Int. J. Plant Sci. 174(7):1014–1048. 2013. ᭧ 2013 by The University of Chicago. All rights reserved. 1058-5893/2013/17407-0004$15.00 DOI: 10.1086/670258 WOOD ANATOMY AND EVOLUTION: A CASE STUDY IN THE BIGNONIACEAE Marcelo R. Pace1,* and Veronica Angyalossy* *Departamento de Botaˆnica, Instituto de Biocieˆncias, Universidade de Sa˜o Paulo, Rua do Mata˜o, 277, Cidade Universita´ria, CEP 05508-090, Sa˜o Paulo, Sa˜o Paulo, Brazil Wood (secondary xylem) is responsible for water transport and has been well-studied anatomically, eco- logically, physiologically, and phylogenetically. Comparative methods can reveal patterns of evolution for xylem traits using knowledge from the phylogenetic history of the taxa and the branching pattern of phylogenies. Bignoniaceae (Lamiales) is a family of pantropical plants of various growth habits that includes trees, shrubs, and lianas, which display diverse wood anatomies and for which robust phylogenies are available. Here we review important aspects in classical wood anatomy and evolution and test hypotheses regarding patterns of wood evolution using the Bignoniaceae as a model. Altogether, 85% of the genera currently recognized in Bignoniaceae were sampled, and 30 characters were delimited and mapped onto a robust phylogeny of the family. Some patterns of wood evolution within the Bignoniaceae seem to have been shaped by ecophysiological and habit aspects in the family. For example, vessels increase in diameter in the lianoid lineages but decrease in trees and shrubs during evolution. Rays in trees have evolved from a mixture of homo- and heterocellular to exclusively homocellular and storied in some lineages, while in the lianas the opposite pattern was recorded. Other patterns are consistent with more general phylogenetic trends; for example, parenchyma increases in abundance from the most basal to the most derived nodes of the phylogeny. Other characters in the family that are delimited and discussed include growth rings, porosity, perforation plates, ray width, and height. This work provides evidence that wood evolution is rather labile and that the evolution of new habits and the occupation of new habitats greatly influence wood evolution. Keywords: Bignonieae, diversification, liana, secondary xylem, Tabebuia, tracheary element. Online enhancement: appendix. Introduction Secondary xylem is formed by a lateral meristem known as the vascular cambium, a meristem with two types of initials: In this special issue dedicated to the evolution and devel- fusiform initials, which are vertically elongated, and ray ini- opment of wood plants, this article aims to summarize some tials, which are radially elongated (Eames and MacDaniels of the most fundamental information on wood anatomy and 1925; Evert 2006). Together they differentiate into the sec- evolution to date and to explore xylem evolution in the Big- ondary xylem (fig. 1), undergoing secondary wall deposition noniaceae (Lamiales), a diverse family of pantropical plants. and lignification, with fusiform initials giving rise to the con- Wood (secondary xylem) first appeared in the common an- ducting cells (tracheids and/or vessels), fibers, and axial pa- cestor of the progymnosperms and all extant woody plants by renchyma and ray initials giving rise to rays, which are mainly ∼ the middle Devonian, at 390 Ma (Beck 1962; Meyer- parenchymatous in nature (Evert 2006), although radial tra- Berthaud et al. 2000, 2010; Decombeix et al. 2005, 2011), cheids (Thompson 1910; Gordon 1912; Eames and Mac- aside from independent evolution of wood in the extinct ar- Daniels 1925), perforated ray cells (Chalk and Chattaway borescent lycophytes and monilophytes (Kenrick and Crane 1933; Van Vliet 1976; Machado et al. 1997; Sonsin et al. 1997; Simpson 2010). Altogether, the extinct progymnosperms 2008), and radial fibers (Lev-Yadun 1994) can also be present and all extant woody plants form a monophyletic group in rays. The tracheids and vessels are nonliving cells at maturity known as the lignophytes (Meyer-Berthaud et al. 2010; Simp- (Eames and MacDaniels 1925; Bailey 1953; Esau 1960; Pen- son 2010), and all of them likely share a homologous genetic nell and Lamb 1997; Groover and Jones 1999; Fukuda 2000; developmental toolkit (Groover 2005). The evolution from a Bolho¨ ner et al. 2012), while fibers can be living or nonliving simple to a more complex vascular system was likely triggered (Eames and MacDaniels 1925; Fahn and Arnon 1963; Itabashi by the occupation of land and by moving from a more mesic et al. 1999; Bolho¨ ner et al. 2012). Axial and ray parenchyma to a drier climate (Kenrick and Crane 1997; Carlquist 2012). are living at maturity (Esau 1960; Carlquist 1961; Catesson 1990; Nakaba et al. 2006, 2008, 2012a, 2012b), except in 1 Author for correspondence; e-mail: [email protected], heartwood (Stewart 1933; Esau 1960; Nakaba et al. 2012b). [email protected]. All the living cells in the wood play a physiological role in Manuscript received August 2012; revised manuscript received February 2013; food storage and transport (Chaffey and Barlow 2001; Nakaba electronically published August 7, 2013. et al. 2006, 2012a; Yamada et al. 2011), embolism repair 1014 PACE & ANGYALOSSY—WOOD EVOLUTION IN BIGNONIACEAE 1015 1957; Bailey and Howard 1941a, 1941b, 1941c). In their ar- ticles, Bailey, Frost, Cheadle, and coauthors suggested a pattern of evolution for both the vessels and the fibers in which both derived cell types depart from an ancestral tracheid (fig. B1; figs. B1–B3 are available online). On the basis of the evolution of these perforate and imperforate tracheary elements, “lines of evolution” were proposed for axial and ray parenchyma of the secondary xylem (Kribs 1935, 1937; Barghoorn 1940, 1941a, 1941b; figs. B2, B3). The evolution of these cell types was based mainly on statistical correlations, first between the type and morphology of tracheary elements and the taxonomic groups (Bailey and Tupper 1918; Frost 1930a, 1930b, 1931) and later on the type of tracheary elements, the types of axial and ray parenchyma cells, and their arrangements (Kribs 1935, 1937). Altogether these putative evolutionary trends were named “major trends of xylem evolution” by Carlquist (1961) and have strongly influenced numerous theories on xylem cell evolution to date. According to these theories, vessels and fi- bers evolved from tracheids, and the more similar a vessel is to a tracheid, the more primitive it would be considered (Bailey and Tupper 1918). Regarding ray evolution, Kribs (1935) sug- gested that the most primitive condition was that of woods with both multiseriate and uniseriate rays cooccurring, with both rays being high and heterocellular in composition. Ac- cording to Kribs (1935), ray evolution involved a gradual de- crease in height and number of upright and square cells as Fig. 1 Drawing illustrating the secondary xylem of Handroanthus chrysotrichus, indicating vessels, fibers, and axial and ray parenchyma seen in longitudinal section, eventually evolving into a ho- in the three planes, transverse, radial, and tangential. Drawn by M. mocellular ray (Kribs 1935; fig. B2). For axial parenchyma, Kubo. the primitive type of axial parenchyma was inferred as apo- tracheal scanty or diffuse, evolving toward progressively larger volumes of parenchyma within the stem and in association (Holbrook and Zwieniecki 1999; Salleo et al. 2004), biological with the vessels (paratracheal parenchyma; Kribs 1937; Carl- defense, or heartwood formation (Stewart 1933; Nakaba et quist 1961; fig. B3). al. 2012b). Since part of the cells are alive in the secondary A caveat of these theories was that the possible mechanisms xylem (sapwood), it is possible, in turn, to perform molecular involved in the evolution of wood were not fully explored. techniques such as DNA and RNA extraction (Oh et al. 2003; Nowadays, it is clear that the environment has an enormous Nieminen et al. 2008), allowing species identification (DNA impact on wood anatomical features (Carlquist 1966, 1975, barcoding of woods; Ho¨ ltken et al. 2012), compilation of gene 1988; Van der Graaff 1974; Van den Oever et al. 1981; Baas expression profiles (Ko and Han 2004; Nieminen et al. 2008), and Schweingruber 1987; Alves and Angyalossy-Alfonso and in situ hybridization (Groover et al. 2006). 2000, 2002), with even closely related taxa having marked Because many cell types constitute the secondary xylem, this differences depending on their growth provenance (e.g., Ilex tissue is considered complex (Evert 2006), and a great deal of spp.; Baas 1973). Some ecological trends are nowadays well diversity in the spatial distribution of its cells can be observed. established for ecological wood anatomy and have been sug- That different taxa can have a totally different distributional gested to be one of the main drivers of wood evolution through pattern of these cells allows us to recognize many plant taxa adaptation (Baas et al. 2003). Vessels, for instance, were shown solely by their wood tissues (Record and Hess 1943; De´tienne to decrease in length and diameter from lower to higher lat- and Jacquet 1983; Schweingruber 1990; reviewed in Wheeler itudes, while the inverse occurs to the abundance of vessels and Baas 1998). Two contrasting examples of such organiza- with scalariform perforation plates and helical thickening tions from tropical woods are seen, for example, in the Sap- (Baas 1973; Van der Graaff and Baas 1974; Baas and Schwein- otaceae and the Leguminosae. Most of the Sapotaceae are dis- gruber 1987; Baas et al. 1983,