Plastids in a Pinch: Coordinating Stress and Developmental Responses Through Retrograde Signalling

Abstract

Plastids are crucial for fuelling and regulating plant growth and development. Photosynthesising chloroplasts provide energy for growth, while other plastids play additional key roles in various aspects of plant physiology. For function and development, plastids greatly depend on nucleus-encoded proteins, and they can modulate the synthesis of these proteins by sending retrograde signals to the nucleus. These signals communicate the developmental and operational status of the plastid, both of which are sensitive to the environment. Abiotic stressors such as drought, salinity, and suboptimal light and temperature conditions can induce changes in chloroplast metabolism, ultrastructure and cellular positioning. In response to specific environmental triggers, retrograde signals reprogramme nuclear gene expression to fine-tune plastid form and function, but also influence whole-plant morphology. Over the past years, the chloroplast responses to stress have become clearer. Various sources of retrograde signals, derived from plastid metabolism, plastid gene expression and altered photosynthetic redox balance, are now known to directly interfere with canonical signalling pathways. However, most of what is known about retrograde signalling originates from studies using artificial stressors, such as chemical treatments or genetic mutations, and its importance in natural environments is still poorly understood. This review highlights the understanding of plastid responses to the environment, as well as the impact generated downstream of retrograde signals, to better understand the role of plastids in abiotic stress resilience of flowering plants.

Keywords: abiotic stress; chloroplasts; environmental adaptation; gene expression regulation; genomes uncoupled; photosynthesis; plant development; retrograde signalling.

Figure 1

Abiotic stressors affect chloroplast ultrastructure (A) and chloroplast positioning within the cell (B). Chloroplast ultrastructure changes under stress include rounding of the chloroplast, increased plastoglobuli size and number, stromule formation, dismantlement of the thylakoid network, grana unstacking, altered numbers of starch granules and chloroplast envelope damage (as indicated by dashed line). (B) Chloroplast positioning is altered under different light and temperature conditions. Under low light, chloroplasts orient along periclinal cell walls, but under high light, they orient along anticlinal cell walls. Positioning in the dark conditions differs between species, with the chloroplast moving to the bottom of the cell in Arabidopsis, but aligning along the anticlinal cell walls in other species. In response to cold under low‐light conditions, chloroplasts also move to the anticlinal cell walls. Representative cells show a side view.

Figure 2

Simplified model for tetrapyrrole biosynthesis, the methylerythritol phosphate pathway and carotenoid biosynthesis pathways in plants. Single arrows indicate direct steps, double arrows indicate indirect steps, enzymes are in italics, and gene names are in bold italics. Boxes correspond to labels directly above/below. Abbreviations: ABA abscisic acid, CEH1 Constitutively Expressing HYDROPEROXIDE LYASE 1, CRTISO CAROTENOID ISOMERASE, DXR 1‐DeoxyXylulose‐5‐phosphate Reductoisomerase, DXS 1‐DeoxyXylulose‐5‐phosphate Synthase, FLU FLUORESCENT IN BLUE LIGHT, FSM fosmidomycin, GUN GENOMES UNCOUPLED, HEMA HEME A, NF norflurazon, PDS phytoene desaturase, POR protochlorophyllide oxidoreductase, PSY phytoene synthase, ZDS ζ ‐carotene desaturase. [Color figure can be viewed at wileyonlinelibrary.com]

Figure 3

Simplified schematic representing four major retrograde signalling sources: (1) intermediates of the tetrapyrrole biosynthesis pathway, (2) signals from altered plastid gene expression, (3) photosynthesis‐derived signals and (4) signals arising from other metabolic pathways. Grey arrows indicate retrograde signals with either promotion (arrowhead) or repression (block arrow) of Singlet Oxygen Responsive Genes/Stress Responsive Genes or Photosynthesis Associated Nuclear Genes/Golden Like transcription factors. The chloroplast is shown in green, and the nucleus is shown in orange. [Color figure can be viewed at wileyonlinelibrary.com]