REVIEW

Irradiance-induced changes in hydraulic architecture1

Uwe G. Hacke

Abstract: The ability to acclimate to a range of light regimes is important, given that shady understory habitats can receive onlya fraction of the light available at the top of the canopy. Sun and shade leaves are known to differ in their set of biochemical andmorphological characteristics. In recent years, much has also been learned about the effect of shade on xylem structure andfunction. Several studies found that shaded plants had narrower xylem conduits than plants growing in full sun. Among themost notable responses induced by shade is a shift of xylem vulnerability to cavitation. Shaded plants are typically morevulnerable to cavitation than plants exposed to full light. This appears to coincide with the construction of weaker intervesseland intertracheid pit membranes in shade. Before entering and after exiting the xylem, water moves through living cells in rootsand leaves, respectively. This nonvascular pathway can be modified by aquaporins. Rapid changes in root and leaf hydraulicconductance in response to changes in light and transpirational demand have been described. The role of aquaporins in theseresponses is discussed.

Key words: aquaporins, hydraulic conductivity, light level, vascular cambium, wood formation, xylem.

Résumé : La capacité d’adaptation a une gamme de régimes lumineux est importante, étant donné que les habitats ombragés ensous-étages peuvent recevoir seulement une fraction de la lumière disponible au dessus de la canopée. On sait que l’ensemble descaractéristiques biochimiques et morphologiques différent entre les feuilles de lumière et d’ombre. Au cours des récentesannées, on a également beaucoup appris au sujet de l’effet de l’ombre sur la structure et le fonctionnement du xylème. Plusieursétudes ont révélé que chez les plantes ombragées le xylème possède des conduits plus étroits que les plantes de pleine lumière.Parmi les réactions les plus remarquables causées par la lumière on note une tendance accrue de la vulnérabilité du xylème a lacavitation. Les plantes ombragées sont typiquement plus vulnérables a la cavitation que les plantes exposées a la pleine lumière.Il semble que ceci coïncide avec la construction de membranes de perforation entre vaisseaux et entre trachéides plus faibles enposition ombragée. Avant l’entrée et après la sortie du xylème, l’eau se déplace via des cellules vivantes dans les racines et lesfeuilles, respectivement. Les aquaporines peuvent modifier ces cheminements non vasculaires. On a décrit les changementsrapides de la conductance hydraulique des racines et des feuilles en réaction aux changements de la luminosité et de la demandede transpiration. L’auteur discute le rôle des aquaporines dans ces réactions. [Traduit par la Rédaction]

Mots-clés : aquaporines, conductivité hydraulique, degré de luminosité, cambium vasculaire, formation du bois, xylème.

IntroductionLight interception and hydraulics are two of the principal veg-

etative functions that must be performed by plants (Niklas 1992).Light has a profound effect on plant morphology and function(Lo Gullo et al. 2010; Walters and Reich 1999). Differences in lightlevel can induce phenotypic plasticity in terms of biomassallocation, leaf morphology, and other plant traits (Schultz andMatthews 1993; Valladares et al. 2000). Plants growing in the un-derstory usually experience reduced evaporative demand (Bladonet al. 2006), which is paralleled by a decreased need for watertransport. In addition, carbon resources tend to be more limitedin shaded plants. As a result, the hydraulic architecture of shadedplants is likely to be altered in multiple ways.

The hydraulic architecture of a tree may be described by thepattern of hydraulic conductances throughout the crown of a tree(Tyree and Zimmermann 2002). In this review, the term “hydrau-lic architecture” is defined rather loosely so that it also includesthe nonvascular pathway for water. Before entering the xylem inroots, and after exiting the xylem conduits in leaf veins, waterflows through living cells. The nonvascular pathway involves thepassage of the root endodermis and the bundle sheath of leaves.Flow through these cells is modified by aquaporins, and root and

leaf hydraulic conductance can change rapidly in response to en-vironmental conditions (Heinen et al. 2009; Laur and Hacke 2013;Sakurai-Ishikawa et al. 2011).

The first part of this review considers irradiance-driven changesin xylem structure and function. The second part focuses on aqua-porins in roots and leaves, and how they respond to changes inlight level.

Leaf-specific conductivityA study comparing hydraulic traits of four conifer species grow-

ing in full sun versus in a shaded understory environment foundthat leaf-specific xylem conductivity (KL) was lower in understoryconifers (Schoonmaker et al. 2010). The KL is equal to the hydraulicconductivity of a stem segment divided by the leaf area distal tothe segment. It is a measure of the “sufficiency” of the segment tosupply water to leaves (Tyree and Zimmermann 2002).

Lower KL values in plants growing in shade have also beenfound in other studies (Barigah et al. 2006; Plavcová et al. 2011;Schultz and Matthews 1993; Shumway et al. 1993). A large totalleaf area in shade is desirable to capture more light. Moreover, inthe absence of water stress, shaded plants can maintain large leaf

Received 8 August 2013. Accepted 28 October 2013.

U.G. Hacke. Department of Renewable Resources, 442 Earth Sciences Building, University of Alberta, Edmonton, AB T6G 2E3, Canada.E-mail for correspondence: uwe.hacke@ualberta.ca.1This paper is part of a Special Issue entitled “New Frontiers in Tree Biology”.

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Botany 92: 437–442 (2014) dx.doi.org/10.1139/cjb-2013-0200 Published at www.nrcresearchpress.com/cjb on 31 October 2013.

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areas even with smaller xylem areas and lower xylem transportefficiency (Plavcová et al. 2011; Schultz and Matthews 1993).

However, the strategy of shifting allocation from hydraulics toleaf area and light interception is not without risk. If xylempressure decreases as a result of increased evaporative demand(e.g., via the formation of a canopy gap) or soil drought, watersupply to the leaves may be insufficient, possibly resulting in stomatalclosure, elevated levels of xylem embolism, and leaf loss. Whenstomata of shaded branches close during periods of water stress tominimize embolism levels, photosynthesis and carbon fixationare also reduced. As a result, there may not be enough carbon tosustain respiration, and shaded branches could become a carbonsink (Protz et al. 2000). Moreover, coping with an increased evap-orative demand would usually require a shift of biomass alloca-tion to roots and the production of new xylem in the medium tolong term (Barigah et al. 2006), and these growth requirementsseem incompatible with prolonged stomatal closure.

Xylem anatomyThe xylem of trees probably accounts for over 99% of the total

length of the flow path from root tips to evaporating surfaces inthe leaf. Profound changes in xylem anatomical traits have beenreported in response to different light levels. Studying leaf xylem,Nardini et al. (2005) found that leaves of sun-adapted species hadwider xylem conduits than species adapted to shady habitats, aswell as larger vein densities. The authors concluded that sun-adapted species have developed a highly efficient conducting sys-tem to supply mesophyll cells with water. Within the crown ofmature beech (Fagus sylvatica L.) trees, there was variation in xylemtraits between branches exposed to full sun and shaded branchesfrom the lower canopy (Lemoine et al. 2002); sun-exposed brancheshad wider vessels than shaded branches. In hybrid poplar stems,vessels of shaded plants were narrower but longer than those ofcontrol plants (Fig. 1; Plavcová et al. 2011). Individual vessel ele-ments of shaded plants were also longer than in control plants.Further, shading resulted in significantly thinner secondary cellwalls in fibers, and this was paralleled by lower wood densities instems of shaded plants (Plavcová et al. 2011), possibly resultingfrom a reduced carbon supply.

An intriguingly complex effect of shade on xylem structure andfunction was found in conifers. In the tracheid-based xylem ofboreal spruce and pine species, the trend for narrower tracheidlumen diameters of shaded plants corresponded with higher wooddensities in stems of shaded trees (Schoonmaker et al. 2010). Tra-cheid length did not differ. Based on narrower tracheid diametersin shaded plants, one would expect to find decreased xylem trans-port capacity in understory conifers. Surprisingly, stems of shadedtrees had similar xylem transport efficiencies (expressed as xylemarea-specific conductivity, KS) as open-grown trees with wider tra-cheids. Scanning electron microscopy (SEM) micrographs re-vealed that this was probably driven by extensive changes in pitstructure (Schoonmaker et al. 2010).

Schulte (2012) recently calculated fluid flow through models oftorus-margo pits based on some of the micrographs published inSchoonmaker et al. (2010). Model results indicated that the largersize of the margo pores of shaded trees (Fig. 2) had a strong effecton the flow through the margo. For the sun pit model, the calcu-lated margo resistivity was more than twice as high as for theshade model. Only a few percent of the largest pores accounted fornearly half of the flow through the margo (Schulte 2012). Such anonlinear relationship between pore size and flow is to be ex-pected based on a predicted diameter to the third power relation-ship with flow for an isolated pore in an infinitely thin plate(Hacke et al. 2004; Schulte 2012; Vogel 2003).

Cavitation resistanceAmong the most notable phenotypic responses induced by

shade is a shift of xylem vulnerability to cavitation (Fig. 3). Shadedtrees typically have more vulnerable xylem (Barigah et al. 2006;Lemoine et al. 2002; Plavcová et al. 2011; Schoonmaker et al. 2010),although there are exceptions to this general trend (Holste et al.2006). While the mechanisms driving cavitation resistance are notcompletely understood, intervessel and intertracheid pits arethought to play an important role in preventing the spread of airfrom embolized conduits to adjacent, functional ones (Tyree andZimmermann 2002). Available evidence indicates that pit mem-brane structure may be altered by shade, and that these changesare associated with changes in cavitation resistance. The follow-ing two case studies illustrate how shade may result in the con-struction of weaker pit membranes.

Transmission electron microscopy images revealed that in-tervessel pit membranes of shaded hybrid poplar plants werethinner than in control plants, which received a higher lightlevel (Plavcová et al. 2011). The association of increased vulnera-bility with thinner pit membranes is consistent with a study on26 angiosperm species, which found correlations between pitmembrane thickness, membrane porosity, and vulnerability toair-seeding (Jansen et al. 2009). Thinner membranes may repre-sent a weaker barrier between air and water-filled vessels, althoughthe link between pit membrane thickness and porosity awaitsfurther study. Further, differences in membrane thickness are

Fig. 1. Mean hydraulic vessel diameter (a), mean vessel length (b),and mean vessel element length (c) in shaded (SH; black bars) andcontrol hybrid poplar plants (C; open bars). * and ** indicatesignificant differences at P < 0.05 and 0.01, respectively(independent two-sample t test). From Plavcová et al. (2011).

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likely related to the mechanical strength of the membrane andto the amount of deflection and enlargement of existing pores(Jansen et al. 2009).

As outlined above, shade also had a profound effect on thestructure of conifer pits (Fig. 2). Based on SEM imaging of a largenumber of pits, Schoonmaker et al. (2010) concluded that margostrands were narrower in understory conifers than in open-grownplants. This, and the fact that there were fewer margo strands inpits of understory conifers, suggests that these strands would bemore likely to tear and prevent the torus from sealing properly. Inaddition, for a given aperture size, understory black spruce (Picea

mariana (Mill.) Britton, Sterns & Poggenb.) trees had smaller torithan their open-grown counterparts. This may mean that the to-rus of shaded plants would be more easily dislodged or that it maynot completely cover the pit aperture, allowing air entry to adja-cent tracheids at less negative xylem pressure than in open-grownplants (Domec et al. 2008; Hacke et al. 2004). Overall, understoryconifers appeared to invest less carbon into torus-margo pits byproducing pit membranes with a more porous but fragile struc-ture, corresponding with relatively efficient transport but increasedxylem vulnerability.

It may also be interesting to test if and how shade affects cellwall chemistry. If lignification patterns were altered, then thismay also have an effect on water transport and vulnerability tocavitation (Voelker et al. 2011).

Cambial activity and gene expressionIrradiance-driven changes in xylem structure and function are

the result of developmental adjustments. In woody plants, theseadjustments are established as a result of altered activity of thevascular cambium. As vessel elements and fibers mature, theirdevelopment is sensitive to environmental conditions. In poplar,the type of xylem that is produced by the cambium is known todiffer in response to different levels of nutrition, water, and light(Arend and Fromm 2007; Fichot et al. 2010; Fromm 2010; Hackeet al. 2010; Harvey and van den Driessche 1997, 1999; Pitre et al.2007; Plavcová and Hacke 2012). In recent years, we have improvedour understanding of the changes in gene expression that accom-pany some of these developmental changes (Janz et al. 2012; Pitreet al. 2010). For instance, Plavcová et al. (2013) reported that threegenes encoding aquaporins of the tonoplast intrinsic protein (TIP)class were up-regulated in the cambial region of poplar plantsreceiving high levels of nitrogen. These plants exhibited en-hanced radial growth, wider vessels and fibers, as well as thinnerfiber walls than plants that only received adequate levels of ni-trogen. Water uptake is essential to drive cell expansion, and ithas been hypothesized that aquaporins play a role in xylogenesisby facilitating the flow of water into the zone of expanding cells(Groover et al. 2010; Hacke et al. 2010). Following this hypothesis,the up-regulation of the three TIPs may be linked with the widervessels found in high-nitrogen plants (Plavcová et al. 2013).

Work with the Arabidopsis model system and Populus trichocarpaTorr. & A. Gray ex Hook. showed that expression of many regula-tory and structural genes related to xylem differentiation is under

Fig. 2. Scanning electron microscopy (SEM) images of a pit membrane from a sun-grown (a) and a shade-grown (b) Picea mariana tree. Lineswere drawn along the margo strands to form polygons demarcating the pores. Scale bars = 1 �m. The sun pit was 13 �m in diameter, and theshade pit was 10 �m in diameter. From Schulte (2012); original SEM images from Schoonmaker et al. (2010).

Fig. 3. Vulnerability curves of four boreal conifer species, (a) Pinusbanksiana (Piba), (b) Pinus contorta (Pico), (c) Picea mariana (Pima), and(d) Picea glauca (Pigl). Trees were grown in an open field (open) or inan aspen-dominated understory (understory). Error bars are 1 SE.(n = 6–9). In all species, stems of shaded plants (solid circles) weremore vulnerable to cavitation than stems of open-grown trees (opencircles). From Schoonmaker et al. (2010).

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the control of NAC domain transcription factor master regulators(Ohtani et al. 2011; Yamaguchi et al. 2011; Zhong et al. 2011).

Much remains to be learned, especially with regard to how geneexpression in the cambial region relates to physiologically rele-vant traits such as cavitation resistance, vessel diameter, and vessellength. Such progress has in part been hindered by an incompleteunderstanding of the structure–function relationships that un-derlie cavitation resistance.

Aquaporin-mediated changes in root and leaf hydraulicconductance

In addition to the developmental plasticity described above,plants are able to respond to dynamic changes in light availabilityby changes in leaf and root hydraulic conductance (Almeida-Rodriguezet al. 2011; Guyot et al. 2012; McElrone et al. 2007; Sakurai-Ishikawa et al.2011). Water transport through roots and leaves involves flowthrough living cells and is therefore potentially modified by aqua-porins.

When light levels and canopy water demand increase, dynamicchanges in root and leaf hydraulic conductance may be requiredto restore the water balance at the whole plant level. Diurnalcycling of fine root hydraulic conductance has been observed in manyspecies (Clarkson et al. 2000; Henzler et al. 1999; Sakurai-Ishikawa et al.2011). However, root hydraulic conductance is not just governedby diurnal cycles, but is also impacted by environmental factors,including light. Canopy shading resulted in a strong decrease inroot hydraulic conductance in Sideroxylon lanuginosum Michx. (McElroneet al. 2007). Conversely, the hydraulic conductance of fine roots ofhybrid poplar increased significantly in response to an increase inirradiance (Almeida-Rodriguez et al. 2011).

In rice, root-specific aquaporins, such as OsPIP2;5, were stronglyinduced by transpirational demand (Sakurai-Ishikawa et al. 2011).Protein levels of root-specific aquaporins peaked 6 h after lightinitiation, while mRNA levels peaked 2 h after light initiation.Changes in fine root hydraulic conductance may occur even be-

fore a peak in protein levels is observed. This could be due togating and the assembly of PIP1-PIP2 heterotetramers in conjunc-tion with their trafficking to the plasma membrane (Maurel et al.2008; Zelazny et al. 2007).

Immunolabeling showed that OsPIP2;5 accumulated in the endoder-mis and adjacent cortex cells, as well as in cells of the vascularcylinder. Sakurai-Ishikawa et al. (2011) suggested that the rapidinduction of root aquaporin gene expression by transpirationaldemand may increase cell-to-cell water movement to sustain ahigh transpiration rate during the light period.

In another study, hybrid poplar plants were subjected to a sud-den increase in evaporative demand, either by increasing the lightlevel or by reducing the relative humidity (Laur and Hacke 2013).Both treatments led to an increase in root water flow and anincrease in the transcript abundance of aquaporin genes in roots(Fig. 4). Interestingly, root water flow increased more rapidly inplants experiencing a decrease in relative humidity than inshaded plants experiencing a sudden increase in light level. Therelatively slow response of shaded plants to increased light maybe due to the stressful growing conditions that these plants expe-rienced. Shade-grown plants were probably energy starved andmay have lacked the resources that are necessary for a rapid ex-pression and activation of aquaporins. Regardless of the reasonsfor the slower response of shaded plants, transcript levels of threePIP1 aquaporin genes closely matched trends in root water flow.

Immunolabeling revealed that PIP1 protein was present in theepidermis and cortex cells, as well as in the endodermis and invascular tissue (Laur and Hacke 2013). In situ hybridization exper-iments suggest that individual aquaporin genes may be expressedin different parts of the root cross section. While one gene, PIP2;10,was highly expressed in the vascular cylinder (Fig. 5), othersshowed higher expression in the cortex (Almeida-Rodriguez et al.2011). More in situ hybridization studies in poplar roots would be

Fig. 4. Effect of a sudden change in transpirational demand on aquaporin transcript amounts in poplar roots. Cumulative aquaporintranscript amounts in roots. Individual genes are labeled with different colours in Web version only. One subset of plants was grown atadequate light level in the growth chamber (“Light control”). Other subsets of plants were grown in shade (“Shade”) or in a humidified box at�95% relative humidity (“High RH”). Shaded plants were exposed to a �4-fold increase in light level. Gene expression was measured 4 h(“Light increase, 4 h”) and 28 h (“Light increase, 28 h”) after the increase in light level. Plants growing at high humidity were removed fromtheir humidified box and were exposed to a �4-fold increase in vapor pressure deficit while light levels remained adequate. Gene expressionwas measured 4 h and 28 h after the decrease in relative humidity. From Laur and Hacke (2013).

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useful to determine the tissue distribution of expression of keyaquaporin genes (such as those identified by Laur and Hacke 2013).

The observed responses by roots to an increase in transpira-tional demand seem to involve shoot-to-root signaling. Molecularsignaling in the phloem would provide hour-scale travel timesfrom shoot to root for most small plants (Turnbull and Lopez-Cobollo2013), but it may not be fast enough in large trees and plants withextensive and deep root systems. In addition, both electric andhydraulic signals may be involved as they have the capacity ofrapidly spreading through the plant body (Grams et al. 2007).

Leaf hydraulic conductance is also impacted by light, althoughthe leaf response to light appears to be highly variable acrossspecies. Some (but not all) species showed light enhancement ofleaf hydraulic conductance within 30 min, according to measure-ments made with a high pressure flowmeter (HPFM) (Tyree et al.2005; Voicu et al. 2008). Rockwell et al. (2011) cautioned that theexact interactions between stomata and the HPFM remain enig-matic and that the concept of aquaporin-mediated, light-inducedchanges of bulk leaf tissue conductivity requires further examina-tion. However, light enhancement of leaf hydraulic conductancewas also found when the evaporative flux method was used (Guyotet al. 2012). A recent review discusses the complex role of aqua-porins in regulating leaf hydraulic conductance in response tochanges in light level (Prado and Maurel 2013).

Many avenues for future research present themselves. For ex-ample, it would be interesting to investigate why species differ inhow leaf hydraulic conductance responds to changes in irradi-ance. New research showed that bundle sheath cells of Arabidopsisplay a key role in controlling leaf hydraulic conductance in re-sponse to stress signals (Shatil-Cohen et al. 2011); it could be testedif bundle sheath cells also play an important role in leaf responsesto changes in light level. On the xylem level, it would be useful tolearn more about the development of intervessel pit membranes,and how it is affected by genes and environment. Finally, changesin irradiance may offer an opportunity to study signaling betweenaboveground plant organs and roots.

AcknowledgementsI wish to thank Frédérique Guinel and the Canadian Botanical

Association for the opportunity to prepare this review for Botany.Work in my laboratory was funded primarily by an Alberta Inge-nuity New Faculty Award and a Natural Sciences and EngineeringResearch Council of Canada (NSERC) Discovery grant. Funding bythe Canada Research Chair program and the Canada Foundationfor Innovation is also acknowledged.

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Fig. 5. In situ mRNA hybridization of an aquaporin gene, PIP2;10,in a root cross section of hybrid poplar. Regions of aquaporinexpression are indicated by dark purple (Web version only) staining.The cross section was taken �30 mm from the root tip. Thisparticular gene was highly expressed in the vascular cylinder. Scalebar = 100 �m. From Almeida-Rodriguez et al. (2011).

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442 Botany Vol. 92, 2014

Published by NRC Research Press

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