The Plant Vascular System: Evolution, Development and FunctionsF

296 Journal of Integrative Plant Biology Vol. 55 No. 4 2013
environments, whereas water and mineral requirements are
primarily acquired from soil environments. Thus, aerial and soil
organs of early land plants were nutritionally interdependent
and, consequently, there was intense selection pressure for the
evolution of an inter-organ transport system to allow access to
the complete spectrum of essential resources for cell growth
and maintenance.
An important feature of early multicellular plants was the
acquisition of plasmodesmata (PD), whose cytoplasmic channels
established a symplasmic continuum throughout the body
of the plant (Lucas et al. 1993). This symplasm allowed for
the exchange of nutrients between the different plant organs.
However, this symplasmic route, in which intracellular cytoplasmic
streaming is arranged in series with intercellular diffusion
through PD, is effective only over rather short distances. For
example, a PD-mediated sucrose flux of 2 × 10 −4 mol m −2 s −1
into heterotrophic cells would satisfy their metabolic demand.
Maximum reported permeability coefficients for sucrose diffusion
through PD are on the order of 6 × 10 −6 ms −1 (Fisher
and Wang 1995). Using this value, diffusion theory predicts that
a significant sucrose concentration drop would be required,
across each adjoining cell wall interface, to sustain this flux
of sucrose from the autotrophic (photosynthetic) cells into the
heterotrophic (water and mineral nutrient acquiring) cells. Thus,
the path length would be limited to only a few cells, arranged in
series, and the size of the organism would be limited to a few
millimeters.
In order for multicellular autotrophs to overcome these
diffusion-imposed size constraints, a strong selection pressure
existed to evolve an axially-arranged tissue system, located
throughout the plant body, with a greatly increased conductivity
for intercellular transport. The solution to this problem began
over 470 Mya and, in combination with prevailing global climate
change, including dramatic changes in atmospheric CO2 levels,
gave rise to the development of the cuticle and stomata,
important adaptations that both reduced tissue dehydration
and increased the capacity for exchange of CO2, thereby
enhancing the rates of photosynthesis (Franks and Brodribb
2005; Ruszala et al. 2011; but see Duckett et al. 2009).
Following acquisition of these two traits, early land plants
evolved cells specialized for long-distance transport of food
and water (Ligrone et al. 2000, 2012; Raven 2003; van Bel
2003; Pittermann 2010). Irrespective of plant group, these cells
became arranged end-to-end in longitudinal files having a simplified
cytoplasm and modified end walls designed to increase
their intra- and intercellular conductivities, respectively.
In land plants, the degree of cellular modifications of transport
cells increases from the bryophytes (pretracheophytes—also
termed non-vascular plants—the liverworts, mosses and hornworts),
to the early tracheophytes, the vascular cryptogams (lycophytes
and pterophytes), on through to seed plants (Ligrone
et al. 2000, 2012; Raven 2003; van Bel 2003). These cell
specializations neatly scale with maximal sizes attained by
each group of land plants. Interestingly, impacts of enhancing
conductivities of cells transporting sugars converges with a
greater influence imposed by evolving water conducting cells
to sustain hydration of aerial photosynthetic tissues.
Evolutionary origins and diversification of food
and water transport systems
Studies based on fossil records and extant (living) bryophytes
have established that developmental programs evolved to form
specialized water and nutrient conducting tissues. Based on
the fossil record, early pretracheophyte land plants appeared
to have developed simple water-conducting conduits having
smooth walls with small pores, likely derived from the presence
of PD. Similar structures are present, for example, in some of
the mosses, the most ancient being termed water-conducting
cells (WCCs) and the more advanced being the hydroids of the
peristomate mosses (Mishler and Churchill 1984; Kenrick and
Crane 1997; Ligrone et al. 2012).
Hydroids often form a central strand in the gametophyte
stem/sporophyte seta in the mosses (Figure 1A, B). During
their development, these hydroid cells undergo various structural
modifications to the cell wall and are dead at maturity
(Figure 1C, D). Although in some cases the hydroid wall may
become thickened, these are considered to be primary in
nature and lack lignin. However, recent studies have indicated
that bryophyte cell walls contain lignin-related compounds,
but these do not impart mechanical strengthening properties
(Ligrone et al. 2012). Although this absence of mechanical
strength served as an impediment to an increase in body size,
it allowed for hydroid collapse during tissue desiccation, and
rapid rehydration following a resupply of water (Figure 1E, F), a
feature that likely minimized cavitation of these WCCs (Ligrone
et al. 2012) (see also later section). This trait may also have
allowed peristomate mosses to expand into dryer habitats.
The evolution of hydroids could have involved modification of
existing WCCs. However, based on the distribution of WCCs
in the early land plants (Figure 2), it seems equally probable
that they arose through an independent developmental
pathway after the loss of perforate WCCs (Ligrone et al.
2012).
The fossil record contains less information on the evolution
of specialized food-conducting cells (FCCs), due in large
part to their less robust characteristics that limited effective
preservation. However, insights can be gained from studies
on extant bryophyte species. As with WCCs, early FCCs were
represented by files of aligned elongated cells in which the
cytoplasmic contents underwent a series of positional and
structural modifications (Figure 3). Here, we will use moss as an
example; in some species (members of the order Polytrichales),