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Wood allocation trade-offs between fiber wall, fiber lumen, and axial parenchyma drive drought resistance in neotropical trees.

ABSTRACT: Functional relationships between wood density and measures of xylem hydraulic safety and efficiency are ambiguous, especially in wet tropical forests. In this meta-analysis, we move beyond wood density per se and identify relationships between xylem allocated to fibers, parenchyma, and vessels and measures of hydraulic safety and efficiency. We analyzed published data of xylem traits, hydraulic properties and measures of drought resistance from neotropical tree species retrieved from 346 sources. We found that xylem volume allocation to fiber walls increases embolism resistance, but at the expense of specific conductivity and sapwood capacitance. Xylem volume investment in fiber lumen increases capacitance, while investment in axial parenchyma is associated with higher specific conductivity. Dominant tree taxa from wet forests prioritize xylem allocation to axial parenchyma at the expense of fiber walls, resulting in a low embolism resistance for a given wood density and a high vulnerability to drought-induced mortality. We conclude that strong trade-offs between xylem allocation to fiber walls, fiber lumen, and axial parenchyma drive drought resistance in neotropical trees. Moreover, the benefits of xylem allocation to axial parenchyma in wet tropical trees might not outweigh the consequential low embolism resistance under more frequent and severe droughts in a changing climate.

SUBMITTER: Janssen TAJ

PROVIDER: S-EPMC7155043 | biostudies-literature | 2020 Apr

REPOSITORIES: biostudies-literature

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Wood allocation trade-offs between fiber wall, fiber lumen, and axial parenchyma drive drought resistance in neotropical trees.

Janssen Thomas A J TAJ Hölttä Teemu T Fleischer Katrin K Naudts Kim K Dolman Han H

Plant, cell & environment 20200203 4

Functional relationships between wood density and measures of xylem hydraulic safety and efficiency are ambiguous, especially in wet tropical forests. In this meta-analysis, we move beyond wood density per se and identify relationships between xylem allocated to fibers, parenchyma, and vessels and measures of hydraulic safety and efficiency. We analyzed published data of xylem traits, hydraulic properties and measures of drought resistance from neotropical tree species retrieved from 346 sources ...[more]

PMID: 31760666

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Project description:The abundance of living cells in wood-mainly as interconnected axial and ray parenchyma networks-varies widely between species. However, the functional significance of this variation and its role in plant ecological strategies is poorly understood, as is the extent to which different parenchyma fractions are favored in relation to soil nutrients and hydraulic functions. We analyzed wood tissue fractions of 16 Australian angiosperm species sampled from two nearby areas with similar climate but very different soil nutrient profiles and investigated structure-function links with soil and tissue nutrient concentrations and other plant traits. We expected the variation in parenchyma fractions to influence nutrient concentrations in wood xylem, and to find species with lower parenchyma fractions and accordingly lower nutrient requirements on lower-nutrient soils. Surprisingly, both axial and ray parenchyma fractions were mostly unrelated to tissue and soil nutrient concentrations, except for nitrogen concentration in stem sapwood. Species from low nutrient soils showed higher fractional P translocation from both leaves and sapwood, but little patterning with respect to tissue nitrogen. While species from high and low nutrient soils clearly clustered along the soil-fertility axis, their tissue composition varied independently from plant functional traits related to construction costs and hydraulic anatomy. Our findings imply that there is considerable variation among species in the nutrient concentrations within different parenchyma tissues. The anatomical composition of wood tissue seems unrelated to plant nutrient requirements. Even though xylem parenchyma is involved in metabolic functions such as nutrient translocation and storage, parenchyma abundance on its own does not directly explain variation in these functions, even in co-occurring species. While parenchyma is highly abundant in wood of angiosperm trees, we are still lacking a convincing ecological interpretation of its variability and role in whole-tree nutrient budgets.

Project description:Background and aimsMost crops have been dramatically altered from their wild ancestors with the primary goal of increasing harvestable yield. A long-held hypothesis is that increased allocation to yield has reduced plant investment in defence and resulted in crops that are highly susceptible to pests. However, clear demonstrations of these trade-offs have been elusive due to the many selective pressures that occur concurrently during crop domestication.MethodsTo provide a robust test of whether increased allocation to yield can alter plant investment in defence, this study examined fruit chemical defence traits and herbivore resistance across 52 wild and 56 domesticated genotypes of apples that vary >26-fold in fruit size. Ninety-six phenolic metabolites were quantified in apple skin, pulp and seeds, and resistance to the codling moth was assessed with a series of bioassays.Key resultsThe results show that wild apples have higher total phenolic concentrations and a higher diversity of metabolites than domesticated apples in skin, pulp and seeds. A negative phenotypic relationship between fruit size and phenolics indicates that this pattern is driven in part by allocation-based trade-offs between yield and defence. There were no clear differences in codling moth performance between wild and domesticated apples and no overall effects of total phenolic concentration on codling moth performance, but the results did show that codling moth resistance was increased in apples with higher phenolic diversity. The concentrations of a few individual compounds (primarily flavan-3-ols) also correlated with increased resistance, primarily driven by a reduction in pupal mass of female moths.ConclusionsThe negative phenotypic relationship between fruit size and phenolic content, observed across a large number of wild and domesticated genotypes, supports the hypothesis of yield-defence trade-offs in crops. However, the limited effects of phenolics on codling moth highlight the complexity of consequences that domestication has for plant-herbivore interactions. Continued studies of crop domestication can further our understanding of the multiple trade-offs involved in plant defence, while simultaneously leading to novel discoveries that can improve the sustainability of crop production.

Project description:We have a fundamental and applied understanding of how differences in the wood chemistry of trees affects the durability of wood products. By comparison, relatively little is known about the ecological causes and consequences of species differences in wood chemistry; even less is known about how or why wood chemistry differs within species, across trees of different sizes. In this study we find strong and consistent differences in wood chemistry of saplings and canopy trees, in several tropical hardwood species. These differences point to the importance of pathogens and tree biomechanics as evolutionary causes of size-dependent changes in wood chemistry. Wood anatomical traits are important correlates of life-history strategies among tree species, yet little is known about wood chemical traits. Additionally, size-dependent changes in wood chemical traits have been rarely examined, although these changes may represent an important aspect of tree ontogeny. Owing to selection for pathogen resistance and biomechanical stability, we predicted that saplings would show higher lignin (L) and wood carbon (Cconv), and lower holocellulose (H) concentrations, compared with conspecific large trees. To test these expectations, we quantified H, L and Cconv in co-occurring Panamanian tree species at the large tree vs. sapling size classes. We also examined inter- and intraspecific patterns using multivariate and phylogenetic analyses. In 15 of 16 species, sapling L concentration was higher than that in conspecific large trees, and in all 16 species, sapling H was lower than that in conspecific large trees. In 16 of 24 species, Cconv was higher in saplings than conspecific large trees. All large-tree traits were unrelated to sapling values and were unrelated to four life-history variables. Wood chemical traits did not show a phylogenetic signal in saplings, instead showing similar values across distantly related taxa; in large trees, only H showed a significant phylogenetic signal. Size-dependent changes in wood chemistry show consistent and predictable patterns, suggesting that ontogenetic changes in wood chemical traits are an important aspect of tree functional biology. Our results are consistent with the hypothesis that at early ontogenetic stages, trees are selected for greater L to defend against cellulose-decaying pathogens, or possibly to confer biomechanical stability.

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Wood allocation trade-offs between fiber wall, fiber lumen, and axial parenchyma drive drought resistance in neotropical trees.

Publications

Wood allocation trade-offs between fiber wall, fiber lumen, and axial parenchyma drive drought resistance in neotropical trees.

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