Dual targeting and retrograde translocation: regulators of plant nuclear gene expression can be sequestered by plastids

Abstract

Changes in the developmental or metabolic state of plastids can trigger profound changes in the transcript profiles of nuclear genes. Many nuclear transcription factors were shown to be controlled by signals generated in the organelles. In addition to the many different compounds for which an involvement in retrograde signaling is discussed, accumulating evidence suggests a role for proteins in plastid-to-nucleus communication. These proteins might be sequestered in the plastids before they act as transcriptional regulators in the nucleus. Indeed, several proteins exhibiting a dual localization in the plastids and the nucleus are promising candidates for such a direct signal transduction involving regulatory protein storage in the plastids. Among such proteins, the nuclear transcription factor WHIRLY1 stands out as being the only protein for which an export from plastids and translocation to the nucleus has been experimentally demonstrated. Other proteins, however, strongly support the notion that this pathway might be more common than currently believed.

Keywords: WHIRLY1; chloroplasts; protein targeting; retrograde signals.

Figure 1

Chloroplasts are involved in the perception of intrinsic triggers controlling plant development and external cues and stresses from the abiotic and the biotic environment. A novel signaling pathway involving chloroplast located proteins that might be translocated to the nucleus in response to the diverse stimuli perceived by chloroplasts (see text) is depicted here. Whirly1 is the only protein for which a bona fide export has been shown to date (arrow with continuous line). This protein is involved in pathogen responses [35,52], but might also play a role in other situations. The NRIP1 protein appears to be released from plastids in response to infection to tobacco with the tobacco mosaic virus [45] but direct evidence for an export is yet missing (arrow with large dotted line). The transcription factor NAC102 is an intriguing candidate for the perception of oxidative stress in chloroplasts [47], but the possibility of its release remains to be investigated (arrow with small dotted line).

Figure 2

Selected mechanisms of protein translocation from chloroplasts to the nucleus. (A) Putative ER mediated transfer of plastid proteins to the nucleus. A periplasmic space formed by ER cisternae and intermembrane space of plastids has been observed under certain conditions (see text). Proteins from the stroma of plastids would need to transverse a single membrane to become included in this space, which is continuous with the envelope of nuclei. To enter the nucleus, proteins would need to cross the inner membrane of the nuclear envelope; (B) Hypothetical release of proteins directly into the cytoplasm. Transient pores might be formed by activity of proteins such as TGD2 being involved in lipid exchange between ER and plastids [90]. Small disruptions in the membrane leading to a leakiness of chloroplasts might occur upon stress. Black dots, released plastidic proteins; red ellipse, protein complex which mediates membrane permeability; NE, nuclear envelope; ER, endoplasmic reticulum; IM, inner membrane; OM, outer membrane.