the plant’s capacity to respond to plastid signals. Our study reveals an intimate link between chloroplast activity and the plant’s susceptibility to stress and emphasizes the need to consider the possible impact of pre-conditioning on retrograde plastid-to-nucleus signaling.

Emerging facets of plastid division regulation

“…Indeed, the Constitutive Activator of AAA-ATPase (CAA33) is not only involved in plastid division but also mediates plastid signalling to the nucleus to induce stress acclimation (Kimková et al 2012). Despite this genomewide gene expression proWling in response to altered plastid division characteristics in Arabidopsis revealed a remarkably low number of genes aVected by altered division status (Maple et al 2011).…”

Arabidopsis FRS4/CPD25 and FHY3/CPD45 work cooperatively to promote the expression of the chloroplast division gene ARC5 and chloroplast division

“…However, the exact mechanism by which this protein operates is unclear. CRUMPLED LEAF (CRL), CDK-DEPENDENT1 (CDT1) and FZO-LIKE (FZL) are further examples of Arabidopsis genes known to be involved in chloroplast division (Asano et al, 2004;Raynaud et al, 2004;Gao et al, 2006;Simkova et al, 2012).…”

Molecular components of stress-responsive plastid retrograde signaling networks and their involvement in ammonium stress

“…22 Similarly, mutation of plastid CAA33 disturbs chloroplast homeostasis by impeding plastid division, interfering with 1 O 2 -mediated plastid-to-nucleus signaling. 24 A further example can be seen in chloroplastic RPS1, involved in plastid protein translation and displaying a role in the synthesis of thylakoid membrane proteins we propose possible plastid retrograde signals for the AMOS1/ EGY1-dependent ammonium stress response (Fig. 1).…”

“…For example, several regulatory molecular components involved in 1 O 2 -mediated plastid-to-nucleus signaling have been identified through extensive genetic mutation screens in the background of the conditional flu mutant, such as EX1, EX2, SOLDAT10, PRL1, CAA33, CAA39 in Arabidopsis. [20][21][22][23][24][25] Two new plastid retrograde signals (PAP and MEcPP) during drought, high light and wounding stress responses have been revealed by two research teams, involving the analysis of the Arabidopsis mutants sal1 and ceh1, which encode the plastid nucleotidase/phosphatase SAL1 and hydroxyl-2-methyl-2-(E)-butenyl4-diphosphate synthase (HDS), respectively. 26,29 Analysis of the rps1 mutant demonstrated that the chloroplast ribosomal protein S1 (RPS1) mediates retrograde signaling to modulate the expression of the heat-responsive nuclear transcription factor HsfA2 and its target genes during heat stress, although the specific plastid retrograde signal is unknown.…”

“…[2][3][4][5][6][7][8][9][10][11][12][13][14][15][16] More recently, several plastid retrograde signaling pathways have been identified to regulate the expression of stress-related nuclear genes during several stresses such as high light, drought, wounding, heat, and excess ammonium. [17][18][19][20][21][22][23][24][25][26][27][28][29][30][31] Based on the new stress-responsive plastid retrograde signaling pathways just reported in 2012 alone, this review will focus on properties of currently proposed molecular components in the plastid retrograde signaling network under stress. We also specifically discuss possible plastid retrograde signals involved in plant response to ammonium stress.…”