There is abundant evidence which shows that, in cereal grains, the most sensitive portion of the life cycle to drought is the stage of floral develop- ment and flowering (Salter and Goode, 1967). Desiccation at this time frequently causes a reduction in the number of seeds set by the plant, and even if a subsequent improvement in water availability occurs, yield re- mains depressed. In maize, for example, experiments involving short expo- sures to desiccation resulted in the largest yield reduction when desiccation occurred during pollen shed (Claassen and Shaw, 1970a,b). There was little overall effect on dry matter production by the plant, and the stalk contained the dry matter that would have been destined for the grain.
Slatyer ( 1969), in an excellent review, points out that there are at least three kinds of effects which result in fewer seeds developing when desicca- tion occurs during flowering. First, the development of the floral primordia may be retarded (Husain and Aspinall, 1970). Second, the egg cell within the embryo sac may abort (Moss and Downey, 1971) or pollen develop- ment may be delayed (Salter and Goode, 1967). Third, the extension of the stamens and styles of the flower or of the pollen tube may be retarded.
Any of these factors could prevent fertilization.
In spite of the large effects of desiccation during floral development and pollination, the physiological factors that are responsible are the least un- derstood of any in the life cycle of the plant. The floral primordia represent centers of intense metabolic activity and, consequently, they are large sinks for photosynthate. Perhaps the reduced supply of photosynthetic products to the sink results in retarded cell division and/or eventual death of certain cells (Husain and Aspinall, 1970). On the other hand, desiccation may have an effect on some essential hormonal or metabolic event in the devel- oping promordia themselves which leads to these kinds of effects.
Ill. Improvement of Drought Response through Breeding and Management
Four points of importance emerge from the foregoing. First, adaptation to dry conditions can significantly improve yield during desiccation. The adaptation so far reported has mostly taken the form of avoidance rather than a change in physiological tolerance to drought.
Second, the various physiological processes contributing to grain yield vary markedly in their susceptibility to drought. For example, cell elonga- tion is affected by quite normal diurnal fluctuations in plant water status, while net photosynthesis requires considerably greater desiccation, and translocation is even less sensitive. The implications of this extend beyond
18 J . S. BOYER AND H. G. MCPHERSON
the breeding and management of cereal crops themselves. For example, the effect of desiccation in crops where the economic yield is vegetative is likely to be greater than in grain producing crops during the grain-filling stage.
Third, the availability of previously accumulated reserves can substan- tially protect yield during desiccation. They may also represent a potential resource for increasing yield under favorable conditions.
Fourth, the physiological factors most likely to be limiting during one part of the season may be unimportant during another part of the season.
For cereal grains, the vegetative phase of growth is probably limited more by cell enlargement than by other factors unless drought is severe. During grain development, however, grain production is probably affected most by the photosynthetic activity of the leaves. The relatively brief flowering period between these stages is important largely because of the potential for disruption of floral development, anthesis, fertilization, and the number of seeds set.
Timing, then, is very important and efforts to find superior performance of certain physiological types may be frustrated unless this is taken into account. It does little good to breed for improved photosynthetic activity, for example, if yield is limited by the effects of early drought on cell en- largement. For an environment in which drought is sporadic, the problem of timing is most difficult, as results could suggest superior performance in one season but inferior performance in another. Thus, it would seem that breeding for improved performance on the basis of field experiments will have the greatest success in those areas where drought occurs in the same part of the growing season year after year. Management, like breed- ing, will be most effective if it is based on a sound understanding of the relative timing of environmental demands and crop sensitivity. Decisions of what crop to plant in given environments, and when to irrigate, should be made against the background of such information.
Unfortunately, the improvement of plant response to drought has been rare, and the writers are aware of only one instance where selection or breeding has succeeded in improving the tolerance of crop varieties to drought (Wright and Jordan, 1970). In this instance, the selection criterion was somewhat specialized and was based on seedling survival during a drought following germination. This approach may or may not have an effect on grain production.
At this time, with our limited and inadequately integrated knowledge of plant performance under desiccating conditions, any suggestion of how to aim a plant improvement program must be tenuous at best. However, it may be helpful to speculate on the problem at this point because such speculation may provide some insight.
PHYSIOLOGY OF WATER DEFICITS IN CEREAL CROPS 19 The ability of a crop to produce a high yield of grain during a dry season probably depends on two fundamentally different phenomena, which may be thought of as drought avoidance on the one hand, and drought tolerance on the other.
Drought avoidance permits a crop to grow longer in a given environ- ment, usually because it is able to tap a larger part of the water stored in the soil (by having a more extensive and well placed root system), or because it uses less water per unit time. Water use rates can be affected both by supply and by demand. Thus, the penetration of the soil by roots and the resistance to water loss by the canopy can have effects on drought avoidance. In a pot experiment, Passioura (1972) forced wheat plants to rely entirely on one seminal root early in the season. The treatment resulted in double the amount of water being available at heading and the plants produced double the yield. Water loss by evapotranspiration from a crop can also change dramatically with changes in the canopy. Ritchie and Bur- nett ( 197 l ), for example, found that evapotranspiration was substantially below potential rates in cotton and grain sorghum until the canopies had developed a certain amount of ground cover. Kerr et al. (1973) found similar effects where the evapotranspiration of a developing maize crop with incomplete ground cover was less than half the rate of an adjacent lucerne crop. The characteristics of stomata and associated diffusive resis- tance to water loss have received considerable attention in recent years and it is well established that they play a role in regulating water loss.
The importance of these characteristics in regulating water use rates of field crops has yet to be established. However, recent work indicates that the substantial differences in diffusive resistances that occur among crops can correlate highly with measured evapotranspiration rates. Kerr et al.
(1973) found a correlation of 0.89 between measured stomatal resistance for maize, paspalum, and lucerne and the resistance to crop evapotranspira- tion based on measurements of half-hourly evapotranspiration rates.
Unfortunately, drought avoidance characters are often developed at the expense of photosynthesis. For example, delaying canopy closure reduces interception of photosynthetically active radiation and may thereby reduce rates of photosynthesis per unit ground area; stomatal closure may inhibit carbon dioxide uptake as well as water loss; and larger root systems can only be developed at the expense of top growth. It would be preferable to identify characters which would not result in a sacrifice of plant growth.
Drought tolerance is potentially more desirable from this point of view, since it would permit a crop to produce more yield at a given tissue water potential. It seems to us that there may be two possible ways of improving drought tolerance in cereal grains. The first would consist of selection for the capacity of cell elongation in seedlings that were subjected to a steady,
20 J. S. BOYER AND H. G. MCPHERSON
but suboptimal water availability. A vermiculite system similar to that used by Meyer and Boyer ( 1972) could be employed, and seedling performance could be judged by eye. Superior seedlings could be removed from the vermiculite, and planted for seed. Since screening could be based on visual criteria, large numbers of individuals could be processed rapidly. This pro- cedure would select for increased rates of cell enlargement during desicca- tion, and superior performance would result from the ability of the plant to compensate osmotically for drought. Increased growth under desiccating conditions should also select for improved rates of protein synthesis and nitrate reductase activity since these are generally positively correlated with high rates of growth. Additional benefits would be increased seedling emer- gence in dry soil and continued leaf growth during moderate drought.
There is also a possibility that elongation of stamens, styles, and possibly germination tubes of pollen grains could be enhanced if the effects of seed- ling selection carried over to flowering.
The second approach to selecting for superior performance would in- volve the growth of plants to an intermediate stage of development, perhaps with several leaves, and the imposition of a drought that could be main- tained for several days. The plants would then be rewatered and scored visually for signs of leaf senescence. Those plants that showed less senes- cence would be used as the seed source for the next generation. This level of selection should retain those plants capable of continued production, or at least those with less death of tissue, under desiccating conditions.
For cereal grains, these two levels of selection for drought tolerance might improve production in two ways: they should promote growth under moderately dry conditions and reduce the tendency for senescence (which is so characteristic of the grasses) in severe conditions. The criteria for selection are predicated on the assumption that there will be at least spo- radic increases in the availability of water and that the crop will be pro- tected by the farmer against the severest droughts. Thus, the production of leaves and the lack of loss of leaf tissue would keep the photosynthetic tissue capable of production when rain came. At the same time, of course, this represents a compromise because selection would be made against the natural tendency for the grasses to fill a small amount of grain while leaf surface senesces. The net result would be an increased production if water were restored, but an increased susceptibility to very severe droughts.
In the native environment, survival in dry conditions may require the production of a few seeds for the next growing season to ensure the con- tinuation of the species. Since desiccation can rapidly become severe and metabolic activity may be inhibited or altered at that time, the genetic mechanisms that control leaf enlargement and senescence must respond rapidly. For the plant, this means that the production of at least a few
PHYSIOLOGY OF WATER DEFICITS IN CEREAL CROPS 21 seeds is assured. Agriculturally, however, severe desiccation represents a very small percentage of the total instances of drought. Furthermore, the economic effects of drought become important long before production is reduced to a few seeds. Therefore, breeding for increased leaf growth and decreased senescence could have a positive effect on agricultural production if it reduced the effects of mild or moderate drought. Furthermore, the approach would have the advantage that it would foster high yields when water availability was high.
It has been suggested (Mederski and Jeffers, 1973) that rather than selecting for drought performance under drought conditions as proposed above, it may be possible to select under optimum growth conditions.
Mederski and Jeffers (1973) found that the yields of existing varieties of soybeans had the same rank order regardless of whether they were grown under moist or water-deficient conditions. While this may apply under some circumstances, it appears that to screen for physiological characteristics that are only called into play during drought one must select under desic- cating conditions. It must be emphasized, however, that selections for seed- ling performance, as suggested above, should be accompanied from the outset by extensive field testing and that selections that appear significant at the seedling level should be continued only if they result in a clear in- crease in grain yield.
The use of cell elongation and leaf senescence as characters for selection of superior drought performance appear to have particular usefulness in rice. Chang et al. ( 1974) have shown that rice varieties capable of growing in uplands were less subject to leaf stunting, leaf rolling, and leaf senes- cence than were the drought-sensitive lowland varieties. Deep rooting and the capacity to withstand a dry spell were correlated as well. There was less delay of heading and panicle exsertion, and spikelet fertility was higher in the upland varieties during drought. Grain yield was generally less sus- ceptible to drought in the upland varieties. These are suggestive of differ- ences in cell enlargement and leaf senescence, which reflect tolerance, but performance was also related to differences in avoidance, such as rooting depth. Thus, rice displays both kinds of response to desiccation and it should provide promising material for selecting for improved drought per- formance either in terms of tolerance or avoidance.
It is also well to note that the two-pronged approach of selecting for increased leaf growth and decreased senescence neglects one important factor: the photosynthetic activity of the leaves. The degree to which differ- ences in photosynthesis might occur in desiccated individuals of a breeding line is unknown, and the selection for less inhibition of photosynthesis would require cumbersome measurements. Nevertheless, the photosynthetic differences that were cited above for species and for different stages of
22 J . S. BOYER AND H. G. MCPHERSON
growth might extend to breeding lines, and it may eventually be worthwhile to explore this area. Attempts to surmount the measurement problems have recently been made (Nelson et al., 1974), and similar approaches may provide advances in the future.
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I.
11.
111.
IV.
BIOLOGICAL SIGNIFICANCE OF ENZYMES ACCUMULATED IN SOIL
S. Kiss, M. Dr6gan-Bularda, and D. Rddulescu
Babes-Bolyai University, Clui-Napoca, Romania
Introduction. ...
Role of Accumulated Soil Enzymes in the Initial Phases of the Decomposition of Organic Residues and of the Transformation of Some Mineral Compounds A. Carbon Cycle.. ...
B. Nitrogen Cycle.. ...
C. Phosphorus Cycle ...
D. Sulfur Cycle.. ...
Enzymatic Activities in Soil under Conditions Unfavorable for the Proliferation of Microorganisms.. ...
A. Physical Factors ...
B. Chemical Factors ...
Summary. ...
References. ...
25 27 27 38 58 64 64 64 69 16 76
I. Introduction
Enzyme activity of soil results from the activity of accumulated enzymes and from the enzymatic activity of proliferating microorganisms. By defini- tion, accumulated enzymes are regarded as enzymes present and active in a soil in which no microbial proliferation takes place. Their amount in terms of weight is very small.
Sources of accumulated enzymes are primarily the microbial cells. En- zymes in soil, however, can also originate from plant and animal residues.
Enzymes accumulated in soil are free enzymes, such as exoenzymes re- leased from living cells, endoenzymes released from disintegrated cells, and enzymes bound to cell constituents (enzymes present in disintegrating cells, in cell fragments, and in viable but nonproliferating cells). Proliferating microorganisms produce enzymes that are released into the soil, while others remain within the multiplying cells.
Free enzymes in soils are adsorbed on organic and mineral soil particles and/or complexed with humic substances. The amount of free enzymes in the soil solution should be much smaller than in the sorbed state. Cells and cell fragments also may exist in an adsorbed state or in suspension.
25
26 s. KISS, M. DRAGAN-BULARDA, AND D. RXDULESCU
In sd solution 1
In adwxbed state In suspension
I
FIG. 1. Components of the enzyme activity in soil.
Components of the enzyme activity of soil' can be classified as shown in Fig. 1 .
Activity of most soil enzymes is assayed in samples in which the prolifer- ation of microorganisms is prevented by the addition of toluene or the microorganisms are killed by irradiation with 7-rays or an electron beam.
Enzyme activity determined under these conditions is due to the accumu- lated enzymes. Dehydrogenase activity in soil is assayed without preventing microbial proliferation. Consequently, the measured activity is due to dehy- drogenases primarily of the proliferating microorganisms.
It is well known that perpetuation of life on our planet is conditioned by the mineralizing action of soil and water microorganisms on the plant and animal residues. It is also well known that the mineralizing action of microorganisms is inseparably related to the activity of enzymes. However, do the enzymes accumulated in soil play a role in decomposition and min- eralization processes, or are these processes attributable exclusively to the proliferating microorganisms? In other words, do the accumulated soil en- ' Presumably, the enzyme activity of water and mud comprises the same compo- nents as that of the soil. It is worth noting in this respect that free, dissolved enzymes (invertase, amylase, cellulase, lipase, protease, phosphatase) have been found in lake waters (Steiner, 1938; Overbeck and Babenzien, 1963, 1964; Reichardt ef al., 1967;
Berman, 1969, 1970; Jones, 1971, 1972; Berman and Moses, 1972; Reichardt, 1973;
Wunderlich, 1973 ) and in sea waters (Goldschmiedt, 1959; Strickland and Sol6rzan0, 1966).