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

Björn Krenz,Tatjana Kleinow,Holger Jeske

doi:10.3389/fpls.2012.00291

Björn Krenz, Tatjana Kleinow + Show 1 more

Open Access

https://doi.org/10.3389/fpls.2012.00291

Copy DOI

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.

Highlights

In plants, transport of endogenous macromolecules such as proteins and nucleic acids over cellular boundaries occurs in a highly selective and regulated manner (Oparka, 2004; Lee and Lu, 2011; Maule et al, 2011; Niehl and Heinlein, 2011; Zavaliev et al, 2011)
Silencing of a cytosolic HSC70-1 was found to impair infection by the monopartite geminivirus tomato yellow leaf curl Sardinia virus (TYLCSV) in N. benthamiana (Lozano-Duran et al, 2011). None of these heat shock protein 70 kDa (HSP70) and HSC70s involved in viral life cycles were located in the chloroplast stroma where cpHSC70-1 was identified to interact with the movement proteins (MPs) of the geminivirus Abutilon mosaic virus (AbMV) (Krenz et al, 2010)
The results of Krenz et al (2010) may demand to widen this concept of geminiviral cellular transfer for AbMV: it may opportunistically hijack different pathways for intracellular transport and plasmodesmata targeting including an alternative route via chloroplasts and stromules with the aid of a plastidal chaperone

Summary

Introduction

Transport of endogenous macromolecules such as proteins and nucleic acids over cellular boundaries occurs in a highly selective and regulated manner (Oparka, 2004; Lee and Lu, 2011; Maule et al, 2011; Niehl and Heinlein, 2011; Zavaliev et al, 2011). 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.

Results

Conclusion