Michael J. Clearwater

Water transport in trees: current perspectives, new insights and some controversies

This review emphasizes recent developments and controversies related to the uptake, transport and loss of water by trees. Comparisons of the stable isotope composition of soil and xylem water have provided new and sometimes unexpected insights concerning spatial and temporal partitioning of soil water by roots. Passive, hydraulic redistribution of water from moister to drier portions of the soil profile via plant root systems may have a substantial impact on vertical profiles of soil water distribution, partitioning of water within and among species, and on ecosystem water balance. The recent development of a technique for direct measurement of pressure in individual xylem elements of intact, transpiring plants elicited a number of challenges to the century-old cohesion-tension theory. The ongoing debate over mechanisms of long-distance water transport has stimulated an intense interest in the phenomenon and mechanisms of embolism repair. Rather than embolism being essentially irreversible, it now appears that there is a dynamic balance between embolism formation and repair throughout the day and that daily release of water from the xylem via cavitation may serve to stabilize leaf water balance by minimizing the temporal imbalance between water supply and demand. Leaf physiology is closely linked to hydraulic architecture and hydraulic perturbations, but the precise nature of the signals to which stomata respond remains to be elucidated. When water transport in trees is studied at multiple scales from single leaves to the whole organism, considerable functional convergence in regulation of water use among phylogenetically diverse species is revealed.

Allocation, stress tolerance and carbon transport in plants: how does phloem physiology affect plant ecology?

Despite the crucial role of carbon transport in whole plant physiology and its impact on plant-environment interactions and ecosystem function, relatively little research has tried to examine how phloem physiology impacts plant ecology. In this review, we highlight several areas of active research where inquiry into phloem physiology has increased our understanding of whole plant function and ecological processes. We consider how xylem-phloem interactions impact plant drought tolerance and reproduction, how phloem transport influences carbon allocation in trees and carbon cycling in ecosystems and how phloem function mediates plant relations with insects, pests, microbes and symbiotes. We argue that in spite of challenges that exist in studying phloem physiology, it is critical that we consider the role of this dynamic vascular system when examining the relationship between plants and their biotic and abiotic environment.

Metabolic analysis of kiwifruit (Actinidia deliciosa) berries from extreme genotypes reveals hallmarks for fruit starch metabolism

Tomato, melon, grape, peach, and strawberry primarily accumulate soluble sugars during fruit development. In contrast, kiwifruit (Actinidia Lindl. spp.) and banana store a large amount of starch that is released as soluble sugars only after the fruit has reached maturity. By integrating metabolites measured by gas chromatography–mass spectrometry, enzyme activities measured by a robot-based platform, and transcript data sets during fruit development of Actinidia deliciosa genotypes contrasting in starch concentration and size, this study identified the metabolic changes occurring during kiwifruit development, including the metabolic hallmarks of starch accumulation and turnover. At cell division, a rise in glucose (Glc) concentration was associated with neutral invertase (NI) activity, and the decline of both Glc and NI activity defined the transition to the cell expansion and starch accumulation phase. The high transcript levels of β-amylase 9 (BAM9) during cell division, prior to net starch accumulation, and the correlation between sucrose phosphate synthase (SPS) activity and sucrose suggest the occurrence of sucrose cycling and starch turnover. ADP-Glc pyrophosphorylase (AGPase) is identified as a key enzyme for starch accumulation in kiwifruit berries, as high-starch genotypes had 2- to 5-fold higher AGPase activity, which was maintained over a longer period of time and was also associated with enhanced and extended transcription of the AGPase large subunit 4 (APL4). The data also revealed that SPS and galactinol might affect kiwifruit starch accumulation, and suggest that phloem unloading into kiwifruit is symplastic. These results are relevant to the genetic improvement of quality traits such as sweetness and sugar/acid balance in a range of fruit species.

Soil fertility induces coordinated responses of multiple independent functional traits

Summary 1. A central goal of functional ecology is to determine how independent functional traits are selectively filtered by environmental conditions to improve our understanding of the mechanisms of community assembly. Soil fertility clearly influences community composition, but it is unclear which plant functional traits are most strongly associated with gradients of increasing nutrient limitation. 2. We hypothesized that leaf economic traits and stem tissue density would be strongly associated with soil fertility given their direct relationship to soil resource acquisition and use. In contrast, we hypothesized that functional traits that are commonly associated with competition for light (maximum height), shade tolerance (seed mass) and resistance to disturbance (bark thickness) would be unrelated to soil fertility. 3. We measured 13 functional traits from 30 tree species occurring in 40 plots across a soil fertility gradient in a mature warm temperate rain forest in Northland, New Zealand. Principal component analysis was used to assess the dimensionality and independence of the functional traits and the soil properties, and regression was used to determine the relationships between community-weighted mean traits and the soil fertility gradient. 4. We observed a coordinated response of multiple independent traits to soil fertility. Consistent with our hypothesis, species associated with low-fertility soils had comparatively ‘slower’ leaves (i.e. low SLA and leaf N and P, and high LDMC and thickness) and higher stem tissue density than species associated with high-fertility soils. 5. Unexpectedly, we observed that species associated with low-fertility soils had larger maximum heights, thicker bark and lower seed mass. Tall trees can persist on poor soils. Thick bark may be a defensive strategy for trees growing in resource-limited sites and large-seeded shade-tolerant species can persist in fertile soils where light is more limiting. 6. Synthesis. Species sorting can occur over short distances in ecosystems where topographically driven variation in soil fertility leads to complete compositional turnover. Inferences about species distributions based on single-trait spectrums can be misleading when environmental gradients sort species by filtering multiple independent traits simultaneously. Identifying the multidimensional trait combinations that promote fitness will advance both theory development and ecological restoration.

An external heat pulse method for measurement of sap flow through fruit pedicels, leaf petioles and other small‐diameter stems

The external heat ratio method is described for measurement of low rates of sap flow in both directions through stems and other plant organs, including fruit pedicels, with diameters up to 5 mm and flows less than 2 g h(-1). Calibration was empirical, with heat pulse velocity (v(h)) compared to gravimetric measurements of sap flow. In the four stem types tested (Actinidia sp. fruit pedicels, Schefflera arboricola petioles, Pittosporum crassifolium stems and Fagus sylvatica stems), v(h) was linearly correlated with sap velocity (v(s)) up to a v(s) of approximately 0.007 cm s(-1), equivalent to a flow of 1.8 g h(-1) through a 3-mm-diameter stem. Minimum detectable v(s) was approximately 0.0001 cm s(-1), equivalent to 0.025 g h(-1) through a 3-mm-diameter stem. Sensitivity increased with bark removal. Girdling had no effect on short-term measurements of in vivo sap flow, suggesting that phloem flows were too low to be separated from xylem flows. Fluctuating ambient temperatures increased variability in outdoor sap flow measurements. However, a consistent diurnal time-course of fruit pedicel sap flow was obtained, with flows towards 75-day-old kiwifruit lagging behind evaporative demand and peaking at 0.3 g h(-1) in the late afternoon.

Vascular functioning and the water balance of ripening kiwifruit (Actinidia chinensis) berries

Indirect evidence suggests that water supply to fleshy fruits during the final stages of development occurs through the phloem, with the xylem providing little water, or acting as a pathway for water loss back to the plant. This inference was tested by examining the water balance and vascular functioning of ripening kiwifruit berries (Actinidia chinensis var. chinensis ‘Hort16A’) exhibiting a pre-harvest ‘shrivel’ disorder in California, and normal development in New Zealand. Dye labelling and mass balance experiments indicated that the xylem and phloem were both functional and contributed approximately equally to the fruit water supply during this stage of development. The modelled fruit water balance was dominated by transpiration, with net water loss under high vapour pressure deficit (Da) conditions in California, but a net gain under cooler New Zealand conditions. Direct measurement of pedicel sap flow under controlled conditions confirmed inward flows in both the phloem and xylem under conditions of both low and high Da. Phloem flows were required for growth, with gradual recovery after a step increase in Da. Xylem flows alone were unable to support growth, but did supply transpiration and were responsive to Da-induced pressure fluctuations. The results suggest that the shrivel disorder was a consequence of a high fruit transpiration rate, and that the perception of complete loss or reversal of inward xylem flows in ripening fruits should be re-examined.

Hydraulic resistance of developing Actinidia fruit.

BACKGROUND AND AIMS Xylem flows into most fruits decline as the fruit develop, with important effects on mineral and carbohydrate accumulation. It has been hypothesized that an increase in xylem hydraulic resistance (RT) contributes to this process. This study examined changes in RT that occur during development of the berry of kiwifruit (Actinidia deliciosa), identified the region within the fruit where changes were occurring, and tested whether a decrease in irradiance during fruit development caused an increase in RT, potentially contributing to decreased mineral accumulation in shaded fruit. METHODS RT was measured using pressure chamber and flow meter methods, the two methods were compared, and the flow meter was also used to partition RT between the pedicel, receptacle and proximal and distal portions of the berry. Dye was used as a tracer for xylem function. Artificial shading was used to test the effect of light on RT, dye entry and mineral accumulation. KEY RESULTS RT decreased during the early phase of rapid fruit growth, but increased again as the fruit transitioned to a final period of slower growth. The most significant changes in resistance occurred in the receptacle, which initially contributed 20 % to RT, increasing to 90 % later in development. Dye also ceased moving beyond the receptacle from 70 d after anthesis. The two methods for measuring RT agreed in terms of the direction and timing of developmental changes in RT, but pressure chamber measurements were consistently higher than flow meter estimates of RT, prompting questions regarding which method is most appropriate for measuring fruit RT. Shading had no effect on berry growth but increased RT and decreased dye movement and calcium concentration. CONCLUSIONS Increased RT in the receptacle zone coincides with slowing fresh weight growth, reduced transpiration and rapid starch accumulation by the fruit. Developmental changes in RT may be connected to changes in phloem functioning and the maintenance of water potential gradients between the stem and the fruit. The effect of shade on RT extends earlier reports that shading can affect fruit vascular differentiation, xylem flows and mineral accumulation independently of effects on transpiration.

Overriding control of methane flux temporal variability by water table dynamics in a Southern Hemisphere, raised bog

There are still large uncertainties in peatland methane flux dynamics and insufficient understanding of how biogeochemical processes scale to ecosystems. New Zealand bogs differ from Northern Hemisphere ombrotrophic systems in climatic setting, hydrology, and dominant vegetation, offering an opportunity to evaluate our knowledge of peatland methane biogeochemistry gained primarily from northern bogs and fens. We report eddy covariance methane fluxes from a raised bog in New Zealand over 2.5 years. Annual total methane flux in 2012 was 29.1 g CH4 m−2 yr−1, whereas during a year with a severe drought (2013) it was 20.6 g CH4 m−2 yr−1, both high compared to Northern Hemisphere bogs and fens. Drier conditions led to a decrease in fluxes from ~100 mg CH4 m−2 d−1 to ~20 mg CH4 m−2 d−1, and subsequent slow recovery of flux after postdrought water table rise. Water table depth regulated the temperature sensitivity of methane fluxes, and this sensitivity was greatest when the water table was within 100 mm of the surface, corresponding to the shallow rooting zone of the dominant vegetation. A correlation between daytime CO2 uptake and methane fluxes emerged during times with shallow water tables, suggesting that controls on methane production were critical in determining fluxes, more so than oxidation. Water table recession through this shallow zone led to increasing methane fluxes, whereas changes in temperature during these periods were not correlated. Models of methane fluxes should consider drought-induced lags in seasonal flux recovery that depend on drought characteristics and location of the critical zone for methane production.

Species assemblage patterns around a dominant emergent tree are associated with drought resistance

Water availability has long been recognized as an important driver of species distribution patterns in forests. The conifer Agathis australis (D. Don) Lindl. (kauri; Araucariaceae) grows in the species-rich forests of northern New Zealand. It is accompanied by distinctive species assemblages, and during summer the soil beneath A. australis is often significantly drier than soils beneath surrounding broadleaved angiosperm canopy species. We used a shade house dry-down experiment to determine whether species that grow close to A. australis differed in drought tolerance physiology compared with species that rarely grow close to A. australis. Stomatal conductance (g(s)) was plotted against leaf water potential (ψ) to identify drought tolerance strategies. Seedlings of species that occur in close spatial association with A. australis (including A. australis seedlings) were most resistant to drought stress, and all displayed a drought avoidance strategy of either declining gs to maintain ψ or simultaneous declines in g(s) and ψ. The species not commonly occurring beneath A. australis, but abundant in the surrounding forest, were the most drought-sensitive species and succumbed relatively quickly to drought-induced mortality with rapidly declining gs and ψ values. These results were confirmed with diurnal measurements of g(s) and assimilation rates throughout the day, and leaf wilting analysis. We conclude that the varied abilities of the species to survive periods of drought stress as seedlings shapes the composition of the plant communities beneath A. australis trees. Furthermore, forest diversity may be impacted by climate change as the predicted intensification of droughts in northern New Zealand is likely to select for drought-tolerant species over drought-intolerant species.

Variation in carbon content and size in developing fruit of Actinidia deliciosa genotypes.

This study identifies the developmental processes contributing to variation in green-fleshed kiwifruit (Actinidia deliciosa (A. Chev.) C.F. Liang et A.R. Ferguson var. deliciosa) fruit dry matter content (DM) and fresh weight (FW) by comparing genotypes with either high or low final DM. Results are compared with the model for fruit development, the tomato (Solanum lycopersicum L.). Differences in final composition were attributable to a higher rate of starch accumulation from 70 days after anthesis in high DM genotypes, with no other consistent differences in accumulation of soluble sugars or organic acids. High DM genotypes had 70% higher starch content and differed from low DM genotypes in the allocation of carbon between storage and other components. DM was negatively correlated with final fruit FW only in high DM genotypes, whereas starch was a constant proportion of dry weight (DW), suggesting a dilution effect rather than an interaction between fruit size and carbohydrate metabolism. Compared with tomato, the organic acids, particularly quinic acid, contributed more to estimated osmotic pressure during growth in FW than the soluble sugars, regardless of final composition or size. Seed mass per unit FW was highest in high DM genotypes, suggesting a previously unrecognised role for kiwifruit seeds in accumulation of carbohydrate by the pericarp. Anatomical comparisons also identified a role for differences in the packing of the two principal cell types, with an increased frequency of the larger cell type correlated with reduced DM. These genotypes demonstrate that kiwifruit differs from tomato in the role of starch as the principal stored carbohydrate, the reduced importance of dilution by growth in FW and the more minor role of the sugars compared with the organic acids during fruit development.