Results from comparative and ecological wood anatomy combined with a number of experimental studies on plant hydraulics have led to a pervasive and longstanding assumption that wider-diameter... Show moreResults from comparative and ecological wood anatomy combined with a number of experimental studies on plant hydraulics have led to a pervasive and longstanding assumption that wider-diameter vessels are more vulnerable to drought- induced embolism than narrower vessels. Although we agree that wider vessels tend to be more vulnerable than narrower vessels within stems and within roots across most species, our current understanding of the diameter-vulnerability link does not offer a mechanistic explanation for why increased vessel diameter should consistently lead to greater vulnerability or vice versa. Causes of drought-induced embolism formation and spread likely operate at the nano-level, especially at gas-liquid-surfactant interfaces inside intervessel pit membranes. We evaluate here new perspectives on drought-induced embolism and its key anatomical and physico-chemical drivers, of which vessel diameter is one of the parameters involved, although its linkage to embolism vulnerability is likely indirect. As such, the diameter-vulnerability link does not imply that species with on average wider vessels are consistently more susceptible to drought-induced embolism compared to species with narrower vessels. Scientific priorities for future progress should focus on more accurate predictions of how water transport in plants is affected by drought, which requires a better mechanistic understanding of xylem network topology and biophysical processes at the nano-scale level in individual vessels that determine embolism formation and spread. Show less
Thonglim, A.; Bortolami, G.; Delzon, S.; Larter, M.; Offringa, R.; Keurentjes, J.J.B.; ... ; Lens, F. 2022
The synergy between drought-responsive traits across different organs is crucial in the whole-plant mechanism influencing drought resilience. These organ interactions, however, are poorly... Show moreThe synergy between drought-responsive traits across different organs is crucial in the whole-plant mechanism influencing drought resilience. These organ interactions, however, are poorly understood, limiting our understanding of drought response strategies at the whole-plant level. Therefore, we need more integrative studies, especially on herbaceous species that represent many important food crops but remain underexplored in their drought response. We investigated inflorescence stems and rosette leaves of six Arabidopsis thaliana genotypes with contrasting drought tolerance, and combined anatomical observations with hydraulic measurements and gene expression studies to assess differences in drought response. The soc1ful double mutant was the most drought-tolerant genotype based on its synergistic combination of low stomatal conductance, largest stomatal safety margin, more stable leaf water potential during non-watering, reduced transcript levels of drought stress marker genes, and reduced loss of chlorophyll content in leaves, in combination with stems showing the highest embolism resistance, most pronounced lignification, and thickest intervessel pit membranes. In contrast, the most sensitive Cvi ecotype shows the opposite extreme of the same set of traits. The remaining four genotypes show variations in this drought syndrome. Our results reveal that anatomical, ecophysiological, and molecular adaptations across organs are intertwined, and multiple (differentially combined) strategies can be applied to acquire a certain level of drought tolerance. Show less
Hydraulic failure resulting from drought-induced embolism in the xylem of plants is a key determinant of reduced productivity and mortality. Methods to assess this vulnerability are difficult to... Show moreHydraulic failure resulting from drought-induced embolism in the xylem of plants is a key determinant of reduced productivity and mortality. Methods to assess this vulnerability are difficult to achieve at scale, leading to alternative metrics and correlations with more easily measured traits. These efforts have led to the longstanding and pervasive assumed mechanistic link between vessel diameter and vulnerability in angiosperms. However, there are at least two problems with this assumption that requires critical re-evaluation: (1) our current understanding of drought-induced embolism does not provide a mechanistic explanation why increased vessel width should lead to greater vulnerability, and (2) the most recent advancements in nanoscale embolism processes suggest that vessel diameter is not a direct driver. Here, we review data from physiological and comparative wood anatomy studies, highlighting the potential anatomical and physicochemical drivers of embolism formation and spread. We then put forward key knowledge gaps, emphasising what is known, unknown and speculation. A meaningful evaluation of the diameter–vulnerability link will require a better mechanistic understanding of the biophysical processes at the nanoscale level that determine embolism formation and spread, which will in turn lead to more accurate predictions of how water transport in plants is affected by drought. Show less
The evolution of xylem vessels from tracheids is put forward as a key innovation that boosted hydraulic conductivity and photosynthetic capacities in angiosperms. Yet, the role of xylem anatomy and... Show moreThe evolution of xylem vessels from tracheids is put forward as a key innovation that boosted hydraulic conductivity and photosynthetic capacities in angiosperms. Yet, the role of xylem anatomy and interconduit pits in hydraulic performance across vesselless and vessel-bearing angiosperms is incompletely known, and there is a lack of functional comparisons of ultrastructural pits between species with different conduit types. We assessed xylem hydraulic conductivity and vulnerability to drought-induced embolism in 12 rain forest species from New Caledonia, including five vesselless species, and seven vessel-bearing species with scalariform perforation plates. We measured xylem conduit traits, along with ultrastructural features of the interconduit pits, to assess the relationships between conduit traits and hydraulic efficiency and safety. In spite of major differences in conduit diameter, conduit density, and the presence/absence of perforation plates, the species studied showed similar hydraulic conductivity and vulnerability to drought-induced embolism, indicating functional similarity between both types of conduits. Interconduit pit membrane thickness (Tm) was the only measured anatomical feature that showed a relationship to significant vulnerability to embolism. Our results suggest that the incidence of drought in rain forest ecosystems can have similar effects on species bearing water-conducting cells with different morphologies. Show less
Dória, L.C.; Meijs, C.; Podadera, D.S.; Del Arco, M.; Smets, E.; Delzon, S.; Lens, F.P. 2019
• Background and Aims Plant survival under extreme drought events has been associated with xylem vulnerability to embolism (the disruption of water transport due to air bubbles in conduits).... Show more• Background and Aims Plant survival under extreme drought events has been associated with xylem vulnerability to embolism (the disruption of water transport due to air bubbles in conduits). Despite the ecological and economic importance of herbaceous species, studies focusing on hydraulic failure in herbs remain scarce. Here, we assess the vulnerability to embolism and anatomical adaptations in stems of seven herbaceous Brassicaceae species occurring in different vegetation zones of the island of Tenerife, Canary Islands, and merged them with a similar hydraulic–anatomical data set for herbaceous Asteraceae from Tenerife.• Methods Measurements of vulnerability to xylem embolism using the in situ flow centrifuge technique along with light and transmission electron microscope observations were performed in stems of the herbaceous species. We also assessed the link between embolism resistance vs. mean annual precipitation and anatomical stem characters.• Key Results The herbaceous species show a 2-fold variation in stem P50 from –2.1 MPa to –4.9 MPa. Within Hirschfeldia incana and Sisymbrium orientale, there is also a significant stem P50 difference between populations growing in contrasting environments. Variation in stem P50 is mainly explained by mean annual precipitation as well as by the variation in the degree of woodiness (calculated as the proportion of lignified area per total stem area) and to a lesser extent by the thickness of intervessel pit membranes. Moreover, mean annual precipitation explains the total variance in embolism resistance and stem anatomical traits.• Conclusions The degree of woodiness and thickness of intervessel pit membranes are good predictors of embolism resistance in the herbaceous Brassicaceae and Asteraceae species studied. Differences in mean annual precipitation across the sampling sites affect embolism resistance and stem anatomical characters, both being important characters determining survival and distribution of the herbaceous eudicots. Show less
Vascular pathogens cause disease in a large spectrum of perennial plants, with leaf scorch being one of the most conspicuous symptoms. Esca in grapevine (Vitis vinifera) is a vascular disease with... Show moreVascular pathogens cause disease in a large spectrum of perennial plants, with leaf scorch being one of the most conspicuous symptoms. Esca in grapevine (Vitis vinifera) is a vascular disease with huge negative effects on grape yield and the wine industry. One prominent hypothesis suggests that vascular disease leaf scorch is caused by fungal pathogen-derived elicitors and toxins. Another hypothesis suggests that leaf scorch is caused by hydraulic failure due to air embolism, the pathogen itself, and/or plant-derived tyloses and gels. In this study, we transplanted mature, naturally infected esca symptomatic vines from the field into pots, allowing us to explore xylem integrity in leaves (i.e. leaf midveins and petioles) using synchrotron-based in vivo x-ray microcomputed tomography and light microscopy. Our results demonstrated that symptomatic leaves are not associated with air embolism. In contrast, symptomatic leaves presented significantly more nonfunctional vessels resulting from the presence of nongaseous embolisms (i.e. tyloses and gels) than control leaves, but there was no significant correlation with disease severity. Using quantitative PCR, we determined that two vascular pathogen species associated with esca necrosis in the trunk were not found in leaves where occlusions were observed. Together, these results demonstrate that symptom development is associated with the disruption of vessel integrity and suggest that symptoms are elicited at a distance from the trunk where fungal infections occur. These findings open new perspectives on esca symptom expression where the hydraulic failure and elicitor/toxin hypotheses are not necessarily mutually exclusive. Show less
Insular woodiness refers to the evolutionary transition from herbaceousness to- wards derived woodiness on (sub)tropical islands and leads to island floras that have a higher proportion of woody... Show moreInsular woodiness refers to the evolutionary transition from herbaceousness to- wards derived woodiness on (sub)tropical islands and leads to island floras that have a higher proportion of woody species compared to floras of nearby continents.Several hypotheses have tried to explain insular woodiness since Darwin’s original observations, but experimental evidence why plants became woody on islands is scarce at best.Here, we combine experimental measurements of hydraulic failure in stems (as a proxy for drought stress resistance) with stem anatomical observations in the daisy lineage (Asteraceae), including insular woody Argyranthemum species from the Canary Islands and their herbaceous continental relatives.Our results show that stems of insular woody daisies are more resistant to drought- induced hydraulic failure than the stems of their herbaceous counterparts. The ana- tomical character that best predicts variation in embolism resistance is intervessel pit membrane thickness (TPM), which can be functionally linked with air bubble dynamics throughout the 3D vessel network. There is also a strong link between TPM vs. degree of woodiness and thickness of the xylem fibre wall vs. embolism resistance, resulting in an indirect link between lignification and resistance to embolism formation.Thicker intervessel pit membranes in Argyranthemum functionally explain why this insular woody genus is more embolism resistant to drought-induced failure compared to the herbaceous relatives from which it has evolved, but additional data are needed to confirm that palaeoclimatic drought conditions have triggered wood formation in this daisy lineage. Show less
Drought-induced xylem embolism is a key process closely related to plantmortality during extreme drought events. However, this process has beenpoorly investigated in crop species to date, despite... Show moreDrought-induced xylem embolism is a key process closely related to plantmortality during extreme drought events. However, this process has beenpoorly investigated in crop species to date, despite the observed declineof crop productivity under extreme drought conditions. Interspecific variation in hydraulic traits has frequently been reported, but less is knownabout intraspecific variation in crops. We assessed the intraspecific variability of embolism resistance in four sunflower (Helianthus annuus L.) accessions grown in well-watered conditions. Vulnerability to embolism was deter-mined by the in situ flow-centrifuge method (cavitron), and possible trade-offsbetween xylem safety, xylem efficiency and growth were assessed. The relationship between stem anatomy and hydraulic traits was also investigated.Mean P50 was −3 MPa, but significant variation was observed between accessions, with values ranging between −2.67 and −3.22 MPa. Embolism resistance was negatively related to growth and positively related to xylem-specifichydraulic conductivity. There is, therefore, a trade-off between hydraulic safetyand growth but not between hydraulic safety and efficiency. Finally, we foundthat a few anatomical traits, such as vessel density and the area of the vessellumen relative to that of the secondary xylem, were related to embolism resistance, whereas stem tissue lignification was not. Further investigations are nowrequired to investigate the link between the observed variability of embolismresistance and yield, to facilitate the identification of breeding strategies toimprove yields in an increasingly arid world. Show less
Cailleret, M.; Jansen, S.; Robert, E.M.R.; Desoto, L.; Aakala, T.; Antos, J.A.; ... ; Martinez-Vilalta, J. 2017
Tree mortality is a key factor influencing forest functions and dynamics, but our understanding of the mechanisms leading to mortality and the associated changes in tree growth rates are still... Show moreTree mortality is a key factor influencing forest functions and dynamics, but our understanding of the mechanisms leading to mortality and the associated changes in tree growth rates are still limited. We compiled a new pan-conti- nental tree-ring width database from sites where both dead and living trees were sampled (2970 dead and 4224 living trees from 190 sites, including 36 species), and compared early and recent growth rates between trees that died and those that survived a given mortality event. We observed a decrease in radial growth before death in ca. 84% of the mortality events. The extent and duration of these reductions were highly variable (1–100 years in 96% of events) due to the complex interactions among study species and the source(s) of mortality. Strong and long-lasting declines were found for gymnosperms, shade- and drought-tolerant species, and trees that died from competition. Angiosperms and trees that died due to biotic attacks (especially bark-beetles) typically showed relatively small and short-term growth reductions. Our analysis did not highlight any universal trade-off between early growth and tree longevity within a species, although this result may also reflect high variability in sampling design among sites. The intersite and interspecific variability in growth patterns before mortality provides valuable information on the nature of the mortality process, which is consistent with our understanding of the physiological mechanisms leading to mortality. Abrupt changes in growth immediately before death can be associated with generalized hydraulic failure and/or bark-beetle attack, while long-term decrease in growth may be associated with a gradual decline in hydraulic performance coupled with depletion in carbon reserves. Our results imply that growth-based mortality algorithms may be a powerful tool for predicting gymnosperm mortality induced by chronic stress, but not necessarily so for angiosperms and in case of intense drought or bark-beetle outbreaks. Show less
Increases in drought-induced tree mortality are being observedin tropical rain forests worldwide and are also likely to affectthe geographical distribution of tropical vegetation. However,the... Show moreIncreases in drought-induced tree mortality are being observedin tropical rain forests worldwide and are also likely to affectthe geographical distribution of tropical vegetation. However,the mechanisms underlying the drought vulnerability and environmental distribution of tropical species have been little studied. We measured vulnerability to xylem embolism (P50) of 13woody species endemic to New Caledonia and with differentxylem conduit morphologies. We examined the relation be-tween P50, along with other leaf and xylem functional traits,and a range of habitat variables. Selected species had P50values ranging between 4.03 and 2.00 MPa with most species falling in a narrow range of resistance to embolism above 2.7 MPa. Embolism vulnerability was significantly correlatedwith elevation, mean annual temperature and percentage ofspecies occurrences located in rain forest habitats. Xylem conduit type did not explain variation in P50. Commonly used functional traits such as wood density and leaf traits were notrelated to embolism vulnerability. Xylem embolism vulnerability stands out among other commonly used functional traits as amajor driver of species environmental distribution. Drought-induced xylem embolism vulnerability behaves as a physiological trait closely associated with the habitat occupation of rainforest woody species. Show less
Lens, F.P.; Vos, R.A.; Charrier, G.; Niet, T. van der; Merckx, V.; Baas, P.; ... ; Janssens, S.B. 2016
Background and Aims Angiosperms with simple vessel perforations have evolved many times independently of species having scalariform perforations, but detailed studies to understand why these... Show moreBackground and Aims Angiosperms with simple vessel perforations have evolved many times independently of species having scalariform perforations, but detailed studies to understand why these transitions in wood evolution have happened are lacking. We focus on the striking difference in wood anatomy between two closely related genera of Adoxaceae, Viburnum and Sambucus, and link the anatomical divergence with climatic and physiological insights. Methods After performing wood anatomical observations, we used a molecular phylogenetic framework to estimate divergence times for 127 Adoxaceae species. The conditions under which the genera diversified were estimated using ancestral area reconstruction and optimization of ancestral climates, and xylem-specific conductivity measurements were performed. Key Results Viburnum, characterized by scalariform vessel perforations (ancestral), diversified earlier than Sambucus, having simple perforations (derived). Ancestral climate reconstruction analyses point to cold temperate preference for Viburnum and warm temperate for Sambucus. This is reflected in the xylem-specific conductivity rates of the co-occurring species investigated, showing that Viburnum lantana has rates much lower than Sambucus nigra. Conclusions The lack of selective pressure for high conductive efficiency during early diversification of Viburnum and the potentially adaptive value of scalariform perforations in frost-prone cold temperate climates have led to retention of the ancestral vessel perforation type, while higher temperatures during early diversification of Sambucus have triggered the evolution of simple vessel perforations, allowing more efficient long-distance water transport. Show less
The water transport pipeline in herbs is assumed to be more vulnerable to drought than in trees due to the formation of frequent embolisms (gas bubbles), which could be removed by the... Show moreThe water transport pipeline in herbs is assumed to be more vulnerable to drought than in trees due to the formation of frequent embolisms (gas bubbles), which could be removed by the occurrence of root pressure, especially in grasses. Here, we studied hydraulic failure in herbaceous angiosperms by measuring the pressure inducing 50% loss of hydraulic conductance (P50) in stems of 26 species, mainly European grasses (Poaceae). Our measurements show a large range in P50 from 20.5 to 27.5 MPa, which overlaps with 94% of the woody angiosperm species in a worldwide, published data set and which strongly correlates with an aridity index. Moreover, the P50 values obtained were substantially more negative than the midday water potentials for five grass species monitored throughout the entire growing season, suggesting that embolism formation and repair are not routine and mainly occur under water deficits. These results show that both herbs and trees share the ability to withstand very negative water potentials without considerable embolism formation in their xylem conduits during drought stress. In addition, structure-function trade-offs in grass stems reveal that more resistant species are more lignified, which was confirmed for herbaceous and closely related woody species of the daisy group (Asteraceae). Our findings could imply that herbs with more lignified stems will become more abundant in future grasslands under more frequent and severe droughts, potentially resulting in lower forage digestibility. Show less
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 betweenxylem... Show moreThe 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 betweenxylem conduits, thus impeding sap transport to the leaves. A well-known hypothesis proposesthat the safety of xylem (its ability to resist embolism formation and spread) should trade offagainst xylem efficiency (its capacity to transport water). We tested this safety–efficiency hypothesis in branch xylem across 335 angiosperm and 89gymnosperm species. Safety was considered at three levels: the xylem water potentials where12%, 50% and 88% of maximal conductivity are lost. Although correlations between safety and efficiency were weak (r2 < 0.086), no species hadhigh 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 safetywere weakly associated (r2 < 0.02 in most cases) with higher wood density, lower leaf- to sap-wood-area and shorter stature. There appears to be no persuasive explanation for the considerable number of species withboth low efficiency and low safety. These species represent a real challenge for understandingthe evolution of xylem. Show less
The water transport pipeline in herbs is assumed to be more vulnerable to drought than in trees due to the formation of frequent embolisms (gas bubbles), which could be removed by the occurrence of... Show moreThe water transport pipeline in herbs is assumed to be more vulnerable to drought than in trees due to the formation of frequent embolisms (gas bubbles), which could be removed by the occurrence of root pressure, especially in grasses. Here, we studied hydraulic failure in herbaceous angiosperms by measuring the pressure inducing 50% loss of hydraulic conductance (P50)in stems of 26 species, mainly European grasses (Poaceae). Our measurements show a large range in P50 from 20.5 to 27.5 MPa, which overlaps with 94% of the woody angiosperm species in a worldwide, published data set and which strongly correlates with an aridity index. Moreover, the P50 values obtained were substantially more negative than the midday water potentials for five grass species monitored throughout the entire growing season, suggesting that embolism formation and repair are not routine and mainly occur under water deficits. These results show that both herbs and trees share the ability to withstand very negative water potentials without considerable embolism formation in their xylem conduits during drought stress. In addition, structure-function trade-offs in grass stems reveal that more resistant species are more lignified, which was confirmed for herbaceous and closely related woody species of the daisy group (Asteraceae). Our findings could imply that herbs with more lignified stems will become more abundant in future grasslands under more frequent and severe droughts, potentially resulting in lower forage digestibility. Show less
Lens, F.P.; Vos, R.A.; Charrier, G.; Niet, T. van der; Merckx, V.S.F.T.; Baas, P.; ... ; Janssens, S.B. 2016
Angiosperms with simple vessel perforations have evolved many times independently of species having scalariform perforations, but detailed studies to understand why these transitions in wood... Show moreAngiosperms with simple vessel perforations have evolved many times independently of species having scalariform perforations, but detailed studies to understand why these transitions in wood evolution have happened are lacking. We focus on the striking difference in wood anatomy between two closely related genera of Adoxaceae, Viburnum and Sambucus, and link the anatomical divergence with climatic and physiological insights. After performing wood anatomical observations, we used a molecular phylogenetic framework to estimate divergence times for 127 Adoxaceae species. The conditions under which the genera diversified were estimated using ancestral area reconstruction and optimization of ancestral climates, and xylem-specific conductivity measurements were performed. Viburnum, characterized by scalariform vessel perforations (ancestral), diversified earlier than Sambucus, having simple perforations (derived). Ancestral climate reconstruction analyses point to cold temperate preference for Viburnum and warm temperate for Sambucus. This is reflected in the xylem-specific conductivity rates of the co-occurring species investigated, showing that Viburnum lantana has rates much lower than Sambucus nigra. The lack of selective pressure for high conductive efficiency during early diversification of Viburnum and the potentially adaptive value of scalariform perforations in frost-prone cold temperate climates have led to retention of the ancestral vessel perforation type, while higher temperatures during early diversification of Sambucus have triggered the evolution of simple vessel perforations, allowing more efficient long-distance water transport. Show less
