Unravelling roots of lianas: a case study in Sapindaceae

Abstract

Background and Aims Roots are key in the evolution of plants, being in charge of critical functions, such as water and nutrient uptake and anchorage of the plant body. Stems of lianescent Sapindaceae conform to the anatomical patterns typical of climbing plants, having cambial variants in their stems and vessel dimorphism in their wood. The roots of these lianas, however, are largely unexplored, so we do not know whether the plant habit has as strong an impact on their anatomy as on the anatomy of their stems. Our aim was, therefore, to thoroughly explore the anatomy of liana roots, underground organs under selective pressure completely different from that experienced by the stems.Methods We studied mature roots of 14 species belonging to five of the six genera currently recognized in the lianoid tribe Paullinieae (Sapindaceae) using traditional methods for macro-and microscopic analyses, as well as micro-computed tomography (micro-CT) techniques.Key Results Roots were shown to be strongly shaped by the lianescent habit in Paullinieae, exhibiting traits of the lianescent vascular syndrome in terms of both wood and overall anatomy. The only way to distinguish root from stem in secondary growth is by the exarch protoxylem position in the roots, as opposed to the endarch position typical of the stems. The most conspicuous trait of the lianescent vascular syndrome, which is the presence of vessel dimorphism, is evident in all roots, and we hypothesize that it helps to create an efficient, safe pathway for water conduction from this organ towards the stems. Other anatomical features present were parenchyma bands, present in the wood of almost all of the analysed species, except for Thinouia and Urvillea, where parenchyma-like fibre bands alternating with ordinary fibres are present. The majority of the roots showed no cambial variants. However, lobed roots were found in Urvillea rufescens and phloem wedges were observed in Serjania lethalis and Serjania caracasana. Neo-formed peripheral vascular strands and cylinders were common in mature roots of Serjania caracasana, and vascular connections were found uniting the peripheral and central vascular cylinders through phloem wedges, as revealed by anatomical and micro-CT analyses. The vascular connections likely represent another key mechanism to create a network that increases the area of vascular tissue and contributes as an additional conduction pathway within these thick roots.Conclusions Some traits from the lianescent vascular syndrome, such as vessel dimorphism, are present in the roots of lianescent Sapindaceae, while others, such as cambial variants common in the stems, are largely absent.

Liana and tree below-ground water competition—evidence for water resource partitioning during the dry season

“…This will result in the activity of tree roots literally being pushed to deeper soil layers where Ψ soil values are still less negative due to the presence of non-exhausted water reserves, which were replenished during the wet season. The ability of lianas to remain active in upper soil layers and to efficiently exploit the small rainfall input (see Figure S1 available as Supplementary Data at Tree Physiology Online) can potentially be attributed to the following reasons: (i) lianas are able to actively lower their osmotic potential to ensure the maintenance of a functional water potential gradient within the liana ( De Guzman et al 2016 , Maréchaux et al 2017 ); and (ii) lianas may be able to form hydraulic bridges by-passing embolized large vessels and ensuring an intact water column by their ability to anatomically adapt bimodal distribution of vessel diameter (i.e., vessel dimorphism) ( Bastos et al 2016 ). The strategy of maintaining an active upper root system might be very beneficial for lianas as this allows them to have a competitive advantage not only for water, but also a strong advantage for accessing nutrients in the upper soil layers, which may account for the dry season growth advantage of lianas as previously noted ( Schnitzer 2005 , Cai et al 2009 ).…”

Climbing since the early Miocene: The fossil record of Paullinieae (Sapindaceae)

“…The combination of peripheral vascular strands (Figs 2A–2C and 4A & 4B ), vessel dimorphism (Figs 2F & 2I and 4B–4D ), wide vessels solitary or in tangential multiples of 2–3 ( Fig 2F and 4C ), narrow vessels in long radial multiples of 2–21 (Figs 2F and 4C & 4D ), alternate intervessel pits with slit-like coalescent apertures (Figs 2G and 2H and 4E ), heterocellular rays, prismatic crystals in axial parenchyma (Figs 3D and 4F ), and dark content (possibly phenolic compounds) in primary vascular parenchyma and ray parenchyma ( Fig 2D and 2E ) support the inclusion of Ampelorhiza in Paullinieae [ 13 , 16 , 18 , 64 , 66 , 92 , 93 , 94 ]. Two wood anatomical characters typical of extant Paullinieae were not observed in the fossils: 1) alternating bands of thin and thick-walled regions in the wood which may either be axial parenchyma alternating with ordinary fibers (e.g., Serjania spp.)…”

“…Although cambial variants are often associated with the climbing habit, the presence of peripheral vascular strands is not sufficient to identify the fossils as stems or roots. Bastos et al [ 16 , 66 ] demonstrated that cambial variants can be found in both organs. In stems of Paullinieae, the pith is conspicuously angular (e.g., triangular, pentangular) in transverse section with primary vascular bundles at the corners [ 19 ].…”

“…The placement of Ampelorhiza within Paullinieae is supported by vessel dimorphism, heterocellular rays, and axial parenchyma strands typically 2-4 cells long. One synapomorphy of Paullinieae that we did not observe in the fossil is wide rays (ray dimorphism); however, we only examined two root fragments and this character is observed in many, but not all, samples from modern roots [ 16 ].…”

“…Finally, we added the character “habit” (0 = self-supporter, 1 = climber) and scored it for all extant species. Although the wood anatomy characters scored for extant species were observed in stems and the fossils are roots, available evidence indicates that differences in wood anatomy between stems and roots within individual plants tend to be quantitative rather than qualitative [ 16 , 65 , 66 ]. The resulting dataset ( S1 Appendix ) comprises 216 tips and 1517 characters with three partitions: anatomy (1-28), ITS (29-882), and trnL intron (883-1517).…”