Evolution of roots

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Nothing is known about the evolutionary origin of roots. Recent molecular genetics shows that angiosperm RAMs and SAMs are controlled by similar mechanisms to maintain stem cell populations, suggesting that roots may be derived from a developmental program associated with the SAM (references cited in Friedman et al., 2004), but genetic data are lacking for fern and lyco-phyte roots. Roots are similarly endogenous in ferns and lycophytes, regardless of whether they branch endogenously (ferns) or exogenously (lycophytes). Of particular importance is determining how the root shifted its initiation site from surface to interior tissue during evolution. Barlow et al. (2004) argued that

Figure 3.14 Irregularly branched rhizomes (A) and line drawing of a rhizome apex in transectional view (B) of Psilotum nudum in hydroponic culture. The original apical cell (a) produces merophytes outlined by heavy lines, and new apical cells (a') are formed in merophytes. (Modified from Takiguchi et al., 1997.) Scale bar 1 cm for (A), 50 |im for (B).

Figure 3.14 Irregularly branched rhizomes (A) and line drawing of a rhizome apex in transectional view (B) of Psilotum nudum in hydroponic culture. The original apical cell (a) produces merophytes outlined by heavy lines, and new apical cells (a') are formed in merophytes. (Modified from Takiguchi et al., 1997.) Scale bar 1 cm for (A), 50 |im for (B).

the evolution of the quiescent center could have resulted in a change of the branching pattern from dichotomous to a so-called herring-bone pattern with endogenous lateral roots; pavement cells intervene to separate two branches of lycophyte roots that may be comparable to the nascent quiescent center. If this is the case, lycophyte roots with dichotomous branching could help clarify the origin of endogenous roots.

3.6 Psilotalean rhizomes (subterranean axes)

The Psilotaceae (whisk ferns) are unique in having no roots throughout their life history. In Psilotum, enation-like leaves form in the aerial stems but not in the subterranean rhizomes. There had been controversy concerning whether such a simple body plan represents a primitive character. However, recent molecular phylogenetic analyses showed clearly that members of the Psilotaceae should be classified as ferns (Pryer et al., 2001, 2004; see Chapter 15).

The most intriguing morphological trait is a tangled subterranean rhizome that branches frequently in equal or unequal fashion, with no regularity (Figure 3.14A). This contrasts with the regular dichotomously branching aerial stems. Such irregularity in the rhizome was once argued to be the result of injuries when growing in the soil, caused by the absence of any protecting tissue, such as a root cap (Bierhorst, 1954). However, Takiguchi et al. (1997) clarified that the rhizome shows a similar complex branching system when cultured hydroponically without obstacles, suggesting that irregular branching is an inherent feature of the Psilotaceae rhizome.

The Psilotaceae rhizome has an apical cell based meristem, but surprisingly several additional apical cells are found in merophytes of the original apical cell (Figure 3.14B). Because these additional apical cells soon produce their own derivatives, it is often difficult to trace which one is the original among several apical cells. Some apical cells develop arbitrarily as new apical meristems, but some others do not and become inactive. Furthermore there is no rule about which direction and how fast these new meristems grow as lateral branches, resulting in the complex rhizome branching system. It is worth noting that superficially dichotomous branching of Psilotaceae rhizomes is caused by the rapid growth of a lateral branch, not through true dichotomy in apical cell behavior. In contrast, the apical meristem of the aerial stems (SAMs) shows the typical organization of fern SAMs. When bifurcated, the apical cell disappears prior to the formation of two new apical cells. This is similar to dichotomous branching in other fern SAMs (Figure 3.9B). Interestingly, some branches of subterranean rhizomes transform directly into aerial stems by an unknown mechanism.

The complex SAM behavior in Psilotaceae rhizomes was interpreted as a crude character compared to other fern SAMs showing lateral or dichotomous branching, and was regarded as an independent unique organ (Takiguchi et al., 1997). However, the aerial SAM with leaves exhibits regulated apical organization including dichotomous branching, like other fern SAMs. Combined with the fact that the site of the lateral branch is strictly regulated in the fern SAMs mentioned above, the lack of leaves in Psilotum rhizomes might facilitate irregular branching as shown in fossil Filicalean ferns (Holmes, 1989) owing to a loss of the constraint provided by the leaf-branch combination.

3.7 Root-producing organs, rhizophores and rhizomorphs

The rhizophore is a leafless, root-producing axial organ unique to the Selaginellaceae (Figure 3.15). It is a historically controversial structure, variously interpreted as a root-producing organ not equivalent to other organs, a transformed stem, or the proximal portion of a root (aerial root) that branches to subterranean roots (Kato and Imaichi, 1997, and references therein). The rhizophore concept has been revised by the work of Imaichi and Kato (1989, 1991) on a temperate Selaginella species of moderate size. The rhizophore arises exoge-nously at each branching point of the lateral shoots. Its apical meristem, which was once called the angle meristem (Jernstedt et al., 1994), has a prominent apical cell with three cutting faces (Figure 3.15B). The apical cell soon disappears (Figure 3.15C) and two new root meristems arise in inner tissues of the rhizophore tip (Figure 3.15D). There is a gap in development between rhizophores

Figure 3.15 Rhizophores of Selaginella caudata (large tropical species, A) and S. kraussiana (moderately sized species, B-E, longisections). (A) Once to three-times dichotomously branched rhizophores (rh) arising from every branching site of lateral shoots. Roots (ro) arise from tips of rhizophores. (B)-(E) Endogenous root development in rhizophores. The apical cell in a just formed rhizophore (B) disappears soon (C), and two root meristems (arrows) are initiated in the inner tissue of the rhizophore tip (D, E). a, apical cell. Scale bar 5 cm for (A), 50 |im for (B)-(D), 100 |im for (E).

Figure 3.15 Rhizophores of Selaginella caudata (large tropical species, A) and S. kraussiana (moderately sized species, B-E, longisections). (A) Once to three-times dichotomously branched rhizophores (rh) arising from every branching site of lateral shoots. Roots (ro) arise from tips of rhizophores. (B)-(E) Endogenous root development in rhizophores. The apical cell in a just formed rhizophore (B) disappears soon (C), and two root meristems (arrows) are initiated in the inner tissue of the rhizophore tip (D, E). a, apical cell. Scale bar 5 cm for (A), 50 |im for (B)-(D), 100 |im for (E).

and endogenous roots. Tropical Selaginella species with large rhizophores usually branch dichotomously three to five times (Figure 3.15A). The branching manner is identical to that of stem dichotomy: prior to bifurcation the apical cell becomes indistinguishable, ceasing oblique divisions (Figure 3.9B). In conclusion, rhizophores are a root-producing, leafless, capless axial organ that is autonomously and dichotomously branched in large species and depauperately unbranched in small species, such as S. uncinata and S. kraussiana.

The Isoetaceae rhizomorph is another root-producing organ. It shows anatomical features common to the Carboniferous Lepidodendrid rhizomorph (Karrfalt, 1984; Stewart and Rothwell, 1993). Roots are formed by the activity of the basal meristem. The basal meristem is an enigma, and has been interpreted as a primary meristem, or as a cambium, or a part of a cambium (Paolillo, 1982, and references therein). However, recent detailed examinations of the initiation and growth of root primordia from the basal meristem, and embryonic roots of

Isoetes species show that the basal meristem has both organogenetic (primary) and thickening (secondary) meristem attributes (Yi and Kato, 2001). The basal meristem does not correspond to any known meristem in other vascular plants.

Rhizomorphs and rhizophores are sometimes compared, but the Selaginella rhizophore and Isoetes rhizomorph show differences in: (1) initiation pattern (exogenous or endogenous origin), (2) growth pattern (definite versus indefinite growth), (3) meristem structure (dome shaped with apical cell versus linear basal meristem with a layer of thin initials), and (4) number of roots produced (two versus many per apex) (Yi and Kato, 2001). The evolutionary relationships of these two root-producing organs, which are unique to the heterosporous ligulate lycopods, need further developmental studies.

3.8 Summary and future goals

Comparative development focusing on meristem behavior has helped define and demarcate plant organs and clarify their origins. It is noteworthy that fern stems with megaphylls (comparable to an exogenous stem branch) have roots that branch endogenously, whereas lycophyte stems with microphylls (not comparable to an exogenous stem branch) have roots that branch exogenously, as the stem does. This may confirm that at least stems and leaves are of telomic origin in ferns, although the origin of fern roots remains an open question. In lycophytes, stems and roots may have been derived from telomic axes, but the leaves were not.

Although developmental studies are still lacking, especially for lycophytes, there seems to be a general rule for behavior of apical meristems of axial organs (stems, roots, Psilotum rhizomes, and Selaginella rhizophores) when they divide. In dichotomous branching, the original apical cell or apical initial cells disappear and are replaced by two new apical cells or two groups of apical initial cells (Figures 3.9B, D, 3.12B). In lateral branching, the original apical cell or apical initial cells are retained and a new apical cell or initial cells are formed exogenously or endogenously in lateral positions (Figures 3.9A, 3.12A). These equal and unequal divisions are also seen in the megaphyll marginal meristem. The equal division associated with cessation of a central part of the marginal meristem results in the bilobed lamina; the unequal division retaining the original marginal meristem results in lateral pinna formation. From these facts, it is plausible that telomic apical meristems acquired the capacity to divide equally and unequally, before stems, leaves, and roots evolved independently in lycophytes and euphyllophytes. The most mysterious evolutionary event is endogenous branching of the meristem, i.e., root meristem initiation in the stem and root.

Meristem branching is similar in the stem, leaf and root, irrespective of whether the meristem has a single apical cell or plural apical initial cells. This might reinforce the organismal theory over the cell theory (Kaplan and Hagemann, 1991); the organismal theory interprets the living protoplasmic mass as a whole, rather than considering its constituent cells as the basic unit. In the cell theory, cell lineages are more significant, whereas for the organismal theory relative special positions are more significant. However, meristem structures correlate well to PD networks, suggesting that meristems with the single or plural initial cells are under different regulatory systems. Furthermore, it remains to be determined whether apical cell based and plural initial cell based meristems differ only in stem cell numbers or whether there are other essential differences.

Extant comparative developmental data show that lycophytes have greater variation in organ diversity and meristem behavior than do ferns. Nevertheless, developmental information on stems, roots, and root-producing organs in lycophytes is very fragmentary, and there are still no evolutionary hypotheses for their origins. Our preliminary examination suggests that the increase or decrease in meristem size could play an important role in meristem division or organ development in lycophytes. To elucidate the meristem behavior, including a change in size, certain markers such as genes expressed in the meristem itself are necessary. Molecular developmental genetics is very helpful for revealing organ identity, and should be extended to studies of ferns and lycophytes. A combination of developmental morphogenesis and developmental molecular genetics in a phylogenetic framework should yield results.

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