Tetrapyrrole Signaling in Plants

Abstract

Tetrapyrroles make critical contributions to a number of important processes in diverse organisms. In plants, tetrapyrroles are essential for light signaling, the detoxification of reactive oxygen species, the assimilation of nitrate and sulfate, respiration, photosynthesis, and programed cell death. The misregulation of tetrapyrrole metabolism can produce toxic reactive oxygen species. Thus, it is not surprising that tetrapyrrole metabolism is strictly regulated and that tetrapyrrole metabolism affects signaling mechanisms that regulate gene expression. In plants and algae, tetrapyrroles are synthesized in plastids and were some of the first plastid signals demonstrated to regulate nuclear gene expression. In plants, the mechanism of tetrapyrrole-dependent plastid-to-nucleus signaling remains poorly understood. Additionally, some of experiments that tested ideas for possible signaling mechanisms appeared to produce conflicting data. In some instances, these conflicts are potentially explained by different experimental conditions. Although the biological function of tetrapyrrole signaling is poorly understood, there is compelling evidence that this signaling is significant. Specifically, this signaling appears to affect the accumulation of starch and may promote abiotic stress tolerance. Tetrapyrrole-dependent plastid-to-nucleus signaling interacts with a distinct plastid-to-nucleus signaling mechanism that depends on GENOMES UNCUOPLED1 (GUN1). GUN1 contributes to a variety of processes, such as chloroplast biogenesis, the circadian rhythm, abiotic stress tolerance, and development. Thus, the contribution of tetrapyrrole signaling to plant function is potentially broader than we currently appreciate. In this review, I discuss these aspects of tetrapyrrole signaling.

Keywords: Mg-protoporphyrin IX; chlorophyll; chloroplast; heme; plastid; plastid signaling; porphyrin; tetrapyrrole.

FIGURE 1

Selected tetrapyrroles from plants. The structures were adapted from Tanaka and Tanaka (2007).

FIGURE 2

The branched tetrapyrrole biosynthetic pathway of plants. The names of the precursors and end products of the branched tetrapyrrole biosynthetic pathway are indicated with gray. Enzyme catalyzed reactions are indicated with gray arrows. The feedback inhibition of glutamyl tRNA reductase by heme is indicated with a gray T bar. The names of proteins, such as regulatory proteins and enzymes, are indicated with black. The tetrapyrrole biosynthetic pathway was adapted from Tanaka and Tanaka (2007) and Tanaka et al. (2011). Genes encoding enzymes or enzyme subunits are indicated with blue. Mutants discussed in the text are indicated with red. gun5, cch, and chlh are mutant alleles of ChlH/GUN5. chld is a mutant allele of ChlD. cs, ch-42, and chli1 are mutant alleles of ChlI1. chli2 is a mutant allele of ChlI2.

FIGURE 3

A model for tetrapyrrole-dependent plastid-to-nucleus signaling in plants. The simplest interpretation of the current data is that heme accumulates in well-functioning chloroplasts and that the accumulation of heme in chloroplasts or the export of heme to the cytosol or nucleus activates a mechanism that induces the expression of PhANGs. The current data do not exclude alternative mechanisms, such as a moonlighting function for an enzyme or regulatory factor that contributes to tetrapyrrole metabolism, such as GUN4, GUN5, or a GUN4-GUN5 complex that affects gene expression in the nucleus. Either the liganded or unliganded versions of GUN4, GUN5, or a GUN4-GUN5 complex might contribute to a plastid-to-nucleus signaling mechanism that regulates the expression of PhANGs. GUN1 interacts with tetrapyrrole-dependent plastid-to-nucleus signaling by an unknown mechanism.