Phloem is the vascular tissue in charge of transport and distribution of the organic nutrients. The phloem is also a pathway to signaling molecules and has a structural function in the plant body. It is typically composed of three cell types: sieve elements, parenchyma, and sclerenchyma. The sieve elements have the main function of transport and typically have lost their nuclei and other organelles in the course of their specialization. Hence, the sieve elements rely on specialized neighboring parenchyma cells to sustain all of their physiological function and activities. All cell types of the phloem may vary morphologically and in their distribution in the tissue, and this diversity is taxonomic and functionally informative. The phloem can be of primary or secondary origin, being derived from either procambium or cambium, respectively. Some vascular plant lineages have exclusive primary phloem, such as the lycophytes, ferns, and the monocotyledons, and the sieve elements will be long living in these taxa. In plants with secondary growth, the secondary phloem is formed, and typically the primary phloem collapses. Because new secondary phloem is constantly formed, the longevity of sieve elements in the secondary plant body is much more reduced. In this chapter, the structure of the phloem and its cell types are described in detail and also some of the known commercial uses of this tissue.
- sieve tube
- sieve tube element
- companion cells
Phloem is the vascular plant tissue responsible for the transport and distribution of sugars produced by the photosynthesis. Since the plant is a continuum, phloem will be found in the external part of root cylinders (Figure 1a), in the stem vascular bundles (Figure 1b) and in the abaxial part of the venations of every single leaf (Figure 1c). While the most common is to have the phloem external to the xylem in roots and stems and abaxial in leaves, some exceptions exist and are usually taxon specific. The phloem found in the inside is named internal or intraxylary phloem (Figure 1b).
As a constitutive tissue in the plant body, phloem functions extrapolate its main function of sugar transport, including transport of signalizing molecules such as mRNAs, hormones, defenses from biotic and abiotic agents, sustenance of the organs, gas exchange, and storage of many ergastic materials, such as starch, calcium oxalate crystals, and tannins. Parenchymatic cells of the phloem can also give rise to new meristems, such as the phellogen or cork cambium. All vascular plants have phloem, which typically includes specialized living conducting cells named sieve elements whose nucleus, ribosomes, and other organelles degenerate during maturation, making sugar transport more efficient. The life and function of these cells will then rely on closely associated parenchyma cells which support the physiological functions of these sieve elements . Although typical phloem is exclusive of vascular plants, rudimentary phloem-like conducting cells are present also in other lineages, such as the bryophyte leptoids, and even outside the plant kingdom, as the trumpet cells of the kelps and phaeophycean algae . The primary phloem derives from the embryo and the apical meristem procambium throughout the life of the plant or from the cambium, in plants with secondary growth.
2. Phloem cell types
The phloem is a complex tissue and is formed typically by three cell types, the sieve elements, the parenchyma cells, and the sclerenchyma cells (Figure 2a–d). Sclerenchyma cells might sometimes be absent in primary and/or secondary phloem. The presence, quantities, and arrangements of these cell types in the tissue commonly vary and may be taxonomic informative [3, 4]. Lists depicting these variations in all phloem cell types are of ultimate importance for complete bark descriptions . What follows is a description of these three major cell types in the phloem.
2.1 Conducting phloem cells
Sieve element is a general term that encompasses all conducting cells of the phloem, both sieve cells and sieve tube elements [1, 6]. The name sieve derives from the strainer appearance given to the cells by the presence of numerous pores crossing their bodies (Figure 2c). These pores are specialized plasmodesmata of wider diameter, and the sieve areas are basically specialized primary pit fields . The sieve pores are usually lined up with callose, which were shown to be related with the formation of the sieve pores in angiosperms, although not in gymnosperms . Large amounts of callose deposit in the sieve areas also when the sieve element loses conductivity, suffers injury, or becomes dormant. Callose in gymnosperms is typically wound callose . Callose can be easily detected with aniline blue under fluorescence or resorcin blue  (Figure 2b and c).
Sieve elements have only primary walls, but sometimes this wall can be very thick receiving the name of nacreous walls (Figure 2d)  and can be present in all major vascular plant lineages . Nacreous walls can be very thick, and some authors have proposed they would be secondary walls [1, 8]. Nacreous walls can almost occlude the entire lumen of the sieve element (Figure 2d); hence, its presence needs to be considered in experiments of sugar translocation. Such thick walls might be related to resistance to high turgor pressures within the sieve elements. Nacreous walls seem to have a strong phylogenetic signal and are much more common in some families, such as
There are basically two types of sieve elements: sieve cells and sieve tube elements. The sieve tube elements are distinguished by the presence of sieve plates, that is, sieve areas with wider and more abundant sieve pores, usually in both extreme ends of the cells, while sieve cells lack sieve plates [1, 6, 8]. A group of connected sieve tube elements form a sieve tube . According to this concept, lycophytes and ferns have sieve cells . However, because of the many differences in the morphology and distribution of protoplasm organelles and chemical substances between the sieve elements of gymnosperms and vascular cryptogams, Evert  suggests the use of “sieve cell” as exclusive to the gymnosperms, leaving the more general term “sieve element” to the lycophytes and ferns.
The longevity of sieve elements varies. In many species it is functional for just one growth season, while for other species they can be functional a couple of years, or in the case of plants that lack secondary growth, they will be living for the entire plant life spam. Palm trees would perhaps be the plants with the oldest conducting sieve tube elements, since some reach 200 years . In other plants, on the other hand, the sieve elements collapse a few cells away from the vascular cambium, corresponding to a fraction of the mm. In a mature tree, most of the secondary phloem will generally be composed of sieve elements no longer conducting. This region is called nonconducting phloem, in opposition to the area where sieve elements are turgid and conducting, called conducting phloem [5, 8] (Figure 2e and f). The term collapsed and noncollapsed phloem and functional and nonfunctional phloem are not recommended, since in some plants the nonconducting phloem keeps its sieve elements intact (Figure 2f), and although large parts of the phloem may not be conducting, the tissue as a whole is certainly still functioning in storage, protection, and even dividing or giving rise to new meristems, such as the phellogen and the dilatation meristem of some rays [5, 8].
2.1.1 Sieve cells and Strasburger cells
Sieve cells are typically very elongated cells with tapering ends (Figure 3b), which lack sieve plates, that is, lack an area in the sieve element where the pores are of a wider diameter. Even though the sieve areas may be more abundant in the terminal parts of the sieve cells, the pores in these terminal areas are of the same diameter as those of the lateral areas of the sieve element. Sieve cells lack P-protein in all stages of development. The sustenance of the sieve cells is carried by specialized parenchyma cells in close contact with the sieve elements, with numerous plasmodesmata, which maintain the physiological functioning of the sieve cells, including the loading and unloading of photosynthates. These cells are known either as albuminous cells or Strasburger cells. The name albuminous was initially coined given the proteinaceous appearance of these cell’s contents. However, because the high protein content is not always present, the name Strasburger cell, paying tribute to its discoverer Erns Strasburger, is recommended over albuminous cells [5, 12]. Strasburger cells in the secondary phloem can be either axial parenchyma cells, as is common in
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 ontogenetically related . 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 . In
Even in lineages of angiosperms where vessels were lost and tracheids re-evolved, such as
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
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 . In Gnetales, the phloem axial parenchyma appears to be intermingling with the sieve cells (Figure 4a) . Some of these axial parenchyma cells act as Strasburger cells .
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
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 (
Within bands of axial parenchyma, canals with a clear epithelium may be formed in many plant groups such as
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 . In the Asian
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) —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 . 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 .
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 fibers or perivascular fibers . 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  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.,
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 (
The rays in the conducting phloem have typically the same organization in terms of width, height, and cellular composition as the secondary xylem. In this respect the rays vary from uniseriate to multiseriate (Figure 7a) and may be homocellular or heterocellular (Figure 7b). Homocellular rays are those composed of cells of one shape, all procumbent or all upright (common in many shrubs). Heterocellular rays are those where more than one cell shape is present together (Figure 7b). Ray composition is appreciated in radial sections.
Because the vascular cambium produces much more xylem to the inside than phloem to the outside, phloem rays typically greatly dilate toward the periphery of the organ (Figure 7c). It is not uncommon that a dilatation meristem longitudinal to the cambium forms in some barks (Figure 7c), especially in families with very wide, wedge-like rays such as the
Rays are typically exclusively parenchymatic; however, in many species sieve elements appear in the rays and are called ray sieve cells or radial sieve cells [5, 28, 29]. These cells were recorded connecting two different sieve tubes (collections of sieve tube elements). Ray sieve elements seem to be present in taxa where perforated ray cells have been also recorded .
3. Structure and development of primary and secondary phloem
3.1 Primary phloem
The primary phloem derives from the embryo in the seed and the procambium from the organ’s apices. Similarly to the primary xylem, the primary phloem is divided in protophloem and metaphloem (Figure 1d), with the protophloem differentiating first, while the plant is still elongating, and the metaphloem differentiating last. The phloem is always exarch, independently of the organ. Protophloem sieve elements sometimes lack companion cells, such as in
The primary phloem is simpler than the secondary phloem and is basically formed by sieve elements and parenchyma cells (Figure 1a–d). Fiber caps are commonly present, and they might be phloematic (Figure 5a). For a discussion on their origin, check the section on fibers above. The position of the phloem is typically external or abaxial to the xylem, but in some lineages the bundles are bicollateral (Figure 1b), and phloem is present both inside and outside (abaxial and adaxial), while in amphivasal bundles, the xylem encircles the phloem (Figure 5d), as in the secondary vascular tissues of some
3.2 Secondary phloem
Being derived from the cambium, the secondary phloem will share a number of characteristics with the secondary xylem. For instance, it is divided in an axial and radial system. The axial system is composed of sieve elements, axial parenchyma cells, and fibers, and the radial system is formed by rays, which are typically parenchymatic (Figure 2a–c). Similar to secondary xylem, the secondary phloem can be storied (Figure 7a) or non-storied (Figure 2b and c), depending whether the cambial mother cells are organized in tiers or not.
Some trees will have growth rings, with an early and a late phloem, both in temperate and tropical regions, but their characterization is only possible with periodical collections . Sometimes, but not always, the fiber band width gives a hint on the presence of growth rings or the formation of very small sieve elements in the late phloem [1, 5].
3.2.1 Secondary phloem of gymnosperms
In conifers (except Gnetales) the secondary phloem is typically marked by an alternation of axial cell types (Figure 3a and b), uniseriate rays, and, in many lineages, axial and radial resin canals (e.g.,
In other gymnosperms, in particular in Gnetales and Cycads, the first remarkable difference is the presence of very wide, multiseriate rays alternating with uniseriate rays. The wide rays in both groups have, however, evolved independently, since Cycads are a sister to all other gymnosperms, while Gnetales are within the conifers, as sister to the Pinaceae [31, 37]. In
Within the Gnetales, in
3.2.2 Secondary phloem of angiosperms
Within the angiosperms, the diversity of phloem cell type arrangements reaches its maximum. The structure can be storied (Figure 7a) or non-storied (Figure 2b and c); sclerenchyma can be present or lacking. The rays may be uni-, bi-, or multiseriate. A large array of secretory cells may be encountered, such as resin canals, laticifers, and mucilaginous cells. Crystalliferous parenchyma is also very common, especially when associated with fibers.
The variation in cell type arrangements can be of taxonomic interest. Sieve elements can vary in morphology and arrangement. They can be solitary (Figure 2f), scattered in the phloem (e.g.,
The presence, type, and arrangements of fibers and sclereids are one of the most informative characters in the bark . In
Phloem parenchyma more commonly constitute the background tissue in the phloem but can also be distributed in bands (Figure 4b and c), radial rows, or even only around the sieve tube elements (Figure 4d) .
4. Phloem activity
The classic theory of phloem transport is that proposed by Ernst Münch , and it involves the formation of an osmotic pressure transport gradient, where certain zones act as sources of sugars (leaves and storage organs), while others act as sinks. Experiments showed that the concentration gradients were always seen to be positive in the direction of flow , supporting Münch’s postulate. In a system where transport goes against the direction of transpiration, its functionality relies on the presence of a plasma membrane across the entire system to create an osmotic pressure, hence the need of a conducting system with living cells . Recent studies have been refining aspects involved in the photosynthate conduction to explain long-distance transports across large trees with such a simple system [44, 45]. A direct role of intracellular calcium has also been reported in the dissolution of nondispersive P-proteins and facilitation of transport . Likely, the anatomical structure of the phloem discussed in the previous sections of this chapter will prove to play a role in the system. For instance, phloem sieve element length scale with the tree sizes and sieve plate type . It was also shown that sieve element’s diameter, length, and pore width increase from the top to the base of the trees [47, 48].
Across the entire pathway, sugars are removed from the system to sustain all cells in the plant body. This mechanism is only possible with the concerted mechanism between sieve elements and their close related cells (Strasburger cells and companion cells), with these accompanying cells constantly channeling substances and macromolecules toward the sieve elements . The Strasburger and companion cells carry the loading and unloading of the sieve elements. Given the function of loading and unloading, the companion cell-sieve tube element size ratio is directly related to being in the source or the sink of sugars . For instance, in leaves the companion cells are typically much larger, for they have the high demand of constantly loading the sieve tubes. In areas of release of the sugars (unloading), the companion cells are much smaller or even absent .
5. Economic uses
In the economic uses, it is not always easy to distinguish the use of the phloem from that of the periderm, since both together compose the bark of a woody plant. The phloem corresponds to the inner bark, and the periderm to the outer bark. The bark has a long history of utilization, from the production of remedies , aphrodisiacs (yohimbe), insecticides , dyes, tannins , angostura, fibers , gums and resins , latex, and flavorings .
In indigenous groups from British Columbia (Canada) and Tanzania, barks from dozens of species of woody plants are used as carbohydrate food, medicine, fibers, and structural material [50, 53]. In Mexico the bark of
The rubber tree,
I would like to express gratitude to Ray F. Evert, Veronica Angyalossy, Carmen Marcati, and André C. Lima for allowing their slide collections to be photographed and Leyde N. Nunes for the photo of
Conflict of interest
The authors declare no conflict of interest.