Abstract:

The evolution of animal and plant vascular systems played a pivotal role in the advancement from simple to complex organisms, through the provision of a delivery system for the distribution of components essential for both metabolism and growth. Interestingly, although these two vascular systems conform to the same general rules of fluid dynamics (Murray 1926; McCulloh et al. 2003), the developmental mechanisms adopted by plants and animals, to generate these long-distance transport systems, have little in common. In animals, the arterial and venous system of tubules circulates blood, as an extracellular fluid, around the body of the organism by means of a pressure gradient generated by the heart. This system allows for the delivery of signal molecules, such as metabolites, peptides and proteins, from sites of production to target tissues. The circulatory nature of the animal vascular system allows for feedback to occur between distantly located tissues and organs.

The Unique Aspects of the Plant Vascular System

The plant vascular system is comprised of xylem and phloem conducting elements. The xylem transpiration system, which conducts water and mineral nutrients from the roots to above ground organs such as stems, leaves, flowers and fruits, is derived from stem cells (termed procambial cells) that differentiate into xylem conducting elements. Upon expansion, these cells undergo a process of programmed cell death (PCD), thereby giving rise to files of tracheary elements that form a low resistance pathway for the flow of water which is driven by a tensional gradient established within the cell walls of transpiring leaves; i.e., water is pulled up the body of the plant. The phloem translocation system, which delivers sugars, amino acids, mineral nutrients and hormones to heterotrophic tissues, is also derived from cambial cells that differentiate into sieve cells and their associated companion cells. In angiosperms, these sieve cells undergo partial PCD, thereby giving rise to files of evacuolate and enucleote cells connected, end-toend, by sieve plates (containing large open pores) to form conducting tubes. Retention of the plasma membrane allows the sieve tube system to function as an osmotic unit; loadingof sugars in the mature leaves (source of photosynthetically fixed sugars) generates a high turgor pressure, whereas unloading of sugars in developing tissues causes a drop in turgor pressure. These osmotically-driven turgor pressures establish a positive pressure gradient that drives the phloem translocation stream from autotrophic to heterotrophic tissues and organs.

Plant Vascular Development

Clearly, an important functional difference between the animal and plant vascular systems is that the latter is non-circulatory in nature; thus, direct feedback signaling cannot occur between mature leaves and, for example, developing shoot meritstems (Lough and Lucas 2006). This raises the interesting question as to the mechanisms developed by plants to coordinate physiological and developmental processes at the whole-plant level. An important facet of plant vascular development relates to the production of functional xylem and phloem conducting tissues. This process must be both spatially and temporally controlled to permit the formation of transport systems that can deliver optimal quantities of water and nutrients to distantlylocated tissues and organs. Recent studies have provided important insights into this process. In this Special Issue, Hirakawa et al. (2010), review our progress in understanding the complex signaling events that underlie regulation of xylem and phloem cell differentiation from procambial cells. The action of non-cell-autonomous signals, involving CLE peptides, is discussed, as is the role of intercellular signaling from both the xylem and phloem as necessary inputs to coordinate vascular organization.

Secondary Growth & Wood Formation

Secondary growth of the plant vascular system is a very important process, as it leads to an expanded  of the cambium, derived from the procambium, gives rise to woody tissues which can afford additional mechanical support – this feature has allowed for the growth of perennial plantsthat can live for several thousand years and reach to heights of 100 meters or more. Obviously, an understanding of the evolutionary processes that have allowed for such longevity, as well as the formation of economically important tissues as wood, are of basic and applied importance. To lead us along this pathway, Du and Groover (2010) provide a review of recent studies in this area that indicate a role for transcriptional networks in regulating plant secondary growth. Future progress in this area will most surely have important applications in terms of engineering forest trees with improved traits.

Phloem as a Vascular Information Superhighway

Although it was long held that the phloem translocation stream carried only nutrients to support the growth of developing tissues, recent studies have revealed the presence of a complex sets of proteins and nucleic acids (Balachandran et al. 1997; Ruiz-Medrano et al. 1999; Lough and Lucas 2006; Lin et al. 2009). These findings support the hypothesis that the phloem functions as an information superhighway (Jorgensen et al. 1998). The presence of mRNA, as well as small interfering (si-) and micro (mi-)RNA, in the angiosperm sieve tube system raised important questions as to their possible roles in coordinating physiological and developmental processes, at the whole-plant level (Lough and Lucas 2006). Wang and Ding (2010) review these new findings and describe the use of plant viroids as a powerful tool to dissect the molecular determinants controlling the entry and exit of RNA species into and out of the sieve tube system.

Important agricultural traits, such as photoperiodic induction of flowering, have long been known to be controlled by florigenic agent(s) delivered to the shoot apex by the phloem (Zeevaar 1962). Recently, an important component of florigen was shown to be FLOWERING LOCUS T, a 20 kDa protein  the sieve tube system for translocation to the shoot apex (Corbesier et al. 2007; Lin et al. 2007; Mathieu et al. 2007; Tamaki et al. 2007). A role for long-distance transport of RNA in leaf development has been established (Ruiz-Medrano et al. 1999; Haywood et al. 2005) and now, in this Special Issue, Hannapel (2010) reviews recent findings that illustrate the role of phloem-delivery of mRNA in the orchestration of tuber formation in the agriculturally important crop, potato. Collectively, these recent discoveries indicate that pioneering studies on the phloem will likely underpin the bioengineering of novel long-distance signaling systems that will afford unique control over such important agronomically important traits as partitioning of photosynthetically fixed carbon.

Cytokinins and Vascular Signaling

It has long been known that plant hormones can be transported through the vascular system. The involvement of a class of phytohormones, known as the cytokinins, in local and longdistance signaling is well established. The role of cytokinins in nitrogen homeostasis has been the subject of intensive investigation by a number of plant scientists. Here, Kudo et al. (2010) review progress in this area of vascular signaling and show that root-to-shoot delivery of trans-zeatin, via the xylem, plays an important role in nitrogen metabolism. Phloem delivery of N⁶-(△²-isopentenyl) adenine-type cytokinins to the roots and developing shoot apices appears to be important for developmental regulation. As cytokinins appear to be involved in the regulation of a multitude of physiological and developmental activities, one could consider this class of phytohormones as true systemic regulators! Knowledge concerning the longdistance transport of cytokinins may well pave the way for engineering of plants with both enhanced nutrient use efficiency and overall yield.

Nitrogen Fixation and Vascular Signaling

Fixation of atmospheric nitrogen in legumes, through a symbiotic relationship with rhizobia, makes an important contribution to global nitrogen nutrition. This plant-rhizobium interaction involves a complex signaling network which is reviewed in this Special Issue by Ferguson et al. (2010). Interestingly, to optimize nitrogen acquisition and utilization, legumes have evolved an intricate mechanism to regulate the level to which their root systems will respond to soil-borne bacteria to allow nodule development. In the presence of adequate exogenously supplied nitrogen, nodulation is down-regulated; this process ensures optimal utilization of carbon allocation – putting it another way, nodulation and rhizobial nitrogen fixation are processes that cost the plant carbon resources that could otherwise be used for growth and cellular maintenance. Ferguson et al. (2010) describe recent insights afforded into the role played by the plant vascular system as an integrator in this process of autoregulation of nodulation. Obviously, a comprehensive understanding of the processed underlying symbiotic nitrogen fixation will have an immeasurable impact not agriculture and its capacity to feed the peoples of the world.

Root-to-shoot Signaling Systems Control Physiological and Developmental Programs

The pioneering studies of Fritz Went (1943) revealed the involvement of root-derived signals that appeared to regulategrowth of the vegetative regions of the plant. The roles of these signals in water use efficiency, control over shoot branching and overall shoot growth are reviewed in this Special Issue by Sieburth and Lee (2010). The identification of a novel protein, BYPASS1, is discussed with respect to its function in interdicting the synthesis of a novel root-to-shoot signal; this molecule may well be a branch product of the carotenoid biosynthetic pathway. Xylem delivery of this BYPASS1-regulated molecule appears to modify shoot growth through its affect on local auxin signaling. Insights from these and other studies on root-to-shoot signaling, via the xylem transpiration stream, suggests the potential for engineering of plants with enhanced agronomic traits, including higher water use efficiency, novel branching patterns and enhanced growth characteristics under non-optimal environmental conditions.

Vascular Defense – a Role for Secondary Metabolites

As mentioned above, secondary growth gave rise to woody perennial plants whose life cycles can span many centuries to even thousands of years. Given that plants are sessile, such longevity can come with a price – they become prime targets for attack by insects and other pathogens, such as various fungi and bacteria. Through the course of their evolution, woody plants have developed a number of strategies to protect themselves from such attacks. Zulak and Bohlmann (2010) delve into pathogen-induced terpenoid biosynthesis as an effective means to produce secondary metabolites that can block the attacks mounted on confers by a range of pests and pathogens. In their review, the authors illustrate how plants use a combination of specialized anatomical features, such as xylem resin ducts, and oleoresin terpenoids to mount a defense against insect attack.

Flavonoids as Local and Long-distance Signaling Agents

A role for flavonoids as low molecular weight signaling molecules is examined in the review by Buer et al. (2010). Here, again, we learn how plants have utilized their capacity for secondary metabolite production to synthesize a wide range of structural variants through the flavonoid branch of the phenylpropanoid pathway. Flavonoids are involved in a broad spectrum of physiological and developmental process, including modulating hormone signaling, functioning as components in such signaling cascades as those involved in legumebacteria symbiosis, and plant defense. Recent studies have shown that flavonoids are transported throughout the plant and, as discussed by Buer et al. (2010), studies on the mode of transport will provide important new insights into the manner inwhich these secondary metabolites influence plant growth and development.

Biofuels Production

Woody perennial plants produce significant biomass on a seasonal basis. The ligno-cellulosic content of the secondary xylem can be utilized as a renewable energy source. As worldwide energy demand increases, many  strategies to expand their use of biomass energy production in ways that will avoid negative effects on food production and security. In this Special Issue, Tang et al. (2010) analyze the capacity for energy production within China using biomass grown on marginal lands. This review nicely highlights the potential associated with bringing approximately 45 million hectares of marginal land into biomass energy production. The biomass cropping systems and approaches being developed in China could well have utility in other regions of Asia.