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.

Mechanism of Dual Targeting of the Phytochrome Signaling Component HEMERA/pTAC12 to Plastids and the Nucleus

“…Molecular understanding of the mechanisms targeting HMR to the nucleus and plastids holds promise for gaining novel insight into the mechanisms of nuclear-plastidial communication (Krause and Krupinska, 2009;Krause et al, 2012). In this study, we have showed that HMR can be directly imported into chloroplasts, where it is processed to the mature form starting from Lys-58 (Figs.…”

“…In this case, the partitioning of the protein between these two compartments is determined by competition and accessibility of the two targeting signals (Karniely and Pines, 2005;Krause and Krupinska, 2009;Krause et al, 2012). For instance, yeast Pir1p contains both a nuclear localization signal and a mitochondrial targeting signal, and its partitioning to these two subcellular compartments is regulated by masking and unmasking of the nuclear localization signal by its binding partner Apn1p (Vongsamphanh et al, 2001).…”

“…It is well documented in yeast (Saccharomyces cerevisiae), animals, and plants that a single gene can produce proteins targeted to dual destinations (Karniely and Pines, 2005;Carrie et al, 2009;Krause et al, 2012). Dual distribution between subcellular compartments can be achieved by two general strategies.…”

Influence of plastids on light signalling and development

“…Additionally, GUN1 contributed to the inhibition of germination by abscisic acid [40]. Similarly, the inhibition of germination by abscisic acid depended on the chloroplast-localized Whirly1 protein [73], which translocates from within the chloroplast to the nucleus [15]. Mutant alleles that activate 3 0 -phosphoadenosine 5 0 -phosphate-dependent plastid-to-nucleus signalling [3] also caused developmental abnormalities in leaves, such as short and round leaves with short petioles, undulating leaves, abnormal leaf vasculature and mesophyll cells [74].…”

“…Thus, plastid-to-nucleus signalling broadly affects plant cells by optimizing chloroplast function and helping to coordinate extrachloroplastic processes with chloroplast function. Known plastid signals include hydrogen peroxide, 3 0 -phosphoadenosine 5 0 -phosphate, b-cyclocitral, methylerythritol cyclodiphosphate, thiols and particular proteins [2,3,9,13,15]. Nonetheless, our knowledge of plastid signals and plastid-to-nucleus signalling mechanisms is incomplete.…”