Trait coordination, mechanical behaviour and growth form plasticity of Amborella trichopoda under variation in canopy openness

Research Article Trait coordination, mechanical behaviour and growth form plasticity of Amborella trichopoda under variation in canopy openness Santiago Trueba*1, Sandrine Isnard1, Daniel Barthélémy2 and Mark E. Olson3  IRD, UMR AMAP, Laboratoire de Botanique et d’Ecologie Végétale Appliquées, Noumea, BPA5, 98800, New Caledonia CIRAD, BIOS Direction, and INRA, UMR AMAP, F-34398 Montpellier, France 3  noma de México, Tercer Circuito s/n de Ciudad Universitaria México, México DF Instituto de Biologıa, Universidad Nacional Auto 04510, México 1 Received: 1 April 2016; Accepted: 12 September 2016; Published: 26 September 2016 Associate Editor: Rafael S. Oliveira Citation: Trueba S, Isnard S, Barthélémy D, Olson ME. 2016. Trait coordination, mechanical behaviour and growth form plasticity of Amborella trichopoda under variation in canopy openness. AoB PLANTS 8: plw068; doi: 10.1093/aobpla/plw068 Abstract. Understanding the distribution of traits across the angiosperm phylogeny helps map the nested hierarchy of features that characterize key nodes. Finding that Amborella is sister to the rest of the angiosperms has raised the question of whether it shares certain key functional trait characteristics, and plastic responses apparently widespread within the angiosperms at large. With this in mind, we test the hypothesis that local canopy openness induces plastic responses. We used this variation in morphological and functional traits to estimate the pervasiveness of trait scaling and leaf and stem economics. We studied the architecture of Amborella and how it varies under different degrees of canopy openness. We analyzed the coordination of 12 leaf and stem structural and functional traits, and the association of this covariation with differing morphologies. The Amborella habit is made up of a series of sympodial modules that vary in size and branching pattern under different canopy openness. Amborella stems vary from self-supporting to semi-scandent. Changes in stem elongation and leaf size in Amborella produce distinct morphologies under different light environments. Correlations were found between most leaf and stem functional traits. Stem tissue rigidity decreased with increasing canopy openness. Despite substantial modulation of leaf size and leaf mass per area by light availability, branches in different light environments had similar leaf area-stem size scaling. The sympodial growth observed in Amborella could point to an angiosperm synapomorphy. Our study provides evidence of intraspecific coordination between leaf and stem economic spectra. Trait variation along these spectra is likely adaptive under different light environments and is consistent with these plastic responses having been present in the angiosperm common ancestor. 2 Keywords: Adaptation; allometry; biomechanics; leaf mass per area; light environment; modulus of elasticity; phenotypic plasticity; plant architecture. * Corresponding author’s e-mail address: C The Authors 2016. Published by Oxford University Press on behalf of the Annals of Botany Company. V This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/ licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited. AoB PLANTS www.aobplants.oxfordjournals.org C The Authors 2016 V 100 Trueba et al.—Trait coordination and structural variation in Amborella trichopoda Introduction 002 AoB PLANTS www.aobplants.oxfordjournals.org C The Authors 2016 V Comparative biology is built on an understanding of the patterns of distribution of organismal characters. Those that uniquely characterize single clades are known as synapomorphies. The nested hierarchy of synapomorphies across the tree of life helps to reconstruct the patterns of relationships between taxa (Nixon and Wheeler 1990). In contrast, characters that arise repeatedly can reflect an array of processes from convergent evolution to shared propensities for evolving similar traits independently, reflecting convergence or parallelism (Harvey and Pagel 1991; Losos 2011; Scotland 2011). To understand the distribution of traits within a group, it is crucial to study as wide an array of lineages as possible. Among the flowering plants, Amborella trichopoda (Amborellaceae), a dioecious woody plant endemic to the moist forests of New Caledonia, has attracted the attention of plant science since the end of the last century, after several phylogenetic studies supported the position of Amborella as the single surviving representative of a lineage sister to all other extant angiosperms (Mathews and Donoghue 1999; Soltis et al. 1999; Mathews and Donoghue 2000; Qiu et al. 2000; Soltis et al. 2000; Amborella Genome Project 2013; Poncet et al. 2013). Because of its phylogenetic position, the analysis of Amborella traits is of interest in understanding the evolution of the ecology, function and structure of flowering plants (Amborella Genome Project 2013). Finding that there are features shared by Amborella and other flowering plants, but not the gymnosperms, could point to angiosperm synapomorphies or important convergent features. On the other hand, finding that there are features shared by Amborella and the gymnosperms but not the rest of the angiosperms could reveal useful information regarding the early sequence of character evolution within the flowering plants. This study focuses on patterns, potentially synapomorphic and homoplasious, currently being documented all across the woody plants. Through the description of Amborella’s architectural and biomechanical organization, combined with analyses of the coordination of functional leaf and stem traits and their variation under different light environments, we can provide elements for understanding the evolution of growth forms in the flowering plants and how these forms vary developmentally under different light conditions. One of the longstanding questions in the study of angiosperm structure concerns the habit and growth form of the earliest flowering plants. Amborella has a multi-stemmed habit with stems that have been described as semiscandent (Feild et al. 2001; Feild and Wilson 2012). This growth habit is often called ‘cane-like’ and seems to be widespread in the ‘basal’ lineages of angiosperms (e.g. Aristolochia, Eupomatia, Illicium, Piper, Sarcandra, Thottea and Trimenia) (Carlquist 1996; 2001; Feild and Arens 2005; Carlquist 2009; Isnard et al. 2012), pointing to a potential angiosperm synapomorphy. The cane-like habit seems to be characterized by a combination of sympodial growth and mechanical laxness, with stems that are relatively long for their tissue stiffnesses (Feild and Arens 2007; Carlquist 2009). The sympodiality and laxity observed in the stems of these cane-like shrubs can be directly assessed by the analysis of their architectural and mechanical p (...truncated)