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Root Water Uptake and Transport: Using Physiological Processes in Global Predictions

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Root Water Uptake and Transport: Using Physiological Processes in Global Predictions trends in plant science Perspectives with cDNA from the Arabidopsis aquaporin Root water uptake and AthPIP1a gene, an abundant transcript fluctu- ated in a pattern that closely resembled the diurnal variation in root hydraulic conductiv- transport: using physiological ity12. Studies of the importance of aquaporins for whole-plant water transport are needed, especially for woody plants, but it is clear that processes in global aquaporins help to orchestrate water move- ment within the plant and that they might determine the balance between apoplastic and predictions symplastic (cell-to-cell) water movement. Many other potential roles remain untested Robert B. Jackson, John S. Sperry and Todd E. Dawson (e.g. whether they facilitate embolism repair13). A second application is a new ability to Plant water loss, regulated by stomata and driven by atmospheric demand, identify roots in the field using molecular cannot exceed the maximum steady-state supply through roots. Just as an tools9–11. Unlike shoots, which can easily be electric circuit breaks when carrying excess current, the soil–plant continuum matched to a specific plant, roots growing in breaks if forced to transport water beyond its capacity. Exciting new molecular, a community are difficult to identify at any biophysical and ecological research suggests that roots are the weakest link taxonomic level, especially fine roots that take along this hydraulic flow path. We attempt here to predict rooting depth and water up water. A new method (Fig. 1) overcomes uptake using the hydraulic properties of plants and the soil, and also to suggest this long-standing limitation by using DNA how new physiological tools might contribute to larger-scale studies of hydraulic sequence variation of the internal transcribed lift, the water balance and biosphere–atmosphere interactions. spacer (ITS), the 18S–26S nuclear ribosomal repeat. The ITS region can be amplified in all lants use water in biochemical reactions, controls of water loss. We examine new mol- plants by using PCR and a set of universal as a solvent and to maintain turgor, but ecular and physiological tools that should help primers14. It evolves fairly rapidly and there- Pmost of the water taken up by plants is to predict the quantity and depth of water use fore can be used to distinguish genera and, transpired to the atmosphere. Globally, plants at larger scales, present a set of predictions for often, species. Such identifications are needed recycle more than half of the ~110 000 km3 yr21 rooting depth that can be tested at scales from for in situ physiological studies and for deter- of precipitation that falls on land each year1. the individual site to the globe, and discuss mining belowground community structure Transpired water moves from soil to plant to potential links between plant biology and the and water uptake at depth9. GenBank now has atmosphere along a continuum of increasingly physical sciences using new global datasets. .9000 ITS sequences online and is growing negative water potential (c), flowing ‘down- rapidly. Extensions of these techniques are hill’ thermodynamically but ‘uphill’ physi- Applying molecular tools to a global also being made for fingerprinting roots (to cally from root to shoot. problem distinguish individual plants within a commu- Plant water loss is a function of stomatal Two recent applications of molecular biology nity). Candidates include randomly amplified conductance and atmospheric demand but, to should contribute to a better understanding of polymorphic DNA, inter-simple-sequence avoid desiccation, it also cannot exceed the rooting depth and water transport: molecular repeats and amplified fragment-length poly- maximum supply rate through roots. In the- studies of plant aquaporins7,8 and the use of morphisms. Such molecular tools should be ory, maximum steady-state supply rates can molecular tools for identifying and studying useful in determining the zone of water uptake be predicted from field data and from trans- roots in the field9–11. Aquaporins are mem- for individual plants and species. They also port models that incorporate soil porosity, pro- brane water-channel proteins that facilitate open new possibilities for in situ studies of files of soil moisture and root density, and the water movement along a passive gradient in c plant physiological and community processes. relationship between whole-plant hydraulic (Ref. 8). In Arabidopsis, .30 genes code for conductance (K) and c (Ref. 2). In practice, aquaporin homologs and cells generally Hydraulic architecture and water flux in such supply rates are difficult to estimate express several different aquaporins at a time. stems and roots because of the challenges of sampling roots Although aquaporins are undoubtedly impor- Stomata are the pressure regulators of the and the soil at depth, and of measuring in situ tant for cytosolic osmoregulation, inhibition plant: they prevent xylem pressure and tissue root activity. New advances are helping to studies in vivo and studies with antisense water status from reaching damaging values integrate the above- and below-ground func- mutants indicate that they are also important by regulating water flow through the tioning of plants (e.g. determining hydraulic for bulk water flow. soil–plant continuum. For this reason, factors limitations along the entire plant flow path and Arabidopsis plants transformed with an that influence the hydraulic conductance of signals that coordinate hydraulic supply3), and antisense construct of the aquaporin PIP1b the continuum (‘hydraulic architecture’) also to understand biosphere–atmosphere interac- gene (one of a class of plasma membrane influence stomatal conductance and transpi- tions (e.g. feedbacks between vegetation and intrinsic proteins) had reduced steady-state ration. This is true regardless of the mecha- climate through water uptake, transpiration levels of PIP1b, water permeability coeffi- nism by which stomata sense water status, a and latent heat fluxes4–6). cients that were three times lower than in con- subject of continued investigation involving This article highlights recent progress in trol plants and five times more root biomass the hormone abscisic acid (ABA) and other understanding the movement of water in the than control plants to compensate for reduced messengers15. Recent studies highlight the soil–plant–atmosphere continuum at a range aquaporin abundance (shoot biomass and importance of xylem cavitation, xylem anatomy of increasing scales. We emphasize root water morphology were unchanged)7. In studies and the architecture of the root system in influ- uptake and transport as the gateway for plant with Lotus japonicus, root hydraulic conduc- encing leaf water supply and plant water use. water supply, complementing traditional tivity varied fivefold during day–night cycles. According to the cohesion–tension theory, emphases on shoot processes and stomatal When mRNAs from the roots were probed capillary forces generated by evaporation 482 November 2000, Vol. 5, No. 11 1360 - 1385/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S01360-1385(00)01766-0 trends in plant science Perspectives Roots from 7 m depth showed approximately one-third cavitation at 22 MPa, but the same Identifying roots using ITS ...GATTACA... degree of cavitation did not occur until approximately 26 MPa in shallow roots and ITS library 210 MPa in shoots (Fig. 2d). Differences in ...TTGTGAC...* vulnerability to cavitation were accompanied ...TTGTGAC... by gradients in xylem tracheid diameters. Mean conduit diameters were more than four ...AGAGACC... times as large in deep roots as in stems of sim- ilar size and were intermediate in shallow n o g i t n roots (Fig. 2e). Such studies illustrate the con- i a c c i tribution that deep roots can make to whole- n f i e l u plant water use and highlight the need to p q m e integrate physiological limits along the entire a s plant flow path. The results also emphasize the R S C T I importance of root hydraulic architecture for P d n water uptake at a range of depths. a DNA extraction Linking plant, soil and climate using transport models In the same way that the specifications of an Unknown root electronic device must match those of the incoming current for optimal performance, the hydraulic properties of a plant should be com- patible with the soil properties to optimize Fig. 1. Identification of roots to species using DNA sequences from the internal transcribed 2,25 spacer (ITS) region of the 18S–26S nuclear ribosomal DNA repeat9,11. The asterisk desig- water use and resource allocation . Process nates a correct match between a root ITS sequence and a shoot sequence for a candidate models of the soil–plant–atmosphere contin- species in the reference database. Extensions of such molecular techniques to distinguish uum can integrate plant architectural and roots of individual plants are also expected. This technique has been used to study plant hydraulic properties with soil properties to community structure and water uptake to 25 m depth9 . predict these optimal combinations and the actual water use for various plant functional types and soils4. from leaves move water from soil to root to radius of xylem conduits19. Flow is generally We illustrate this approach here, using a leaf under increasingly negative pressures. more efficient in longer conduits because model that is unusual because it incorporates However, because xylem water is under ten- water passes through fewer pit membranes, variable K properties within both plant and sion, conduits can cavitate (fill with air). which restrict flow. Studies comparing xylem soil25,26. At each time step, the model deter- Recent studies comparing the vulnerability of anatomy in roots and shoots have shown that mines the gradient in c along the flow path roots and shoots have shown that roots (espe- roots typically have longer and larger con- from bulk soil to leaves and c-dependent cially small roots) are typically more vulner- duits20. Although little is known about the changes in K.
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