The Plant Vascular System: Evolution, Development and FunctionsF

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William J. Lucas (Corresponding author) Abstract Insights into Plant Vascular Biology 295 The emergence of the tracheophyte-based vascular system of land plants had major impacts on the evolution of terrestrial biology, in general, through its role in facilitating the development of plants with increased stature, photosynthetic output, and ability to colonize a greatly expanded range of environmental habitats. Recently, considerable progress has been made in terms of our understanding of the developmental and physiological programs involved in the formation and function of the plant vascular system. In this review, we first examine the evolutionary events that gave rise to the tracheophytes, followed by analysis of the genetic and hormonal networks that cooperate to orchestrate vascular development in the gymnosperms and angiosperms. The two essential functions performed by the vascular system, namely the delivery of resources (water, essential mineral nutrients, sugars and amino acids) to the various plant organs and provision of mechanical support are next discussed. Here, we focus on critical questions relating to structural and physiological properties controlling the delivery of material through the xylem and phloem. Recent discoveries into the role of the vascular system as an effective long-distance communication system are next assessed in terms of the coordination of developmental, physiological and defense-related processes, at the whole-plant level. A concerted effort has been made to integrate all these new findings into a comprehensive picture of the state-of-the-art in the area of plant vascular biology. Finally, areas important for future research are highlighted in terms of their likely contribution both to basic knowledge and applications to primary industry. Keywords: Evolution; vascular development; phloem; xylem; nutrient delivery; long-distance communication; systemic signaling. Lucas WJ, Groover A, Lichtenberger R, Furuta K, Yadav SR, Helariutta Y, He XQ, Fukuda H, Kang J, Brady SM, Patrick JW, Sperry J, Yoshida A, López-Millán AF, Grusak MA, Kachroo P (2013) The plant vascular system: Evolution, development and functions. J. Integr. Plant Biol. 55(4), 294–388. Introduction The plant vascular system carries out two essential functions, namely the delivery of resources (water, essential mineral nutrients, sugars and amino acids) to the various plant organs, and provision of mechanical support. In addition, the vascular system serves as an effective long-distance communication system, with the phloem and xylem serving to input information relating to abiotic and biotic conditions above and below ground, respectively. This combination of resource supply and delivery of information, including hormones, peptide hormones, proteins and RNA, allows the vascular system to engage in the coordination of developmental and physiological processes at the whole-plant level. Over the past decade, considerable progress has been made in terms of our understanding of the developmental and physiological programs involved in the formation and function of the plant vascular system. In this review, we have made every effort to integrate these new findings into a comprehensive picture of the state-of-the-art in this important facet of plant biology. We also highlight potential areas important for future research in terms of their likely contribution both to basic knowledge and applications to primary industry. Evolution of the Plant Vascular System Why the need for a vasculature system? For plants as photosynthetic autotrophs, the evolutionary step from uni- to multi-cellularity conferred an important selective advantage in terms of division of labor; i.e., functional specialization of tissues/organs to more effectively extract, and compete for, essential resources in aquatic and terrestrial environments. Successful colonization of terrestrial environments, by plants, depended upon positioning of organs in both aerial and soil environments to meet their autotrophic requirements. For example, for photosynthetic efficiency, sufficient levels of light only co-occur with a supply of CO2 in aerial
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),
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The Plant Vascular System: Evolution, Development and FunctionsF

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