The induction of stromule formation by a plant DNA-virus in epidermal leaf tissues suggests a novel intra- and intercellular macromolecular trafficking route

Abstract

Stromules are dynamic thin protrusions of membrane envelope from plant cell plastids. Despite considerable progress in understanding the importance of certain cytoskeleton elements and motor proteins for stromule maintenance, their function within the cell has yet to be unraveled. Several viruses cause a remodulation of plastid structures and stromule biogenesis within their host plants. For RNA-viruses these interactions were demonstrated to be relevant to the infection process. An involvement of plastids and stromules is assumed in the DNA-virus life cycle as well, but their functional role needs to be determined. Recent findings support a participation of heat shock cognate 70 kDa protein (cpHSC70-1)-containing stromules induced by a DNA-virus infection (Abutilon mosaic virus, AbMV, Geminiviridae) in intra- and intercellular molecule exchange. The chaperone cpHSC70-1 was shown to interact with the AbMV movement protein (MP). Bimolecular fluorescence complementation confirmed the interaction of cpHSC70-1 and MP, and showed a homo-oligomerization of either protein in planta. The complexes were detected at the cellular margin and co-localized with plastids. In healthy plant tissues cpHSC70-1-oligomers occurred in distinct spots at chloroplasts and in small filaments extending from plastids to the cell periphery. AbMV-infection induced a cpHSC70-1-containing stromule network that exhibits elliptical dilations and transverses whole cells. Silencing of the cpHSC70 gene revealed an impact of cpHSC70 on chloroplast stability and restricted AbMV movement, but not viral DNA accumulation. Based on these data, a model is suggested in which these stromules function in molecule exchange between plastids and other organelles and perhaps other cells. AbMV may utilize cpHSC70-1 for trafficking along plastids and stromules into a neighboring cell or from plastids into the nucleus. Experimental approaches to investigate this hypothesis are discussed.

A Violaxanthin Deepoxidase Interacts with a Viral Suppressor of RNA Silencing to Inhibit Virus Amplification

“…Stromules have been found to be induced by effector-triggered immunity, and chloroplastlocalized N receptor-interacting protein1 (NRIP1) was transported from chloroplasts into the nucleus during this process through stromules (Caplan et al, 2015). Moreover, in Abutilon mosaic virus-infected leaves, a plastid-targeted heat shock cognate 70-kD protein (chaperone) was found to interact with Abutilon mosaic virus movement protein in the stromules (Krenz et al, 2010), which may facilitate viral transport from chloroplasts into a neighboring cell or the nucleus (Krenz et al, 2012). Therefore, the stromule conduits may be a pathway by which ZmVDEm is transported from chloroplasts back into the cytoplasm upon SCMV infection.…”

“…Chloroplast stromules, which are thin projections of stroma-filled tubules emerging from the surface of chloroplasts, have been reported to be associated with abiotic and biotic stresses (Gray et al, 2012;Krenz et al, 2012;Caplan et al, 2015). Although the biological significance of stromules remains unclear, accumulating evidence indicated that the stromules function in trafficking proteins (Krenz et al, 2012;Hanson and Sattarzadeh, 2013;Caplan et al, 2015). Stromules have been found to be induced by effector-triggered immunity, and chloroplastlocalized N receptor-interacting protein1 (NRIP1) was transported from chloroplasts into the nucleus during this process through stromules (Caplan et al, 2015).…”

Low-Phosphate Induction of Plastidal Stromules Is Dependent on Strigolactones But Not on the Canonical Strigolactone Signaling Component MAX2

“…Stromule induction has been observed in relation to biotic stresses like plant viral infection (Krenz et al, 2012) and abiotic stresses like heat (Holzinger et al, 2007). In many instances, stromules were observed in close contact with nuclei (Kwok and Hanson, 2004;Holzinger et al, 2007;Caplan et al, 2015).…”

Stromuling when stressed!

“…The cpHSC70-1-containing stromules detected upon an Abutilon mosaic virus (AbMV, plant ssDNA virus, Geminiviridae)-infection that was also in close association with the nucleus, appeared to interconnect plastids and extended from plastids outward to the cell periphery. This led to speculations of intra-and intercellular geminiviral transport in association with stromules [22,23]. A geminiviral nucleoprotein complex moves out of the plant nucleus via plasmodesmata into the adjacent cell to systemically infect the plant.…”

“…Other constructs have also been reported to visualize stromules, e.g. chloroplast-localized heat shock cognate 70-kDa protein (cpHSC70-1) [22,23], outer envelope protein 16 -2.1, -2.2 and -1.3 [24] and mutants of the Arabidopsis resistance protein RPW8.2 [25].…”