Sci30264 Plant Anatomy and Physiology 1/2012 Endodermis and passage cell Bualuang FAIYUE, PhD. Endodermis and passage cell
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1 1. Endodermis and its development Endodermis is the innermost layer of the root cortex (Esau, 1965; Brundrett et al., 1990; Fahn, 1990; Peterson and Enstone, 1996). It is characterised by Casparian strip or Casparian band (Fig. 1) on the radial wall and the cross wall (or transverse wall) of the cell (Esau, 1965; Clarkson and Robards, 1975; Russell, 1977; Steudle and Peterson, 1998; Taiz and Zeiger, 2006). Fig. 1 Diagram of endodermal cell with Casparian strip on cross wall and radial wall (Fahn, 1990) Endodermis in the root of plants has three developmental states (Esau, 1965; Ferguson and Clarkson, 1975; Russell, 1977; Brundrett et al., 1990; Fahn, 1990; Peterson and Enstone, 1996; Seago et al., 2000a; Miyamoto et al., 2001; Soukup et al., 2002; Sottnikova and Lux, 2003). In the first state (state I) endodermis has only the Casparian strip in the radial wall and the transverse wall. The strip may extend over the whole of the radial width of the wall (Clarkson and Robards, 1975) or only one-third of endodermal areas (Ressell, 1977). Esau (1965) stated that the Casparian strip was formed during early stages of the root development. The strip usually takes place within a few millimeters from the root tip (Clarkson and Bobards, 1975), and matures at page 1
2 the same time or prior to the maturity of the primary vascular system (Esau, 1965; Fahn, 1990). There are several studies with respect to the appearance of endodermis and Casparian strip in the root of both terrestrial and aquatic plants. Clarkson and Robards (1975) together with Russell (1977) indicated that the Casparian band in the root of barley (Hordeum vulgare) was usually observed about 5 mm from the root apex. Ferguson and Clarkson (1975) reported that endodermal cells in Maize (Zea mays cv. Giant White Horsetooth) have fully developed Casparian bands in the whole region of mm from the apex. Also Peterson and Lefcourt (1990) reported that the Casparian band in lateral roots of broad bean (Vicia faba L. cv. Windsor) matures at 5 mm from the tip. Maize (Zea mays L.) which grown in hydroponic culture developed a Casparian strip at distances between 25 and 30 mm from the root tip (Freundl et al., 1998). In addition, Seago et al. (2000a) reported that Casparian bands in the endodermis of Pickerel weed (Pontederia cordata L.) were observed within 5 mm from the adventitious root tip. Seago et al. (2000b) also reported that White water lily (Nymphaea odorata Ait.) were observed endodermal Casparian bands within 10 mm of the root tip. In Gentian (Gentiana asclepiadea) Casparian bands appear at the distance about 4 mm from the root tip (Sottnikova and Lux, 2003). It can be concluded that the distance of the appearance of the endodermal Casparian strip varies depending on plant species. The chemical composition of the Casparian strip are still controversial between lignin and suberin substances. For example, Esau (1965) commented that the Casparian strip might be composed of lignin or suberin or both. Gemmell (1969) stated that Casparian strip was localized on the wall with lignin or suberin deposits. Clarkson and Robards (1975) concluded that suberin and lignin were the major components in Casparian bands. Similarly, Russell (1977) and Fahn (1990) indicated that the Casparian strips were deposited by lignin and suberin. Also Steudle and Peterson (1998) pointed out that the structure of Casparian band consisted of suberin and/or lignin. Equally, Brundrett (1999) defined that the endodermis is cylinder of cells with suberised wall. Moreover, Taiz and Zeiger (2006) described that the Casparian strip was impregnated with hydrophobic substance such as suberin. page 2
3 Although, there are various arguments about the components of Casparian strip, it can be concluded that suberin and lignin are the main substance in endodermal Casparian strip. Because of suberin and lignin, Casparian strip acts as a barrier to water and solute movement; it breaks the continuity of apoplastic pathway (Clarkson and Robards, 1975; Russell, 1977; Brundrett et al., 1990; Fahn, 1990; Steudle et al., 1993; Brundrett, 1999; Miyamoto et al., 2001; Ranathunge et al.,2004; Taiz and Zeiger, 2006). Casparian strip forces substances to enter endodermal cells by crossing their membranes (Esau, 1965; Salisbury and Ross, 1992; Taiz and Zeiger, 2006) as show in Fig. 2. So, the plasma membrane of endodermis is the final point that the root could control the entry of any solutes (Salisbury and Ross, 1992). Fig. 2 Casparian strip blocks apoplastic pathways of water at the endodermis (Salisbury and Ross, 1992) In the second state (state II) the endodermis is deposited with suberin (forming layers of suberin or suberin lamellae) over the entire inner tangential wall and the part of radial walls (Fig. 3) ( Esua,1965; Ferguson and Clarkson, 1975; Russell, 1977; Brundrett et al., 1990; Fahn, 1990; Peterson and Enstone, 1996; Seago et al., 2000a; Miyamoto et al., 2001; Soukup et al., 2002; Sottnikova and Lux, 2003). The deposition of suberin in endodermal cells was reported by Clarkson and Robards (1975) that these suberin lamellae page 3
4 decreased the movement of water and calcium into the stele of barley (cv. Midas) and marrow (Cucurbita pepo cv. Greenbush). Fig. 3 Diagram shows the position of thickening walls (X) and Casparian strip in the endodermis (Russell, 1977) In the final state (state III), a layer of cellulose is deposited along the inside of suberin lamellae (Esau, 1965; Clarkson and Robards, 1975; Ferguson and Clarkson, 1975; Russell, 1977; Brundrett et al., 1990; Fahn, 1990; Peterson and Enstone, 1996; Seago et al., 2000a; Miyamoto et al., 2001; Soukup et al., 2002; Sottnikova and Lux, 2003). The thick cellulosic wall of the state III cell normally appears either as O type when cellulose deposits around the cell or as C type when it deposits only on the radial wall and inner tangential wall (Clarkson and Robards, 1975). The thick wall of endodermis may become lignified (Esau, 1965; Fahn, 1990) and may have pits (Esau, 1965). As illustrated by Russell (1977), the mature endodermal cell with thickened wall has pits and plasmodesmata (Fig. 4). Moreover, Peterson and Enstone (1996) illustrated the picture of pits in the inner tangential walls of Smilax sp. root, and indicated that suberin lamellae and thick walls of the endodermis do not prevent ion movement through the stele by symplastic pathway. page 4
5 Fig. 4 Four plasmodesmata (arrow) at the pit of mature endodermal cells (Russell, 1977) However, the developmental states of endodermis are incomplete in some plants. For example, Seago et al. (2000a,b) reported that Pickerel weed (Pontederia cordata L.), Marsh marigold (Caltha palustris L.), and White water lily (Nymphaea odorata Ait.) developed state I of endodermis only, as shown in Fig. 5. A B C Fig. 5 Endodermal Casparian band state I (arrow) of (A) Pickerel weed (Pontederia cordata L.), (B) Marsh marigold (Caltha palustris L.) and (C)White water lily (Nymphaea odorata Ait.) (Seago et al., 2000a,b) page 5
6 2. Passage cell Sci30264 Plant Anatomy and Physiology 1/2012 The thickening walls of the endodermis do not develop simultaneously in all endodermal cells. The first development occurs opposite the phloem groups and then spread to the part of endodermal cells opposite the xylem (Esau, 1965; Gemmell, 1969; Clarkson and Robards, 1975; Fahn, 1990); as a consequence, the endodermal cells opposite the xylem have only Casparian strip because of the delay on the wall development, and these cells are called Passage cells (Esau, 1965; Clarkson and Robards, 1975; Fahn, 1990; Peterson and Enstone, 1996) as shown in Fig. 6. However, passage cells may remain as unmodified walls or develop to the thick wall state II and III later (Esau, 1965; Fahn, 1990; Peterson and Enstone, 1996). Fig. 6 Cross section of an ash tree (Fraxinus sp.) root staining with Fluorol for suberin lamellae in exodermis (ex) and endodermis (en) with passage cells (arrows) (Brundrett, 1999) Suberin lamella on the wall of endodermis is a hydrophobic mixture between lipids and phenolic compounds (Brundrett, 1999). It is derived from polymerization of unsaturated fatty, and this process activated by oxidases and peroxidases. The later enzymes are translocated to endodermis via the sieve element of the phloem. Due to this reason the greatest amount of suberin is mainly deposited on inner wall of endodermis and passage cells mostly occur opposite the xylem (Clarkson and Robards, 1975; Fahn, 1990). This was supported by the work of Sottnikova and Lux (2003) who reported that suberin page 6
7 lamellae in the endodermis of Gentian (Gentiana asclepiadea) first appeared in the cells opposite the phloem poles (Fig. 7). Fig. 7 Casparian band in the endodermis (arrow) of Gentiana asclepiadea root at a distance of 5 mm from the apex (Sottnikova and Lux, 2003) The meaning of passage cells was given by Esau (1965, p.493) that The name passage cells is based on the assumption that the cells allow a limited transfer of material between the cortex and the vascular cylinder This assumption was supported by Clarkson et al. (1971) (see Fahn(1990)) who concluded that water and phosphate in Barley roots can pass into the stele via passage cells. Furthermore, Peterson and Enstone (1996) pointed out that calcium and magnesium were transferred into the stele through passage cells. So, passage cells in the root are the areas that solutes from cortex can pass to the stele. page 7
8 References Brundrett M. (1999) Roots. [online] CSIRO Forestry and Forest Products. Available from: [accessed 21 February 2007] Brundrett M, Kendrick B, Peterson CA Efficinet Lipid Staining in Plant Material with Sudan Red 7B or Fluoral Yellow 088 in Polyethylene Glycol-Glycerol. Biotechnic&Histochemistry 66, Brundrett M, Murase G, Kendrick B Comparative Anatomy of Roots and Mycorrhizae of Common Ontario Trees. Canadian Journal of Botany-Revue Canadienne De Botanique 68, Clarkson DT, Robards AW The endodermis, its structural development and physiological role. In the development and function of roots. Edited by J.G. Torrey and D.T. Clarkson. Academic Press, London, pp Esau K Plant Anatomy. 2 nd edition. John Wiley & Sons, Inc., New York. Fahn A Plant anatomy. 4 th ed. Pergamon press, Oxford. Ferguson IB, Clarkson DT Ion Transport and Endodermal suberization in the Roots of Zea mays. New Phytol 75, Freundl E, Steudle E, Hartung W Water uptake by roots of maize and sunflower affects the radial transport of abscisic acid and its concentration in the xylem. Planta 207, Gemmell AR Developmental Plant Anatomy. Edward Arnold Publishers. Miyamoto N, Steudle E, Hirasawa T, Lafitte R Hydraulic conductivity of rice roots. Journal of Experimental Botany 52, Peterson CA, Enstone DE Functions of passage cells in the endodermis and exodermis of roots. Physiologia Plantarum 97, Peterson CA, Lefcourt BEM Development of endodermal Casparian bands and xylem in lateral roots of broad bean. Can. J. Bot. 68, Ranathunge K, Kotula L, Steudle E, Lafitte R Water permeability and reflection coefficient of the outer part of young rice roots are differently affected by closure of water channels (aquaporins) or blockage of apoplastic pores. Journal of Experimental Botany 55, page 8
9 Russell RS Plant root systems: their function and interaction with the soil. McGraw-Hill Book company, London. Salisbury FB and Ross CW Plant physiology. 4 th ed. Wadsworth puplishing company, California. Schreiber L, Franke R, Hartmann KD, Ranathunge K, Steudle E The chemical composition of suberin in apoplastic barriers affects radial hydraulic conductivity differently in the roots of rice (Oryza sativa L. cv. IR64) and corn (Zea mays L. cv. Helix). Journal of Experimental Botany 56, Seago JL, Peterson CA, Enstone DE. 2000a. Cortical development in roots of the aquatic plant Pontederia cordata (Pontederiaceae). American Journal of Botany 87, Seago JL, Peterson CA, Kinsley LJ, Broderick J. 2000b. Development and structure of the root cortex in Caltha palustris L. and Nymphaea odorata Ait. Annals of Botany 86, Sottnikova A, Lux A Development, dilation and subdivision of cortical layers of gentian (Gentiana asclepiadea) root. New Phytologist 160, Soukup A, Votrubova O, Cizkova H Development of anatomical structure of roots of Phragmites australis. New Phytologist 153, Steudle E, Murrmann M, Peterson CA Transport of Water and Solutes across Maize Roots Modified by Puncturing the Endodermis - Further Evidence for the Composite Transport Model of the Root. Plant Physiology 103, Steudle E, Peterson CA How does water get through roots? Journal of Experimental Botany 49, Taiz L and Zeiger E Plant physiology. 4 th ed. Sinauer Associates, Inc., Publishers, Massachusetts. page 9
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