# 7: Modified and secondary plasmodesmata in higher plants

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primary plasmodesmata

secondarily-modified plasmodesmata

secondary plasmodesmata

Secondary PD formation

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Fig. 1

 

 

 

 

 

In 1996, Ehlers and Kollmann presented beautiful diagrams that clarified certain misconceptions relating to the use of the term ‘secondary’ and ‘secondarily modified’ as applied to plasmodesmata. This information was presented at the 3rd International Workshop on Basic and Applied Research in Plasmodesmal Biology, at Zichron Yakov, Israel in 1996.

During extension growth, it is quite possible that  degradation of outer wall material during stretching and concomitant new wall formation, can deform plasmodesma -- even branched ones, such that the 'arm' of the branches, appear further apart. This does not   constitute 'modification', simply, the  cell walls are extending laterally, thereby "stretching" the plasmodesmata, and deforming them.

The literature contains many references to morphologically distinct plasmodesmatal forms, some of which are branched, may have median cavities, or may be discontinuous and form branched half plasmodesmata. However, branching, formation of median cavities or nodules, does not warrant calling them "secondary plasmodesmata."  I have chose to review one paper in which the authors mistakenly refer to secondary plasmodesmata simply because the plasmodesmata in question are associated with viruses! This is not acceptable use of terminology, and it is important that the record be corrected.

This Factfile was prepared specifically to define the essential differences between primary plasmodesmata; secondarily modified plasmodesmata and secondary plasmodesmata.

 

IT is important that the terms primary, secondary and secondarily modified should be applied correctly when describing plasmodesmal structure and or origin.  

In many instances, the term "secondary plasmodesmata” is used when describing the effect that virus movement through plasmodesmata apparently has on the structure of plasmodesma, with the semi-automatic assumption that whenever viruses are involved, plasmodesma must be described as secondary! This is a misnomer and represents sloppy use of terminology, as will be explained in this Factfile.

In an article dealing with maize streak virus (MSV) in Zea mays, Dickinson, Halder and Woolston (1996) discussed the structure of the leaf blade, and the effect that infection by maize streak virus had on plasmodesmal structure. The authors made no reference to the large body of accepted evidence and information relating to the structure of the maize vascular bundle, and its plasmodesma. This is an example of a case where reference to the literature could have saved misinterpretation as occurs in the Dickinson et al., (1996) paper. Indeed, there are NO secondary plasmodesma in grasses. The anatomy of the maize and other grass leaves have been described in detail in past papers (see Evert et al. 1977; Ehlers and Kollmann, R (1996) Evert, et al.1978; Evert et al. 1985; Robinson-Beers and Evert, 199l and Botha 1992) for good examples of plasmodesmal structure, especially in Zea mays.

During extension growth, it is quite possible that  degradation of outer wall material during stretching and concomitant new wall formation, can deform plasmodesma -- even branched ones, such that the 'arm' of the branches, appear further apart. This does not   constitute 'modification', simply, the  cell walls are extending laterally, thereby "stretching" the plasmodesmata, and deforming them.

The literature contains many references to morphologically distinct forms of plasmodesmata, which may be branched, may have median cavities, or may be discontinuous and branched half plasmodesmata. However, branching, formation of median cavities or nodules, does not warrant calling them "secondary plasmodesmata."  I have chose to review one paper in which the authors mistakenly refer to secondary plasmodesmata simply because the plasmodesmata in question are associated with viruses! This is not acceptable use of terminology, and it is important that the record be corrected.

This Factfile was prepared specifically to define the essential differences between primary plasmodesmata; secondarily modified plasmodesmata and secondary plasmodesmata.

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Primary plasmodesmata.
By definition these are plasmodesmata that develop during the formation of the cell wall (phragmoplast) and then, only during cytokinesis.

When plasmodesmata are formed in the phragmoplast of differentiating cells, they are usually unbranched, but can, upon thickening of the wall, (particularly during the ageing process), can feasibly become extended as the wall thickens, and can become branched, possibly due to entrapment of the ER. Branches and median cavities are considered to be modifications of simple primary plasmodesmata, and are more correctly referred to as secondary modifications of primary plasmodesmata NOT as "secondary plasmodesmata." Click HERE to return to the Index.

Secondarily-modified plasmodesmata.

By definition these are primary plasmodesmata that have become modified during the later stages of cell growth and development, or through virus interaction or transmission are described as being secondarily-modified.

They are either indicative of lateral "divisions" of pre-existing cell connections ( Ehlers and Kollmann, 1996) or may possibly arise as a result of fusion of neighbouring plasmodesmata, due to local and highly restricted wall digestion (Jones, 1976). Lucas and Gilbertson (1994) support the latter mode of formation, but add that additional digestion could allow new cytoplasmic strands to appear, and that these technically constitute "secondary plasmodesmata." However, this term is confusing as it should be applied in an ontogenetic sense, and should not be based upon a morphological difference, especially where no direct evidence of the process exists or has been presented.

It should be clear therefore; that modifications of primary plasmodesmata must occur post-cytokinetically. Their potential mechanism of formation has been discussed frequently in the literature (see Ehlers and Kollmann, 1996, Lucas, Ding and van der Schoot, 1993).

The term "secondarily-modified plasmodesmata" is very widely accepted, and refers to those plasmodesmata which become modified and where there is strong evidence for some modification to the primary structure of the plasmodesmata. It is well-accepted that plant viruses must alter the structure of plasmodesmata to enable or allow viral passage through these otherwise complex structures. Click HERE to return to the Index.

Secondary plasmodesmata.

By definition, these are plasmodesmata that are formed de novo in the plant body, post cytokinesis, within formed cell walls, or between a graft union, or within sectorial chimeras See the  Ehlers and Kollmann paper for a full discourse.

Secondarily-formed plasmodesmal connections, refer to post cytokinetically-formed plasmodesmata, and are thus truly de novo, "secondary plasmodesmata." Put another way, primary plasmodesmata may undergo certain morphological changes during their functional lifetime, but they remain primary in terms of their ontogeny. Also, primary plasmodesmata may undergo some modifications during the maturation and ageing process, but, they do not change significantly from those that are produced during the first stages of cell division (see Ehlers and Kollmann 1996).

In contrast, there is some evidence for de novo formation of secondary plasmodesmata in the literature. One would expect a gradual loss of cell to cell connectivity with time, within regions where lasting extension growth of cell walls occurs in combination with continuous cell division has to occur for extended periods of time (Ehlers and Kollmann 1996). Under these conditions, one could assume a complete loss of connectivity in specialised wall areas. For example, the interface between differentiating epidermal and subepidermal cells, or between bundle sheath cells and vascular tissue, and possibly, between the radial walls of the progeny of the vascular cambium. In order to avoid isolation within these regions, de novo formation of truly secondary plasmodesmata must occur at these interfaces.

The term "secondary plasmodesmata" is thus correctly used ONLY where there is evidence of newly formed plasmodesmata in pre-existing cell walls that lacked plasmodesmata. Click HERE to return to the Index.

Turning to the situation in monocotyledons and specifically to Zea mays reported in the paper by Dickinson, Halder and Woolston (1996).There can be not are there, ANY secondary plasmodesmata in Zea mays. As far as can be ascertained from the literature, all plasmodesmata in Zea mays are primary, that is, they are formed during cytokinesis. The plasmodesmata between the bundle sheath cells and underlying vascular parenchyma may, however, become modified as the leaf ages. These would be secondarily-modified plasmodesmata according to the definition given earlier.

The article in question (Dickinson, Halder and Woolston (1996)) does not show any clear evidence for modification, nor do the authors identify the cell types with which the plasmodesmata illustrated in Figs. 5-6 in their paper, occur. The author's immunogold label is difficult to interpret and may be somewhat non-specific, more especially in Figs. 6b and d, where there is evidence of "labelling" within the primary cellulosic cell wall, some distance from the plasmodesmata! Fig. 6b is not convincing and the state of plasmolysis in Fig. 6c would generally be considered unacceptable from an ultrastructural point of view. Whilst apparently 'granular' material is evident within the plasmodesmata in Fig 6 a and 6c, the authors make no attempt to demonstrate structural changes within the plasmodesmata. They make no use of cross sections in their interpretation. Plasmodesmal structure and indeed, evidence for alteration due to the maize streak virus ORF1 would have been better illustrated in high-resolution cross sections, taken from sections showing different interfaces to those shown, but not described.

What is more confusing is the statement (on page 58) where the authors state that the "effect of PV1 on plasmodesmata is as yet, unclear" They go on to say that PV1 "clearly associates with secondary plasmodesmata, but we can only speculate on whether it associates more strongly with secondary plasmodesmata or whether it actually induces the formation of secondary plasmodesmata."  So, what is needed is more careful use of terminology - plant virus research is very important, but what is more important, is that the correct, or most appropriate terminology is applied at all times. Clearly, the term "secondarily modified' may be used -- but then only where is good evidence for some modification to the structure of the primary plasmodesmata - whether this is due to say, branching, or due to a clear, well-illustrated plasmodesmata-virus interaction. The loose application of the term secondary plasmodesmata should be avoided and can only be applied to those plasmodesmata that are formed post-cytokinesis. The electron micrographs in this particular paper are not that convincing either in terms of the plasmodesmal structure, nor for the virus localization for that matter. The bundle sheath cells of Zea mays do not have such secondary plasmodesmal structures, nor could they form in the cell interfaces illustrated by the authors, and no evidence for them having undergone some sort of modification is presented in this paper at at all.

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Fig. 1.

Fig. 1 shows branches as secondary modifications of primary plasmodesmata, developing during wall thickening. PL, plasmalemma; W, wall layers; ML middle lamella; NW, new wall layers; D, dictyosomes; G, Golgi vesicles. Modified and redrawn from: "Plasmodesmata in cell growth and differentiation". p 68-73. 3rd Intl. Workshop on Basic and Applied Research in Plasmodesmal Biology, Zichron Yakov, Israel.

 

 

 

 

 

 

 

 

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Selected references.

Aoki, K., Kragler, F., Xonconostle-Caares, B. and Lucas, W. (2002)  A subclass of plant heat shock cognate 70 chaperones carries a motif that facilitates trafficking through plasmodesmata.  PNAS  99 (25):16342-16347

Badelt, K., White, R., Overall, R. and Vesk, M. (1994)  Ultrastructural Specializations of the cell wall sleeve around plasmodesmata.  American Journal of Botany  81, 1422-1427.

Baluska, F., Cvrckova, F., Kendrick-Jones, J. and Volkmann, D. (2001)  Sink plasmodesmata as gateways for phloem unloading. Myosin VIII and calreticulin as molecular determinants of sink strength?  Plant Physiology  126, 39-46.

Blackman, L.M. and Overall, R.L. (2001)  Structure and function of plasmodesmata.  Australian Journal of Plant Physiology  28 (7):709-727.

Botha CEJ (1992) Plasmodesmal distribution, structure and frequency in relation to assimilation in C3 and C4 grasses in southern Africa. Planta 187: 348-358

Citovsky, V. (1993)  Probing plasmodesmal transport with plant viruses.  Plant Physiology  102, 1071-1076.

Dickinson VJ Halder J Woolston CJ (1996) The product of maize streak virus ORF V1 is associated with secondary plasmodesmata and is first detected with the onset of viral lesions. Virology 220: 51-59

Ehlers, K and Kollmann, R (1996) Formation of branched plasmodesmata in regenerating Solanum nigrum-protoplasts. Planta 199: 126-138

Evert RF Eschrich W Heyser W (1977) Distribution and structure of the plasmodesmata in mesophyll and bundle-sheath cells of Zea mays L. Planta 136: 77 89

Evert RF Eschrich W Heyser W (1978) Leaf structure in relation to solute transport and phloem loading in Zea mays L. Planta 138: 279 294

Evert RF, Botha CEJ, Mierzwa RJ (1985) Free-space marker studies on the leaf of Zea mays L. Protoplasma 126: 62 73

Evert, RF, Russin WA, and Botha CEJ, (1996) Distribution and frequency of plasmodesmata in relation to photoassimilate pathways and phloem loading in the barley leaf. Planta 198: 572-579

Robinson-Beers K, Evert, RF, (199lb) Fine structure of plasmodesmata in mature leaves of sugarcane. Planta 184: 307 318

Jones MGK (1976) The origin and development of plasmodesmata. In: Gunning BES Robards, AW (eds) Intercellular communication in plants: Studies on plasmodesmata. Springer, Berlin Heidelberg New York , pp81-105

Kollmann, R Ehlers, K, Glockmann Ch., and Schulz M (1996) Plasmodesmata in cell growth and differentiation. Proceedings of the Third International Workshop on Basic and Applied Research on Plasmodesmata Pp 68-73. Zichron Yakov, Israel.

Lucas, WJ, Ding, B, Van der Schoot, C (1993) Plasmodesmata and the supracellular nature of plants. New Phytol. 125: 435-476