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1.I.2 The Plant Plasmodesmata (PPD) Family [formerly 1.A.26]

Plasmodesmata in plants are functionally like gap junctions in animals, allowing the passage of small molecules of less than 1000 Da between cells by forming transcytoplasmic bridges that span the cell walls. Transport of hormones, growth factors, proteins and protein nucleic acid complexes has also been documented. Plant viruses such as tobacco mosaic virus (TMV) parasitize the plasmodesmata for the transport of their own nucleoproteins between cells. For this purpose they may modify the channels so as to increase its diameter. TMV synthesizes a 30kDa 'movement' protein, P30, that functions as a chaperone protein to bind and unfold the TMV RNA and target it through the plasmodesmata. P30 is believed to increase the size exclusion limit of the plasmodesmata. The structure, function and biogenesis of the plasmodesmata have been reviewed by Maule, 2008. Benitez-Alfonzo et al. (2010; 2011) discuss the structure and function of these channels and the ways in which viruses bring about functional changes that allow macromolecular trafficking to occur. (see also Amari et al., 2010)

Plasmodesmata (Pds) mediate symplastic communication between neighbouring cells. Pds provide the potential for the exchange of informational molecules acting as conduits for a range of transcription factors [4], small RNAs [[5•] and [6•]], and pathogenic [[7] and [8]] and non-pathogenic RNAs. They regulate the loading of physiologically and developmentally important molecules into the phloem.  They allow transfer of small molecules and macromolecules between cells of different species, such as betweeen host and parasitic plants (Leblanc et al. 2012; Kim et al. 2014).

Pds formed during cytokinesis are plasma membrane (PM)-lined pores that bridge the cell wall and a central axial element of appressed endoplasmic reticulum (ER) (called the desmotubule). The indentification of plasmodesmal proteins is discussed by Faulkner et al. (2011) and Benitez-Alfonso and Maule (2011).

To date, about 30 proteins have been described as having some association with Pds. Using a viral movement protein (MP) as a substrate, a Pd-located kinase (PAPK) with the potential to phosphorylate MP and other non-cell-autonomous proteins (NCAPs) was identified [16]. These include reversibly glycosylated polypeptide (RGP), heat shock cognate 70 proteins, a β-1,3-glucanase and proteins similar to RNA-binding proteins, including the DEAD box RNA helicase eIF4A [17]. Class 1 RGPs associate with Arabidopsis Pds [18].

A new family of eight Pd transmembrane receptor-like proteins are type-1 membrane proteins, called Pd-located proteins 1 (PDLP1). They comprise an apoplastic receptor-like domain, a single transmembrane domain and a short C-terminal cytoplasmic tail. They influence Pd trafficking. A further family of Pd proteins are small (22 kDa) proteins with a callose-binding domain and a C-terminal unstructured arm GPI-anchored into the PM. Located at the neck region of Pds, these are positioned for interaction with callose deposited in the wall. The existence in Pds of β-1,3-glucanases and this callose-binding protein support the importance of callose in Pd control [[14] and [23]].

Finally, there are a number of increased size exclusion limit (ise) mutants [24]. ISE2 encodes a DEVH box RNA helicase involved in posttranscriptional gene silencing. ise2 mutants show altered Pd structure (increased branching), and seedling growth and developmental phenotypes. ISE2 may affect Pd structure through regulation of RNA metabolism and consequent gene expression.

 Cellular components and proteins localised to plasmodesmata

Component

Function/Comment

Actin

Cytoskeletal component of Pds. Possibly used to traffic molecules through the pore, and/or to control the SEL.

Actin regulating proteins (Arp3 homologues)

Suggestion that Pds may act as actin-filament organising centres, or that Arp proteins are involved in Pd regulation

Acid phosphatase

Function unknown but possibly involved in callose synthesis

At-4/1

Protein interacting with Tomato spotted wilt virus movement protein. 4/1 proteins show similarities to myosin-, kinesin- and ankaryn-like proteins.

ATPase

Provision of energy at the Pd pore.  Specific function unknown.

Callose

Used to seal Pds during wounding or pathogen attack.  May also control the SEL.

Calreticulin

A calcium-sequestering protein that may regulate Ca²+ levels and help control the SEL

Centrin

A calcium-binding cytoskeletal protein that may control the SEL

Connexin-like proteins

A number of proteins have either been found in cell-wall extracts or inferred by cross-reaction with connexin antibodies.  Most convincingly shown by Yahalom et al. (1991), but other studies have failed to provide clear localisation data, and one putative connexion later proved to be a protein-kinase-like protein

Eukaryotic inititation factor 4A

Identified from Chara corallina

β-1,3-Glucanase

Identified from Chara corallina and Arabidopsis. In the latter, shown to target as a GFP fusion to Pds. Knock-out mutant plants showed reduced GFP diffusion through Pds.

Heat shock cognate 70

Identified from Chara corallina and homologous to HSc70 from Nicotiana and shown to carry a Pd trafficking signal.

Myosin

A motor protein that may be used to traffic molecules through the pore, or may link the desmotubule to the plasma membrane. Could be used to control the SEL.  A unique plant myosin (myosin VIII) has been localised to, and may be specialised for, Pds

Pectin

A component of  the cell wall that is enriched around Pds

Pectin methylesterase (PME)

An enzyme involved in pectin de-esterification, it interacts with viral movement proteins and has been hypothesised to act as a Pd receptor protein

Peroxidase

Function unknown

Plasmodesmata located protein 1 (PDLP1)

A family of type I membrane receptor-like proteins targeted solely to Pds and with the property of changing reciprocally trafficking of GFP following altered expression. PDLP1 also carries a 21 amino acid signal sufficient for targeting proteins to Pds via the Golgi-ER secretory pathway.

PRms

A pathogenesis-related protein that both localises to, and moves through, Pds.  Function unknown, but may only transiently reside in Pds

Protein kinases

Involved in the phosphorylation or viral movement proteins, and possibly endogenous trafficking proteins.  May be used for protein phosphorylation signalling and control of the SEL.

Reversibly Glycosylated polypeptide (Class 1) - C1RGP

A 41 kDa protein identified from maize and Arabidopsis and shown to target Pds as GFP fusion. Usually associated with the Golgi apparatus, the function of these proteins is not known.

RNA binding proteins

Identified from Chara corallina

RTM1 protein

A protein that restricts the entry of Tobacco etch virus in the phloem.  May only transiently reside in Pds

Ubiquitin

May be involved in the turnover of Pd proteins, or the removal of Pds

Vesicle trafficking proteins

May be involved in delivery of exogenous structural or cargo proteins to Pds, and may be hijacked by viral movement protein to gain transport to the pore.  May also be involved in transport through the pore on the plasma membrane

WD40 repeat-containing protein

Function unknown, but likely to be involved in protein-protein interactions, so may be a docking or receptor protein

α-amylase

Function at Pds unknown

26- and 27-kDa proteins

Functions unknown, but PAP27 cross-reacts with a connexin32 antibody (see above)

45-kDa protein

Function unknown

5'-nucleotidase

Function unknown

Maize root proteins

Antibodies JIM64 and JIM67 raised against two unknown proteins label Pds.  Their functions are unknowKim et al. 2014).

Pds formed during cytokinesis are plasma membrane (PM)-lined pores that bridge the cell wall and a central axial element of appressed endoplasmic reticulum (ER) (called the desmotubule). The indentification of plasmodesmal proteins is discussed by Faulkner et al. (2011) and Benitez-Alfonso and Maule (2011).

To date, about 30 proteins have been described as having some association with Pds. Using a viral movement protein (MP) as a substrate, a Pd-located kinase (PAPK) with the potential to phosphorylate MP and other non-cell-autonomous proteins (NCAPs) was identified [16]. These include reversibly glycosylated polypeptide (RGP), heat shock cognate 70 proteins, a β-1,3-glucanase and proteins similar to RNA-binding proteins, including the DEAD box RNA helicase eIF4A [17]. Class 1 RGPs associate with Arabidopsis Pds [18].

A new family of eight Pd transmembrane receptor-like proteins are type-1 membrane proteins, called Pd-located proteins 1 (PDLP1). They comprise an apoplastic receptor-like domain, a single transmembrane domain and a short C-terminal cytoplasmic tail. They influence Pd trafficking. A further family of Pd proteins are small (22 kDa) proteins with a callose-binding domain and a C-terminal unstructured arm GPI-anchored into the PM. Located at the neck region of Pds, these are positioned for interaction with callose deposited in the wall. The existence in Pds of β-1,3-glucanases and this callose-binding protein support the importance of callose in Pd control [[14] and [23]].

Finally, there are a number of increased size exclusion limit (ise) mutants [24]. ISE2 encodes a DEVH box RNA helicase involved in posttranscriptional gene silencing. ise2 mutants show altered Pd structure (increased branching), and seedling growth and developmental phenotypes. ISE2 may affect Pd structure through regulation of RNA metabolism and consequent gene expression.

 Cellular components and proteins localised to plasmodesmata

Component

Function/Comment

Actin

Cytoskeletal component of Pds. Possibly used to traffic molecules through the pore, and/or to control the SEL.

Actin regulating proteins (Arp3 homologues)

Suggestion that Pds may act as actin-filament organising centres, or that Arp proteins are involved in Pd regulation

Acid phosphatase

Function unknown but possibly involved in callose synthesis

At-4/1

Protein interacting with Tomato spotted wilt virus movement protein. 4/1 proteins show similarities to myosin-, kinesin- and ankaryn-like proteins.

ATPase

Provision of energy at the Pd pore.  Specific function unknown.

Callose

Used to seal Pds during wounding or pathogen attack.  May also control the SEL.

Calreticulin

A calcium-sequestering protein that may regulate Ca²+ levels and help control the SEL

Centrin

A calcium-binding cytoskeletal protein that may control the SEL

Connexin-like proteins

A number of proteins have either been found in cell-wall extracts or inferred by cross-reaction with connexin antibodies.  Most convincingly shown by Yahalom et al. (1991), but other studies have failed to provide clear localisation data, and one putative connexion later proved to be a protein-kinase-like protein

Eukaryotic inititation factor 4A

Identified from Chara corallina

β-1,3-Glucanase

Identified from Chara corallina and Arabidopsis. In the latter, shown to target as a GFP fusion to Pds. Knock-out mutant plants showed reduced GFP diffusion through Pds.

Heat shock cognate 70

Identified from Chara corallina and homologous to HSc70 from Nicotiana and shown to carry a Pd trafficking signal.

Myosin

A motor protein that may be used to traffic molecules through the pore, or may link the desmotubule to the plasma membrane. Could be used to control the SEL.  A unique plant myosin (myosin VIII) has been localised to, and may be specialised for, Pds

Pectin

A component of  the cell wall that is enriched around Pds

Pectin methylesterase (PME)

An enzyme involved in pectin de-esterification, it interacts with viral movement proteins and has been hypothesised to act as a Pd receptor protein

Peroxidase

Function unknown

Plasmodesmata located protein 1 (PDLP1)

A family of type I membrane receptor-like proteins targeted solely to Pds and with the property of changing reciprocally trafficking of GFP following altered expression. PDLP1 also carries a 21 amino acid signal sufficient for targeting proteins to Pds via the Golgi-ER secretory pathway.

PRms

A pathogenesis-related protein that both localises to, and moves through, Pds.  Function unknown, but may only transiently reside in Pds

Protein kinases

Involved in the phosphorylation or viral movement proteins, and possibly endogenous trafficking proteins.  May be used for protein phosphorylation signalling and control of the SEL.

Reversibly Glycosylated polypeptide (Class 1) - C1RGP

A 41 kDa protein identified from maize and Arabidopsis and shown to target Pds as GFP fusion. Usually associated with the Golgi apparatus, the function of these proteins is not known.

RNA binding proteins

Identified from Chara corallina

RTM1 protein

A protein that restricts the entry of Tobacco etch virus in the phloem.  May only transiently reside in Pds

Ubiquitin

May be involved in the turnover of Pd proteins, or the removal of Pds

Vesicle trafficking proteins

May be involved in delivery of exogenous structural or cargo proteins to Pds, and may be hijacked by viral movement protein to gain transport to the pore.  May also be involved in transport through the pore on the plasma membrane

WD40 repeat-containing protein

Function unknown, but likely to be involved in protein-protein interactions, so may be a docking or receptor protein

α-amylase

Function at Pds unknown

26- and 27-kDa proteins

Functions unknown, but PAP27 cross-reacts with a connexin32 antibody (see above)

45-kDa protein

Function unknown

5'-nucleotidase

Function unknown

Maize root proteins

Antibodies JIM64 and JIM67 raised against two unknown proteins label Pds.  Their functions are unknown

References associated with 1.I.2 family:

Amari, K., E. Boutant, C. Hofmann, C. Schmitt-Keichinger, L. Fernandez-Calvino, P. Didier, A. Lerich, J. Mutterer, C.L. Thomas, M. Heinlein, Y. Mély, A.J. Maule, and C. Ritzenthaler. (2010). A family of plasmodesmal proteins with receptor-like properties for plant viral movement proteins. PLoS Pathog 6: e1001119. 20886105
Benitez-Alfonso, Y., C. Faulkner, C. Ritzenthaler, and A.J. Maule. (2010). Plasmodesmata: gateways to local and systemic virus infection. Mol. Plant Microbe Interact. 23: 1403-1412. 20687788
Benitez-Alfonso, Y., D. Jackson, and A. Maule. (2011). Redox regulation of intercellular transport. Protoplasma 248: 131-140. 21107619
Faulkner, C. and A. Maule. (2011). Opportunities and successes in the search for plasmodesmal proteins. Protoplasma 248: 27-38. 20922549
Kim, G., M.L. LeBlanc, E.K. Wafula, C.W. dePamphilis, and J.H. Westwood. (2014). Plant science. Genomic-scale exchange of mRNA between a parasitic plant and its hosts. Science 345: 808-811. 25124438
Leblanc, M., G. Kim, and J.H. Westwood. (2012). RNA trafficking in parasitic plant systems. Front Plant Sci 3: 203. 22936942
Maule, A.J. (2008). Plasmodesmata: structure, function and biogenesis. Curr. Opin. Plant Biol. 11: 680-686. 18824402
Yahalom, A., R.D. Warmbrodt, D.W. Laird, O. Traub, J.P. Revel, K. Willecke, and B.L. Epel. (1991). Maize mesocotyl plasmodesmata proteins cross-react with connexin gap junction protein antibodies. Plant Cell 3: 407-417. 1668654