John S. Boyer

Plant Productivity and Environment

An analysis of major U.S. crops shows that there is a large genetic potential for yield that is unrealized because of the need for better adaptation of the plants to the environments in which they are grown. Evidence from native populations suggests that high productivity can occur in these environments and that opportunities for improving production in unfavorable environments are substantial. Genotypic selection for adaptation to such environments has already played an important role in agriculture, but the fundamental mechanisms are poorly understood. Recent scientific advances make exploration of these mechanisms more feasible and could result in large gains in productivity.

Osmotic adjustment and the inhibition of leaf, root, stem and silk growth at low water potentials in maize

The expansion growth of plant organs is inhibited at low water potentials (Ψw), but the inhibition has not been compared in different organs of the same plant. Therefore, we determined elongation rates of the roots, stems, leaves, and styles (silks) of maize (Zea mays L.) as soil water was depleted. The Ψw was measured in the region of cell expansion of each organ. The complicating effects of transpiration were avoided by making measurements at the end of the dark period when the air had been saturated with water vapor for 10 h and transpiration was less than 1% of the rate in the light. Growth was inhibited as the Ψw in the region of cell expansion decreased in each organ. The Ψw required to stop growth was-0.50,-0.75, and-1.00 MPa, in this order, in the stem, silks, and leaves. However, the roots grew at these Ψw and ceased only when Ψw was lower than-1.4 MPa. The osmotic potential decreased in each region of cell expansion and, in leaves, roots and stems, the decrease was sufficient to maintain turgor fully. In the silks, the decrease was less and turgor fell. In the mature tissue, the Ψw of the stem, leaves and roots was similar to that of the soil when adequate water was supplied. This indicated that an equilibrium existed between these tissues, the vascular system, and the soil. At the same time, the Ψw was lower in the expanding regions than in the mature tissues, indicating that there was a Ψw disequilibrium between the growing tissue and the vascular system. The disequilibrium was interpreted as a Ψw gradient for supplying water to the enlarging cells. When water was withheld, this gradient disappeared in the leaf because Ψw decreased more in the xylem than in the soil, indicating that a high flow resistance had developed in the xylem. In the roots, the gradient did not decrease because vascular Ψw changed about the same amount as the soil Ψw. Therefore, the gradient in Ψw favored water uptake by roots but not leaves at low Ψw. The data show that expansion growth responds to low Ψw differently in different growing regions of the plant. Because growth depends on the maintenance of turgor for extending the cell walls and the presence of Ψw gradients for supplying water to the expanding cells, several factors could have been responsible for these differences. The decrease of turgor in the silks and the loss of the Ψw gradient in the leaves probably contributed to the high sensitivity of these organs. In the leaves, the gradient loss was so complete that it would have prevented growth regardless of other changes. In the roots, the maintenance of turgor and Ψw gradients probably allowed growth to continue. This difference in turgor and gradient maintenance could contribute to the increase in root/shoot ratios generally observed in water-limited conditions.

Sugar Input, Metabolism, and Signaling Mediated by Invertase: Roles in Development, Yield Potential, and Response to Drought and Heat

Invertase (INV) hydrolyzes sucrose into glucose and fructose, thereby playing key roles in primary metabolism and plant development. Based on their pH optima and sub-cellular locations, INVs are categorized into cell wall, cytoplasmic, and vacuolar subgroups, abbreviated as CWIN, CIN, and VIN, respectively. The broad importance and implications of INVs in plant development and crop productivity have attracted enormous interest to examine INV function and regulation from multiple perspectives. Here, we review some exciting advances in this area over the last two decades, focusing on (1) new or emerging roles of INV in plant development and regulation at the post-translational level through interaction with inhibitors, (2) cross-talk between INV-mediated sugar signaling and hormonal control of development, and (3) sugar- and INV-mediated responses to drought and heat stresses and their impact on seed and fruit set. Finally, we discuss major questions arising from this new progress and outline future directions for unraveling mechanisms underlying INV-mediated plant development and their potential applications in plant biotechnology and agriculture.

Osmoregulation, solute distribution, and growth in soybean seedlings having low water potentials.

Soybean (Glycine max (L.) Merr.) seedlings osmoregulate when the supply of water is limited around the roots. The osmoregulation involves solute accumulation (osmotic adjustment) by the elongating region of the hypocotyls. We investigated the relationship between growth, solute accumulation, and the partitioning of solutes during osmoregulation. Darkgrown seedlings were transplanted to vermiculite containing 1/8 (0.13 x) the water of the controls. Within 12–15 h, the osmotic potential of the elongating region had decreased to-12 bar, but it was-7 bar in the controls. This osmoregulation involved a true solute accumulation by the hypocotyls, since cell volume and turgor were virtually the same regardless of the water regime. The hypocotyls having low water potentials elongated slowly but, when deprived of their cotyledons, did not elongate or accumulate solute. This result indicated a cotyledonary origin for the solutes and a dependence of slow growth on osmotic adjustment. The translocation of nonrespired dry matter from the cotyledons to the seedling axis was unaffected by the availability of water, but partitioning was altered. In the first 12 h, dry matter accumulated in the elongating region of the 0.13 x hypocotyls, and osmotic adjustment occurred. The solutes involved were mostly free amino acids, glucose, fructose, and sucrose, and these accounted for most of the increased dry weight. After osmotic adjustment was complete, dry matter ceased to accumulate in the hypocotyls and bypassed them to accumulate in the roots, which grew faster than the control roots. The proliferation of the roots resulted in an increased root/shoot ratio, a common response of plants to dry conditions.Osmotic adjustment occurred in the elongating region of the hypocotyls because solute utilization for growth decreased while solute uptake continued. Adjustment was completed when solute uptake subsequently decreased, and uptake then balanced utilization. The control of osmotic adjustment was therefore the rate of solute utilization and, secondarily, the rate of solute uptake. Elongation was inhibited by unknown factors(s) despite the turgor and substrates associated with osmotic adjustment. The remaining slow elongation depended on osmotic adjustment and represented some optimum between the necessary inhibition for solute accumulation and the necessary growth for seedling establishment.

CO2 and Water Vapor Exchange across Leaf Cuticle (Epidermis) at Various Water Potentials

Cuticular properties affect the gas exchange of leaves, but little is known about how much CO2 and water vapor cross the cuticular barrier or whether low water potentials affect the process. Therefore, we measured the cuticular conductances for CO2 and water vapor in grape (Vitis vinifera L.) leaves having various water potentials. The lower leaf surface was sealed to force all gas exchange through the upper surface, which was stoma-free. In this condition both gases passed through the cuticle, and the CO2 conductance could be directly determined from the internal mole fraction of CO2 near the compensation point, the external mole fraction of CO2, and the CO2 flux. The cuticle allowed small amounts of CO2 and water vapor to pass through, indicating that gas exchange occurs in grape leaves no matter how tightly the stomata are closed. However, the CO2 conductance was only 5.7% of that for water vapor. This discrimination against CO2 markedly affected calculations of the mole fraction of CO2 in leaves as stomatal apertures decreased. When the leaf dehydrated, the cuticular conductance to water vapor decreased, and transpiration and assimilation diminished. This dehydration effect was largest when turgor decreased, which suggests that cuticular gas exchange may have been influenced by epidermal stretching.

Stress Physiology and the Distribution of Plants

C. B. Osmond is a professor in the Department of Environmental Biology, Australian National University in Canberra City, Australia, and formerly was director of the Biological Sciences Center, Desert Research Institute, University of Nevada, Reno, NV 89506. M. P. Austin is a visiting fellow in the Department of Environmental Biology, Australian National University, Canberra City, Australia. J. A. Berry is a faculty member in the Department of Plant Biology, Carnegie Institution of Washington, Stanford, CA 94305. W. D. Billings is a professor in the Department of Botany, Duke University, Durham, NC 27706. J. S. Boyer is a professor in the Department of Soil and Crop Sciences, Texas A & M University, College Station, TX 77843-2474. J. W. H. Dacey is an associate scientist in the Department of Biology, Woods Hole Oceanographic Institution, Woods Hole, MA 02543. P. S. Nobel is a professor in the Department of Biology, University of California, Los Angeles, CA 90024. S. D. Smith is an assistant research professor at the Department of Biological Sciences, University of Nevada, Las Vegas, NV 89514. W. E. Winner is an assistant professor and director of the Laboratory of Air Pollution, Department of Plant Pathology and Physiology, Virginia Polytechnic Institute and State University, Blacksburg, VA 24061. ? 1987 American Institute of Biological Sciences. Nearly every perturbation of a plant community results in stress

Sensitivity of cell division and cell elongation to low water potentials in soybean hypocotyls

SummaryThe response of cell division and cell elongation to low cell water potentials was studied in etiolated, intact soybean hypocotyls desiccated either by withholding water from seedlings or by subjecting hypocotyls to pressure. Measurements of hypocotyl water potential and osmotic potential indicated that desiccation by withholding water resulted in osmotic adjustment of the hypocotyls so that turgor remained almost constant. The adjustment appeared to involve transport of solutes from the cotyledons to the hypocotyl and permitted growth of the seedlings at water potentials which would have been strongly inhibitory had adjustment not occurred. Growth was ultimately inhibited in hypocotyls due to inhibition of cell division and cell elongation to a similar degree. The inhibition of cell elongation appeared to result from a change in the minimum turgor necessary for growth. On the other hand, when intact hypocotyls were exposed to pressure for 3 h, osmotic adjustment did not occur, turgor decreased, and the sensitivity of growth to low cell water potentials increased, presumably due to inhibition of cell elongation. Thus, although cell division was sensitive to low cell water potentials in soybean hypocotyls, cell elongation had either the same sensitivity or was more sensitive, depending on whether the tissue adjusted osmotically. Osmotic adjustment of hypocotyls may represent a mechanism for preserving growth in seedlings germinating in desiccated soil.

Mycorrhizal Enhancement of Water Transport in Soybean

Mycorrhizae produced by Endogone mosseae decrease the resistance to water transport in soybean (Glycine max L.). The decrease was associated with an increase in the growth of shoots but not of roots.

Control of the rate of cell enlargement: Excision, wall relaxation, and growth-induced water potentials

A new guillotine thermocouple psychrometer was used to make continuous measurements of water potential before and after the excision of elongating and mature regions of darkgrown soybean (Glycine max L. Merr.) stems. Transpiration could not occur, but growth took place during the measurement if the tissue was intact. Tests showed that the instrument measured the average water potential of the sampled tissue and responded rapidly to changes in water potential. By measuring tissue osmotic potential (Ψs), turgor pressure (Ψp) could be calculated. In the intact plant, Ψs and Ψp were essentially constant for the entire 22 h measurement, but Ψs was lower and Ψp higher in the elongating region than in the mature region. This caused the water potential in the elongating region to be lower than in the mature region. The mature tissue equilibrated with the water potential of the xylem. Therefore, the difference in water potential between mature and elongating tissue represented a difference between the xylem and the elongating region, reflecting a water potential gradient from the xylem to the epidermis that was involved in supplying water for elongation. When mature tissue was excised with the guillotine, Ψs and Ψp did not change. However, when elongating tissue was excised, water was absorbed from the xylem, whose water potential decreased. This collapsed the gradient and prevented further water uptake. Tissue Ψp then decreased rapidly (5 min) by about 0.1 MPa in the elongating tissue. The Ψp decreased because the cell walls relaxed as extension, caused by Ψp, continued briefly without water uptake. The Ψp decreased until the minimum for wall extension (Y) was reached, whereupon elongation ceased. This was followed by a slow further decrease in Y but no additional elongation. In elongating tissue excised with mature tissue attached, there was almost no effect on water potential or Ψp for several hours. Nevertheless, growth was reduced immediately and continued at a decreasing rate. In this case, the mature tissue supplied water to the elongating tissue and the cell walls did not relax. Based on these measurements, a theory is presented for simultaneously evaluating the effects of water supply and water demand associated with growth. Because wall relaxation measured with the psychrometer provided a new method for determining Y and wall extensibility, all the factors required by the theory could be evaluated for the first time in a single sample. The analysis showed that water uptake and wall extension co-limited elongation in soybean stems under our conditions. This co-limitation explains why elongation responded immediately to a decrease in the water potential of the xylem and why excision with attached mature tissue caused an immediate decrease in growth rate without an immediate change in Ψp

Conceptual framework for drought phenotyping during molecular breeding

Drought is a major threat to agricultural production and drought tolerance is a prime target for molecular approaches to crop improvement. To achieve meaningful results, these approaches must be linked with suitable phenotyping protocols at all stages, such as the screening of germplasm collections, mutant libraries, mapping populations, transgenic lines and breeding materials and the design of OMICS and quantitative trait loci (QTLs) experiments. Here we present a conceptual framework for molecular breeding for drought tolerance based on the Passioura equation of expressing yield as the product of water use (WU), water use efficiency (WUE) and harvest index (HI). We identify phenotyping protocols that address each of these factors, describe their key features and illustrate their integration with different molecular approaches.