Plasmodesmata and the control of symplastic transport

Abstract

‘There are holes in the sky where the rain gets in, but they’re ever so small that's why rain's so thin’ In 1879 Eduard Tangle discovered cytoplasmic connections between cells in the cotyledons of Strychnos nuxvomica, which he interpreted to be protoplasmic contacts. This led him to hypothesize that ‘the protoplasmic bodies . . . are united by thin strands passing through connecting ducts in the walls, which put the cells into connection with each other and so unite them to an entity of higher order’ (Carr 1976). This challenged the then current view that cells functioned as autonomous units. It was after much research in many other species and cell types that Strasburger, in 1901, named these structures plasmodesmata (Carr 1976). During the division and differentiation of meristematic cells, plasmodesmata are formed across each developing cell plate, allowing cytoplasmic and endomembrane continuity to occur between all daughter cells, and ultimately, between all cells in a developing tissue (Mezitt & Lucas 1996). Those plasmodesmata that form during cell division are termed primary plasmodesmata (Jones 1976). Those that form de novo across existing cell walls are called secondary plasmodesmata (Ehlers & Kollmann 2001). The formation of secondary plasmodesmata allows cells to increase their potential for molecular trafficking and allows connections to be created between cells that are not related cytokinetically. As cells expand and differentiate, their fate determines the extent to which their cytoplasmic connectivity to other cells is maintained (Mezitt & Lucas 1996). Some cell types, such as those of the leaf mesophyll, remain closely connected to their neighbours, and may even lay down additional plasmodesmata to increase the continuity (Ding et al. 1992a). In other areas of the plant, for instance in vascular tissue, certain cells greatly reduce the number of plasmodesmata in their adjoining walls (Gamalei 1989). In this way, the cytoplasmic continuity can be altered depending on the tissue type (Botha & Evert 1988; Brown et al. 1995). However, although reductions in the number of plasmodesmata are common, only guard cells surrounding stomata (Erwee, Goodwin & van Bel 1985; Palevitz & Hepler 1985) and differentiating xylem elements (Lachaud & Maurousset 1996) lose all symplastic connections In all other cells, of connection is This that the is termed the However, the is not the that but is into each by of plasmodesmata & Goodwin 1985; & Kollmann 2001). are of as structures that can be and to with the of cells and on types of plasmodesmata and plasmodesmata of a the cell plasmodesmata on of the by a of plasmodesmata are in and and in form in plasmodesmata may be in primary and this form to in et al. plasmodesmata are in the such as and & Lucas et al. plasmodesmata are in and to structures & van et al. primary and secondary plasmodesmata are in during tissue may form with plasmodesmata to During the that in plasmodesmata are to plasmodesmata by a that the formation of between adjoining et al. et al. 2001). through plasmodesmata between vascular cells in a plasmodesmata and with Evert and & through plasmodesmata between vascular cells in a The of the as a The cytoplasmic to the of that the of the the of the with and & and of the of plasmodesmata in and cell cytoplasmic on in et al. of the to During the into a with a the of the cell This an that to form by the of a protoplasmic between of cell et al. to the of plasmodesmata on & Lucas & & & & et al. plasmodesmata as in the cell & each by the which is between In the of the a of the & Lucas et al. Lucas & of the & to a with an et al. that as a The in an and & & Evert et al. It is that cytoplasmic and the between the and a as the cytoplasmic & to cell to cell & Lucas & However, trafficking between cells the & Goodwin of the in the the is and the cytoplasmic may be with The are to in a that may the into a number of et al. et al. & & Lucas & & Evert Lucas & Lucas et al. & et al. This to reduce the of the cytoplasmic that are between and in et al. It is that these may be of an that can the of and which may to plasmodesmata in to cell to cell & et al. 1996). an of surrounding the of the the that may to the of the & & et al. & the of plasmodesmata to this a of in species and of the & Evert et al. is the that to the of and not and of many small through plasmodesmata the cytoplasmic et al. et al. and et al. 1985; & Lucas et al. this and may the cytoplasmic & that was not cytoplasmic was by with although by a of that cytoplasmic on the of that the of small by and that through plasmodesmata is the for et al. & 1989). that the is closely with and the a potential for between structures of the et al. that the as a to be a with an & de & that and between cells and these in the However, to between cells to the This that may between cells the that the et al. that small into the of a cell of into adjoining can only occur through the the occur in by the by the by of to the cytoplasmic of the by through the cytoplasmic This of may be plasmodesmata between and cells, as is in but the a between the of the and the of the cell et al. & van Bel & are the of the to occur by The is as the of plasmodesmata in that for that increase the and are all to by through the cytoplasmic of plasmodesmata Lucas et al. the in which occur in the are not as plasmodesmata are of in their It is that the of an and between The can be by with a number of and other although many that the of plasmodesmata was between and in Lucas et al. and cell types can a & Goodwin 1985; et al. that for many cells the is higher these the that determines the of a through plasmodesmata is the & that the of is to the of the and that small in the in the of molecular on these was that the of in the cytoplasmic of a is This is a that to (Ding et al. and & Goodwin However, a of the & that the may be to a that a to the potential of the an increase in to may the of that can through the to and increase the of to & et al. of through plasmodesmata may be as may a between a of the with other plasmodesmata et al. & and can trafficking (Mezitt & Lucas et al. & trafficking is by et al. and by a number of can through plasmodesmata in of where plasmodesmata are in and a & et al. However, of is in of where plasmodesmata are and a et al. et al. 2001). in the of plasmodesmata during of a tissue to be symplastic is in but this with to symplastic as cells and & van et al. In cells in the and are connected by but so as in the the and are cell et al. & Goodwin that the symplastic of cells in tissue was during but as formation was of trafficking that plasmodesmata are in and in was to between cells in leaf and all and was to in the of et al. between cell to be a cell not the into the of cotyledons although the into the of et al. During of plasmodesmata to be by a that of the developing tissue & Kollmann The that the by the surrounding cells and not the and that of symplastic be a for may a number of depending on the tissue and species of plant, the of plasmodesmata and the of such as and to the et al. & & Some that this may and of the of the & that these elements are in a in the of the & 2001). The is by the that of and not to the of small that through plasmodesmata by that and are not in the of In of the by in a of the of plasmodesmata in et al. and an increase in the of plasmodesmata to & 1996). However, by with was in which a was into a that the which by not between cells & that may form a which a The to be in an in the and cells of species & 2001). The is to be closely with & et al. and the to et al. other that the to the endomembrane to between cells in the but not in the et al. This that the may through plasmodesmata the is a can between cells in this way, may be that other a on the the through plasmodesmata the In are for this to of as all the the of the et al. to the of through In cells, of molecular and the of the & although this be to an increase in plasmodesmata the et al. In cells, a the of (Ding et al. and of even in with a The of and the of the as that the to the & a for the of the cytoplasmic & et al. an only in to plasmodesmata et al. and be by & et al. 2001). of these a that a for as as & as a for a may be by may occur the of the plasmodesmata by the of and the of the but occur only the the a to the of plasmodesmata & and the increase in the of cytoplasmic a in the of this & This the to the & et al. to this that of to & Goodwin et al. and the that to cell walls plasmodesmata et al. et al. In and to plasmodesmata in & and the to plasmodesmata et al. 2001). is in the of the but that However, although in cytoplasmic to increase the of cytoplasmic with the and not et al. 2001). et al. that a was and was with the of This was to the of a to be to and plasmodesmata et al. of this led to altered et al. and may be a to as the of et al. et al. and et al. all to be The of plasmodesmata that of by may an in are to their in to In to the of the by that to are to with that as a of In cells, of between cells the of & However, to between The of plasmodesmata a of and the for In the plasmodesmata to (Ding & & In an increase in the of by of not an in the of cells, that plasmodesmata not 1996). tissue to in that the of plasmodesmata to to the as the of the In to the these In the was for a of & Goodwin these that a between cells, as occur during of cells their neighbours, an in tissue of to an In the the increase in may be with the to increase into can In a of of the to increase in to between and in & Lucas that was to plasmodesmata in a However, although to the potential of cells, on the the which is a of & that their to the that of and occur the and the and that only the is by that may the to which in the cytoplasmic and the by et al. in & of to increase symplastic of the in & cytoplasmic of & Goodwin to in a of with in & In plasmodesmata to be to a of a that their in between cells and plasmodesmata to although the of are that this may be in to as a However, plasmodesmata in the of by the surrounding & van & van 2001). During is plasmodesmata & but and to be in and in During the of to was but after was of in these cells the of & to In in was of & Goodwin the of plasmodesmata to in the the potential of and plasmodesmata with to in the cytoplasmic which the (Botha & et al. that a in the and an of in the of be by of the tissue with an of that is in the to be in cells to in areas to plasmodesmata in a a in the & but not an of the It is to although the of are to be other many that can the the that may be only in to is to be by in of by of an increase in cytoplasmic and only in to and not to & Lucas et al. that plasmodesmata may be a for in et al. is in as a of can occur in the of across & However, in the is by which plasmodesmata the between and vascular cells (Botha et al. During that is a to on but to plasmodesmata during by the & in and the surrounding walls of with & In these was but be the that formation of plasmodesmata be an this plasmodesmata in with many other & & & et al. et al. and In in a to with et al. & and to and & plasmodesmata in to and a in the that that the and on et al. 2001). & that of in with a number of other these that of be a by to their and & et al. & In to in the of their can be altered in tissue types the are of plasmodesmata and & Goodwin a of into and that the between This that the is not a with but is into and the on the of are to and in et al. & Kollmann & 2001). As guard cells differentiate, is across the on the of the cell plasmodesmata and the guard cell & Lucas Palevitz & Hepler In differentiating xylem tissue of many plasmodesmata are in the that xylem elements to the surrounding However, during the of cell the by the of across of the (Lachaud & Maurousset 1996). The of is to into to a of plasmodesmata the et al. 1996). This by of et al. et al. across the It that a in the between the and in This in the the differentiation of cells during the to of across plasmodesmata the (Mezitt et al. 2001). the of plasmodesmata may the and of such as the molecular that that to of symplastic During the in the of plasmodesmata are et al. 2001). Some of this to occur by the of plasmodesmata to plasmodesmata et al. However, that many plasmodesmata are during leaf of these plasmodesmata are during the of leaf cell are in the of these plasmodesmata in the and are during leaf It that these plasmodesmata are for a during which the leaf as a for et al. 2001). In the between cells in areas of the during the to et al. plasmodesmata in the of as cells into cells Bel & van is during a the the of et al. that symplastic is a to and and differentiation in the of and the potential a symplastic This of symplastic in the of but to of & 2001). In these cells, a to with a of the in these cells & et al. 2001). can be for the as for In plasmodesmata of those to secondary between cells not & Kollmann 1996). The of in these may to a for this in the and of between plasmodesmata and and that may the of and through types of & Lucas of the of was by that the that determines the of was in the It is that that between the and cell of are for During the many and discovered to in that to be the of 2001). The to all of the and in of and which to the and the In cells in the and cell & 1985; 1989). where cell is not related to the was that be between & In the the number of and of the although these are formed cells in the and & The was the to between cells & The was in the of the although was to the and The that between cells was by of into leaf cells et al. and et al. that the was not only of trafficking between cells in the leaf and the et al. but the and between cells in et al. 1995). However, is that although can into the and in mesophyll, that the is to with the into the of the This that of the is in the and that of the even in the of the is other may through plasmodesmata (Mezitt & Lucas 1996) but this may not be the for all such to the of a to the and a to cell to cell et al. The a in the of et al. that a is to the trafficking of an and et al. that a with a in the of but allowing of the & that an that is in to between This was in and was in the cells of the and of the was only in cells of the of the of in and of and are by of In to the of in a number of and to in a the not is only in the and of the is in all of the et al. The is only in the and but the in the with in the and et al. 1996). only in the in all the but with a of into et al. In the only in the cell in which the is that this not between cells of the & 2001). only in a small of cells the in the and a cells in the It is that the is to the and then through the into the of the by on the allows of the et al. number of that and & that to in which the is only in the of the the can be in a number of cell & and which can developing et al. 1996). The can the into the but not in the et al. 1996). an only on cells in and not on cells in the & In other such as and in the not all & 2001). In the of a a called et al. et al. & It is that a small by to a in to that are for is only in a small of cells the of the but the is to into of the where the cell to et al. et al. In to the symplastic to be by other and by et al. that the is through the and to the The is to through the into the where and the the to cell the et al. et al. by & van that the of symplastic to It that an of as for may between areas of the that are not et al. the of in the the of the of a into cells of In in cells and to cells are the in to the fate of cells et al. that of the The a for formation of the and that this not form an et al. In that the is only in the vascular but the is in the vascular tissue and in the et al. 2001). In the of in the vascular was and but in the was This that the cytoplasmic cell the vascular through into the where that was the the cell to and that of a in the as the can be to et al. 2001). the that the of and is for and may to for the is not in the of the the of in an The is to a et al. a of in which plasmodesmata et al. the trafficking of et al. the of and is is not that cell to but that not their of and a of allowing this of to the plasmodesmata into cells, but the their into cells to a and between the and the plasmodesmata in meristematic the that with a for the of a the the and the developing of the the is in the of all cell The cell walls are with of number of to but these are in this by van in this However, many of the to between cells in the through the to in In between of the and their to be in et al. through the & It be that although a number of to through the plasmodesmata that elements and cells of the and to in that this of This that trafficking in the occur in of may be with between each and However, that such a of the and even that for such as The and is that trafficking and through the is and not on with In to are a through the in in with and the can in The allows the of and in the and can cell to the during the et al. may this and other to the of through the to the of in developing of et al. et al. a and the of to with & 2001). This can with are that is to cell to cell through plasmodesmata et al. and can through the et al. in to other may be through the by with et al. 2001). can in a to is in that not for a to the during The by to as a that can the of through the & to through the and in of of the which may be in was to and in and the of a for into developing of a that and the & Lucas of trafficking that is this et al. that of the leaf a through the and a in leaf The to the areas of the as in and that the of was to trafficking of the et al. 2001). This not that the altered in tissue of the was to the a secondary such as a the as by However, this the of trafficking in It that as in the to and et al. & Lucas & in is a to et al. & are to through for can guard cells of but are these cells in tissue et al. that is by of into a cells can into cells and the allowing of the et al. & that can to cells that not the the of that with the which as & et al. 2001). The are to be species & which can the and in et al. in a that the of & This is as a a number of that the are not for of the a to and and are for the and of the et al. 2001). that additional are and that and symplastic in is to be the only in which a was to with plasmodesmata to the of and cell to As many on in that into cells with a et al. Lucas & et al. et al. 1995). The that trafficking can occur in the of a that these to be of to This led to a as to may that by and to & by and & Lucas 1996). for and plasmodesmata an that can be and by to them to & 2001). the vascular & Lucas & et al. 1996). the to for this a of that is by the of & and that are to the is in of & However, the the to the are into and of the vascular tissue et al. & van Bel Some through plasmodesmata as to such as and by to the allowing the to through the et al. 1995). such as and not but through the as & & et al. of by and to allowing the to as a and for which plasmodesmata & & et al. Lucas & The of that a for is to the of and can of those that as that et al. which be In of this was that the of a which an can and with & & 1995). However, be to this and into such as those by Some to be related to et al. and for the of The is the of Some this was to the of plasmodesmata in cells to cell to cell & et al. & et al. The to to plasmodesmata & et al. in with the and the et al. only in plasmodesmata (Ding et al. et al. et al. et al. 2001). The et al. and with the and et al. & & et al. et al. The to form a with the and many of as the for the to the et al. et al. & The a and with an altered with which and although the to et al. a that this to but was to plasmodesmata between cells, and with to et al. 2001). However, a that is to and in the of a of current for et al. The is in of the as is the but to the for to be In cells, and in the and of to the that the a in trafficking & & and for the & cells on a leaf of the The is to plasmodesmata in the walls between the cells in the is in the the is only in plasmodesmata the to plasmodesmata in the walls between elements to the for as a that a and et al. et al. the the with the and in the et al. However, are that between the elements et al. and although for not to plasmodesmata et al. and of that can with a number of such as that may during et al. and with to and an of the during et al. 2001). The of is to that may be in The with et al. et al. an that the in cell this was for with other and to et al. on the and of this of the et al. to plasmodesmata et al. and to et al. that is a for a in in the are discovered in to the the of and the related & and and in the of et al. et al. 2001). and are only in elements and their is to and not a of et al. et al. of such may these by of the through plasmodesmata in the potential was discovered the to for that with the a to be for through plasmodesmata et al. 2001). was to with the and in was of and was to the cytoplasmic which may be that the may be to a et al. a of in through the endomembrane and with the are to is with of to the small of in and the in that are of et al. 1995). to such to but of the the et al. of the in with is to be that a of the and are for and potential by the the of between cells but was the & in tissue are to as are the The that elements and cells are in this by van in this and not be with many is a between through plasmodesmata in and into and through the vascular tissue & Lucas 1996). may be a for into the the between the vascular cells and the cell & & but of into the is the are with the of and in the of that their et al. only a & et al. additional the are to a et al. 1995). In the of to and as as to the cell to plasmodesmata et al. 2001). can in their with plasmodesmata and the to the to plasmodesmata in the a (Ding et al. although this plasmodesmata a It that the is not in the & but even plasmodesmata are not by this in is for in et al. 2001). In the of to all plasmodesmata in the those that elements and cells et al. the plasmodesmata in and et al. 2001). of plasmodesmata as in the walls between cells are The current that is in which plasmodesmata as structures that can of the that through many plasmodesmata such as those in is that are in between plasmodesmata in and a In the that of discovered in types of in et al. & in the not be to that and their be into that the This of a is only to with the that types of plasmodesmata et al. a small number of discovered by et al. 1995). The of to be in plasmodesmata discovered is a for that to the of and to the of may to the of that to that the is of other is that the of of not that be discovered through this Some may only with plasmodesmata to their may on ever to in is the of et al. et al. to a on that is not primary in (Mezitt et al. 2001). the of on a for the the of the tissue such as that for the & et al. be to the of and The for the is not to of and but to in this with the to the molecular of The are by by the and The to for and for the of in form for