Gas diffusion kinetics drive embolism spread in angiosperm xylem: evidence from flow-centrifuge experiments and modelling

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: April 19, 2023

Abstract Understanding xylem embolism formation is challenging due to dynamic changes and multiphase interactions in conduits. If spread involves gas movement xylem, we hypothesise that it affected by time. We measured hydraulic conductivity (K h ) flow-centrifuge experiments over one hour at a given pressure temperature for stem samples of three angiosperm species. Temporal K 5, 22, 35°C, various pressures were compared modelled recently embolised vessel the centre centrifuge sample. 22°C showed maximum relative increases between 6% 40%, decreases 41% 61% low high centrifugal speed, respectively. Logarithmic species-specific, most pronounced during first 15 minutes. Embolism started near edges gradually increased centre. Moreover, strongly correlated with concentration vessel. Although mostly pressure-driven, our experimental data indicate time, conduit characteristics, are involved their role diffusion. Gas diffusion, however, does not cover entire process spread.

Language: Английский

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Xylem sap residue in cut-open conduits can affect gas discharge in pneumatic experiments

bioRxiv (Cold Spring Harbor Laboratory), Journal Year: 2023, Volume and Issue: unknown

Published: Aug. 9, 2023

Summary Considerable progress has been made in understanding the mechanisms of embolism formation based on pneumatic method, which relies gas discharge measurements. Here, we test assumption that cut-open conduits are gas-filled when samples cut at high water potentials. We performed vulnerability curves (VC) with Pneumatron and analysed sap extraction from vessels Citrus branches, while optical method was applied as a reference method. VCs 11 additional angiosperms were to generalise our findings. found an increase during early stages dehydration, affected VC . Xylem not absorbed immediately by surrounding tissue branches. The amount discharged increased until all residue absorbed, near turgor loss point. By analysing slope VCs, could correct VC, evidenced strong agreement resistance between Since residual some species slightly reduce species, propose apply easy correction for this novel artefact. Automated measurements also required because its time resolution.

Language: Английский

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Further Test of Pneumatic Method in Constructing Vulnerability Curves Using Six Tree Species with Contrasting Xylem Anatomy

Forests, Journal Year: 2023, Volume and Issue: 14(2), P. 293 - 293

Published: Feb. 2, 2023

The pneumatic method is a novel determining vulnerability to embolism in plants, yet it remains unclear whether this suitable for all species with different xylem anatomy. In study, using six tree contrasting anatomy, including four vessel-bearing (diffuse-porous wood and ring-porous wood) two tracheid-bearing (non-porous wood), we test the reliability of by comparing hydraulic methods also considering turgor loss point native embolism. Vessel length distribution cut-open vessel volume were evaluated silicone injection technique. Additionally, synthesized published data find out consistency between methods. Results showed that there was maximum 10-folds difference mean diameter varying from 30 56 μm among species. estimated open ranges 0.064 0.397 mL, 14% tube vacuum reservoir. For species, good methods, evidenced significantly overestimated because bad consistencies plant water relations. Data synthesis suggested can accurately measure but not Our study provided further evidence accurate most thus has potential be widely used hydraulics field. However, proposed precise calculation air discharge should take into account vessels wide long vessels.

Language: Английский

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Remaining uncertainties in the Pneumatic method

New Phytologist, Journal Year: 2022, Volume and Issue: 237(2), P. 384 - 391

Published: Dec. 20, 2022

The integrity of the plant water transport system is crucial for performance and survival (Rowland et al., 2015). To estimate vulnerability to drought-induced embolism (blockage flow in conduits by air bubbles), a number methods have been developed generate curves (VCs), that is, relationship between xylem level potential (Cochard 2013). However, since report 'cutting-under-tension' artifact (Wheeler 2013), all published VCs may need be re-examined, researchers carefully avoid artifacts 2013; Zhang & Holbrook, 2014). As newly method, Pneumatic method (the manual or automated Pneumatron) measures volume discharged from terminal shoots (Pereira 2016, 2020). This assumes increase during desiccation mainly extracted embolized conduits, it believed non-hydraulic, economical, less time-consuming method. also generates P50 (water causing 50% embolism) values comparable other some studies 2016; Bittencourt 2018; Pereira 2020; Paligi 2021; see summary Brum 2023). All current both advantages limitations (Skelton Diaz, 2020), so does We pointed out uncertainties our early study (Chen 2021) could improved solving these uncertainties. In an article this issue New Phytologist, al. (2023; pp. 374–383), provided explanations on issues we raised before, but think fundamental remain not well addressed. main criticism reply Letter (2023) earlier incorrectly performed experiment, stopped measurement too early, which resulted underestimated ADmax (maximum discharged) resistance. Here, claim presented 'stop early' late' previous paper, clearly stopping time would affect estimation VCs, termed as 'two-plateau' concern (see fig. 6 Chen 2021, define 'plateau' stage maintains stable value relatively long duration; diagram Fig. 1 here). Our using plateau overestimate vulnerability, whereas 2 underestimate due source 2. Furthermore, believe (AD) at only represents maximum dischargeable vessels, includes sources, example, tissue shrinkage, cracks pith discussion). Therefore, measured ADmax, rather separated into two stages, uncertainties, mechanistic explanations. misinterpreted 'incorrect implementation underestimation ADmax' they did address directly. Additionally, new data obtained Pneumatron (constructed following Trabi Supporting Information Methods S1) agree with generated pneumatic device (Fig. S1), supporting concerns showing there were no technological biases study. A diagrammatic representation sources stem spread embolisms use under conditions well-hydrated (a), moderate dehydration (b), severe (c), full (d) stages. green color indicates functioning vessels red distal end stem, are isolated vessels. white orange colors indicate cut-open intact neighboring basal end, respectively. Arrows direction extraction. insets show status pits connecting adjacent refers information S9 (2021) S4 (2016). right column (refers shows kinetics (ΔVi, μl) (e) one representative sample Lasiococca comberi method; percentage against different segments (f); comparison plateaus (blue) (red) (g), respectively, L. comberi. See detailed descriptions (2021). pattern was first reported 2021). Interestingly, now found multi-plateaus (> 2) when lasts enough (c. > 8 d; Figs 2, S2–S6). paper (fig. showed AD desiccation, increased reached certain (plateau 1), then again another 2). Similarly, 'two- multi-plateau' can studies, including who (2020) reproduced S7–S9). Notably, combining replicates figure 1g, S7), easily masked great variation among samples small compared completely dehydrated late stage. questioned reliability measurements used extremely low estimated potential. While predicted negative potentials might reliable directly values, change 'multi-plateau' (also S1). patterns suggest should ignored addressed carefully. hypothesized explained isolation cut part branch, visually illustration here 1). gas dynamics model Jansen Yang (2022), apparatus discharges while water-filled excluded. Thus, initial close because cavitated apparatus. section 1b), more prone their proximity discussion about open vessel later). Then, starts connects 1e), reaches second (or third) most embolize 1d). Importantly, include likely stage, calculated (PAD) undoubtedly underestimates Although lower reasonable if Uncertainties section). essential determination definite, quantitative, easy-to-follow criterion has established even now. degree leaves important indicator experiment For (2016) initially described 'when Ψx than limit pressure chamber (−10 MPa) branches had lost leaves'. study, followed 'leaves severely desiccated, crispy, started shed' 'the increasing decrease' 2021), occurred −2 −7 MPa let continue dehydrate d), occurrence third many (Figs (2018) defined last point branch where fully embolized'. maintain within 24 h' 'measurements dehydrated'. Generally, hard follow. First, rare took time, example d S2–S6), generally −10 3 These durations reaching final Second, second) short varies species probably associated anatomy needs further case covers wide range (e.g. longer study; Table S1 interpreted chambers measure accurately (range −4 commercial equipment). uncertainty easy happen follow protocol (2016), qualitatively 'ADmax, its (lowest Ψx)'. brought methodology. By recent standard (Trabi 2023), stop doing maintained stable. 1e) being exclude possibility difficulties measuring potentials, especially highly resistant those drying slowly. words, reach plateau. Third, technique quantify whole vivo, arbitrarily decide timing measurement. Obviously, unknown whether 100% criteria, suggesting insufficient thus well. very occur plants enough. tested visualization micro-CT) check before total cumulative saturation reductions potential' 'reach device'. after period 2), typically several days much At already declined below MPa, obvious shrinkage appearance. rules. An S7). Based model, paradoxical suggestion twice P50'. Because users methods, impractical suggestion. On contrary, given construct claimed woody cracks, leaky tissue, occur, connected conduits. concluded common problems tree species. disagree micro-CT images connect Meanwhile, cautious dry necessarily equal amount evidence non-vessel cause value. connections 3; Video challenging assumption 'if do area influence extraction'. Combretum griffithii, liana big area, 24-h dehydration, three 48 h S10). supported 10 20 studied (Table S2) xylems piths entire over 60 −5.51 −9.41 MPa; 3, S11; large abundant parenchyma tissues. contaminate treated argued detected 7 sections micro-CT. m) After underwater, tubing scanning. segment wrapped parafilm reduce scanning reason expect artificial preparation apparatus, place exposed quickly. Further experimental support parts contributed discharge that, stems (by quick air-injection) 28–33% It suggested fast glue block (Zhang 2018) leaking pith, treatment leakage positions still tested. declines strongly shrinkage. 'stable cases, sometimes, decrease S2–S6, S7, 6a suggests affected factors, such areas shrunk 4.5–14.0%, 2.9–12.1%, lumen varied S12). contribution vary across extent VC parameters remains unclear. solved avoided simply paying 'careful attention practices' (2023). cut-open-vessel effect like 'Unlike sampling hydraulic measurements, material filled purpose'; additional tests needed 'r-shaped' high cases −1 S2–S6 When performing measurement, contact outside clear seeding embolism. pre-existing embolism, vessels) (Brodersen Guan If true, result overestimation least four Citrus sinensis vulnerable S8) Other treatment, same numerous minimize far away (Torres-Ruiz contrast, extract adjunct (Jansen 2022). Also, calculation PAD level. diffusion speed through pit membranes orders magnitude bulk flow, relative importance farther depends anatomy, membrane thickness, connectivity, on. traits differ considerably introduce species-specific direction. quantifies 2022), theory, correct curve initiates spreads toward end. Otherwise, excluding events heterogeneity along stages (See S2), consistently S13). synthesis derived traditional reference general agreements (but diverged : line caution paid apply large-scale Sergent correlation solve mentioned earlier, misleading terms eco-physiological performance. behaved cavitation initiation (less negative) (in −0.5 e.g. figs 1, give us frequent recovery diurnal basis. confirmed 'non-s-shaped' enough, regarding how perform natural world. possible unlikely initiated MPa. validate re-verified noticed validating often mixed, collected literature comparing 2018). revealed individual (Shen recommend careful approach controversies methodology settled, intraspecific variation, single avoided. discharging overestimates lack pathway opposite effect. vulnerability. effects merged, methods. analogous content, correlated process spreading desiccation. Simply content easier, plotting produce 's-shaped' similar S4), decline (Hao 4 correlation, ongoing structural physiological processes related process. getting helpful, shape underlying mechanisms matter. conclusion, potentially efficient time-saving remain. Before widely massive dataset, discussed pattern, verified. Surely, novel advance scientific knowledge, perfect solid data. We, therefore, test correlations, generating up Some done track ends discharge. insights pointing evidence-based promote improvement advancement understanding central topic physiology ecology. Rather invalidating wish help improve authors thank Peng-Yun Yan, Lu Han, Lian-Bin Tao, Weng-Zhuang assistance Si-Qi Li, Yu-Hang He, En-Guo Rong, Zhuang-Sheng Xiao, Lin designing constructing devices. work funded National Natural Science Foundation China (32071735, 41861144016, 31570406, 31861133008), 'Light West China' Program Southeast Asia Biodiversity Research Institute, Chinese Academy Sciences (151C53KYSB20200019), Yunnan Provincial Technology Department (2018HB068), Revitalization Talents Support Plan (YNWR-QNBJ-2019177). PM acknowledges financial CAS-TWAS President's Fellowship International Doctoral Students. Y-JZ Open Fund CAS Key Laboratory Tropical Forest Ecology. Y-JC, conceived designed Y-JC experiments. analyzed wrote revised manuscript input J-LZ. equally work. Comparison device. S2 dynamic changes (PAD, %) Microcos paniculate S3 Lagerstroemia tomentosa S5 griffithii S6 yunnanense S7 Reproduction 5 (2020), 'two Plateaus', non-stable S8 Plateaus' sinensis. (2021), Plateaus'. S10 (side cross-section directions) S11 tropical c. laboratory potentials. S12 S13 determine branch. five determining Tissue monitoring. Vulnerability measurements. air-discharging Species observation crack dehydration. Movie three-dimensional Please note: Wiley responsible functionality any supplied authors. Any queries (other missing material) directed Phytologist Central Office. publisher content) corresponding author article.

Language: Английский

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Assessing vulnerability to embolism and hydraulic safety margins in reed‐like Restionaceae

Plant Biology, Journal Year: 2024, Volume and Issue: 26(4), P. 633 - 646

Published: April 8, 2024

Abstract The African Restionaceae (Poales), the dominant graminoid layer in megadiverse Cape Floristic Region of South Africa, are distributed across a wide range moisture availability, yet currently there is very little known about underlying hydraulics this group. We tested two methods for measuring culm vulnerability to embolism, optical and pneumatic methods, three species Cannomois ranging habitat from semi‐riparian ( virgata ) dryland parviflora C. congesta ). Estimates xylem were coupled with measures turgor loss point (Ψ TLP minimum field water potential MD assess hydraulic safety margins. produced similar estimates P 50 , but differed 12 88 . All quite vulnerable –1.9 MPa ), −2.3 −2.4 Ψ aligned stress, highest values found Consistent differences between resulted consistent margins 0.96 ± 0.1 onset embolism occurring 0.43 0.04 after all species. Our study demonstrates that restio occupancy dry environments involves more than evolution highly resistant xylem, suggesting other aspects relations key understanding trait–environment relationships

Language: Английский

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Lianas in tropical dry seasonal forests have a high hydraulic efficiency but not always a higher embolism resistance than lianas in rainforests

Annals of Botany, Journal Year: 2024, Volume and Issue: 134(2), P. 337 - 350

Published: May 9, 2024

Abstract Background and Aims Lianas have higher relative abundance biomass in drier seasonal forests than rainforests, but whether this difference is associated with their hydraulic strategies unclear. Here, we investigate lianas of seasonally dry are safer more efficient water transport rainforest lianas, explaining patterns liana abundance. Methods We measured traits on five pairs congeneric the tribe Bignonieae two contrasting forest sites: wet ‘Dense Ombrophilous Forest’ Central Amazonia (~2 months) ‘Semideciduous Seasonal inland Atlantic Forest (~6 months). also gathered a broader database, including 197 trees 58 species from different tropical forests, to compare safety between habits types. Key Results both had high similar efficiency exhibited variability resistance embolism across types when phylogenetic relationships were taken into account. Three genera rainforest, positive margins despite lower predawn potential values lianas. did not find safety–efficiency trade-off. Merging our results previously published data revealed independent Conclusions The detected here probably favours rapid growth differences highlight that some highly vulnerable may rely other mechanisms cope drought. Future research lethal dehydration threshold connection could offer further insights dynamics under climatic threats.

Language: Английский

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Xylem sap residue in cut-open conduits can affect gas discharge in pneumatic experiments

Tree Physiology, Journal Year: 2024, Volume and Issue: unknown

Published: July 24, 2024

Abstract Considerable attention has been paid to addressing methodological concerns related measurements of embolism in conduits angiosperm xylem. A fast, easy and cheap method is based on gas extraction from dehydrating samples obtain pneumatic vulnerability curves (VCs). Here, we tested the assumption that cutting open leads gas-filled lumina when these are cut air at fairly high water potentials, which required detect intact conduits. We performed VCs with Pneumatron for 12 species extracted sap cut-open vessels branches nine under early stages branch dehydration. The optical was applied Citrus plants as an alternative reference estimate resistance. found increase discharge during dehydration, affected most studied. Xylem residue not absorbed immediately by surrounding tissue six but gradually disappeared over time progressive amount discharged increased until all residual absorbed, embolism. conclude xylem affects represents a novel artifact can easily be corrected for. Yet, it remains unclear why exactly air–water meniscus did fully withdraw conduit end wall species. By analyzing slope time, could improve estimations resistance, evidenced strong agreement between methods. Since some slightly underestimate propose apply correction this time-resolution taken Pneumatron.

Language: Английский

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Scales and scaling in Tree Physiology

Tree Physiology, Journal Year: 2024, Volume and Issue: 44(8)

Published: Aug. 1, 2024

Journal Article Accepted manuscript Scales and scaling in Tree Physiology Get access Maurizio Mencuccini CREAF, 08193, Bellaterra, Barcelona, SpainICREA, 08010, Spain Corresponding author: [email protected] https://orcid.org/0000-0003-0840-1477 Search for other works by this author on: Oxford Academic PubMed Google Scholar Physiology, tpae100, https://doi.org/10.1093/treephys/tpae100 Published: 13 August 2024 history Received: 03 Accepted: 09

Language: Английский

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