Acid waters in tank bromeliads: Causes and potential consequences.

PREMISE: The consequences of acidity for plant performance are profound, yet the prevalence and causes of low pH in bromeliad tank water are unknown despite its functional relevance to key members of many neotropical plant communities. METHODS: We investigated tank water pH for eight bromeliad species in the field and for the widely occurring Guzmania monostachia in varying light. We compared pH changes over time between plant and artificial tanks containing a solution combined from several plants. Aquaporin transcripts were measured for field plants at two levels of pH. We investigated relationships between pH, leaf hydraulic conductance, and CO2 concentration in greenhouse plants and tested proton pump activity using a stimulator and inhibitor. RESULTS: Mean tank water pH for the eight species was 4.7 ± 0.06 and was lower for G. monostachia in higher light. The pH of the solution in artificial tanks, unlike in plants, did not decrease over time. Aquaporin transcription was higher for plants with lower pH, but leaf hydraulic conductance did not differ, suggesting that the pH did not influence water uptake. Tank pH and CO2 concentration were inversely related. Fusicoccin enhanced a decrease in tank pH, whereas orthovanadate did not. CONCLUSIONS: Guzmania monostachia acidified its tank water via leaf proton pumps, which appeared responsive to light. Low pH increased aquaporin transcripts but did not influence leaf hydraulic conductance, hence may be more relevant to nutrient uptake.

Hydraulic conductance, resistance, and resilience: how leaves of a tropical epiphyte respond to drought.

PREMISE: Because of its broad range in the neotropical rainforest and within tree canopies, the tank bromeliad Guzmania monostachia was investigated as a model of how varying leaf hydraulic conductance (Kleaf ) could help plants resist and recover from episodic drought. The two pathways of Kleaf , inside and outside the xylem, were also examined to determine the sites and causes of major hydraulic resistances within the leaf. METHODS: We measured leaf hydraulic conductance for plants in the field and laboratory under wet, dry, and rewetted conditions and applied physiological, anatomical, and gene expression analysis with modeling to investigate changes in Kleaf . RESULTS: After 7 d with no rain in the field or 14 days with no water in the glasshouse, Kleaf decreased by 50% yet increased to hydrated values within 4 d of tank refilling. Staining to detect embolism combined with modeling indicated that changes outside the xylem were of greater importance to Kleaf than were changes inside the xylem and were associated with changes in intercellular air spaces (aerenchyma), aquaporin expression and inhibition, and cuticular conductance. CONCLUSIONS: Low values for all conductances during drying, particularly in pathways outside the xylem, lead to hydraulic resilience for this species and may also contribute to its broad environmental tolerances.

Connecting active to passive fluorescence with photosynthesis: a method for evaluating remote sensing measurements of Chl fluorescence.

Recent advances in the retrieval of Chl fluorescence from space using passive methods (solar-induced Chl fluorescence, SIF) promise improved mapping of plant photosynthesis globally. However, unresolved issues related to the spatial, spectral, and temporal dynamics of vegetation fluorescence complicate our ability to interpret SIF measurements. We developed an instrument to measure leaf-level gas exchange simultaneously with pulse-amplitude modulation (PAM) and spectrally resolved fluorescence over the same field of view - allowing us to investigate the relationships between active and passive fluorescence with photosynthesis. Strongly correlated, slope-dependent relationships were observed between measured spectra across all wavelengths (Fλ , 670-850 nm) and PAM fluorescence parameters under a range of actinic light intensities (steady-state fluorescence yields, Ft ) and saturation pulses (maximal fluorescence yields, Fm ). Our results suggest that this method can accurately reproduce the full Chl emission spectra - capturing the spectral dynamics associated with changes in the yields of fluorescence, photochemical (ΦPSII), and nonphotochemical quenching (NPQ). We discuss how this method may establish a link between photosynthetic capacity and the mechanistic drivers of wavelength-specific fluorescence emission during changes in environmental conditions (light, temperature, humidity). Our emphasis is on future research directions linking spectral fluorescence to photosynthesis, ΦPSII, and NPQ.

Plant compartment and biogeography affect microbiome composition in cultivated and native Agave species.

Desert plants are hypothesized to survive the environmental stress inherent to these regions in part thanks to symbioses with microorganisms, and yet these microbial species, the communities they form, and the forces that influence them are poorly understood. Here we report the first comprehensive investigation of the microbial communities associated with species of Agave, which are native to semiarid and arid regions of Central and North America and are emerging as biofuel feedstocks. We examined prokaryotic and fungal communities in the rhizosphere, phyllosphere, leaf and root endosphere, as well as proximal and distal soil samples from cultivated and native agaves, through Illumina amplicon sequencing. Phylogenetic profiling revealed that the composition of prokaryotic communities was primarily determined by the plant compartment, whereas the composition of fungal communities was mainly influenced by the biogeography of the host species. Cultivated A. tequilana exhibited lower levels of prokaryotic diversity compared with native agaves, although no differences in microbial diversity were found in the endosphere. Agaves shared core prokaryotic and fungal taxa known to promote plant growth and confer tolerance to abiotic stress, which suggests common principles underpinning Agave-microbe interactions.

A tale of two plasticities: leaf hydraulic conductances and related traits diverge for two tropical epiphytes from contrasting light environments.

We compared the effects of different light environments on leaf hydraulic conductance (Kleaf ) for two congeneric epiphytes, the tank bromeliads Guzmania lingulata (L.) Mez and Guzmania monostachia (L.) Rusby ex Mez. They occur sympatrically at the study site, although G. monostachia is both wider ranging and typically found in higher light. We collected plants from two levels of irradiance and measured Kleaf as well as related morphological and anatomical traits. Leaf xylem conductance (Kxy ) was estimated from tracheid dimensions, and leaf conductance outside the xylem (Kox ) was derived from a leaky cable model. For G. monostachia, but not for G. lingulata, Kleaf and Kxy were significantly higher in high light conditions. Under both light conditions, Kxy and Kox were co-limiting for the two species, and all conductances were in the low range for angiosperms. With respect to hydraulic conductances and a number of related anatomical traits, G. monostachia exhibited greater plasticity than did G. lingulata, which responded to high light chiefly by reducing leaf size. The positive plasticity of leaf hydraulic traits in varying light environments in G. monostachia contrasted with negative plasticity in leaf size for G. lingulata, suggesting that G. monostachia may be better able to respond to forest conditions that are likely to be warmer and more disturbed in the future.

Plant hydraulics as a central hub integrating plant and ecosystem function: meeting report for 'Emerging Frontiers in Plant Hydraulics' (Washington, DC, May 2015).

Water plays a central role in plant biology and the efficiency of water transport throughout the plant affects both photosynthetic rate and growth, an influence that scales up deterministically to the productivity of terrestrial ecosystems. Moreover, hydraulic traits mediate the ways in which plants interact with their abiotic and biotic environment. At landscape to global scale, plant hydraulic traits are important in describing the function of ecological communities and ecosystems. Plant hydraulics is increasingly recognized as a central hub within a network by which plant biology is connected to palaeobiology, agronomy, climatology, forestry, community and ecosystem ecology and earth-system science. Such grand challenges as anticipating and mitigating the impacts of climate change, and improving the security and sustainability of our food supply rely on our fundamental knowledge of how water behaves in the cells, tissues, organs, bodies and diverse communities of plants. A workshop, 'Emerging Frontiers in Plant Hydraulics' supported by the National Science Foundation, was held in Washington DC, 2015 to promote open discussion of new ideas, controversies regarding measurements and analyses, and especially, the potential for expansion of up-scaled and down-scaled inter-disciplinary research, and the strengthening of connections between plant hydraulic research, allied fields and global modelling efforts.

Allocation tradeoffs among chaparral shrub seedlings with different life history types (Rhamnaceae).

PREMISE OF THE STUDY: California chaparral shrub species have different life history types: Nonsprouters (NS) are killed by fire and persist through a fire-stimulated seed bank; facultative sprouters (FS) reestablish by a combination of vegetative sprouting and seeding; and obligate sprouters (OS) reestablish exclusively by sprouting. Nonsprouters and FS establish seedlings in open-canopy postfire environments, whereas OS establish seedlings between fires in the shady understory. We hypothesized that allocation differences among seedlings of postfire sprouters and nonsprouters and regeneration niche differences would lead to contrasting patterns in biomass accumulation (NS > FS > OS, in sun; OS > FS > NS, in shade). METHODS: Seedlings of three species from each life history type were grown in sun and 75% shade. We measured net carbon assimilation and biomass accumulation after one year. KEY RESULTS: Biomass accumulation was similar in the sun except FS>OS. In the shade, NS had lower biomass than FS and OS. Assimilation rates, nitrogen relations, and allocation differences could not fully explain biomass accumulation differences. Instead, biomass accumulation was inversely related to water-stress tolerance and shade tolerance. Additionally, OS and FS differed in root/shoot allocation even though both are sprouters. CONCLUSIONS: Seedling growth and carbon assimilation rates were divergent among three life history types and were consistent with differences in tolerance to water stress and shade or sun regeneration niches, but not tradeoffs in sprouting-related allocation differences per se.

Contractile roots in succulent monocots: convergence, divergence and adaptation to limited rainfall.

Contractile roots (CRs) that pull shoots further down in the soil are a possible example of convergent evolution in two monocot families, the Agavaceae and the Asphodelaceae. The association between CRs, water uptake and habitat aridity was investigated for agaves, yuccas and aloes by assessing the occurrence of CRs and the amount of root contraction for glasshouse-grown plants with respect to mean annual rainfall of their native habitats. Structural features of CRs as well as root hydraulic conductance were compared with those of non-contractile roots (NCRs). CRs occurred in 55% of the 73 species examined, including 64% of the agaves and 85% of the yuccas, but in none of the aloes despite the occurrence of CRs in related genera. The phylogenetic distribution of CRs was consistent with multiple acquisitions or losses of the trait. The amount of root contraction showed a highly significant negative relationship with mean annual rainfall, although other environmental factors may also be important. Radial hydraulic conductance of the basal (contractile) zone exceeded that of the midroot zone for CRs; for NCRs, the opposite was true. Thus, CRs in the species examined may provide a mechanism for greater water uptake near the soil surface in regions with limited rainfall.

Root-soil contact for the desert succulent Agave deserti in wet and drying soil.

To investigate the extent and size of root-soil air gaps that develop during soil drying, resin casts of roots of the desert succulent Agave deserti Engelm. were made in situ for container-grown plants and in the field. Plants that were draughted in containers for 7 and 14 d had 24 and 34% root shrinkage, respectively, leading to root-soil air gaps that would reduce the hydraulic conductivity at the root-soil interface by a factor of about 5. When containers were vibrated during drought, root-soil air gaps were greatly diminished, and the predicted conductivity at the interface was similar to that of the control (moist soil). For plants in the field (4 and 6 wk after the last rainfall), root shrinkage was greater than for container-grown plants, but root-soil contact on the root periphery was greater, which led to a higher predicted hydraulic conductivity at the root-soil interface. To test the hypothesis that root-soil air gaps would help to limit water efflux from roots in drying soil, the water potentials of the soil, root, and shoot of plants from vibrated containers (with gaps eliminated or reduced) and non-vibrated containers were compared. The soil water potential was lower for vibrated containers after 14 d of drought, suggesting more rapid depletion of soil water due to better root-soil contact, and the root water potential was lower as well, suggesting greater water loss by roots in the absence of root-soil air gaps. Thus, air gaps could benefit A. deserti by helping to maintain a higher root water potential in the early stages of drought and later by limiting root water loss at the root-soil interface when the water potential exceeds that of the soil.

Root-stem junctions of a desert monocotyledon and a dicotyledon: hydraulic consequences under wet conditions and during drought.

Junctions between shoot-borne main roots and stems, which are a crucial part of the water-flow pathway in plants, were investigated for the leaf succulent Agave deserti Engelm. and the sympatric stem succulent Ferocactus acanthodes (Lem.) Britton & Rose under wet conditions and during 21 d of drying in soil. During soil drying, the hydraulic conductance per unit pressure gradient (Kh ) declined dramatically in the junctions and to a lesser extent in the roots, but not in stems. The decline in junction Kh was particularly important for A. deserti, which lacks vessels in its stem, because even under wet conditions its Kh was lower in stems and junctions than in roots. For both species, the decline in Kb was due to embolism in the connective tracheary elements at the junction. Such connective elements may be particularly vulnerable to embolism due to their large areas of unlignified primary cell wall. Because the embolism is reversible, the junctions act as rectifiers. Thus, high Kh under wet conditions allows for rapid water uptake following rainfall, and low Kh during drought helps limit water loss from the succulent shoots to a dry soil.

Leaf hydraulic conductance for a tank bromeliad: axial and radial pathways for moving and conserving water.

Epiphytic plants in the Bromeliaceae known as tank bromeliads essentially lack stems and absorptive roots and instead take up water from reservoirs formed by their overlapping leaf bases. For such plants, leaf hydraulic conductance is plant hydraulic conductance. Their simple strap-shaped leaves and parallel venation make them suitable for modeling leaf hydraulic conductance based on vasculature and other anatomical and morphological traits. Plants of the tank bromeliad Guzmania lingulata were investigated in a lowland tropical forest in Costa Rica and a shaded glasshouse in Los Angeles, CA, USA. Stomatal conductance to water vapor and leaf anatomical variables related to hydraulic conductance were measured for both groups. Tracheid diameters and numbers of vascular bundles (veins) were used with the Hagen-Poiseuille equation to calculate axial hydraulic conductance. Measurements of leaf hydraulic conductance using the evaporative flux method were also made for glasshouse plants. Values for axial conductance and leaf hydraulic conductance were used in a model based on leaky cable theory to estimate the conductance of the radial pathway from the vein to the leaf surface and to assess the relative contributions of both axial and radial pathways. In keeping with low stomatal conductance, low stomatal density, low vein density, and narrow tracheid diameters, leaf hydraulic conductance for G. lingulata was quite low in comparison with most other angiosperms. Using the predicted axial conductance in the leaky cable model, the radial resistance across the leaf mesophyll was predicted to predominate; lower, more realistic values of axial conductance resulted in predicted radial resistances that were closer to axial resistance in their impact on total leaf resistance. Tracer dyes suggested that water uptake through the tank region of the leaf was not limiting. Both dye movement and the leaky cable model indicated that the leaf blade of G. lingulata was structurally and hydraulically well-suited to conserve water.

Root contraction helps protect the "living rock" cactus Ariocarpus fissuratus from lethal high temperatures when growing in rocky soil.

PREMISE OF THE STUDY: We investigated how the "living rock" cactus Ariocarpus fissuratus, like other low-growing desert plants, can endure potentially lethal high temperatures at the soil surface. Specifically, we examined how shoot descent by root contraction in the presence or absence of soil rocks influences shoot temperatures and transpiration. • METHODS: Root contraction was identified by measuring shoot descent and anatomical analysis. Temperatures and transpiration were measured for plants at two heights in sandy and rocky soil, and temperature tolerances were determined by vital staining. • KEY RESULTS: Plants embedded in rocky soil survived an extreme heat episode, unlike plants in sandy soil, though rocks did not moderate low temperatures. Root contraction occurred regardless of season and soil moisture. Xylem conduits (wide-band tracheids) formed a compressible lattice that decreased root length as rays enlarged the root base radially. Plant position in the soil did not affect transpiration. • CONCLUSIONS: Contractile roots pulled plants of A. fissuratus into the soil at rates of 6-30 mm yr(-1). Maintaining shoots level with the soil surface kept plant temperatures below the high lethal temperature and improved survivorship in soil shaded by surface rocks.

Root deployment and shoot growth for two desert species in response to soil rockiness.

Soil texture, as well as the presence of rocks, can determine the water status, growth, and distribution of plants in arid environments. The effects of soil rockiness and soil particle size distribution on shoot and root growth, root system size, rooting depth, and water relations were therefore investigated for the Crassulacean acid metabolism leaf succulent Agave deserti and the C(4) bunchgrass Pleuraphis rigida after precipitation events during the summer and winter/spring rainfall periods in the northwestern Sonoran Desert. The soils at the field site varied from sandy (<3% rocks by volume) to rocky (up to 35% rocks), with greater water availability at higher water potentials for sandy than for rocky soils. Although A. deserti was absent from the sandiest sites, its shoot and root growth during both rainfall periods were greatest in comparatively sandier sites and decreased as the soil rock content increased. Furthermore, A. deserti had twofold greater root surface area, root : leaf area ratio, and mean rooting depth at sandier than at rocky sites. As for A. deserti, shoot growth was greater for P. rigida at the sandier sites than at the rockier sites, even though its root surface area and mean rooting depth did not vary significantly. After early spring rainfall events, the leaf water potential for A. deserti did not differ between rocky and sandy sites, but transpiration rates were almost twofold greater at rocky than at sandy sites. During the same period, P. rigida had lower leaf water potentials and 25% lower transpiration rates at rocky than at sandy sites. The greater variability in the deployment of the root systems of A. deserti in response to soil rockiness may reflect its evergreen habit and slower growth, which allow it to endure periods of lower water availability than does P. rigida, whose leaves die during drought.

Plasma membrane aquaporins play a significant role during recovery from water deficit.

The role of plasma membrane aquaporins (PIPs) in water relations of Arabidopsis was studied by examining plants with reduced expression of PIP1 and PIP2 aquaporins, produced by crossing two different antisense lines. Compared with controls, the double antisense (dAS) plants had reduced amounts of PIP1 and PIP2 aquaporins, and the osmotic hydraulic conductivity of isolated root and leaf protoplasts was reduced 5- to 30-fold. The dAS plants had a 3-fold decrease in the root hydraulic conductivity expressed on a root dry mass basis, but a compensating 2.5-fold increase in the root to leaf dry mass ratio. The leaf hydraulic conductance expressed on a leaf area basis was similar for the dAS compared with the control plants. As a result, the hydraulic conductance of the whole plant was unchanged. Under sufficient and under water-deficient conditions, stomatal conductance, transpiration rate, plant hydraulic conductance, leaf water potential, osmotic pressure, and turgor pressure were similar for the dAS compared with the control plants. However, after 4 d of rewatering following 8 d of drying, the control plants recovered their hydraulic conductance and their transpiration rates faster than the dAS plants. Moreover, after rewatering, the leaf water potential was significantly higher for the control than for the dAS plants. From these results, we conclude that the PIPs play an important role in the recovery of Arabidopsis from the water-deficient condition.