Variations in wood anatomy in Afrotropical trees with a particular emphasis on radial and axial parenchyma.

BACKGROUND AND AIMS: Understanding anatomical variations across plant phylogenies and environmental gradients is vital for comprehending plant evolution and adaptation. Previous studies on tropical woody plants have paid limited attention to quantitative differences in major xylem tissues, which serve specific roles in mechanical support (fibres), carbohydrate storage and radial conduction (radial parenchyma, rays), wood capacitance (axial parenchyma) and water transport (vessels). To address this gap, we investigate xylem fractions in 173 tropical tree species spanning 134 genera and 53 families along a 2200-m elevational gradient on Mount Cameroon, West Africa. METHODS: We determined how elevation, stem height and wood density affect interspecific differences in vessel, fibre, and specific axial (AP) and radial (RP) parenchyma fractions. We focus on quantifying distinct subcategories of homogeneous or heterogeneous rays and apotracheal, paratracheal and banded axial parenchyma. KEY RESULTS: Elevation-related cooling correlated with reduced AP fractions and vessel diameters, while fibre fractions increased. Lower elevations exhibited elevated AP fractions due to abundant paratracheal and wide-banded parenchyma in tall trees from coastal and lowland forests. Vasicentric and aliform AP were predominantly associated with greater tree height and wider vessels, which might help cope with high evaporative demands via elastic wood capacitance. In contrast, montane trees featured a higher fibre proportion, scarce axial parenchyma, smaller vessel diameters and higher vessel densities. The lack of AP in montane trees was often compensated for by extended uniseriate ray sections with upright or squared ray cells or the presence of living fibres. CONCLUSIONS: Elevation gradient influenced specific xylem fractions, with lower elevations showing elevated AP due to abundant paratracheal and wide-banded parenchyma, securing greater vessel-to-parenchyma connectivity and lower embolism risk. Montane trees featured a higher fibre proportion and smaller vessel diameters, which may aid survival under greater environmental seasonality and fire risk.

Adjustment of storage capacity for non-structural carbohydrates in response to limited water availability in two temperate woody species.

Reserves of non-structural carbohydrates (NSC) stored in living cells are essential for drought tolerance of trees. However, little is known about the phenotypic plasticity of living storage compartments (SC) and their interactions with NSC reserves under changing water availability. Here, we examined adjustments of SC and NSC reserves in stems and roots of seedlings of two temperate tree species, Acer negundo L. and Betula pendula Roth., cultivated under different substrate water availability. We found that relative contents of soluble NSC, starch and total NSC increased with decreasing water availability in stems of both species, and similar tendencies were also observed in roots of A. negundo. In the roots of B. pendula, soluble NSC contents decreased along with the decreasing water availability, possibly due to phloem decoupling or NSC translocation to shoots. Despite the contrast in organ responses, NSC contents (namely starch) positively correlated with proportions of total organ SC. Individual types of SC showed markedly distinct plasticity upon decreasing water availability, suggesting that water availability changes the partitioning of organ storage capacity. We found an increasing contribution of parenchyma-rich bark to the total organ NSC storage capacity under decreasing water availability. However, xylem SC showed substantially greater plasticity than those in bark. Axial storage cells, namely living fibers in A. negundo, responded more sensitively to decreasing water availability than radial parenchyma. Our results demonstrate that drought-induced changes in carbon balance affect the organ storage capacity provided by living cells, whose proportions are sensitively coordinated along with changing NSC reserves.

Relationships between trunk radial growth and fruit yield in apple and pear trees on size-controlling rootstocks.

BACKGROUND AND AIMS: Understanding the mutual co-ordination of vegetative and reproductive growth is important in both agricultural and ecological settings. A competitive relationship between vegetative growth and fruiting is often highlighted, resulting in an apparent trade-off between structural growth and fruit production. However, our understanding of factors driving this relationship is limited. METHODS: We used four scions grafted onto a series of size-controlling rootstocks to evaluate the relationships between the annual fruit yield and radial growth of trunks, branches and roots. To assess tree radial growth, we measured ring widths on extracted tree cores, which is an approach not frequently used in a horticultural setting. KEY RESULTS: We found that the yield and radial growth were negatively related when plotted in absolute terms or as detrended and normalized indices. The relationship was stronger in low vigour trees, but only after the age-related trend was removed. In contrast, when trunk radial growth was expressed as basal area increment, the negative relationship disappeared, suggesting that the relationship between trunk radial growth and fruit yield might not be a true trade-off related to the competition between the two sinks. The effect of low yield was associated with increased secondary growth not only in trunks but also in branches and roots. In trunks, we observed that overcropping was associated with reduced secondary growth in a subsequent year, possibly due to the depletion of reserves. CONCLUSIONS: Our results show that variation in annual fruit yield due to tree ageing, weather cueing and inherent alternate bearing behaviour is reflected in the magnitude of secondary growth of fruit trees. We found little support for the competition/architecture theory of rootstock-induced growth vigour control. More broadly, our study aimed at bridging the gap between forest ecology and horticulture.

Mechanical properties and structure-function trade-offs in secondary xylem of young roots and stems.

Bending and torsional properties of young roots and stems were measured in nine woody angiosperms. The variation in mechanical parameters was correlated to wood anatomical traits and analysed with respect to the other two competing functions of xylem (namely storage and hydraulics). Compared with stems, roots exhibited five times greater flexibility in bending and two times greater flexibility in torsion. Lower values of structural bending and structural torsional moduli (Estr and Gstr, respectively) of roots compared with stems were associated with the presence of thicker bark and a greater size of xylem cells. Across species, Estr and Gstr were correlated with wood density, which was mainly driven by the wall thickness to lumen area ratio of fibres. Higher fractions of parenchyma did not translate directly into a lower wood density and reduced mechanical stiffness in spite of parenchyma cells having thinner, and in some cases less lignified, cell walls than fibres. The presence of wide, partially non-lignified rays contributed to low values of Estr and Gstr in Clematis vitalba. Overall, our results demonstrate that higher demands for mechanical stability in self-supporting stems put a major constraint on xylem structure, whereas root xylem can be designed with a greater emphasis on both storage and hydraulic functions.

Vessel diameter is related to amount and spatial arrangement of axial parenchyma in woody angiosperms.

Parenchyma represents a critically important living tissue in the sapwood of the secondary xylem of woody angiosperms. Considering various interactions between parenchyma and water transporting vessels, we hypothesize a structure-function relationship between both cell types. Through a generalized additive mixed model approach based on 2,332 woody angiosperm species derived from the literature, we explored the relationship between the proportion and spatial distribution of ray and axial parenchyma and vessel size, while controlling for maximum plant height and a range of climatic factors. When factoring in maximum plant height, we found that with increasing mean annual temperatures, mean vessel diameter showed a positive correlation with axial parenchyma proportion and arrangement, but not for ray parenchyma. Species with a high axial parenchyma tissue fraction tend to have wide vessels, with most of the parenchyma packed around vessels, whereas species with small diameter vessels show a reduced amount of axial parenchyma that is not directly connected to vessels. This finding provides evidence for independent functions of axial parenchyma and ray parenchyma in large vesselled species and further supports a strong role for axial parenchyma in long-distance xylem water transport.

Vessel-associated cells in angiosperm xylem: Highly specialized living cells at the symplast-apoplast boundary.

BACKGROUND: Vessel-associated cells (VACs) are highly specialized, living parenchyma cells that are in direct contact with water-conducting, dead vessels. The contact may be sparse or in large tight groups of parenchyma that completely surrounds vessels. VACs differ from vessel distant parenchyma in physiology, anatomy, and function and have half-bordered pits at the vessel-parenchyma juncture. The distinct anatomy of VACs is related to the exchange of substances to and from the water-transport system, with the cells long thought to be involved in water transport in woody angiosperms, but where direct experimental evidence is lacking. SCOPE: This review focuses on our current knowledge of VACs regarding anatomy and function, including hydraulic capacitance, storage of nonstructural carbohydrates, symplastic and apoplastic interactions, defense against pathogens and frost, osmoregulation, and the novel hypothesis of surfactant production. Based on microscopy, we visually represent how VACs vary in dimensions and general appearance between species, with special attention to the protoplast, amorphous layer, and the vessel-parenchyma pit membrane. CONCLUSIONS: An understanding of the relationship between VACs and vessels is crucial to tackling questions related to how water is transported over long distances in xylem, as well as defense against pathogens. New avenues of research show how parenchyma-vessel contact is related to vessel diameter and a new hypothesis may explain how surfactants arising from VAC can allow water to travel under negative pressure. We also reinforce the message of connectivity between VAC and other cells between xylem and phloem.

An ecophysiological and developmental perspective on variation in vessel diameter.

Variation in xylem vessel diameter is one of the most important parameters when evaluating plant water relations. This review provides a synthesis of the ecophysiological implications of variation in lumen diameter together with a summary of our current understanding of vessel development and its endogenous regulation. We analyzed inter-specific variation of the mean hydraulic vessel diameter (Dv ) across biomes, intra-specific variation of Dv under natural and controlled conditions, and intra-plant variation. We found that the Dv measured in young branches tends to stay below 30 µm in regions experiencing winter frost, whereas it is highly variable in the tropical rainforest. Within a plant, the widest vessels are often found in the trunk and in large roots; smaller diameters have been reported for leaves and small lateral roots. Dv varies in response to environmental factors and is not only a function of plant size. Despite the wealth of data on vessel diameter variation, the regulation of diameter is poorly understood. Polar auxin transport through the vascular cambium is a key regulator linking foliar and xylem development. Limited evidence suggests that auxin transport is also a determinant of vessel diameter. The role of auxin in cell expansion and in establishing longitudinal continuity during secondary growth deserve further study.

A global analysis of parenchyma tissue fractions in secondary xylem of seed plants.

Parenchyma is an important tissue in secondary xylem of seed plants, with functions ranging from storage to defence and with effects on the physical and mechanical properties of wood. Currently, we lack a large-scale quantitative analysis of ray parenchyma (RP) and axial parenchyma (AP) tissue fractions. Here, we use data from the literature on AP and RP fractions to investigate the potential relationships of climate and growth form with total ray and axial parenchyma fractions (RAP). We found a 29-fold variation in RAP fraction, which was more strongly related to temperature than with precipitation. Stem succulents had the highest RAP values (mean ± SD: 70.2 ± 22.0%), followed by lianas (50.1 ± 16.3%), angiosperm trees and shrubs (26.3 ± 12.4%), and conifers (7.6 ± 2.6%). Differences in RAP fraction between temperate and tropical angiosperm trees (21.1 ± 7.9% vs 36.2 ± 13.4%, respectively) are due to differences in the AP fraction, which is typically three times higher in tropical than in temperate trees, but not in RP fraction. Our results illustrate that both temperature and growth form are important drivers of RAP fractions. These findings should help pave the way to better understand the various functions of RAP in plants.

Weak tradeoff between xylem safety and xylem-specific hydraulic efficiency across the world's woody plant species.

The evolution of lignified xylem allowed for the efficient transport of water under tension, but also exposed the vascular network to the risk of gas emboli and the spread of gas between xylem conduits, thus impeding sap transport to the leaves. A well-known hypothesis proposes that the safety of xylem (its ability to resist embolism formation and spread) should trade off against xylem efficiency (its capacity to transport water). We tested this safety-efficiency hypothesis in branch xylem across 335 angiosperm and 89 gymnosperm species. Safety was considered at three levels: the xylem water potentials where 12%, 50% and 88% of maximal conductivity are lost. Although correlations between safety and efficiency were weak (r(2)  < 0.086), no species had high efficiency and high safety, supporting the idea for a safety-efficiency tradeoff. However, many species had low efficiency and low safety. Species with low efficiency and low safety were weakly associated (r(2)  < 0.02 in most cases) with higher wood density, lower leaf- to sapwood-area and shorter stature. There appears to be no persuasive explanation for the considerable number of species with both low efficiency and low safety. These species represent a real challenge for understanding the evolution of xylem.

The amount of parenchyma and living fibers affects storage of nonstructural carbohydrates in young stems and roots of temperate trees.

PREMISE OF THE STUDY: Concentrations of nonstructural carbohydrates (NSCs) are used as proxies for the net carbon balance of trees and as indicators of carbon starvation resulting from environmental stress. Woody organs are the largest NSC-storing compartments in forest ecosystems; therefore, it is essential to understand the factors that affect the size of this important storage pool. In wood, NSC are predominantly deposited in ray and axial parenchyma (RAP); however, direct links between nutrient storage and RAP anatomy have not yet been established. Here, we tested whether the NSC storage capacity of wood is influenced by the amount of RAP. METHODS: We measured NSC concentrations and RAP fractions in root and stem sapwood of 12 temperate species sampled at the onset of winter dormancy and in stem sapwood of four tropical trees growing in an evergreen lowland rainforest. The patterns of starch distribution were visualized by staining with Lugol's solution. KEY RESULTS: The concentration of NSCs in sapwood of temperate trees scales tightly with the amount of RAP and living fibers (LFs), with almost all RAP and LFs being densely packed with starch grains. In contrast, the tropical species had lower NSC concentrations despite their higher RAP and LFs fraction and had considerable interspecific differences in starch distribution. CONCLUSIONS: The differences in RAP and LFs abundance affect the ability of sapwood to store NSC in temperate trees, whereas a more diverse set of functions of RAP might be pronounced in species growing in a tropical environment with little seasonality.