Unconventional protein secretion in plants: a critical assessment

Abstract

Unconventional protein secretion (UPS) is a collective term for mechanisms by which cytosolic proteins that lack a signal peptide ("leaderless secretory proteins" (LSPs)) can gain access to the cell exterior. Numerous examples of UPS have been well documented in animal and yeast cells. In contrast, our understanding of the mechanism(s) and function of UPS in plants is very limited. This review evaluates the available literature on this subject. The apparent large numbers of LSPs in the plant secretome suggest that UPS also occurs in plants but is not a proof. Although the direct transport of LSPs across the plant plasma membrane (PM) has not yet been described, it is possible that as in other eukaryotes, exosomes may be released from plant cells through fusion of multivesicular bodies (MVBs) with the PM. In this way, LSPs, but also small RNAs (sRNAs), that are passively taken up from the cytosol into the intraluminal vesicles of MVBs, could reach the apoplast. Another possible mechanism is the recently discovered exocyst-positive organelle (EXPO), a double-membrane-bound compartment, distinct from autophagosomes, which appears to sequester LSPs.

Pea Border Cell Maturation and Release Involve Complex Cell Wall Structural Dynamics

“…Although intriguing, our work provides no evidence of any specific putative secretory mechanism(s) that may be involved. However, it is worth noting that a recent review highlighted the current paucity of knowledge relating to unconventional modes of protein secretion in plants, and this also may apply to polysaccharides (Robinson et al, 2016). Nevertheless, labeling data are consistent with the occurrence of XAG in the washed-out material and in border cell extractions (Fig.…”

The Plant Trans-Golgi Network: Not Just a Matter of Distinction

“…In addition to conventional secretion via TGN, exemplified by SYP61 and SCAMP2 vesicles, evidence pointing to the existence of TGN-independent, unconventional protein secretion pathways is accumulating, which may be implicated in cell wall protein transport (for review, see De Marchis et al, 2013;Davis et al, 2016a;Robinson et al, 2016;van de Meene et al, 2017).…”

Unconventional Transport Routes of Soluble and Membrane Proteins and Their Role in Developmental Biology

“…In the extracellular space, these macromolecules have been shown to have crucial roles in normal physiology as well as in human diseases such as cancer, infection, and metabolic and autoimmune disorders [9,10,11,12,13,14,15]. In plants, the situation is different because there are many putative leaderless secretory proteins but very few of them have been experimentally demonstrated to localize to the apoplast and their physiological role determined [4]. The only exception now is Helja, a mannose-specific jacalin-related lectin in sunflower seedlings [16].…”

“…Recently, the identification of an increasing number of secreted signal peptide-lacking proteins, also called leaderless secretory proteins, revealed the existence of unconventional protein secretion (UPS) pathways where these proteins bypass intermediate compartments involved in secretion or exocytosis, such as the Golgi apparatus [4]. Current studies are increasing the number of proteins known to traffic through the UPS pathways which can be broadly categorized as following: (i) leaderless proteins directly secreted and translocated across the PM, by means of vesicular and non-vesicular UPS pathways; (ii) soluble or transmembrane proteins with ER localization subsequently transported to the PM, or to the vacuole, or to the extra cellular space bypassing the Golgi apparatus; (iii) proteins normally functioning in the conventional membrane traffic with an additional unconventional role; and (iv) proteins involved in unusual or unexplored intra- and intercellular pathways and organelle biogenesis (Figure 1).…”