Part VI Evolution of Transport Tissues Ch23.Qxd 2/7/05 3:43 PM Page 478 Ch23.Qxd 2/7/05 3:43 PM Page 479
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Ch23.qxd 2/7/05 3:43 PM Page 477 Part VI Evolution of Transport Tissues Ch23.qxd 2/7/05 3:43 PM Page 478 Ch23.qxd 2/7/05 3:43 PM Page 479 23 The Evolutionary History of Roots and Leaves C. Kevin Boyce The long distance transport system of plants links the two primary sites of assimilation from the environment, root, and leaf. The evolutionary history underlying that simple statement is extremely complex when the full diver- sity of vascular plants over the last 400 million years is taken into account. In the larger context of this volume, stems may be considered primarily as the link between root and leaf, but roots and leaves have each evolved inde- pendently in a number of plant lineages, and it is only the stem connecting those termini that can be deemed homologous across the vascular plants. Though it is understandable that the angiosperms that dominate the modern world have been the primary focus of physiological investigation, it is important to keep in mind that the period of angiosperm dominance represents only the last quarter of vascular plant history (Wing et al., 1993; Knoll and Niklas, 1987). A comparative, evolutionary context can allow assessment of the degree to which results from angiosperm exemplars can be extended to other groups and vascular plants as a whole. The fossil record can also point toward living taxa that provide opportunities for physiological comparisons of independently derived but functionally simi- lar structures, such as with roots and leaves. The first vascular plants consisted of small, unadorned axes, which were responsible both for photosynthesis and assimilation of water and nutri- ents. Roots have evolved at least twice (Kenrick, 2002a; Gensel et al., 2001; Raven and Edwards, 2001). The roots found in the lycopod and euphyllo- phyte lineages (Fig. 23.1) have evolved independently and those of free- sporing euphyllophytes differ from the seed plants in key respects. Leaves have had an even more complicated history. The lycopods, again, have independently evolved leaves, simple linear structures. Members of the euphyllophyte clade have evolved laminate leaves at least four times (Boyce and Knoll, 2002), and patterns of morphological evolution have been com- plex in two of these lineages, ferns, and seed plants. 479 Ch23.qxd 2/7/05 3:43 PM Page 480 480 23. The Evolutionary History of Roots and Leaves Figure 23.1 Evolutionary relationships of the vascular plants discussed in this chapter. Lineages with extant members are in boldface. The zosterophylls s. l. are a paraphyletic group of fossils in which the lycopod clade is nested, and the trimerophytes are a paraphyletic group of fossils in which the extant euphyllophyte clades are nested. The sphenophytes includes the extant Equisetales, as well as the extinct Sphenophyllales and Pseudoborniales mentioned in the text. The evolutionary diversification represented here happened very rapidly; the basal- most branch between lycophytes and euphyllophytes would have occurred shortly before the beginning of the Devonian (410 MA) and all lineages within the euphyllophytes diverged by the end of Devonian (360 MA), although much diversification within these lineages occurred over later time. Phylogeny of extant taxa follows Pryer and colleagues (2001). The significance of this evolutionary history for understanding the physi- ology of long distance transport is at least threefold. First, transport within the termini of root and leaf is an important part of the transport system as a whole (see Chapters 5, 7, and 8). Second, the fact that stems in early land plants were initially responsible for all functions now associated with root and leaf emphasizes that specialization for long distance transport is itself a secondary function convergently evolved in a number of groups. Third, the initial evolution of lateral organs and subsequent changes in their geometry has likely had a strong, direct influence on stem vascular anatomy through hormonal inputs during development (Stein, 1993). This chapter focuses on the evolutionary relationships of the roots and leaves of extant vascular plants as documented with the fossil record, as well as some of the physio- logical and developmental implications of these relationships for the trans- port system. The role that fossils can play in this discussion differ for the organ types. Roots are rarely preserved and, when found, they may be difficult to assign to any particular clade (Raven and Edwards, 2001). As a result, the fossil record can provide trends in rooting depth through time (Driese and Mora, 2001; Algeo and Scheckler, 1998) and general information about plant body plans (Rothwell, 1995), but discussion of root morphology or Ch23.qxd 2/7/05 3:43 PM Page 481 Roots 481 anatomy must rely more on information from living taxa placed in a phy- logenetic context. Leaf fossils are abundant in many depositional settings, but are typically found detached from the parent axis (Chaloner, 1986). As a result, knowledge of leaf morphologies through time is good for the envi- ronments in which fossilization can occur, but it is some times difficult to determine the phylogenetic affinities of fossil leaf taxa, and it is usually not possible to estimate the size and architecture of the parent plant. It previously had been expected that fossils would play a vital role in phy- logeny reconstruction by providing character state combinations not found among living taxa (Donoghue et al., 1989). However, phylogenetic hypothe- ses inferred using fossil plant morphologies (Nixon et al., 1994, Rothwell and Serbet,1994; Doyle and Donoghue, 1992; Crane, 1985) have been robustly refuted by more recent molecular phylogenies (Magallón and Sanderson, 2002; Bowe et al., 2000; Chaw et al., 2000; Winter et al., 1999). This is a testa- ment to the frequently high degree of evolutionary convergence between distantly related plant lineages. However, the fact that there has been too much convergence for morphology to provide a reliable source of informa- tion for phylogeny reconstruction demonstrates that fossils are essential for understanding morphological evolution because inferences of ancestral morphologies and evolutionary patterns from phylogenies will frequently be incorrect. For example, a single origin for roots and for leaves would be the most parsimonious conclusion in light of how common these structures are across the phylogeny of extant vascular plants (Schneider et al., 2002). However, the fossil record indicates that the evolution of plant morphology has been far from parsimonious. In addition to the obscuring of phyloge- netic signal by the noise of frequent evolutionary convergence, the mor- phologies of living plants can also be directly misleading. As the angiosperms have undergone an immense radiation (as did the seed plants before that), other groups that formerly had much greater ecophysiological ranges have been marginalized and undergone a biased loss of morphological diversity. For example, the tree habit and secondary growth have evolved in several groups other than the seed plants, but this would not be guessed from exclu- sive observation of the modern world. Roots Evolution of Plant Body Plans and Rooting Structure Function The first vascular plants did not have roots. A similar situation is found today in Psilotum, although apparently a secondary derivation of this state (Fig. 23.1) (Pryer et al., 2001; Bierhorst, 1971). Although of obvious impor- tance, the evolution of roots is only one of several major evolutionary Ch23.qxd 2/7/05 3:43 PM Page 482 482 23. The Evolutionary History of Roots and Leaves innovations that have affected both how plants interact with their substrate and the possible architectures of aboveground structure. These innova- tions, which also have included shifts away from sporophyte dependence on the gametophyte and the evolution of bipolar growth, have greatly affected both assimilation and transport processes. Adequate hydraulic supply is possible in bryophytes with only diffusion and wicking of water along the surface of aerial axes (Hébant, 1977). The largest trees require bipolar growth and secondary vascular production in root and stem to sup- ply aboveground tissues. A diversity of morphologies between these end members is documented in the fossil record of vascular plants. The most morphologically simple Silurian and Early Devonian fossil plants (e.g., Cooksonia-like fossils, first appearing approximately 425 million years ago [hereafter abbreviated as MA]) are determinate, dichotomously branching sporophytes a few centimeters tall (Edwards and Fanning, 1985) that have been reconstructed as gametophyte-dependent (Rothwell, 1995). Functions such as nutrient acquisition, substrate anchorage, and symbiotic interactions that are attributed to the sporophyte roots in living vascular plants would likely have been performed exclusively by the gametophyte, although only the sporophyte is known for these particular fossils. A similar arrangement is found in the extant bryophytes, in which the gametophytes have rhizoids for absorption and anchorage. Bryophyte gametophytes also support mycorrhizal symbioses (Read et al., 2000). It has been hypothesized that a fungal partnership was essential for terrestrial colonization by land plants (Pirozynski and Malloch, 1975), and spores from the Ordovician have been interpreted as those of glomalean fungi (Redecker et al., 2000). During the early history of this symbiosis, fungal interaction was likely restricted to the plant gametophyte. In more morphologically