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New frontiers in the three‐dimensional visualization of plant structure and function
Author(s) -
Brodersen Craig R.,
Roddy Adam B.
Publication year - 2016
Publication title -
american journal of botany
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.218
H-Index - 151
eISSN - 1537-2197
pISSN - 0002-9122
DOI - 10.3732/ajb.1500532
Subject(s) - biology , visualization , function (biology) , evolutionary biology , artificial intelligence , computer science
For thousands of years, humans have acknowledged the existence of structures and organisms that exist at a scale unresolvable with the naked eye. Not until the invention of the compound microscope in the late 1500s were structures magnifi ed suffi ciently to reveal the previously unseen ( Bolam, 1973 ). Th e resulting observations were revolutionary and radically altered contemporary thinking on the structure and function of living organisms. Pioneering work by Nehemiah Grew (1682) and Marcello Malpighi (1686) identifi ed what at the time were considered novel structures in plants. Grew clearly recognized that plant tissues needed to be conceptualized in three dimensions (3D) because they were composed of microscopic structures with distinct spatial relationships. He made some of the fi rst attempts at reconstructing vascular elements in 3D by introducing depth and perspective to his illustrations ( Figs. 1A, 2 ), and almost certainly dealt with the technological limitations of visualizing the inner depths of opaque, 3D tissues ( Fig. 1B ). Grew’s illustrations provided the fi rst indications of how complex and varied the internal organization of plants can be ( Fig. 2 ), and in the subsequent 300 years, our understanding of the spatial organization of plant vascular systems has increased signifi cantly. However, major obstacles have persisted in understanding the fundamental relationships between xylem structure and function, which are directly related to the challenge of visualizing 3D structures with traditional, two-dimensional techniques. Since Grew’s time, the advent of photography and advanced histological techniques have signifi cantly improved the visualization and reproduction of xylem networks compared with manual illustrations. Yet, to reconstruct the pathway that water traverses through roots and stems, hundreds of serial cross sections are needed. Th ose sections must then be stacked in perfect alignment to reconstruct the xylem network manually, which is a signifi cant and tedious task. As a consequence, the 3D internal structure of plants has remained largely unexplored. Th e development of the optical shuttle technique ( Zimmermann and Tomlinson, 1966 ) was a major step forward. Using traditional serial sectioning and light microscopy, the optical shuttle method exposes each serial section onto subsequent frames of motion picture fi lm, thereby assigning the axial position of each serial section to a specifi c point in time. Playing the movie in the forward or reverse direction allows the viewer to quickly explore extraordinarily complex xylem networks. Indeed, much of what we know about xylem network connectivity and development originates from optical shuttle serial sectioning and the tireless eff orts of early pioneers. For example, what appeared in two-dimensional cross sections of palm stems to be a random, scattered distribution of vascular bundles were actually an elegant and effi cient arrangement of bifurcating tissues ( Zimmermann et al., 1982 ). Even with the development of the optical shuttle method, manual reconstruction of xylem networks remains a significant obstacle. Advancements in nondestructive, 3D imaging technologies are beginning to overcome many limitations of manual serial sectioning and are providing new insight into the spatial organization of plants in both extant and fossilized material. In this essay we highlight recent advancements in nondestructive 3D imaging that have the potential to fundamentally change our knowledge of plant anatomy and physiology. Nuclear magnetic resonance (NMR) imaging is gaining popularity for the study of plant vascular function, and plantspecifi c facilities have emerged to meet the growing demand (e.g., Wageningen NMR Centre). NMR imaging has the advantage of being noninvasive, allowing researchers to study intact, living plants and monitor the functional status of xylem and phloem networks without disrupting the positive and negative pressures that drive 1 Manuscript received 17 December 2015; revision accepted 20 January 2016. Yale University, School of Forestry & Environmental Studies, 195 Prospect Street, New Haven, Connecticut 06511 USA 2 Author for correspondence: (e-mail: craig.brodersen@yale.edu) doi:10.3732/ajb.1500532 O N T H E N AT U R E O F T H I N G S New Ideas and Directions in Botany

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