Xylem-dwelling pathogen unaffected by local xylem vessel network properties in grapevines (Vitis spp.).

BACKGROUND AND AIMS: Xylella fastidiosa (Xf) is the xylem-dwelling bacterium associated with Pierce's disease (PD), which causes mortality in agriculturally important species, such as grapevine (Vitis vinifera). The development of PD symptoms in grapevines depends on the ability of Xf to produce cell-wall-degrading enzymes to break up intervessel pit membranes and systematically spread through the xylem vessel network. Our objective here was to investigate whether PD resistance could be mechanistically linked to xylem vessel network local connectivity. METHODS: We used high-resolution X-ray micro-computed tomography (microCT) imaging to identify and describe the type, area and spatial distribution of intervessel connections for six different grapevine genotypes from three genetic backgrounds, with varying resistance to PD (four PD resistant and two PD susceptible). KEY RESULTS: Our results suggest that PD resistance is unlikely to derive from local xylem network connectivity. The intervessel pit area (Ai) varied from 0.07 ±â€…0.01 mm2 mm-3 in Lenoir to 0.17 ±â€…0.03 mm2 mm-3 in Blanc do Bois, both PD resistant. Intervessel contact fraction (Cp) was not statically significant, but the two PD-susceptible genotypes, Syrah (0.056 ±â€…0.015) and Chardonnay (0.041 ±â€…0.013), were among the most highly connected vessel networks. Neither Ai nor Cp explained differences in PD resistance among the six genotypes. Bayesian re-analysis of our data shows moderate evidence against the effects of the traits analysed: Ai (BF01 = 4.88), mean vessel density (4.86), relay diameter (4.30), relay density (3.31) and solitary vessel proportion (3.19). CONCLUSIONS: Our results show that radial and tangential xylem network connectivity is highly conserved within the six different Vitis genotypes we sampled. The way that Xf traverses the vessel network may limit the importance of local network properties to its spread and may confer greater importance on host biochemical responses.

Hydraulic failure as a primary driver of xylem network evolution in early vascular plants.

The earliest vascular plants had stems with a central cylindrical strand of water-conducting xylem, which rapidly diversified into more complex shapes. This diversification is understood to coincide with increases in plant body size and branching; however, no selection pressure favoring xylem strand-shape complexity is known. We show that incremental changes in xylem network organization that diverge from the cylindrical ancestral form lead to progressively greater drought resistance by reducing the risk of hydraulic failure. As xylem strand complexity increases, independent pathways for embolism spread become fewer and increasingly concentrated in more centrally located conduits, thus limiting the systemic spread of embolism during drought. Selection by drought may thus explain observed trajectories of xylem strand evolution in the fossil record and the diversity of extant forms.

Xylem network connectivity and embolism spread in grapevine(Vitis vinifera L.).

Xylem networks are vulnerable to the formation and spread of gas embolisms that reduce water transport. Embolisms spread through interconduit pits, but the three-dimensional (3D) complexity and scale of xylem networks means that the functional implications of intervessel connections are not well understood. Here, xylem networks of grapevine (Vitis vinifera L.) were reconstructed from 3D high-resolution X-ray micro-computed tomography (microCT) images. Xylem network performance was then modeled to simulate loss of hydraulic conductivity under increasingly negative xylem sap pressure simulating drought stress conditions. We also considered the sensitivity of xylem network performance to changes in key network parameters. We found that the mean pit area per intervessel connection was constant across 10 networks from three, 1.5-m stem segments, but short (0.5 cm) segments fail to capture complete network connectivity. Simulations showed that network organization imparted additional resistance to embolism spread beyond the air-seeding threshold of pit membranes. Xylem network vulnerability to embolism spread was most sensitive to variation in the number and location of vessels that were initially embolized and pit membrane vulnerability. Our results show that xylem network organization can increase stem resistance to embolism spread by 40% (0.66 MPa) and challenge the notion that a single embolism can spread rapidly throughout an entire xylem network.

In vivo pressure gradient heterogeneity increases flow contribution of small diameter vessels in grapevine.

Leaves lose approximately 400 H2O molecules for every 1 CO2 gained during photosynthesis. Most long-distance water transport in plants, or xylem sap flow, serves to replace this water to prevent desiccation. Theory predicts that the largest vessels contribute disproportionately to overall sap flow because flow in pipe-like systems scales with the fourth power of radius. Here, we confront these theoretical flow predictions for a vessel network reconstructed from X-ray µCT imagery with in vivo flow MRI observations from the same sample of a first-year grapevine stem. Theoretical flow rate predictions based on vessel diameters are not supported. The heterogeneity of the vessel network gives rise to transverse pressure gradients that redirect flow from wide to narrow vessels, reducing the contribution of wide vessels to sap flow by 15% of the total. Our results call for an update of the current working model of the xylem to account for its heterogeneity.

Whole root system water conductance responds to both axial and radial traits and network topology over natural range of trait variation.

Current theory and supporting research suggests that radial transport is the most limiting factor to root water uptake, raising the question whether only absorbing root length and radial conductivity matter to water uptake. Here, we extended the porous pipe analytical model of root water uptake to entire root networks in 3D and analysed the relative importance of axial and radial characteristics to total uptake over parameter ranges reported in the literature. We found that network conductance can be more sensitive to axial than radial conductance of absorbing roots. When axial transport limits uptake, more dichotomous topology, especially towards the base of the network, increases water uptake efficiency, while the effect of root length is reduced. Whole root system conductance was sensitive to radial transport and length in model lupin (Lupinus angustifolius L.), but to axial transport and topology in wheat (Triticum aestivum L.), suggesting the root habit niche space of monocots may be constrained by their loss of secondary growth. A deep tap root calibrated to oak (Quercus fusiformis J. Buchholz) hydraulic parameters required 15 times more xylem volume to transport comparable amounts of water once recalibrated to parameters from juniper (Juniperus ashei Small 1901), showing that anatomical constraints on axial conductance can lead to significant trade-offs in woody roots as well. Root system water uptake responds to axial transport and can be limited by it in a biologically meaningful way.

Variations in xylem embolism susceptibility under drought between intact saplings of three walnut species.

A germplasm collection containing varied Juglans genotypes holds potential to improve drought resistance of plant materials for commercial production. We used X-ray computed microtomography to evaluate stem xylem embolism susceptibility/repair in relation to vessel anatomical features (size, arrangement, connectivity and pit characteristics) in 2-year-old saplings of three Juglans species. In vivo analysis revealed interspecific variations in embolism susceptibility among Juglans microcarpa, J. hindsii (both native to arid habitats) and J. ailantifolia (native to mesic habitats). Stem xylem of J. microcarpa was more resistant to drought-induced embolism as compared with J. hindsii and J. ailantifolia (differences in embolism susceptibility among older and current year xylem were not detected in any species). Variations in most vessel anatomical traits were negligible among the three species; however, we detected substantial interspecific differences in intervessel pit characteristics. As compared with J. hindsii and J. ailantifolia, low embolism susceptibility in J. microcarpa was associated with smaller pit size in larger diameter vessels, a smaller area of the shared vessel wall occupied by pits, lower pit frequency and no changes in pit characteristics as vessel diameters increased. Changes in amount of embolized vessels following 40 days of re-watering were minor in intact saplings of all three species highlighting that an embolism repair mechanism did not contribute to drought recovery. In conclusion, our data indicate that interspecific variations in drought-induced embolism susceptibility are associated with species-specific pit characteristics, and these traits may provide a future target for breeding efforts aimed at selecting walnut germplasm with improved drought resistance.

Box-Counting Dimension Revisited: Presenting an Efficient Method of Minimizing Quantization Error and an Assessment of the Self-Similarity of Structural Root Systems.

Fractal dimension (FD), estimated by box-counting, is a metric used to characterize plant anatomical complexity or space-filling characteristic for a variety of purposes. The vast majority of published studies fail to evaluate the assumption of statistical self-similarity, which underpins the validity of the procedure. The box-counting procedure is also subject to error arising from arbitrary grid placement, known as quantization error (QE), which is strictly positive and varies as a function of scale, making it problematic for the procedure's slope estimation step. Previous studies either ignore QE or employ inefficient brute-force grid translations to reduce it. The goals of this study were to characterize the effect of QE due to translation and rotation on FD estimates, to provide an efficient method of reducing QE, and to evaluate the assumption of statistical self-similarity of coarse root datasets typical of those used in recent trait studies. Coarse root systems of 36 shrubs were digitized in 3D and subjected to box-counts. A pattern search algorithm was used to minimize QE by optimizing grid placement and its efficiency was compared to the brute force method. The degree of statistical self-similarity was evaluated using linear regression residuals and local slope estimates. QE, due to both grid position and orientation, was a significant source of error in FD estimates, but pattern search provided an efficient means of minimizing it. Pattern search had higher initial computational cost but converged on lower error values more efficiently than the commonly employed brute force method. Our representations of coarse root system digitizations did not exhibit details over a sufficient range of scales to be considered statistically self-similar and informatively approximated as fractals, suggesting a lack of sufficient ramification of the coarse root systems for reiteration to be thought of as a dominant force in their development. FD estimates did not characterize the scaling of our digitizations well: the scaling exponent was a function of scale. Our findings serve as a caution against applying FD under the assumption of statistical self-similarity without rigorously evaluating it first.

Interplay between PDL and nonlinear effects in coherent polarization multiplexed systems.

We analyzed the mechanism of the interplay between PDL and fiber nonlinear effects in 112 Gb/s DP-QPSK systems and showed that PDL can generate large data-dependent optical peak power variations that can worsen nonlinear tolerance and cause an additional 1.4 dB Q-penalty.