*2.1.2 Sieve tube elements and companion cells*

A synapomorphy of the angiosperms is the presence of sieve tube elements and companion cells, both sister cells derived from the asymmetrical division of a single mother cell. In some instances, these mother cells can divide many times, creating assemblages of sieve tube elements and parenchyma cells

#### **Figure 3.**

*The secondary phloem of conifers. (a) Transverse section of the secondary phloem of Sequoia sempervirens (Cupressaceae) showing alternating tangential bands of sieve cells, axial parenchyma, and fibers, interrupted by uniseriate rays. (b). Longitudinal radial section (LR) of the secondary phloem of Sequoia sempervirens (Cupressaceae) showing alternating tangential bands of sieve cells, axial parenchyma, and fibers, interrupted by uniseriate rays. Sieve pores distributed across the walls of long sieve cells. (c). LR section of Pinus strobus (Pinaceae) showing the elongated marginal ray cells in close contact with the sieve cells. These are the Strasburger cells. f and rectangular symbol = fibers, s and \* = the sieve cells, p and dot = axial parenchyma cells rich in tannins. Scalebars: a, b = 100 μm, c = 50 μm.*

ontogenetically related [15]. Sieve tube elements have specialized areas in the terminal parts of the sieve elements in which a sieve plate is present (**Figures 2b** and **c**). Within the sieve plate, the pores are much wider than those of the lateral sieve areas, evidencing a specialization of these areas for conduction [16]. In *Cucurbita*, the pores in the sieve plate have up to 10 μm in diameter, while the pores in the lateral sieve areas are of about 0.1 μm [7, 17]. The protoplast of sieve tube elements contain a specific constitutive protein called P-protein (P from phloem, also known as slime; **Figure 2b**), which in some taxa (e.g., *Leguminosae*) is nondispersive and can be seen as coagula inside of the sieve element [18].

Even in lineages of angiosperms where vessels were lost and tracheids reevolved, such as *Winteraceae* in the *Magnoliids* and *Trochodendraceae* in the *eudicots*, sieve elements and companion cells are present [19], suggesting the independent evolution of these two plant vascular tissues derived from the same meristem initials. Since the sieve tube element loses its nucleus and ribosomes, the companion cell is the cell responsible for the metabolic life of the sieve elements, including the transport of carbohydrates in and out the sieve elements [7]. Companion cells may be arranged in vertical strands, with two to more cells (**Figure 2b**). Other parenchyma cells around the sieve tube integrate with the companion cells and can also act in this matter [7]. Typically, the cells closely related with the sieve tube elements die at the same time as the sieve element loses conductivity.

Sieve tube elements vary morphologically. The sieve plates can be transverse to slightly inclined (**Figure 2b**) or very inclined (**Figure 2c**) and contain a single sieve area (**Figure 2b**) or many (**Figure 2c**). When one sieve area is present, the sieve plate is named simple sieve plate, while when two to many are present, the sieve plates are called compound sieve plates. Compound sieve plates typically occur in sieve tube elements with inclined to very inclined sieve plates (**Figure 2c**). In addition, sieve elements with compound sieve plates are typically longer than those with simple sieve plates. Evolution to sieve elements of both sieve area types has been recorded in certain lineages, such as in *Arecaceae*, *Bignoniaceae*, and *Leguminosae* [5, 20], and to the present it is not still clear why the evolution of distinct morphologies would be or not beneficial. The only clear pattern is that compound sieve plates appear in long sieve elements [1], and phloem with a lot of fibers generally has compound sieve plates [20].

#### **2.2 Parenchyma**

In the primary phloem, just one type of parenchyma is present and typically intermingles with the sieve elements (**Figure 1d**). In the secondary structure, there are two types of parenchyma: axial parenchyma and ray parenchyma (**Figures 2b**, **c**, **3b**, **c**), derived, respectively, from the fusiform and ray initials of the cambium.

The axial parenchyma in conifers commonly is arranged in concentric, alternating layers (**Figure 3a** and **b**). These parenchyma cells contain a lot of phenolic substances, which were viewed as a defense mechanism against bark attackers [21]. In Gnetales, the phloem axial parenchyma appears to be intermingling with the sieve cells (**Figure 4a**) [22]. Some of these axial parenchyma cells act as Strasburger cells [13].

In angiosperms, the distribution of the axial phloem parenchyma is more varied, and it may appear as a background tissue where other cells are dispersed or may be in bands (**Figure 4b** and **c**) and radial rows or sieve-tube-centric (**Figure 4d**) [5, 20]. The distribution of axial phloem parenchyma is commonly related to the abundance of fibers or sclereids. In species with more fibers, it is common to have a more organized arrangement of the parenchyma. For example, in *Robinia pseudoacacia* (*Leguminosae*) there are parenchyma bands in either side

**7**

**Figure 4.**

of the concentric fiber bands (**Figure 4c**). When very large quantities of sclerenchyma are present, such as in the secondary phloem of *Carya* (*Juglandaceae*) or in *Fridericia*, *Tanaecium*, *Tynanthus*, and *Xylophragma* (*Bignoniaceae*), the

*sp, secondary phloem; sx, secondary xylem. Scalebars: a = 50 μm; b, d = 200 μm; c = 100 μm.*

*Phloem axial parenchyma distribution in secondary phloem. (a) Ephedra tweediana (Ephedraceae) TS, showing sieve cells interspersed by axial parenchyma cells (arrows). Six to five cells away from the cambium, the sieve cells already lose conductivity and collapse with axial parenchyma cells enlarging (top arrow). (b) Lannea discolor (Anacardiaceae) TS showing axial parenchyma with tannins arranged in narrow bands (arrows). There are also other parenchyma cells with less content dispersed in the phloem. Note also the fibers in concentric bands. (c) Robinia pseudoacacia (Leguminosae) TS showing bands of axial parenchyma associated with the fiber bands and sieve tube elements in clusters with simple sieve plates staining with resorcin blue. (d) Fridericia nigrescens (Bignoniaceae) TS with sieve tubes surrounded by sieve-tube-centric axial parenchyma. The tissue background corresponds to the fibers. c, cambium; sx, secondary xylem; c, cambium;* 

*Phloem: Cell Types, Structure, and Commercial Uses DOI: http://dx.doi.org/10.5772/intechopen.88162*

*Phloem: Cell Types, Structure, and Commercial Uses DOI: http://dx.doi.org/10.5772/intechopen.88162*

*Plant Science - Structure, Anatomy and Physiology in Plants Cultured in Vivo and in Vitro*

die at the same time as the sieve element loses conductivity.

Sieve tube elements vary morphologically. The sieve plates can be transverse to slightly inclined (**Figure 2b**) or very inclined (**Figure 2c**) and contain a single sieve area (**Figure 2b**) or many (**Figure 2c**). When one sieve area is present, the sieve plate is named simple sieve plate, while when two to many are present, the sieve plates are called compound sieve plates. Compound sieve plates typically occur in sieve tube elements with inclined to very inclined sieve plates (**Figure 2c**). In addition, sieve elements with compound sieve plates are typically longer than those with simple sieve plates. Evolution to sieve elements of both sieve area types has been recorded in certain lineages, such as in *Arecaceae*, *Bignoniaceae*, and *Leguminosae* [5, 20], and to the present it is not still clear why the evolution of distinct morphologies would be or not beneficial. The only clear pattern is that compound sieve plates appear in long sieve elements [1], and phloem with a lot of fibers generally has compound sieve

In the primary phloem, just one type of parenchyma is present and typically intermingles with the sieve elements (**Figure 1d**). In the secondary structure, there are two types of parenchyma: axial parenchyma and ray parenchyma (**Figures 2b**, **c**, **3b**, **c**), derived, respectively, from the fusiform and ray initials of the cambium. The axial parenchyma in conifers commonly is arranged in concentric, alternating layers (**Figure 3a** and **b**). These parenchyma cells contain a lot of phenolic substances, which were viewed as a defense mechanism against bark attackers [21]. In Gnetales, the phloem axial parenchyma appears to be intermingling with the sieve cells (**Figure 4a**) [22]. Some of these axial parenchyma cells act as Strasburger

In angiosperms, the distribution of the axial phloem parenchyma is more varied, and it may appear as a background tissue where other cells are dispersed or may be in bands (**Figure 4b** and **c**) and radial rows or sieve-tube-centric (**Figure 4d**) [5, 20]. The distribution of axial phloem parenchyma is commonly related to the abundance of fibers or sclereids. In species with more fibers, it is common to have a more organized arrangement of the parenchyma. For example, in *Robinia pseudoacacia* (*Leguminosae*) there are parenchyma bands in either side

ontogenetically related [15]. Sieve tube elements have specialized areas in the terminal parts of the sieve elements in which a sieve plate is present (**Figures 2b** and **c**). Within the sieve plate, the pores are much wider than those of the lateral sieve areas, evidencing a specialization of these areas for conduction [16]. In *Cucurbita*, the pores in the sieve plate have up to 10 μm in diameter, while the pores in the lateral sieve areas are of about 0.1 μm [7, 17]. The protoplast of sieve tube elements contain a specific constitutive protein called P-protein (P from phloem, also known as slime; **Figure 2b**), which in some taxa (e.g., *Leguminosae*) is nondispersive and can be seen as coagula inside of the sieve element [18]. Even in lineages of angiosperms where vessels were lost and tracheids reevolved, such as *Winteraceae* in the *Magnoliids* and *Trochodendraceae* in the *eudicots*, sieve elements and companion cells are present [19], suggesting the independent evolution of these two plant vascular tissues derived from the same meristem initials. Since the sieve tube element loses its nucleus and ribosomes, the companion cell is the cell responsible for the metabolic life of the sieve elements, including the transport of carbohydrates in and out the sieve elements [7]. Companion cells may be arranged in vertical strands, with two to more cells (**Figure 2b**). Other parenchyma cells around the sieve tube integrate with the companion cells and can also act in this matter [7]. Typically, the cells closely related with the sieve tube elements

**6**

plates [20].

cells [13].

**2.2 Parenchyma**

#### **Figure 4.**

*Phloem axial parenchyma distribution in secondary phloem. (a) Ephedra tweediana (Ephedraceae) TS, showing sieve cells interspersed by axial parenchyma cells (arrows). Six to five cells away from the cambium, the sieve cells already lose conductivity and collapse with axial parenchyma cells enlarging (top arrow). (b) Lannea discolor (Anacardiaceae) TS showing axial parenchyma with tannins arranged in narrow bands (arrows). There are also other parenchyma cells with less content dispersed in the phloem. Note also the fibers in concentric bands. (c) Robinia pseudoacacia (Leguminosae) TS showing bands of axial parenchyma associated with the fiber bands and sieve tube elements in clusters with simple sieve plates staining with resorcin blue. (d) Fridericia nigrescens (Bignoniaceae) TS with sieve tubes surrounded by sieve-tube-centric axial parenchyma. The tissue background corresponds to the fibers. c, cambium; sx, secondary xylem; c, cambium; sp, secondary phloem; sx, secondary xylem. Scalebars: a = 50 μm; b, d = 200 μm; c = 100 μm.*

of the concentric fiber bands (**Figure 4c**). When very large quantities of sclerenchyma are present, such as in the secondary phloem of *Carya* (*Juglandaceae*) or in *Fridericia*, *Tanaecium*, *Tynanthus*, and *Xylophragma* (*Bignoniaceae*), the

sieve-tube-centric parenchyma appears (**Figure 4c**) and, as the name suggests, is surrounding the sieve tubes [8, 20, 23].

Although collectively described and referred to as axial phloem parenchyma, it is important to note that in many plants there will be distinct groups of phloem parenchyma within the phloem with quite different ergastic contents and therefore presumed different functions. Some of these specialized parenchyma cells may be considered secretory structures. Within a single plant, it is not uncommon that while some cells have crystals (especially when in contact with sclerenchyma), others have tannins, starch, and other substances. In apple trees (*Malus domestica*, *Rosaceae*) three types of axial parenchyma have been recorded: (1) crystal-bearing cells, (2) tannin- and starch-containing cells, and (3) those with no tannin or starch, which integrate with the companion cells [15].

Within bands of axial parenchyma, canals with a clear epithelium may be formed in many plant groups such as *Pinaceae*, *Anacardiaceae*, *Apiales*, a feature with strong phylogenetic signal. Some phloem parenchyma cells also act in the sustenance and support of the sieve elements, even when not derived from the same mother cell [7]. In longitudinal section, the axial phloem parenchyma may appear fusiform (not segmented) or in two up to several cells per strand [5].

While the phloem ages and moves away from the cambium, its structure dramatically change, and typically axial parenchyma cells enlarge (**Figures 4a** and **b**, **6c**), divide, and store more ergastic contents toward the nonconducting phloem. In plants with low fiber content, the dilatation undergone by the parenchyma cells typically provokes the collapse of the sieve elements. The axial parenchyma in the nonconducting phloem can dedifferentiate and give rise to new lateral meristems. In plants with multiple periderms, typically new phellogens are formed within the secondary phloem, compacting within the multiple periderms large quantities of dead, suberized phloem. In plants with variant secondary growth, especially lianas, new cambia might differentiate from axial phloem parenchyma cells [24]. In the Asian *Tetrastigma* (*Vitaceae*), new cambia were recorded differentiating from primary phloem parenchyma cells [25].

#### **2.3 Sclerenchyma**

Sclerenchymatic cells are those with thick secondary walls, commonly lignified. Sclerenchyma can be present or not in the phloem, and when present it typically gives structure to the tissue. For instance, a phloem with concentric layers of sclerenchyma cells is called stratified (**Figures 2e**, **3a**, and **4c**) [5]—not to be confused with storied, regarding the organization of the elements in tangential section. In Leguminosae, bands of phloem are associated to the concentric fiber bands (**Figure 4c**).

Older phloem shows more sclerification than younger phloem, and the sclerenchyma may also act as a barrier to bark attackers [21]. The sclerenchyma is typically divided in two categories: fibers and sclereids. These cell types differ mainly in form and size, but origin has also been used to distinguish them [26].

#### *2.3.1 Fibers*

Fibers are long and slender cells, derived from meristems, the fiber primordia [1, 26, 27]. In the primary phloem, fiber caps are sometimes found in association with the protophloem (**Figure 5a**) and are named protophloem fibers. Since only an ontogenetic study can evidence whether these fibers indeed differentiate within the protophloem, a term coined in the nineteenth century German and American literature, pericyclic fibers, has been recommended to be used instead of primary phloem

**9**

**Figure 5.**

*Phloem: Cell Types, Structure, and Commercial Uses DOI: http://dx.doi.org/10.5772/intechopen.88162*

*2.3.2 Sclereids*

fibers or perivascular fibers [5]. In the monocotyledons, fibers are commonly an important component of the vascular bundles (**Figure 5b**–**d**). Commonly these fibers are associated with the phloem (**Figure 5b**), but they might also be associated with the xylem (**Figure 5c**) or be central in the vascular bundle (**Figure 5d**). These fibers are not, however, understood as part of either phloem or xylem; although they are of vascular nature, they differentiate directly from procambium.

Sclereids may have different forms and sizes (**Figure 6a**–**c**). Within the phloem, they are more typically square or polygonal (stone cells) and contain numerous pits and conspicuous pit canals. Holdheid [26] defines that a sclereid is a cell derived from the belated sclerification of a parenchyma cell, and that is in fact the rule in the majority of cases (**Figure 6a** and **b**). However, there are lineages in which the sclereids differentiate very close to the cambium (e.g., *Pleonotoma*, *Bignoniaceae*, **Figure 6c**; [20]), and it would be untrue to claim that the derivatives had a stage as a mature parenchyma cell [1]. In these cases, the form is enough to define the sclereid. On the other hand, there are cases where long and slender cells derive from previously mature parenchyma cells and are morphologically difficult to distinguish from fibers. In these cases, these cells are called fiber sclereids and may be even in concentric layers, such as in apple trees and pears (*Malus domestica* and *Pyrus* 

*Vascular fibers associated to eudicot and monocot primary structure. (a) Pericyclic fiber cap (fc) and primary phloem (pp) in Perianthomega vellozoi (Bignoniaceae). Secondary phloem (sp) beginning to be produced. Vascular bundles in monocotyledons. (b) Vascular bundle in the climber Calamus manan (Arecaceae) with fibers toward the phloem side. Phloem in two strands around a wide metaxylem vessel. (c) Vascular bundle of Vellozia alata (Velloziaceae), with fiber cap toward the xylem side. Phloem on the top side of the picture. (Picture credit to Marina Blanco Cattai). (d) Amphivasal bundle of Philodendron with fibers in the center of* 

*the vascular bundle and phloem surrounding it. Scalebars: a, b = 100 μm, c, d = 50 μm.*

fibers or perivascular fibers [5]. In the monocotyledons, fibers are commonly an important component of the vascular bundles (**Figure 5b**–**d**). Commonly these fibers are associated with the phloem (**Figure 5b**), but they might also be associated with the xylem (**Figure 5c**) or be central in the vascular bundle (**Figure 5d**). These fibers are not, however, understood as part of either phloem or xylem; although they are of vascular nature, they differentiate directly from procambium.
