John B. Passioura

Roots and drought resistance

Passioura, J.B., 1983. Roots and drought resistance. Agric. Water Manage., 7: 265–280. The influence of roots on the yield of water-limited crops is analysed with the help of the identity: yield = water used × water-use efficiency × harvest index Despite being severely water-stressed, many droughted crops leave substantial amounts of apparently available water in the subsoil at maturity. The factors influencing this amount are outlined, particularly those concerning the morphology of the root system. Prospects for improving yield by extracting the residual water are discussed. Because roots are difficult to harvest, water-use efficiency is usually defined as above-ground-biomass/water-used. It follows that the more assimilate a plant transfers to its roots the lower will be its water-use efficiency. There is presumably an optimal root/ shoot ratio (in terms of water relations) at which above-ground biomass is maximal for a given water supply. This ratio appears to exceed the optimum in many cases. For a given biomass, the yield of a grain crop depends in part on the pattern of water use during the season, because harvest index is often related to the proportion of the total water supply that is used after anthesis. For crops relying on a limited supply of stored water, a high axial resistance to flow in the roots may ensure that water in the subsoil is not used so quickly that too little remains at anthesis for the plants to set and fill an adequate number of grains. A breeding program aimed at changing this resistance in wheat roots is described. Finally, the principles are discussed on which physiological research can be useful in improving drought resistance. The need to dissect water-limited yield into largely independent components is emphasised, for such a dissection greatly improves the focus of the research.

Soil water status affects the stomatal conductance of fully turgid wheat and sunflower leaves

Wheat and sunflower were grown in pots that could be enclosed in a pressure chamber, with the shoot in a cuvette. Applying an appropriate pneumatic pressure to the roots enabled the leaves to be kept fully turgid despite any drying of the soil. The leaf conductance of plants was followed while the soil dried. Remarkably, this conductance fell with falling soil water content no matter whether the leaves were kept fully turgid or not. It is concluded that the roots sensed the drying of the soil and sent a message to the leaves which induced stomatal closure.

Environmental biology and crop improvement

The average yield of Australias major grain crop, wheat, rose at its fastest rate ever during the last decade. The environmental biology behind this advance was predominantly ecological and nutritional - endemic root diseases were controlled through better management of inoculum levels, and the consequently healthier crops were more responsive to fertiliser, especially nitrogen. Applying nitrogen fertilisers became less risky; farmers used much more and thereby achieved much higher yields. Despite Australias reputation for being drought prone, its crop yields have not hitherto been typically limited by water - poor health and poor nutrition have been more influential. Improvements in the management of health and nutrition have resulted in many crops now being limited by water, so the effectiveness with which that water is used in producing grain has become more important - capturing more of it, using it effectively in producing photosynthate, and ensuring that a large fraction of that photosynthate is converted into grain. Further improvement will come from the steady 1% per year achieved by breeders, overlain by agronomic advances based on deeper ecophysiological understanding of the interaction between roots and soil biota, how roots access resources in the subsoil, and the basis of spatial variation in yield across a paddock.

Improving Productivity of Crops in Water-Limited Environments

Abstract This review deals with improving the performance of dryland crops in dry, mainly semiarid, environments. Although such crops are often limited by water, the development of the notion of water-limited potential yield has shown that their yields are often limited strongly by other factors. These factors are explored by dissecting the water-limited potential yield into a framework involving four largely independent components, namely, the potential water supply for the crop; the fraction of that water supply that is transpired; the efficiency with which the crop exchanges water for CO 2 in producing biomass (Transpiration Efficiency); and the fraction of the biomass that ends up in the grain (Harvest Index). This framework is used to explore a wide range of agronomic possibilities for managing crops so as to get close to the water-limited potential, including managing previous crops, forages and fallows to increase soil water at sowing; reducing evaporative losses from the soil surface; ensuring that sowing and flowering occur at the right times; maximizing soil water extraction by the crop; and ensuring that there is adequate water available during late floral development and grain filling. Such operations often involve trade-offs and risks that must be managed.

Soil structure and plant growth: Impact of bulk density and biopores

Compacted soils are not uniformly hard; they usually contain structural cracks and biopores, the continuous large pores that are formed by soil fauna and by roots of previous crops. Roots growing in compacted soils can traverse otherwise impenetrable soil by using biopores and cracks and thus gain access to a larger reservoir of water and nutrients. Experiments were conducted in a growth chamber to determine the plant response to a range of uniform soil densities, and the effect of artificial and naturally-formed biopores. Barley plants grew best at an intermediate bulk density, which presumably represented a compromise between soil which was soft enough to allow good root development but sufficiently compact to give good root-soil contact. Artificial 3.2 mm diameter biopores made in hard soil gave roots access to the full depth of the pot and were occupied by roots more frequently than expected by chance alone. This resulted in increased plant growth in experiments where the soil was allowed to dry. Our experiments suggest that large biopores were not a favourable environment for roots in wet soil; barley plants grew better in pots containing a network of narrow biopores made by lucerne and ryegrass roots, responded positively to biopores being filled with peat, and some pea radicles died in biopores. A theoretical analysis of water uptake gave little support to the hypothesis that water supply to the leaves was limiting in either very hard or very soft soil. The net effect of biopores to the plant would be the benefits of securing extra water and nutrients from depth, offset by problems related to poor root-soil contact in the biopore and impeded laterals in the compacted biopore walls.

Hydraulic Resistance of Plants. II. Effects of Rooting Medium, and Time of Day, in Barley and Lupin

Barley and lupin plants were grown in pots designed to fit inside a pressure chamber. The pots contained sand, soil, or nutrient solution. Transpiration rates were varied over a wide range. At a given transpiration rate, Q, the balancing pressure, p, of a plant was determined; p is the pneumatic pressure that must be applied to the roots in the pressure chamber to have a cut in the xylem of the shoot on the verge of bleeding. The relation between p and Q, p(Q), was non-linear and hysteretic for solution- grown plants, but was remarkably linear for plants grown in sand or soil, i.e. the data for a given plant on a given occasion conformed closely to the equation p =po + rQ, where po and r were constants. Even though p(Q) was linear for the plants grown in sand or soil, po was often much larger than Δπ, the difference in osmotic pressure between the external solution and the xylem of the root, so that the apparent hydraulic resistance of the plants, i.e. (p-Δπ)/Q, depended strongly on Q. Furthermore, po changed diurnally and was typically 100-200 kPa higher in the afternoon than in the morning. These results are discussed in relation to the equations that are commonly used to describe water flow through plants. It is postulated that r represents the true hydraulic resistance of the plant, which is independent of Q in the plants grown in soil or sand but may vary diurnally, and that the discrepancy between po and Δπ represents either an additional and hitherto unrecognized difference in osmotic pressure across the membranes of the root that intercept the transpiration stream, or a pressure required to open valves through which the water has to pass, with the valves possibly being located in the plasmodesmata.

Phenotyping for drought tolerance in grain crops: when is it useful to breeders?

Breeding for drought tolerance in grain crops is not a generic issue. Periods of drought vary in length, timing and intensity and different traits are important with different types of drought. The search for generic drought tolerance using single-gene transformations has been disappointing. It has typically concentrated on survival of plants suffering from severe water stress, which is rarely an important trait in crops. More promising approaches that target complex traits tailored to specific requirements at the different main stages of the life of a crop, during: establishment, vegetative development, floral development and grain growth are outlined. The challenge is to devise inexpensive and effective ways of identifying promising phenotypes with the aim of aligning them with genomic information to identify molecular markers useful to breeders. Controlled environments offer the stability to search for attractive phenotypes or genotypes in a specific type of drought. The recent availability of robots for measuring large number of plants means that large numbers of genotypes can be readily phenotyped. However, controlled environments differ greatly from those in the field. Devising pot experiments that cater for important yield-determining processes in the field is difficult, especially when water is limiting. Thus, breeders are unlikely to take much notice of research in controlled environments unless the worth of specific traits has been demonstrated in the field. An essential link in translating laboratory research to the field is the development of novel genotypes that incorporate gene(s) expressing a promising trait into breeding lines that are adapted to target field environments. Only if the novel genotypes perform well in the field are they likely to gain the interest of breeders. High throughput phenotyping will play a pivotal role in this process.

Genetically Engineered Plants Resistant to Soil Drying and Salt Stress: How to Interpret Osmotic Relations?

We cal1 your attention to ”Overexpression of A’Pyrroline-5-Carboxylate Synthetase Increases Proline Production and Confers Osmotolerance in Transgenic Plants” by Kavi Kishor et al. [(1995) Plant Pkysiol. 108: 1387-13941. This is a report on a proline (Pro)-accumulating transgenic tobacco, which the authors claim expresses “osmotic adjustment” (last paragraph, p. 1393), ”osmoprotection” (abstract), and ”osmotolerance” (title). We are not aware of any accepted definitions of ”osmotolerance” and ”osmoprotection” with respect to drought. We would, however, like to address the well-defined phenomenon of osmotic adjustment, as treated in this paper. We would like to point out that the interpretation of plant water relations and osmotic adjustment in this paper is in serious error. Osmotic adjustment involves the net accumulation of solutes in a cell in response to a fall in the water potential of the cell’s environment. As a consequence of this net accumulation, the osmotic potential of the cell is lowered, which in turn attracts water into the cell and tends to maintain turgor pressure. Osmotic adjustment must be distinguished from the lowering of osmotic potentia1 (increase in solute concentration) that accompanies any loss of water from a cell, and therefore must be measured in cells of defined water status, preferably full turgor. It is totally wrong to say that osmotic adjustment ”facilitates the maintenance of osmotic potential during water stress . . . ” (p. 1390). Osmotic adjustment facilitates the maintenance of tuvgor by lowering osmotic potential. The authors compound this fallacy during their discussion of table I (p. 1391), which shows that the osmotic potential of their transgenic plants was unaffected or even perhaps increased by the stress treatment. The data show that the transgenic plants were probably even less able to adjust osmotically than were the wild-type plants. If the authors wish to claim that overexpression of Pro does confer resistance to drought or salinity through osmotic adjustment, then they must measure osmotic adjustment correctly [e.g. J.M. Morgan (1992) Aust. J. Plant Pkysiol. 19: 67-76], they must demonstrate a link between osmotic adjustment and growth under stress, and they must demonstrate that the overexpression of Pro accounts for any osmotic adjustment. The authors seem to have been so enthralled by their expectations that overexpression of Pro would enhance ”osmotolerance” that they have completely misunderstood their own data in the context of osmotic adjustment. Transgenic plants have the potential to be powerful and to aid in helping us understand and manipulate the responses of plants to stress, but they can only be so when studied with the help of a sound background in stress physiology.

Hydraulic resistance of plants. III: Effects of NaCl in barley and lupin

Barley (salt-tolerant) and white lupin (salt-sensitive) were grown in sand in pots designed to fit within a pressure chamber. The sand was irrigated with a nutrient solution to which increasing amounts of NaCl were added daily in increments of 10-25 mol m-3. For a range of transpiration rates (Q), the hydrostatic pressure of the leaf xylem sap of an intact plant was measured by applying sufficient air pressure (p) to the root system to raise the pressure of this sap to zero. The relation between p and Q was linear, i.e. of the form p = po + rQ. Po, the intercept on the p axis, reflects the difference in osmotic pressure across the root, and it is assumed that r, the slope of this relation, gives the hydraulic resistance of the plant. In NaCl-treated barley, r remained constant as the NaCl in the soil solution was increased to 200 mol m-3 over 10 days, and differed little from that of the controls. Po increased by about the same amount as the increase in osmotic pressure of the soil solution. This indicates near-perfect osmotic behaviour by the roots, and consistent with this, osmotic pressure of sap expressed from the cut shoot base generally changed little with increasing NaCl, for a given transpiration rate. In NaCl-treated lupin, by contrast, r increased continually from 25 to 150 mol m-3 NaCI, when it was four times that of the controls. Beyond 75 mol m-3, po increased less than increases in the osmotic pressure of the soil solution, which suggests that salts were then leaking into the root xylem. However, the osmotic pressure of the xylem sap flowing through the petiole did not start to increase until 3 days later when the external solution was over 120 mol m-3, suggesting that substantial amounts of NaCl were being removed from the xylem sap before it reached the petiole.

Rapid environmental changes that affect leaf water status induce transient surges or pauses in leaf expansion rate.

We subjected wheat and barley plants to rapid environmental changes, and monitored leaf elongation rates for several hours thereafter. Changes in light, humidity or salinity caused sudden rises (if the leaf water status rose) or falls (if the leaf water status fell) in leaf elongation rate, followed by a recovery phase that lasted 20–60 min. After a step change in light or humidity, the growing leaf eventually resumed its original elongation rate, although the shoot water status, as monitored by leaf thickness, differed markedly. Salinity, on the other hand, produced a persistent change in leaf elongation rate, which settled down to a lower steady rate after the transient response was over. To determine whether the sudden changes in leaf elongation rate were due to changes in leaf water relations, we kept shoots fully hydrated through the environmental changes by automatically pressurising the roots to maintain leaf xylem on the point of bleeding. This annulled the environmental effects on leaf water status, and thereby largely removed the changes in leaf elongation rate. The only exception was at the dark:light transition, when the leaf elongation rate of pressurised plants rose sharply (in contrast to that of unpressurised plants, which fell), then underwent damped oscillations before settling at about its initial value. The sudden excursions of leaf growth in unpressurised plants accompanying the environmental changes were undoubtedly due to changes in leaf water status. The subsequent, generally complete, return of the leaf elongation rate to its initial value within an hour, despite the persistent change in leaf water status, suggests that a control system is operating at a time scale of tens of minutes that eventually overrides, partially or completely, the rapid effects of changes in leaf water status.