Parenchyma underlies the interspecific variation of xylem hydraulics and carbon storage across 15 woody species on a subtropical island in Japan

Abstract

Parenchyma is an important component of the secondary xylem. It has multiple functions and its fraction is known to vary substantially across angiosperm species. However, the physiological significance of this variation is not yet fully understood. Here, we examined how different types of parenchyma (ray and axial parenchyma, and axial parenchyma in direct contact with vessels [APV]) are coordinated with three essential xylem functions: water conduction, storage of non-structural carbohydrate (NSC), and mechanical support. Using branch sapwood of 15 co-occurring drought-adapted woody species from the subtropical Bonin Islands, Japan, we quantified ten xylem anatomical traits and examined their linkages to hydraulic properties, storage of soluble sugars and starch, and sapwood density. The fractions of APV and axial parenchyma in the xylem transverse sections were positively correlated with the percentage loss of conductivity in the native condition, whereas that of ray parenchyma was negatively correlated with the maximum conductivity across species. Axial and ray parenchyma fractions were positively associated with concentrations of starch and NSC. The fraction of parenchyma was independent of sapwood density, regardless of parenchyma type. We also identified a negative relationship between hydraulic conductivity and NSC storage and sapwood density, mirroring the negative relationship between the fractions of parenchyma and vessels. These results suggest that parenchyma fraction underlies species variation in xylem hydraulic and carbon use strategies, wherein xylem with a high fraction of axial parenchyma may adopt an embolism repair strategy through an increased starch storage with low cavitation resistance.

Parenchyma fractions drive the storage capacity of nonstructural carbohydrates across a broad range of tree species

“…We did not find significant relationships between NSCs and %RAP in subtropical and tropical tree species, therefore partially refuting our first hypothesis. Because our results are contradictory to the results of Kawai et al (2021), who found that RAP fractions were significantly associated with NSC content in the branches of 15 subtropical woody species, our low sample size (21 species) might not fully represent the variability in NSCs and RAP encountered in these climates. Additionally, RAP performs several major functions in tropical species, such as water storage and defense against pathogens, that may be less important in temperate species (Plavcová et al, 2016).…”

“…Parenchyma fractions might act as a proxy for NSC storage capacity, and recent studies showed positive correlations between RAP and NSC content in woody stems and branches (Plavcová et al, 2016; Godfrey et al, 2020; Chen et al, 2020; Kawai et al, 2021; Pratt et al, 2021). Although, these studies focused on a limited number of species, data suggest that the roles of RP and AP are distinct among species and climates.…”

“…Although, these studies focused on a limited number of species, data suggest that the roles of RP and AP are distinct among species and climates. For example, Chen et al (2020) found that NSC content was related to RAP and AP, but not RP in 19 temperate broadleaf tree species, while Kawai et al (2021) showed both AP and RP were associated with NSC content in the branches of 15 subtropical woody species. In addition, Plavcová et al (2016) found significantly lower NSC content but higher RAP volume in juvenile stems of four tropical species compared to 12 temperate species.…”

Wood Nutrient-Water-Density Linkages Are Influenced by Both Species and Environment

“…Moreover, as transpiration creates negative hydraulic pressures, surrounding tissues should, if hydrated, be able to provide water to the vascular tissues to reduce the risk of embolism. The structural mechanisms responsible for enhancing the water storage capacity in trees are underpinned by the anatomical configuration of the woody tissues with both capillary storage compartments (i.e., open vessels, tracheids, fibers, intercellular spaces, and cracks) and elastic storage compartments (i.e., living parenchyma cells) likely to be relevant ( Borchert and Pockman, 2005 ; Scholz et al, 2008 ; Jupa et al, 2016 ; Kawai et al, 2021 ). Not only the anatomic features define plant water storing capacity but also the chemical compounds with osmotic activity play an essential role in plant osmotic adjustment ( Turner and Jones, 1980 ; Turner, 2018 ; Signori-Müller et al, 2021 ).…”

Functional traits and water‐transport strategies of woody species in an insular environment in a tropical forest

“…Studies have shown that trade‐offs between secondary xylem and leaf structure promote adjustments concerning rates of water supply, hydraulic conductivity (Cosme et al, 2017; Olson, 2020), and embolism resistance (Lens et al, 2011; Li et al, 2016; Skelton et al, 2018). Such changes involve the distribution and volume of different cell types of secondary xylem (Tng et al, 2018; Percolla et al, 2021; Kawai et al, 2022); the frequency, grouping, and width of vessel elements (Dória et al, 2016); the thickness of the intervascular pit membrane (Plavcová et al, 2011; Dória et al, 2018); the degree of wood density (Chave et al, 2009; Ziemińska et al, 2020); and the amount of leaf area and stomatal density (Rossatto and Kolb, 2013). These adjustments can occur in varied combinations, and knowing the relative contribution of each to support continued water transport at the species level can help reveal plant strategies to survive different environments.…”