Wood development is strictly regulated by various phytohormones and auxin plays a central regulatory role in this process. However, how the auxin signaling is transducted in developing secondary ...xylem during wood formation in tree species remains unclear.
Here, we identified an Aux/INDOLE-3-ACETIC ACID 9 (IAA9)-AUXIN RESPONSE FACTOR 5 (ARF5) module in Populus tomentosa as a key mediator of auxin signaling to control early developing xylem development.
PtoIAA9, a canonical Aux/IAA gene, is predominantly expressed in vascular cambium and developing secondary xylem and induced by exogenous auxin. Overexpression of PtoIAA9m encoding a stabilized IAA9 protein significantly represses secondary xylem development in transgenic poplar. We further showed that PtoIAA9 interacts with PtoARF5 homologs via the C-terminal III/IV domains. The truncated PtoARF5.1 protein without the III/IV domains rescued defective phenotypes caused by PtoIAA9m. Expression analysis showed that the PtoIAA9-PtoARF5 module regulated the expression of genes associated with secondary vascular development in PtoIAA9m- and PtoARF5.1-overexpressing plants. Furthermore, PtoARF5.1 could bind to the promoters of two Class III homeodomain-leucine zipper (HD-ZIP III) genes, PtoHB7 and PtoHB8, to modulate secondary xylem formation.
Taken together, our results suggest that the Aux/IAA9-ARF5 module is required for auxin signaling to regulate wood formation via orchestrating the expression of HD-ZIP III transcription factors in poplar.
• Vulnerability to cavitation and conductive efficiency depend on xylem anatomy. We tested a large range of structure-function hypotheses, some for the first time, within a single genus to minimize ...phylogenetic ‘noise' and maximize detection of functionally relevant variation. • This integrative study combined in-depth anatomical observations using light, scanning and transmission electron microscopy of seven Acer taxa, and compared these observations with empirical measures of xylem hydraulics. • Our results reveal a 2 MPa range in species' mean cavitation pressure (MCP). MCP was strongly correlated with intervessel pit structure (membrane thickness and porosity, chamber depth), weakly correlated with pit number per vessel, and not related to pit area per vessel. At the tissue level, there was a strong correlation between MCP and mechanical strength parameters, and some of the first evidence is provided for the functional significance of vessel grouping and thickenings on inner vessel walls. In addition, a strong trade-off was observed between xylem-specific conductivity and MCP. Vessel length and intervessel wall characteristics were implicated in this safety-efficiency trade-off. • Cavitation resistance and hydraulic conductivity in Acer appear to be controlled by a very complex interaction between tissue, vessel network and pit characteristics.
Cell death of xylem elements is manifested by rupture of the tonoplast and subsequent autolysis of the cellular contents. Metacaspases have been implicated in various forms of plant cell death but ...regulation and execution of xylem cell death by metacaspases remains unknown.
Analysis of the type II metacaspase gene family in Arabidopsis thaliana supported the function of METACASPASE 9 (AtMC9) in xylem cell death. Progression of xylem cell death was analysed in protoxylem vessel elements of 3-d-old atmc9 mutant roots using reporter gene analysis and electron microscopy.
Protoxylem cell death was normally initiated in atmc9 mutant lines, but detailed electron microscopic analyses revealed a role for AtMC9 in clearance of the cell contents post mortem, that is after tonoplast rupture. Subcellular localization of fluorescent AtMC9 reporter fusions supported a post mortem role for AtMC9. Further, probe-based activity profiling suggested a function of AtMC9 on activities of papain-like cysteine proteases.
Our data demonstrate that the function of AtMC9 in xylem cell death is to degrade vessel cell contents after vacuolar rupture. We further provide evidence on a proteolytic cascade in post mortem autolysis of xylem vessel elements and suggest that AtMC9 is part of this cascade.
Vascular plants (Tracheophytes) have adapted to a variety of environments ranging from arid deserts to tropical rainforests, and now comprise >250 000 species. While they differ widely in appearance ...and growth habit, all of them share a similar specialized tissue system (vascular tissue) for transporting water and nutrients throughout the organism. Plant vascular systems connect all plant organs from the shoot to the root, and are comprised of two main tissue types, xylem and phloem. In this review we examine the current state of knowledge concerning the process of vascular tissue formation, and highlight important mechanisms underlying key steps in vascular cell type specification, xylem and phloem tissue patterning, and, finally, the differentiation and maturation of specific xylem cell types.
Variation in angiosperm vessel diameter is of major functional significance. In the light of recent models predicting optimal vessel taper given resistance imposed by conductive path length, we ...tested the prediction that plant size should predict vessel diameter, with dryland plants having narrower vessels for their stem sizes. We assembled a comparative dataset including vessel and stem diameter measurements from 237 species from over 40 angiosperm orders across a wide range of habits and habitats. Stem diameter predicted vessel diameter across self‐supporting plants (slope 0.36, 95% CI 0.32–0.39). Samples from 142 species from five communities of differing water availability showed no tendency for dryland plants to have narrower vessels. Predictable relationships between vessel diameter and stem diameter mirrored predictable relationships between stem length and diameter across self‐supporting species. That vessels are proportional to stem diameter and stem diameter is proportional to stem length suggests that taper in relation to conductive path length gives rise to the vessel diameter–stem diameter relationship. In turn, plant size is related to climate, leading indirectly to the vessel–climate relationship: vessels are likely narrower in drier communities because dryland plants are on average smaller, not because they have narrow vessels for their stem sizes.
Summary
Xylem conduits have lignified walls to resist crushing pressures. The thicker the double‐wall (T) relative to its diameter (D), the greater the implosion safety. Having safer conduits may ...incur higher costs and reduced flow, while having less resistant xylem may lead to catastrophic collapse under drought. Although recent studies have shown that conduit implosion commonly occurs in leaves, little is known about how leaf xylem scales T vs D to trade off safety, flow efficiency, mechanical support, and cost.
We measured T and D in > 7000 conduits of 122 species to investigate how T vs D scaling varies across clades, habitats, growth forms, leaf, and vein sizes.
As conduits become wider, their double‐cell walls become proportionally thinner, resulting in a negative allometry between T and D. That is, narrower conduits, which are usually subjected to more negative pressures, are proportionally safer than wider ones. Higher implosion safety (i.e. higher T/D ratios) was found in asterids, arid habitats, shrubs, small leaves, and minor veins.
Despite the strong allometry, implosion safety does not clearly trade off with other measured leaf functions, suggesting that implosion safety at whole‐leaf level cannot be easily predicted solely by individual conduits' anatomy.
Stomata play a significant role in the Earth's water and carbon cycles, by regulating gaseous exchanges between the plant and the atmosphere. Under drought conditions, stomatal control of ...transpiration has long been thought to be closely coordinated with the decrease in hydraulic capacity (hydraulic failure due to xylem embolism). We tested this hypothesis by coupling a meta‐analysis of functional traits related to the stomatal response to drought and embolism resistance with simulations from a soil–plant hydraulic model. We report here a previously unreported phenomenon: the existence of an absolute limit by which stomata closure must occur to avoid rapid death in drought conditions. The water potential causing stomatal closure and the xylem pressure at the onset of embolism formation were equal for only a small number of species, and the difference between these two traits (i.e. safety margins) increased continuously with increasing embolism resistance. Our findings demonstrate the need to revise current views about the functional coordination between stomata and hydraulic traits and provide a mechanistic framework for modeling plant mortality under drought conditions.
Currently, phloem transport in plants under field conditions is not well understood. This is largely the result of the lack of techniques suitable for the measurement of the physiological properties ...of phloem.
We present a model that interprets the changes in xylem diameter and live bark thickness and separates the components responsible for such changes. We test the predictions from this model on data from three mature Scots pine trees in Finland. The model separates the live bark thickness variations caused by bark water capacitance from a residual signal interpreted to indicate the turgor changes in the bark.
The predictions from the model are consistent with processes related to phloem transport. At the diurnal scale, this signal is related to patterns of photosynthetic activity and phloem loading. At the seasonal scale, bark turgor showed rapid changes during two droughts and after two rainfall events, consistent with physiological predictions. Daily cumulative totals of this turgor term were related to daily cumulative totals of canopy photosynthesis. Finally, the model parameter representing radial hydraulic conductance between phloem and xylem showed a temperature dependence consistent with the temperature-driven changes in water viscosity.
We propose that this model has potential for the continuous field monitoring of tree phloem function.
The cambium which produces wavy-grained xylem in spruce differs from normal cambium by a higher frequency of oblique anticlinal divisions and a higher rate of intrusive growth of fusiform initials. ...Since the orientation, either to the left or to the right, of the divisions and the overlaps achieved by the growting tips is uniform within the areas called domains, the domain pattern of the cambium is reflected in the pattern of grain undulations in the xy1em. The domain pattern moves longitudinally about 0.7 mm during the production of l mm of xylem. A visible expression of the movement is the obliquity of undulation lines on the radial face of the wavy xylem.
Long-distance transport of nitrate requires xylem loading and unloading, a successive process that determines nitrate distribution and subsequent assimilation efficiency. Here, we report the ...functional characterization of NRT1.8, a member of the nitrate transporter (NRT1) family in Arabidopsis thaliana. NRT1.8 is upregulated by nitrate. Histochemical analysis using promoter-β-glucuronidase fusions, as well as in situ hybridization, showed that NRT1.8 is expressed predominantly in xylem parenchyma cells within the vasculature. Transient expression of the NRT1.8:enhanced green fluorescent protein fusion in onion epidermal cells and Arabidopsis protoplasts indicated that NRT1.8 is plasma membrane localized. Electrophysiological and nitrate uptake analyses using Xenopus laevis oocytes showed that NRT1.8 mediates low-affinity nitrate uptake. Functional disruption of NRT1.8 significantly increased the nitrate concentration in xylem sap. These data together suggest that NRT1.8 functions to remove nitrate from xylem vessels. Interestingly, NRT1.8 was the only nitrate assimilatory pathway gene that was strongly upregulated by cadmium (Cd²⁺) stress in roots, and the nrt1.8-1 mutant showed a nitrate-dependent Cd²⁺-sensitive phenotype. Further analyses showed that Cd²⁺ stress increases the proportion of nitrate allocated to wild-type roots compared with the nrt1.8-1 mutant. These data suggest that NRT1.8-regulated nitrate distribution plays an important role in Cd²⁺ tolerance.
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