Linking drought‐induced xylem embolism resistance to wood anatomical traits in Neotropical trees

Abstract

Summary Drought‐induced xylem embolism is considered to be one of the main factors driving mortality in woody plants worldwide. Although several structure–functional mechanisms have been tested to understand the anatomical determinants of embolism resistance, there is a need to study this topic by integrating anatomical data for many species. We combined optical, laser, and transmission electron microscopy to investigate vessel diameter, vessel grouping, and pit membrane ultrastructure for 26 tropical rainforest tree species across three major clades (magnoliids, rosiids, and asteriids). We then related these anatomical observations to previously published data on drought‐induced embolism resistance, with phylogenetic analyses. Vessel diameter, vessel grouping, and pit membrane ultrastructure were all predictive of xylem embolism resistance, but with weak predictive power. While pit membrane thickness was a predictive trait when vestured pits were taken into account, the pit membrane diameter‐to‐thickness ratio suggests a strong importance of the deflection resistance of the pit membrane. However, phylogenetic analyses weakly support adaptive coevolution. Our results emphasize the functional significance of pit membranes for air‐seeding in tropical rainforest trees, highlighting also the need to study their mechanical properties due to the link between embolism resistance and pit membrane diameter‐to‐thickness ratio. Finding support for adaptive coevolution also remains challenging.

Pore constrictions in intervessel pit membranes provide a mechanistic explanation for xylem embolism resistance in angiosperms

“…There are three possible reasons why modelled embolism resistance does not match the absolute values of the measured P 12 values, and these reasons may not be mutually exclusive. First, the values obtained from Model 1 are based on embolism propagation estimates for a single pit membrane model with a certain thickness, while P 12 and P 50 values represent hydraulically weighted losses of conductivity at the vessel network level, which is affected by various structural xylem parameters, such as vessel grouping and the ratio of T PM to pit membrane area (Levionnois et al ., 2021).…”

“…Angiosperm species with thick pit membranes were found to be more resistant to drought‐induced embolism than species with thin pit membranes (Jansen et al ., 2009; Li et al ., 2016a,b; Dória et al ., 2019; Trueba et al ., 2019; Thonglim et al ., 2020; Levionnois et al ., 2021). This functional link between T PM and P 50 , which is the xylem water potential corresponding to a 50% loss in maximum hydraulic conductivity ( P 50 , MPa), is valid at the interspecific (Li et al ., 2016a,b), intrageneric (Lens et al ., 2011; Plavcová & Hacke, 2012; Scholz et al ., 2013) and intraspecific level (Schuldt et al ., 2016).…”

Root plasticity under abiotic stress

“…Drought directly hampers root growth and development ( Comas et al, 2013 ; Gupta et al, 2020 ), and low water uptake by the roots puts extra tension on xylem tissue. Without acclimation of the xylem, this may cause embolism of the xylem resulting in hydraulic failure ( Sevanto, 2014 ; Levionnois et al, 2020 ; Li et al, 2021 ). Drought stress also affects nutrient uptake as nutrient mobility and diffusion is hampered ( Rouphael et al, 2012 ; He and Dijkstra, 2014 ).…”

“…Such root xylem distributions have been proposed to provide high hydraulic conductance while reducing the risk of hydraulic failure ( Li et al, 2021 ). Large xylem cells with high conductivity can allow for deeper rooting ( Strock et al, 2020 ), but under prolonged stress, most drought-tolerant crops opt for numerous small xylem vessels ( Klein et al, 2020 ; Ramachandran et al, 2020 ; Strock et al, 2020 ), which can have big consequences for plant survival under drought ( Scoffoni et al, 2017 ; Levionnois et al, 2020 ). In poplar salt stress resulted in reduced xylem cells and vessel diameters ( Junghans et al, 2006 ), while in tomato roots lignified xylem cells increased under salt stress ( Sánchez-Aguayo et al, 2004 ).…”

From cells to stems: the effects of primary vascular construction on drought‐induced embolism in fern rhizomes

“…Other cellular traits, such as pit membrane thickness, have been almost ubiquitously demonstrated to scale with resistance to drought‐induced embolism in woody and herbaceous seed plant stems (Li et al ., 2016; Dória et al ., 2019; Kaack et al ., 2019; Levionnois et al ., 2020; Thonglim et al ., 2020; Kaack et al ., 2021) and fern leaves (Brodersen et al ., 2014). While no scalable relationship exists between conduit size and pit membrane thickness within a cell type (i.e.…”