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The Plant Vascular System: Evolution, Development and Functions

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The Plant Vascular System: Evolution, Development and Functions Journal of Integrative Plant Biology 2013, 55 (4): 294–388 Invited Expert Review The Plant Vascular System: Evolution, Development and Functions William J. Lucas1∗, Andrew Groover2, Raffael Lichtenberger3, Kaori Furuta3, Shri-Ram Yadav3, Yka¨ Helariutta3, Xin-Qiang He4, Hiroo Fukuda5, Julie Kang6, Siobhan M. Brady1, John W. Patrick7, John Sperry8, Akiko Yoshida1, Ana-Flor Lopez-Mill´ an´ 9, Michael A. Grusak10 and Pradeep Kachroo11 1Department of Plant Biology, College of Biological Sciences, University of California, Davis, CA 95616, USA 2US Forest Service, Pacific SW Res Stn, Institute for Forest Genetics, Davis, CA 95618, USA 3Institute of Biotechnology/Department of Biology and Environmental Sciences, University of Helsinki, FIN-00014, Finland 4State Key Laboratory of Protein and Plant Gene Research, College of Life Sciences, Peking University, Beijing 100871, China 5Department of Biological Sciences, Graduate School of Science, The University of Tokyo, 7-3-1 Hongo, Bunkyo-ku, Tokyo 113-0033, Japan 6Biology Department, University of Northern Iowa, Cedar Falls, IA, USA 7School of Environmental and Life Sciences, The University of Newcastle, Callaghan, NSW 2308, Australia 8Biology Department, University of Utah, 257S 1400E Salt Lake City, UT 84112, USA 9Plant Nutrition Department, Aula Dei Experimental Station (CSIC), P.O. Box 13034, E-50080, Zaragoza, Spain 10USDA-ARS Children’s Nutrition Research Center, Department of Pediatrics, Baylor College of Medicine, 1100 Bates Street, Houston, TX 77030, USA 11Department of Plant Pathology, College of Agriculture, University of Kentucky, Lexington, KY 40546, USA All authors contributed equally to the preparation of this manuscript. ∗Corresponding author Tel: +1 530 752 1093; Fax: +1 530 752 5410; E-mail: [email protected] Available online on 5 March 2013 at http://www.jipb.net and http://www.wileyonlinelibrary.com/journal/jipb doi: 10.1111/jipb.12041 Table of Contents I. Introduction 295 II. Evolution of the Plant Vascular System 295 III. Phloem Development & Differentiation 300 IV. Molecular Mechanisms Underlying Xylem Cell Differentiation 307 V. Spatial & Temporal Regulation of Vascular Patterning 311 VI. Secondary Vascular Development 318 VII. Physical and Physiological Constraints on Phloem Transport Function 321 VIII. Physical & Physiological Constraints on Xylem Function 328 IX. Long-distance Signaling Through the Phloem 339 X. Root-to-shoot Signaling 347 XI. Vascular Transport of Microelement Minerals 351 XII. Systemic Signaling: Pathogen Resistance 356 XIII. Future Perspectives 361 XIV. Acknowledgements 362 XV. References 362 C 2013 Institute of Botany, Chinese Academy of Sciences Insights into Plant Vascular Biology 295 Abstract 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 William J. Lucas events that gave rise to the tracheophytes, followed by analysis of the (Corresponding author) 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, Lopez-Mill´ an´ AF, Grusak MA, Kachroo P (2013) The plant vascular system: Evolution, development and functions. J. Integr. Plant Biol. 55(4), 294–387. picture of the state-of-the-art in this important facet of plant Introduction biology. We also highlight potential areas important for future research in terms of their likely contribution both to basic The plant vascular system carries out two essential functions, knowledge and applications to primary industry. 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 Evolution of the Plant Vascular System system, with the phloem and xylem serving to input informa- Why the need for a vasculature system? tion relating to abiotic and biotic conditions above and below ground, respectively. This combination of resource supply and For plants as photosynthetic autotrophs, the evolutionary step delivery of information, including hormones, peptide hormones, from uni- to multi-cellularity conferred an important selective proteins and RNA, allows the vascular system to engage in the advantage in terms of division of labor; i.e., functional spe- coordination of developmental and physiological processes at cialization of tissues/organs to more effectively extract, and the whole-plant level. compete for, essential resources in aquatic and terrestrial Over the past decade, considerable progress has been environments. Successful colonization of terrestrial environ- made in terms of our understanding of the developmental and ments, by plants, depended upon positioning of organs in both physiological programs involved in the formation and function of aerial and soil environments to meet their autotrophic require- the plant vascular system. In this review, we have made every ments. For example, for photosynthetic efficiency, sufficient effort to integrate these new findings into a comprehensive 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 specializations neatly scale with maximal sizes attained by primarily acquired from soil environments. Thus, aerial and soil each group of land plants. Interestingly, impacts of enhancing organs of early land plants were nutritionally interdependent conductivities of cells transporting sugars converges with a and, consequently, there was intense selection pressure for the greater influence imposed by evolving water conducting cells evolution of an inter-organ transport system to allow access to to sustain hydration of aerial photosynthetic tissues. the complete spectrum of essential resources for cell growth and maintenance. An important feature of early multicellular plants was the Evolutionary origins and diversification of food acquisition of plasmodesmata (PD), whose cytoplasmic chan- and water transport systems nels established a symplasmic continuum throughout the body of the plant (Lucas et al. 1993). This symplasm allowed for Studies based on fossil records and extant (living) bryophytes the exchange of nutrients between the different plant organs. have established that developmental programs evolved to form However, this symplasmic route, in which intracellular cytoplas- specialized water and nutrient conducting tissues. Based on mic streaming is arranged in series with intercellular diffusion the fossil record, early pretracheophyte land plants appeared through PD, is effective only over rather short distances. For to have developed simple water-conducting conduits having example, a PD-mediated sucrose flux of 2 × 10−4 mol m−2 s−1 smooth walls with small pores, likely derived from the presence into heterotrophic cells would satisfy their metabolic demand. of PD. Similar structures are present, for example, in some of Maximum reported permeability coefficients for sucrose diffu- the mosses, the most ancient being termed water-conducting sion through PD are on the order of 6 × 10−6 ms−1 (Fisher cells (WCCs) and the more advanced being the hydroids of the and Wang 1995). Using this value, diffusion theory predicts that peristomate mosses (Mishler and Churchill 1984; Kenrick and a significant sucrose concentration drop would be required, Crane 1997; Ligrone et al. 2012). across each adjoining cell wall interface, to sustain this flux Hydroids often form a central strand in the gametophyte of sucrose from the autotrophic (photosynthetic) cells into the stem/sporophyte seta in the mosses (Figure 1A, B). During heterotrophic (water and mineral nutrient acquiring) cells. Thus, their development, these hydroid cells undergo various struc- the path length would be limited to only a few cells,
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