Increasing axial parenchyma fraction in the Malagasy Magnoliids facilitated the co‐optimisation of hydraulic efficiency and safety

Aritsara, Amy Ny Aina; Razakandraibe, Vonjisoa M; Ramananantoandro, Tahiana; Gleason, Sean M.; Cao, Kaihua

doi:10.1111/nph.16969

Cited by 20 publications

(19 citation statements)

References 107 publications

(175 reference statements)

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“…The amount of NSCs was also greater in angiosperms than in gymnosperms, which translated into different associations between NSCs and RAP. In conifers, the proportion of axial parenchyma that constitutes secondary xylem is usually much lower than that of angiosperms (Spicer, 2014;Aritsara et al, 2020), although we found no significant differences. This configuration may emphasize the role of axial parenchyma in maintaining water transport in the angiosperm vessels (Spicer, 2014).…”

Section: Relationships Between Nscs and Rap Fractionscontrasting

confidence: 73%

“…It has been suggested that axial parenchyma can influence hydraulic capacitance in angiosperms by releasing water into vessels in periods of drought (Morris et al, 2018). Additionally, vessel to axial parenchyma connectivity would facilitate xylem hydraulic optimization, suggesting that plants may need axial parenchyma to surround and service vessels (Aritsara et al, 2020; Ziemińska et al, 2020). Therefore, the physiological function of both types of parenchyma could be very different, calling for a careful consideration of xylem structure for a better understanding of tree ecological strategies.…”

Section: Discussionmentioning

confidence: 99%

“…For example, the tensile strength of individual xylem rays was found to be three times higher than the radial strength of all xylem cells in Fagus sylvatica (Burgert and Eckstein, 2001), suggesting the importance of RP for tree mechanical integrity (Zheng and Martinez‐Cabrera, 2013). Although total RAP proportion was not correlated with hydraulic properties (Jacobsen et al, 2007; Pratt et al, 2007; Poorter et al, 2010; Fortunel et al, 2014), the amount of AP was positively correlated with hydraulic capacitance in tropical species that had higher AP fractions around wide vessels (Morris et al, 2018; Aritsara et al, 2020).…”

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confidence: 99%

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

Zhang

Mao

Fortunel

et al. 2022

American J of Botany

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Premise: Nonstructural carbohydrates (NSCs) play a key role in tree performance and functioning and are stored in radial and axial parenchyma (RAP) cells. Whether this relationship is altered among species and climates or is linked to functional traits describing xylem structure (wood density) and tree stature is not known. Methods: In a systematic review, we collated data for NSC content and the proportion of RAP in stems for 68 tree species. To examine the relationships of NSCs and RAP with climatic factors and other functional traits, we also collected climatic data at each tree's location, as well as wood density and maximum height. A phylogenetic tree was constructed to examine the influence of species' evolutionary relationships on the associations among NSCs, RAP, and functional traits.Results: Across all 68 tree species, NSCs were positively correlated with RAP and mean annual temperature, but relationships were only weakly significant in temperate species and angiosperms. When separating RAP into radial parenchyma (RP) and axial parenchyma (AP), both NSCs and wood density were positively correlated with RP but not with AP. Wood in taller trees was less dense and had lower RAP than in shorter trees, but height was not related to NSCs. Conclusions: In trees, NSCs are stored mostly in the RP fraction, which has a larger surface area in warmer climates. Additionally, NSCs were only weakly linked to wood density and tree height. Our analysis of evolutionary relationships demonstrated that RAP fractions and NSC content were always closely related across all 68 tree species, suggesting that RAP can act as a reliable proxy for potential NSC storage capacity in tree stems.

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Section: Relationships Between Nscs and Rap Fractionscontrasting

confidence: 73%

Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

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

Zhang

Mao

Fortunel

et al. 2022

American J of Botany

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“…Thus, the recovery of hydraulic conductivity is less dependent on stored carbon. This opposing strategy may also be related to the different functions performed by RAP in roots and stems (Zheng & Martínez‐Cabrera, 2013; Secchi et al ., 2017; Aritsara et al ., 2021). In agreement with Morris et al .…”

Section: Discussionmentioning

confidence: 99%

Functional trade‐offs are driven by coordinated changes among cell types in the wood of angiosperm trees from different climates

et al. 2023

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Summary Wood performs several functions to ensure tree survival and carbon allocation to a finite stem volume leads to trade‐offs among cell types. It is not known to what extent these trade‐offs modify functional trade‐offs and if they are consistent across climates and evolutionary lineages. Twelve wood traits were measured in stems and coarse roots across 60 adult angiosperm tree species from temperate, Mediterranean and tropical climates. Regardless of climate, clear trade‐offs occurred among cellular fractions, but did not translate into specific functional trade‐offs. Wood density was negatively related to hydraulic conductivity (Kth) in stems and roots, but was not linked to nonstructural carbohydrates (NSC), implying a functional trade‐off between mechanical integrity and transport but not with storage. NSC storage capacity was positively associated with Kth in stems and negatively in roots, reflecting a potential role for NSC in the maintenance of hydraulic integrity in stems but not in roots. Results of phylogenetic analyses suggest that evolutionary histories cannot explain covariations among traits. Trade‐offs occur among cellular fractions, without necessarily modifying trade‐offs in function. However, functional trade‐offs are driven by coordinated changes among xylem cell types depending on the dominant role of each cell type in stems and roots.

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“…This is consistent with our current observations that as the available water increases, plants choose to widen the diameter of vessels or tracheids downstream (i.e., in branches) of the water transport pathway, therefore, matches the usually wider conduits upstream (i.e., in roots) of the pathway, to enable their branches to get stronger competitiveness for light and carbon uptake (Pfautsch et al ., 2016). The safety versus efficiency trade-off theory in the xylem claimed that when the tension to pull sufficient water and transport through the stem exceeds the physical limits, the risk of cavitations in the xylem of branches will inevitably increase (Tyree & Zimmermann, 2002;Aritsara et al ., 2021;. This will gradually reduce the gap with the cavitation vulnerability in roots, resulting in the decrease ofP 50 root -branch along environmental aridity gradients.…”

Section: Ai Drives Hydraulic Vulnerability Segmentation By Affecting ...mentioning

confidence: 99%

Hydraulic vulnerability segmentation between branches and roots increases with environmental aridity

Tang

Liu

et al. 2022

Preprint

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The hydraulic vulnerability segmentation hypothesis proposes that plant branches are more resistant to cavitation than roots, namely, the difference in vulnerability to cavitation between branches and roots is positive ( P > 0). However, it is not clear how this phenomenon can vary along environmental aridity gradients. We compiled the above hypothesis with 105 woody species from four biomes with increasing aridity, by compiling functional traits related to hydraulic properties and anatomical structures of branches and roots. We investigated the relationships between P and several environmental factors that are associated with aridity. We found a positive P across species, which supported the hydraulic vulnerability segmentation hypothesis, and P increased significantly with environmental aridity. Branch xylem hydraulic conductivity changed from “more efficient” (e.g., wider conduit, higher hydraulic conductivity) to “safer” (e.g., narrower conduit, more negative P) in response to increased aridity, while root xylem hydraulic conductivity remained unchanged across aridity gradients. Our results demonstrated that hydraulic vulnerability segmentation is more pronounced for species from arid regions. Changes in branch traits may be responsible for hydraulic vulnerability segmentation between branches and roots.

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Increasing axial parenchyma fraction in the Malagasy Magnoliids facilitated the co‐optimisation of hydraulic efficiency and safety

Cited by 20 publications

References 107 publications

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

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

Functional trade‐offs are driven by coordinated changes among cell types in the wood of angiosperm trees from different climates

Hydraulic vulnerability segmentation between branches and roots increases with environmental aridity

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