Plant Endoplasmic Reticulum

Abstract

The plant endoplasmic reticulum (ER) is responsible for the synthesis and often storage of a large group of proteins and lipids that enter the secretory pathway. This multifunctional organelle, which also represents one of the calcium storage compartments in plant cells, has currently received considerable attention from the research community because of features unique to plants that make it particularly interesting for biotechnology. Here, the principles behind ER dynamics in plants, and the molecular factors that control the rapid remodelling and network configuration of the organelle are discussed. Correlations between ER morphology and function indicate the potential to enhance protein storage by merely increasing the capacity of the organelle through altering its shape.

Key Concepts:

  • The endoplasmic reticulum in plants rapidly changes ‘shape’.

  • The ER is composed of a polygonal network of tubules and cisternae that readily interconvert.

  • The ER membrane shaping proteins, reticulons, affect ER curvature whereas root hair defective 3 (RHD3) may affect tubule fusion.

  • ER network movement is driven by actin and myosin in plants.

  • The ER is physically connected to Golgi bodies in plant cells.

Keywords: endoplasmic reticulum; Golgi bodies; network remodelling; movement; reticulons; RHD3

Figure 1.

ER and Golgi bodies in an Arabidopsis leaf epidermal cell. Numerous Golgi bodies (red) appear to associate with the ER (green). ER tubules (arrowhead) and cisternae (arrow) are highlighted. Scale bar 2 μm.

Figure 2.

Electron micrograph showing dilated ER due to overproduction of a heterologous protein tagged with an HDEL ER retention motif. The arrowhead highlights the surface of the ER and ribosomes that are attached. The heterologous protein is detected with specific antibodies and secondary antibodies conjugated to 10 nm colloidal gold. ER, endoplasmic reticulum; V, vacuole; CW, cell wall.

Figure 3.

Cortical ER network dynamics in tobacco leaf epidermal cells. A single image of a luminal ER marker (GFP‐HDEL) is shown (a). Two additional consecutive images of the same area of the cell were taken 10 s apart and pseudo (i.e. false) coloured blue and magenta. These images were then superimposed onto one another to indicate how much the ER remodels over a 20 s time frame (b). Note: regions in white reflect areas of the network that are present in all images and are therefore relatively static over the 20 s time frame. Scale bar 5 μm.

Figure 4.

Overexpression of RTNLB3‐eYFP with GFP‐calnexin in tobacco leaf epidermal cells. RTNLB3‐eYFP (a) locates to the ER tubules (arrow) and cisternal rims (arrowhead). GFP‐calnexin (b) is present in the ER cisternae (arrowhead), with reduced protein levels in the tubules (arrowhead; compare (b) and (d) where the signal in (d) has been increased through image processing). The merged image clearly shows RTNLB3 on the cisternal rims. Scale bar 2 μm.

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References

Boevink P, Cruz S, Hawes C, Harris N and Oparka KJ (1996) Virus‐mediated delivery of the green fluorescent protein to the endoplasmic reticulum of plant cells. Plant Journal 10: 935–941.

Boevink P, Oparka K, Santa Cruz S et al. (1998) Stacks on tracks: the plant Golgi apparatus traffics on an actin/ER network. Plant Journal 15: 441–447.

Chen J, Stefano G, Brandizzi F and Zheng H (2011) Arabidopsis RHD3 mediates the generation of the tubular ER network and is required for Golgi distribution and motility in plant cells. Journal of Cell Science 124: 2241–2252.

Crofts AJ, Leborgne‐Castel N, Hillmer S et al. (1999) Saturation of the endoplasmic reticulum retention machinery reveals anterograde bulk flow. Plant Cell 11: 2233–2248.

Foissner I, Menzel D and Wasteneys GO (2009) Microtubule‐dependent motility and orientation of the cortical endoplasmic reticulum in elongating characean internodal cells. Cell Motility and the Cytoskeleton 66: 142–155.

Hara‐Nishimura I, Shimada T, Hatano K, Takeuchi Y and Nishimura M (1998) Transport of storage proteins to protein storage vacuoles is mediated by large precursor‐accumulating vesicles. Plant Cell 10: 825–836.

Hardham AR, Takemoto D and White RG (2008) Rapid and dynamic subcellular reorganisation following mechanical stimulation of Arabidopsis epidermal cells mimics responses to fungal and oomycete attack. BMC Plant Biology 8(63): doi:10.1186/1471‐2229‐1188‐1163

Hawes C (2012) The ER/Golgi interface – is there anything in‐between? Frontiers in Plant Science 3: 73 doi:10.3389/fpls.2012.00073

Hwang H‐H and Gelvin SB (2004) Plant proteins that interact with VirB2, the Agrobacterium tumefaciens pilin protein, mediate plant transformation. Plant Cell 16: 3148–3167.

Lee HY, Bowen CH, Popescu GV et al. (2012) Arabidopsis RTNLB1 and RTNLB2 Reticulon‐Like proteins regulate intracellular trafficking and activity of the FLS2 immune receptor. Plant Cell 23: 3374–3391.

Lee H, Sparkes I, Gattolin S et al. (2013) An Arabidopsis reticulon and the atlastin homolgue RHD3‐like2 act togeher in shaping the tubular endoplasmic reticulon. New Phytologist 197: 481–489.

Nziengui H, Bouhidel K, Pillon D et al. (2007) Reticulon‐like proteins in Arabidopsis thaliana: structural organization and ER localization. FEBS Letters 581: 3356–3362.

Peremyslov VV, Prokhnevsky AI and Dolja VV (2010) Class XI myosins are required for development, cell expansion, and f‐actin organization in Arabidopsis. Plant Cell Online 22(6): 1883–1897.

Quader H and Schnepf E (1986) Endoplasmic reticulum and cytoplasmic streaming: fluorescence microscopical observations in adaxial epidermis cells of onion bulb scales. Protoplasma 131: 250–253.

Ridge RW, Uozumi Y, Plazinski J, Hurley UA and Williamson RE (1999) Developmental transitions and dynamics of the cortical ER of Arabidopsis cells seen with green fluorescent protein. Plant and Cell Physiology 40: 1253–1261.

Runions J, Brach T, Kuhner S and Hawes C (2006) Photoactivation of GFP reveals protein dynamics within the endoplasmic reticulum membrane. Journal of Experimental Botany 57: 43–50.

daSilva LL, Snapp EL, Denecke J et al. (2004) Endoplasmic reticulum export sites and Golgi bodies behave as single mobile secretory units in plant cells. Plant Cell 16: 1753–1771.

Sparkes I (2010) Motoring around the plant cell:insights from plant myosins. Biochemical Society Transactions 38: 833–838.

Sparkes I (2011) Recent advances in understanding plant myosin function:life in the fast lane. Molecular Plant 4: 805–812.

Sparkes IA, Ketelaar T, de Ruijter NC and Hawes C (2009a) Grab a Golgi: laser trapping of Golgi bodies reveals in vivo interactions with the endoplasmic reticulum. Traffic 10: 567–571.

Sparkes I, Runions J, Hawes C and Griffing L (2009b) Movement and remodeling of the endoplasmic reticulum in nondividing cells of tobacco leaves. Plant Cell 21: 3937–3949.

Sparkes I, Tolley N, Aller I et al. (2010) Five Arabidopsis reticulon isoforms share endoplasmic reticulum location, topology, and membrane shaping properties. Plant Cell 22: 1333–1343.

Stefano G, Renna L, Moss T, McNew JA and Brandizzi F (2012) In Arabidopsis, the spatial and dynamic organization of the endoplasmic reticulum and Golgi apparatus is influenced by the integrity of the C‐terminal domain of RHD3, a non‐essential GTPase. Plant Journal 69: 957–966.

Stephenson JLM and Hawes CR (1986) Stereology and stereometry of the endoplasmic reticulum during differentiation in the maize root cap. Protoplasma 131: 32–46.

Takemoto D, Jones DA and Hardham AR (2003) GFP‐tagging of cell components reveals the dynamics of subcellular re‐organisation in response to infection of Arabidopsis by oomycete pathogens. Plant Journal 33: 775–792.

Tolley N, Sparkes I, Craddock CP et al. (2010) Transmembrane domain length is responsible for the ability of a plant reticulon to shape endoplasmic reticulum tubules in vivo. Plant Journal 64: 411–418.

Tolley N, Sparkes IA, Hunter PR et al. (2008) Overexpression of a plant reticulon remodels the lumen of the cortical endoplasmic reticulum but does not perturb protein transport. Traffic 9: 94–102.

Toyooka K, Okamoto T and Minamikawa T (2000) Mass transport of proform of a KDEL‐tailed cysteine proteinase (SH‐EP) to protein storage vacuoles by endoplasmic reticulum‐derived vesicle is involved in protein mobilization in germinating seeds. Journal of Cell Biology 148: 453–464.

Ueda H, Yokota E, Kutsuna N et al. (2010) Myosin‐dependent endoplasmic reticulum motility and F‐actin organization in plant cells. Proceedings of the National Academy of Sciences of the USA 107: 6894–6899.

Voeltz GK, Prinz WA, Shibata Y, Rist JM and Rapoport TA (2006) A class of membrane proteins shaping the tubular endoplasmic reticulum. Cell 124: 573–586.

Yan R, Shi Q, Hu X and Zhou X (2006) Reticulon proteins: emerging players in neurodegenerative diseases. Cellular and Molecular Life Sciences 63: 877–889.

Yokota E, Ueda H, Hashimoto K et al. (2011) Myosin XI‐dependent formation of tubular structures from endoplasmic reticulum isolated from tobacco cultured cells, BY‐2. Plant Physiology 156: 129–143.

Further Reading

Brandizzi F and Barlowe C (2013) Organisation of the ER‐Golgi interface for membrane traffic control. Nature Reviews Molecular Cell Biology 14: 382–392.

Friedman JR and Voeltz GK (2011) The ER in 3D: a multifunctional dynamic membrane network. Trends in Cell Biology 21: 709–711.

Goyal U and Blackstone C (2013) Untangling the web: mechanisms underlying ER network formation. Biochimica et Biophysica Acta 1833: 2492–2498.

Hawes C, Osterrieder A, Sparkes IA and Ketelaar T (2010) Optical tweezers for micromanipulation of plant cytoplasm and organelles. Current Opinion in Plant Biology 13: 731–735.

Hepler PK (1982) Endoplasmic reticulum in the formation of cell plate and plasmodesmata. Protoplasma 111: 121–133.

Sparkes I, Hawes C and Frigerio L (2011) FrontiERs:movers and shapers of the higher plant cortical endoplasmic reticulum. Current Opinion in Plant Biology 14: 658–665.

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How to Cite close
Sparkes, Imogen A(Nov 2013) Plant Endoplasmic Reticulum. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0001673.pub2]