Advances in agronomy volume 27

Leaf water potentials A and net photosynthesis B for maize that was desiccated throughout most of the grain-fill period by withholding water from the soil.. In vegetative maize about 30

ADVANCES IN

AGRONOMY VOLUME 27

CONTRIBUTORS TO THIS VOLUME

ADVANCES IN

AGRONOMY

Prepared under the Auspices of the

AMERICAN SOCIETY OF AGRONOMY

VOLUME 2 7

Edited by N C BRADY International Rice Research Institute

1975

ACADEMIC PRESS New York San Francisco London

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COPYRIGHT 0 1975, BY ACADEMIC PRESS, INC

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PRINTED IN THE UNITED STATES OF AMERICA

CONTENTS

CONTRIBUTORS TO VOLUME 27

PREFACE

PHYSIOLOGY OF WATER DEFICITS IN CEREAL CROPS J s BOYER AND H G MCPHERSON I I1 I11 I I1 111 IV I I1 111 IV V VI Introduction

Sensitivity of Desiccation

Improvement of Drought Response through Breeding and Management

References

BIOLOGICAL SIGNIFICANCE OF ENZYMES ACCUMULATED IN SOIL S Kiss M DR~CAN.BULARDA AND D RADULESCU Introduction

Role of Accumulated Soil Enzymes in the Initial Phases of the Decomposition of Organic Residues and of the Transformation of Some Compounds

Enzymatic Activities in Soil under Conditions Unfavorable for the Proliferation of Microorganisms

Summary

References

RESPONSES OF PLANTS TO AIR POLLUTANT OXIDANTS IRWIN P TINC AND ROBERT L HEATH Introduction

Biochemical and Physiological Effects

Development and Predisposition to Oxidant Injury

Environmental Factors Influencing Susceptibility and Sensitivity

The Role of Stomata

Conclusions

References

PHYSIOLOGICAL BIOCHEMICAL AND GENETIC BASIS OF HETEROSIS SURESH K SINHA AND RENU KHANNA I Introduction

I1 Heterosis in Heterotrophs and Autotrophs

V

ix

xi

1

2

17

22

25

27

64

76

76

89

93

105

107

1 1 1

117

118

123

124

CONTENTS

vi

111

IV

V

VI

VII

VIII

IX

X

Occurrence of Heterosis 125

Evaluation of Heterosis 125

Manifestation of Heterosis 126

Present Theories of Heterosis 127

Physiological and Genetic Analysis of Heterosis 130

Synthesis 166

Programming in Heterotic Hybrids 168

Future Outlook 169

References 170

FERTILIZERS FOR USE UNDER TROPICAL CONDITIONS 0 P ENGELSTAD AND D A RUSSEL I Introduction 175

I1 Brief Description of Tropics 176

111 History of Fertilizer Use in the Tropics 182

IV Agronomic Considerations 186

V Fertilizer Technology Developments 202

References 204

FOREST SITE QUALITY EVALUATION I N THE UNITED STATES WILLARD H CARMEAN I Introduction 209

I1 History of Site Quality Estimation in the United States 211

111 Methods for Estimating Site Quality 212

IV Conclusions 255

Appendix: Common and Scientific Names of Tree Species 257

References 258

THE ROLE OF REMOTE SENSING I N DETERMINING THE DISTRIBUTION AND YIELD OF CROPS MARVIN E BAUER I Introduction 271

I1 Remote Sensing Development 272

111 Physical Basis for Remote Sensing 274

IV Agricultural Applications of Remote Sensing 291

V Future Role of Agricultural Remote Sensing 300

References 301

I

11

111

IV

V

VI

VII

VIII

CHEMICAL MONITORING OF SOILS FOR ENVIRONMENTAL QUALITY

AND ANIMAL AND HUMAN HEALTH DALE E BAKER AND LEON C H E S N l N

Introduction

Soil Pollution Sources

Soil and Waste Composition Monitoring

Methods of Chemical Analysis

Monitoring of Macroelements

Monitoring of Microelements

Toxic Trace Elements Organometallic Complexes

Recommendations for Continuing Research

References

306 307 316 323 327 343 358 364 366 SUBJECT INDEX 375

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CONTRIBUTORS Numbers in parentheses indicate the pages on which the authors’ contributions begin DALE E BAKER (305), Department of Agronomy, The Pennsylvania State

University, University Park, Pennsylvania

MARVIN E BAUER (271 ) , Laboratory for Applications of Remote Sensing, Purdue University, West Lafayette, Indiana

J S BOYER ( l ) , Departments o f Botany and Agronomy, University of

Illinois, Urbana, Illinois

WILLARD H CARMEAN (209), USDA Forest Service, North Central Forest

Experiment Station, St Paul, Minnesota

LEON CHESNIN ( 305 ) , Department of Agronomy, University of Nebraska, Lincoln, Nebraska

M DRAGAN-BULARDA (25), BabepBolyai University, Cluj-Napoca,

Romania

0 P ENGELSTAD ( 175 ) , Division o f Agricultural Development, National Fertilizer Development Center, Tennessee Valley Authority, Muscle Shoals, Alabama

ROBERT L HEATH (89), Department of Biology, University of California, Riverside, California

RENU KHANNA* ( 123), Water Technology Centre, Indian Agricultural

Research Institute, New Delhi, India

S KISS (25), BabepBolyai University, Cluj-Napoca, Romania

H G MCPHERSON ( 1 ) , Plant Physiology Division, Department o f Scientific and Industrial Research] Palmerston North, New Zealand

D R ~ D U L E S C U (25 ) , BabepBolyai University] Cluj-Napoca, Romania

D A RUSSEL ( 175), Division of Agricultural Development, National Fertilizer Development Center, Tennessee Valley Authority, Muscle Shoals, Alabama

SURESH K SINHA ( 123), Water Technology Centre, Indian Agricultural

Research Institute, New Delhi, India

IRWIN P RNG ( 8 9 ) , Department of Biology, University of California, Riverside, California

* Present address: School of Life Sciences, Jawaharlal Nehru University, New Delhi, India

ix

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PREFACE

Soil and crop scientists continue to focus their attention on pressing human problems, two of the most important of which are food supplies and environmental contamination These two topics receive prominent

attention in Volume 27 as has been the case in the two preceding volumes

Two papers deal with the effects of environmental contamination on

crops and soils The influence of air pollutant oxidants on plants is re- viewed along with the chemical monitoring of soils for pollutants These papers emphasize societal concerns for environmental contamination and attempts by soil and crop scientists to deal with this emerging problem Research aimed at obtaining a better understanding of factors affecting crop production is presented in three papers Heterosis is the subject of one, with emphasis being given to the physiological and genetic basis for

this phenomenon The physiology of drought as it affects cereal crops is reviewed along with the genetic potential for drought resistance The third paper focuses on fertilizer use in the tropics, with emphasis on agronomic responses peculiar to these areas Each of these excellent reviews will be helpful to scientists concerned with food production

Research on the evaluation of the physical environment in which plants grow is covered in three papers First, work on forest site quality evalua- tion is reviewed and summarized Emphasis is placed on methods of evaluating the site quality Second, research on remote sensing as a means

of determining crop distribution is evaluated The physical basis for sensing this distribution and the agricultural applications of remote sensing receive major attention in this excellent review The third paper focuses

on enzymes in soils, their role in microbial transformations and their activities under conditions where microbial activity is minimized

The authors of the papers presented herein are to be congratulated on these excellent reviews I join their colleagues in thanking them for their contributions

N C BRADY

xi

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PHYSIOLOGY OF WATER DEFICITS IN CEREAL CROPS

J S Boyer and H G McPherson Departments of Botany and Agronomy, University of Illinois, Urbana, Illinois, and Plant Physiology Division, Department of Scientific and Industrial Research,

Palmerrton North, New Zeoland

111 Improvement of Drought Response through Breeding and Management

I Introduction

A number of central physiological processes contribute to the formation

of grain in crops Major ones are photosynthesis and the translocation of photosynthate to the grain, cell division and enlargement, and the accumu- lation and transport of nutrient elements for storage in the grain and for

the general functioning of cell metabolism These processes must occur during the appropriate stages of development, and consequently the timing

of each contribution is important Superimposed on this set of circum- stances is the suitability of the environment for supplying light, water, and nutrients for the completion of each stage of growth

This review is devoted to how the availability of a specific environmental factor, water, affects grain production in crops Higher plants must encoun- ter desiccation at least once in their life cycle, late in seed development when the embryo and stored reserves undergo desiccation prior to seed release However, in addition to this period of exposure, other episodes

of drought frequently occur, and there is probably no other factor that limits grain production so extensively and unpredictably Yield reductions from drought may be large enough to result in no grain at all, and even moderate drought can markedly affect grain production

In spite of the frequency and importance of this problem, little is known about the physiological reasons for the diminution of grain production dur-

1

2 J S BOYER AND H G MCPHERSON

ing dry periods Salter and Goode (1967), in an extensive review, de-

scribed numerous experiments that show reduced yield when drought oc- curred during various stages of crop development In that portion of their

review devoted to cereal grains, however, only 2 of the total 114 papers

report measurements of physiological parameters that might affect grain

yield under dry conditions Yoshida (1972), in his description of the physi-

ology of grain production, was unable to find any data to describe the effects of drought,

In this review we will present some recent work on the physiological mechanisms that underlie the reductions in yield caused by drought in cereal crops of the family Gramineae Because of the growing literature

on the broad metabolic aspects of desiccation in plants, we will emphasize that which provides insight for grain production The reader is encouraged

to consult Hsiao (1973) or Kozlowski (1968, 1972) for more general

by which the photosynthetic capacity of the crop is influenced by drought Leaf desiccation can cause a marked inhibition in the photosynthetic

activity per unit of leaf (Hsiao, 1973) An example of this can be seen

in Fig 1, which describes an experiment conducted by the authors at the

Climate Laboratory in Palmerston North, New Zealand Net photosynthesis

in maize was inhibited in two sets of plants (termed low VP and high

VP pretreatments) when water was supplied to the soil at one-seventh the rate of the controls, beginning in early grain-fill and continuing for the rest of the growing season For the grain-filling period as a whole, photo- synthesis in the desiccated plants was only a small percentage of that in the controls, and there was a considerable reduction in grain yield (see next page)

Measurements of leaf water potentials in these plants (Fig 1A) showed

PHYSIOLOGY OF WATER DEFICITS IN CEREAL CROPS 3

Time (days since star; of desiccation)

FIG 1 Leaf water potentials (A) and net photosynthesis (B) for maize that was desiccated throughout most of the grain-fill period by withholding water from the soil The pretreatments consisted of growing the plants throughout the vegetative

period at different humidities during the day: low VP = leaf-air vapor pressure difference of 26 mb (0); high VP = leaf-air vapor pressure difference of 5 mb ( 0 )

The humidities were equalized during pollination and grain-fill

that the decline in photosynthesis was related to the degree of plant desicca- tion At leaf water potentials of -18 to -20 bars, the rate of photosynthesis was 15% of the controls or less (Fig 1B) Under these conditions, there were no symptoms of desiccation other than a slight gray cast to the leaves,

so that the presence of inhibitory desiccation was difficult to detect visually

In this species as well as in many others, visual symptoms, if they occur

at all, frequently appear after much photosynthetic activity has been lost They therefore do not provide a very useful index of plant water deficits, and quantitative methods of measuring plant water status are to be pre- ferred (Boyer, 1969; Kramer, 1969)

4 J S BOYER AND H G MCPHERSON

Since net photosynthesis can be affected by either a decrease in gross photosynthesis or an increase in respiration, the cause of the decrease in photosynthetic activity need not be associated with a change in photosyn- thesis itself With a few exceptions, however, (Schneider and Childers,

1941 ; Upchurch et al., 1955; Brix, 1962), dark-respiration generally de-

creases, although substantial respiration may still take place after photo-

synthesis has ceased (Brix, 1962; Boyer, 1970a) In those cases where

dark respiration increased, the increase was observed only initially and was

small (Schneider and Childers, 1941; Brix, 1962) Photorespiration, or

carbon dioxide loss in the light, also was inhibited and had a sensitivity

more like that of photosynthesis (Boyer, 1971 b ) It is clear therefore that

the decline in net photosynthesis cannot be attributed to a rise in respira- tion but instead must involve a reduction in gross photosynthesis

At the same time that net photosynthesis decreases, there generally is

a decrease in transpiration which reflects the closure of the stomata in re- sponse to leaf desiccation The decline in transpiration often parallels the decline in photosynthesis, and this has been interpreted to indicate that

stornatal closure limits both processes (Hsiao, 1973)

There is little doubt that stornatal closure restricts the entry of carbon dioxide into the leaf, but the supply may or may not control the rate of photosynthesis, depending on how severe is stornatal closure An additional test of the importance of stornatal closure is required in this situation I n

a recent examination of the response of sunflower leaves to desiccation,

Boyer (1971b) used an increase in the ambient concentration of carbon dioxide to provide such a test Despite the increased availability of carbon dioxide to the cells within the leaf, the rate of photosynthesis did not change in the desiccated plants, Boyer concluded that photosynthesis could not be limited by stornatal closure in this particular case and suggested that changes at the chloroplast level probably account for the changes in photosynthetic activity Wardlaw ( 1967) also showed that increased ex-

ternal carbon dioxide did not diminish the inhibition of photosynthesis dur- ing drought in wheat

Since these experiments suggest the possibility of chloroplast changes during leaf desiccation, several investigators have isolated chloroplasts from

desiccated leaf tissue (Nir and Poljakoff-Mayber, 1967; Fry, 1970, 1972; Boyer and Bowen, 1970; Potter and Boyer, 1973; Keck and Boyer, 1974)

They showed that electron transport and photophosphorylation are inhib- ited, and there are reports that carbon dioxide fixation by isolated chloro-

plasts is also reduced (Plaut, 1971 ; Plaut and Bravdo, 1973) The changes

in electron transport have been demonstrated in vivo (Boyer and Bowen,

1970; Boyer, 1971 a,b), and they parallel the inhibition of photosynthesis

PHYSIOLOGY OF WATER DEFICITS IN CEREAL CROPS 5

in sunflower It seems, then, that in the short term photosynthesis may

be affected by changes at the chloroplast level or by stomatal effects Since photosynthesis can be so severely inhibited by desiccation, and since some of the effects appear to be subcellular, to what extent will photo- synthesis recover after supplying water to the soil? When desiccation has been mild and of short duration, virtually complete photosynthetic recovery has been observed (Boyer, 1971 a) However, when it is more severe, pho- tosynthesis may show aftereffects of desiccation There appear to be two types of aftereffects First, there may be incomplete recovery of leaf water potential, which causes photosynthesis to remain below the levels of the controls (Boyer, 1971a) Second, there may be a direct aftereffect of drought on the photosynthetic process (Boyer, 1971a) Both depend on the severity of desiccation: the more severe is desiccation, the more severe are its aftereffects

The first kind of aftereffect appears to be caused by breaks in water columns or other modifications of the pathway for water transport in the plant (Boyer, 1971a) The net result is that the resistance to liquid water transport increases within the plant If it increases enough, desiccation of the leaves may continue despite rewatering of the soil, and leaf death then ensues However, if partial rehydration takes place, the resistance to water transport decreases over a period of days, and the plant gradually returns

to normal hydration levels During this time, photosynthesis is frequently inhibited

The second kind of aftereffect occurs when the leaves return to full hy- dration after rewatering In sunflower leaves that were mature during desic- cation, photosynthesis continued to be affected by the previous dry period (Boyer, 1971a) in spite of a return of the leaves to high water potentials Chloroplast recovery required 12-1 5 hours, but stomatal apertures re- mained reduced for several days (Boyer, 1971a) The inhibition was corre- lated with partial stomatal closure, but other aspects of photosynthesis may also have played a part For whole sunflower plants, there was evidence that older leaves never recovered their former levels of photosynthesis and that a return to high photosynthetic activities had to await regrowth of the plant

The extent of our knowledge of photosynthesis at low leaf water poten- tials is rather limited and involves only a few species From these data, however, it seems that the response differs between species and may change

as the age of the plant varies For example, photosynthesis in pine, tcimato, and sunflower seems to behave similarly as leaf water potentials decline (Brix, 1962; Boyer, 1970a) For young maize, however, photosynthesis

is more sensitive and soybean photosynthesis is less sensitive than in these

6 J S BOYER AND H G MCPHERSON

a

species (Boyer, 1970b) In all these cases, stornatal behavior generally paralleled photosynthetic behavior The photosynthetic decline was greatest between leaf water potentials of -10 and -20 bars

Plant maturity may also influence the response of photosynthetic activity

to desiccation Limited data suggest that the sensitivity decreases with age

In vegetative maize about 30 days after planting, photosynthesis declined

to 70% of that in the well watered plants when leaf water potentials de- creased to -12 bars (Boyer, 1970a,b) During grain-fill, however, this degree of inhibition was not observed until leaf water potentials had de- creased to about -16 bars (Fig 2) A similar decrease in sensitivity has been found for stornatal closure in wheat (Frank et al., 1973)

These differences between species and even between different ages of the same plants suggest that plants may be capable of adapting to water availability Jordan and Ritchie ( 1971 ) showed that stomata remained open in field-grown cotton plants having leaf water potentials that caused closure in laboratory-grown plants (which were presumably less subject

to desiccation beforehand) McCree ( 1974) demonstrated a similar phe- nomenon in the laboratory with plants having different moisture prehis- tories It seems likely that some type of photosynthetic differences should also have occurred in these plants

In order to test whether prior exposure to desiccating conditions could affect the photosynthetic behavior of plants during a subsequent period

of desiccation, we conducted experiments in maize subjected to two differ-

Leaf Woter Potentiol(bars)

4

FIG 2 Net photosynthesis in maize at various leaf water potentials and two plant

ages The 65-day plants ( 0 ) were those described in Fig 1 (Dekalb XLAS) for the early portion of the grain-filling period The 30day plants (0) were grown under similar conditions but are those shown in Fig 5 (GSC 50 single cross) The younger plants had not tasseled

PHYSIOLOGY OF WATER DEFICITS IN CEREAL CROPS 7

ent desiccation pretreatments The plants were pretreated by growing them throughout the entire vegetative period in air having two different humidi- ties during the day (low VP pretreatment = leaf-air vapor pressure differ- ence of 26 mb = low humidity; high V P pretreatment = leaf-air vapor pressure difference of 5 mb = high humidity) Otherwise, the plants were grown under identical conditions in well watered soil The net result was that the two sets of plants were subjected to a different evaporative demand during the day, which caused leaf water potentials to average 1 bar lower

in the low VP plants than in the high VP plants (although there was con- siderable variation between leaves because of mutual shading by other plants in the stand) At tasseling, identical high VP conditions (5 mb) were imposed on all plants so that pollination occurred under favorable moisture conditions After pollination, the soil was desiccated in half the plants, and the desiccated plants received one-seventh the amount of water received by the controls for the remainder of the growing season Figure 1 shows the results for the two pretreatment conditions and indi- cates that there were significant differences in leaf water potentials and net photosynthesis in the two sets of plants during desiccation in the grain- filling period The plants that previously had been grown at low humidities exhibited high leaf water potentials and high rates of photosynthesis for

a longer time than their counterparts that had not previously been subjected

to dry conditions There were no important differences in photosynthesis between the controls

Table I shows that the grain yield by the desiccated plants differed ac- cording to the pretreatment Those previously exposed to dry conditions produced 7970 kg ha-', and those previously exposed to moist conditions

TABLE I Grain Yield of Maize When Water Was Withheld throughout Most

of the Grain Fill Period Plantsa Low VP pretreatmentb High VP pretreatmentb

Control 11,700 kg.ha-l 10,500 kg.ha-*

0 Leafwater potentials were -3 to -4 bars and -18 to -20 bars in

control and desiccated plants, respectively, throughout most of the

desiccation period

b Pretreatments consisted of growing plants in different humidities

during the day (low VP = leaf-air vapor pressure difference of 26 mb;

high VP = leaf-air vapor pressure difference of 5 mb) throughout

vegetative period Desiccation occurred after humidities had been

equalized (leaf-air vapor pressure difference 5 mb)

8 J S BOYER AND H G MCPHERSON

produced 4930 kg ha-', a result that is in a direction predicted from the

photosynthetic measurements Thus, the saving in grain production was quite substantial in the desiccated plants that had previously experienced

dry conditions This amount of grain production (68% of the control for the low VP plants) is a considerable accomplishment for plants having

so little photosynthesis (37% of the control when integrated) during the grain-filling period The grain produced by the controls, however, was rela- tively unaffected by the pretreatment ( 10,500 and 11,700 kg ha-l)

The results of this experiment suggest that (1) plants can adapt to desic- cation in some way that preserves grain production, and ( 2 ) plants can mobilize photosynthate produced before the grain-filling period and use

it to fill the grain

The adaptation of the plants could take two forms: avoidance of low leaf water potentials or tolerance to low leaf water potentials Figure 3

shows that there was little difference in the tolerance of photosynthesis

to low leaf water potentials in the two sets of plants For both, net photo- synthesis was inhibited initially at leaf water potentials of about -8 bars and became zero at leaf water potentials of about -1 8 to -20 bars However, less water was used under well watered conditions by plants from the dry

pretreatment than by those without the dry pretreatment (Fig 4 ) This

resulted in the conservation of soil water, and consequently leaf water po- tential (Fig l A ) , transpiration (Fig 4), and photosynthesis (Fig l B) were preserved in the adapted plants for a longer time than in the un- adapted plants I n this case, it appears that adaptation to desiccation took

I20

"0 - 4 - 8 -12 -16 - 2 0 - 2 4

Leaf Water Potentiol ( b a r s ) FIG 3 Net photosynthesis during grain-fill in maize at various leaf water poten- tials after pretreatment under two humidity conditions See Fig 1 for details of the experiment 0, Low vapor pressure (VP) pretreatment; 0 , high VP pretreatment

PHYSIOLOGY OF WATER DEFICITS IN CEREAL CROPS 9

by withholding water from the soil after pretreatment under two humidity conditions

See Fig 1 for details of the experiment 0, Low vapor pressure (VP) pretreatment;

0 , high VP pretreatment

the form of avoidance rather than tolerance, and the fundamental ability

of the protoplasm to carry on metabolism at low leaf water potentials was

unaltered, or at the most only slightly altered While it is true that adapta-

tion took the form of avoidance in this instance, the possibility remains

that other kinds of desiccation pretreatments might cause improved toler-

ance of the plants to dry conditions It would seem that further investiga-

tion of this possibility may be worthwhile

The ability of the plants to mobilize reserves for grain-filling when cur-

rent photosynthate became unavailable is a result quite distinct from the

problem of adaptation Table I1 shows that plants from the two pretreat-

ments formed grain roughly in proportion to the total dry matter that had

been accumulated during the growing season (Table 11), not according

to the dry matter produced during grain-fill alone (Table 11) Adaptation

had little effect on this trend Thus, adaptation simply caused more dry

matter to be accumulated by the plants, and this in turn permitted higher

grain yield (Table I )

The vegetative portions of the desiccated plants actually lost weight to

the grain as reserves were transported to the developing ears (Table 11)

Thus, as export of photosynthate from the leaf declined, reserves from

other parts of the plant compensated for the reduction in transport to the

grain Since the proportion of weight lost by the vegetative portions of the

desiccated plants was similar for both pretreatments, there was relatively

10 J S BOYER AND H G MCPHERSON

TABLE I1

Dry Weights in Maize When Water Was Withheld throughout Most

of the Grain-Fill Period

Parameter

Low VP pretreatment" High VP pretreatmenta

Grain

Shoots at end of season

Gain by shoots during grain fill

Gain by nongrain parts of shoot

Grain :shoot, end of season

Grain :gain by shoots during

during grain-fill

grain-fill

Controlb (g p1-9

Desic- catedh (g PI-.')

Controlh (g p1-9

Desic- cated* (g PI-')

101 rt 6

195 2C 1 1

68 rt 3 -26 rt 2 0.52

62 4

154 k I

42 f 3 -17 -t 5

0.40 1.48

a Pretreatment consisted of growing plants in different humidities during the day (low

VP = leaf-air vapor pressure difference of 26 mb; high VP = leaf-air vapor pressure dif- ference of 5 mb) throughout vegetative period Desiccation occurred after humidities had been equalized (leaf-air vapor pressure difference = 5 mb)

Leaf water potentials were -3 to - 4 bars and - 18 to -20 bars in control and desic-

cated plants, respectively, throughout most of desiccation period (see Fig 1 A) Standard

deviations are shown beside means for 9 to 10 plants

little difference in the ability of the plants to mobilize these reserves (Table

11) This suggests that maize had a fundamental and fairly constant capacity for using reserves for grain-filling under our conditions

Table I11 shows that, of the components of yield, the single grain weight changed by the largest amount with desiccation This suggests that the size

of the sink represented by ear number and grain number was virtually the same for all plants, as would be expected since pollination was completed before the drought occurred Thus, the differences in grain yield between the adapted and nonadapted plants can be attributed to differences in the total amount of photosynthates accumulated by the plants, not to differ- ences in the ability of the plants to mobilize reserves or in the strength

of the sink for photosynthate represented by the grain

The capability of maize to mobilize reserves for grain-filling indicates that a considerable amount of potential grain dry weight is present but never reaches the grain under good moisture conditions We do not know whether most crops exhibit the same tendency to accumulate unused photo- synthate in favorable environments, but, if so, it is clear that some method

of utilizing these reserves for grain-filling under all conditions could benefit yield considerably

PHYSIOLOGY OF WATER DEFICITS IN CEREAL CROPS 11

TABLE 111

Components of Yield in Maize When Water Was Withheld throughout

Most of the Grain-Fill Period

~ ~~

Low VP pretreatmentD High VP pretreatment"

Ears per plant I .o * 0 0 I .o * 0 0 1 .o * 0.0 1 .o f 0.0 Rows per ear 16.7 f 1.4 16.0 * 1.7 16.4 f 1.7 16.5 f 1.4

Florets per ear 784 + 79 740 f 75 746 f 61 694 f 29

Filled grains per ear 471 i- 88 444 * 35 451 f 80 371 f 32

Single grain weight 0.314 5 0.02 0.227 + 0.02 0.295 + 0.04 0.168 * 0.02

Pretreatments consisted of growing plants in different humidities during the day (low

VP = leaf-air vapor pressure difference of 26 mb; high VP = leaf-air vapor pressure differ- ence o f 5 mb) throughout vegetative period Desiccation occurred after humidities had been equalized (leaf-air vapor pressure difference = 5 mb)

* Leaf water potentials were -3 to - 4 bars and - 18 to -20 bars in control and desic- cated plants, respectively, throughout most of desiccation period (see Fig 1A) Standard deviations are shown beside means for 9 to 10 plants

Although photosynthesis is important for grain production in cereal crops, the transport of photosynthetic products is also essential for the for- mation of yield In maize, about half of the dry matter accumulated by the shoot is ultimately moved into the grain Thus, the process operates

on a large scale, and any inhibition of it is likely to result in a reduction

in yield

It is generally agreed that drought results in a diminution of the recent photosynthate transported to developing grain Wardlaw ( 1967, 1969,

1971 ) has shown that the rate of translocation of recently fixed 14C was

reduced in wheat growing under desiccating conditions Translocation in maize growing in the field showed a similar behavior (Brevedan and Hodges, 1973)

This reduction in rates of translocation could result either from a reduc- tion in the amount of photosynthate available for transport or from a direct inhibition of the translocation process Wardlaw (1969) attempted to dis- tinguish between these possibilities by manipulating the amount of photo- synthetic tissue (the source) relative to the amount of utilizing tissue (the sink) in wheat When the relative amount of sink in the desiccated plants was increased, the velocity of transport became the same as in the controls, although the total quantity of "C transported was less than in the controls Wardlaw ( 1969) interpreted these results to indicate that the translocation

12 J S BOYER AND H G MCPHERSON

mechanism itself was relatively unaffected by desiccation, and that the effects of desiccation on the source and sink accounted for most of the changes in translocation However, Brevedan and Hodges ( 1973) suggest

the reverse, that “C translocation may be more severely affected than pho- tosynthesis during drought in the field

From the experiments with maize described in the previous section, it

is clear that translocation was less sensitive than photosynthesis to low leaf water potentials Leaf photosynthesis virtually ceased (Fig 1B) while dry weight from other parts of the desiccated plants continued to accumu- late in the grain (Table 11) The proportion of dry weight transported to the grain was about as large in the desiccated plants as in the controls (Table 11) Consistent with this finding is the work of Asana and Basu

(1963) with wheat They found that an inhibition of photosynthesis early

in the grain-filling period was compensated by translocation of stem re-

serves Thus, these findings agree with the concept of Wardlaw (1969)

that reductions in the translocation of recent photosynthate do not reflect

an effect on the translocation mechanism itself, but rather on the availabil- ity of photosynthate for export from the leaf

C NUTRITIONAL QUALITY

We have so far mainly considered the effects of drought on the quantity

of grain production Probably just as important from the human standpoint, however, are its effects on the nutritional quality of the grain In addition

to the caloric value of the grain, the other major component of nutritional quality is the protein content and amino acid composition of the grain

Miller (1938) pointed out that the bread-making quality of wheat (largely

a function of grain protein content) is affected by the dryness of the grow- ing season For wheat, the percentage of protein increases during a drought, although total yield decreases Evidently, the total protein production is inhibited but total carbohydrate production is inhibited even more

In the vegetative portions of the plant, this order is reversed and protein synthesis appears to be reduced before photosynthesis decreases signifi- cantly Recent studies of nitrate reductase synthesis illustrate the point

In vegetative maize, nitrate reductase is an unstable enzyme that must be

continually synthesized (Beevers and Hageman, 1969) Unfavorable tem-

perature, CO, levels, and water availability reduce the activity of the en-

zyme (Beevers and Hageman, 1969; Morilla et d., 1973) largely because

of an inhibition of protein synthesis Desiccation of the leaves resulted in

a marked inhibition of nitrate reductase activity (60-70% ) at leaf water

potentials of -6 to -8 bars (Morilla et al., 1973) Photosynthesis had de-

clined only 10-20% at these water potentials, however (Boyer, 1970b),

PHYSIOLOGY OF WATER DEFICITS IN CEREAL CROPS 13 although the plants used for these measurements were somewhat older than

those used by Morilla et af ( 1973 )

In addition to the importance of nitrate reductase as an indicator of protein synthesis by the crop, the drought-induced decline in nitrate reduc- tase activity is significant in another respect Nitrate reductase is the first enzyme involved in the enzymatic reduction of nitrate and its eventual in- corporation into proteins as the amino form Because the enzyme has low enough activities to control the flux of reduced nitrogen for the plant, a lower activity of the enzyme means a lower flux of reduced nitrogen and consequently a decreased capability for protein production (Beevers and Hageman, 1969) For maize, which gains most of its nitrogen during vege- tative growth and anthesis, a reduction in nitrogen content of the plant means a reduction in nitrogen that can eventually be made available to the grain

Hageman and co-workers have shown correlations between the total yield, the protein yield, and the seasonal activity of nitrate reductase in

maize and wheat lines (Croy and Hageman, 1970; Deckard et al., 1973)

Since most nitrogen uptake occurs in the first half of the growth period

in maize, the protein of the grain must be derived primarily from nitrogen that has previously been a part of vegetative proteins Thus, it is to be expected that, as grain fills, early storage represents mostly carbohydrate but later it consists of a considerable amount of protein, which is derived from nitrogenous compounds released from the vegetative tissues as senes- cence takes place

In view of this behavior, selections for high nitrate reductase activity and high vegetative protein could possibly be reflected in higher grain pro- tein in certain crops The correlations shown by the Hageman group sug- gest that this avenue of selection ought to be valuable to pursue As it

is also clear, however, that little is known about the drought response of protein synthesis in grain, it might be beneficial to study the response within the grain itself The proteins of the vegetative portions of the plant must

be dissembled before transport to the seed, and protein synthesis by the seed is a major activity during grain fill

Leaf enlargement can be reduced by only small degrees of desiccation, generally long before photosynthesis is affected (Boyer, 1973; Hsiao, 1973) Rates of enlargement are most rapid when leaf water potentials are -1.5 to -2.5 bars, and they decline markedly when leaf water potentials

fall below these values (Fig 5 ) In maize, sunflower, and soybean, leaf

enlargement was reduced to 25% of the well watered controls or less when

14 J S BOYER AND H G MCPHERSON

Leaf Water Potential (bars)

FIG 5 Leaf elongation and net photosynthesis in maize having various leaf water potentials The 30-day-old plants were growing in soil from which water was with- held For the leaf enlargement data, the plants were placed in a dark, humid chamber

for 36 hours a t 26"C, and measurements of water potential and leaf length were made before and after the last 24 hours under those conditions Net photosynthesis

of intact shoots was measured by infrared gas analysis Leaf water potentials were determined with a thermocouple psychrometer using the isopiestic technique (Boyer, 1969) on leaf disks from the same leaves on which the physiological measurements were made Data from Boyer (1970a)

leaf water potentials decreased to -4 bars (Boyer, 1968, 1970a) The steepness of the decline indicates that modest changes in the evaporative conditions or in the soil water supply will have a considerable effect on leaf growth In fact, the transition from night to day or a change in the humidity of the air is frequently enough to bring about a significant altera- tion in the rate of growth (Boyer, 1968; Acevedo el al., 1971)

In view of this high sensitivity, it is curious that, at maximum rates of leaf growth, leaf water potentials are -1.5 to -2.5 bars when the soil may have a water potential of -0.1 bar to -0.3 bar (Fig 5 ) Cell enlargement requires turgor to extend the cell wall and also requires a gradient in water potential to bring water into the enlarging cell In growing cells, the yielding

of the cell walls under the action of turgor effectively places a limit on the maximum turgor that can occur This in turn controls the water poten- tial of the cell relative to its environment and hence a gradient in water potential is formed Thus, the water potential of leaves remains below the

PHYSIOLOGY OF WATER DEFICITS IN CEREAL CROPS 15

water potential of the water supply for as long as growth occurs Growth then reflects a balance between expansion on the one hand and the gradient

in water potential that supplies the water for expansion, on the other

(Boyer, 1968) This appears to be the reason that leaf water potentials are -1.5 to -2.5 bars instead of virtually zero when plants are growing in

well watered soil

Short periods of desiccation, such as might occur during a clear summer day, have a reversible effect on leaf growth (Acevedo et al., 1971), and

rapid rates resume when leaf water potentials return to -1.5 to -2.5 bars

If leaf water potentials are continuously less than optimum for several days, however, there is evidence that leaves may not grow at the original rate

upon rewatering (Boyer, 1970a) Therefore, the duration of a drought

has an effect on the subsequent regrowth of the vegetative plant

Low leaf water potentials also influence leaf production through their effects on leaf initiation in meristems and subsequent rates of cell division The rate of leaf initiation may become slower or even cease as desiccation

proceeds (Husain and Aspinall, 1970), and there is evidence that cell divi-

sion may be reduced (Terry er al., 1971; Kirkham er al., 1972; Meyer

and Boyer, 1972; McCree and Davis, 1974) In general, cell enlargement appears to be more sensitive than cell division (Meyer and Boyer, 1972),

although Kirkham et al (1972) found an early effect of osmotic solutions

on cell division

It is important to note that in certain field situations such as saline soils

or the leaves at the tops of tall trees, leaves grow even though water poten-

tials may be continuously more negative than -4 bars It therefore seems

certain that leaves are capable of adjusting in some way so that enlargement

is less affected than in those cases described by Boyer (1968, 1970a) and

Acevedo et al ( 197 1 ) The investigation of how these adaptations occur should be highly worthwhile

Some investigations have shown that the adaptations may take the form

of adjustments in the osmotic potentials of cell contents Thus, Meyer and Boyer ( 1972) described an internal osmotic compensation that caused the

tissue osmotic potential to change by the same amount as the water poten- tial in soybean hypocotyls The overall effect of the compensation was to keep turgor high, which resulted in less inhibition of cell enlargement than

occurred when compensation did not take place Greacen and Oh (1972) have shown a similar phenomenon in roots Goode and Higgs (1973) and Biscoe (1972) report that compensation may occur in leaves and Stewart

(1971 ) found a slight accumulation of solutes

As the rate of leaf production in forage crops so directly affects the economic yield, the ability to modify the drought response of leaves would

be valuable In an encouraging development, Singh er al (1973) reported

16 J S BOYER AND H G MCPHERSON

that gibberellic acid partially reversed (by about one-third) the effects of drought on wheat leaf growth

Although low leaf water potentials have a large effect on the rate of production of new leaf area, they also cause the loss of existing leaf area For the adaptation study in maize described earlier, leaf senescence was accelerated in the desiccated plants compared to that in the controls (Fig

6 ) Again, those plants that had previously been exposed to dry conditions (low VP pretreatment) retained viable leaves for a longer time than those plants that had not been exposed, probably because the former plants had high leaf water potentials for a longer time before desiccation became

severe (Fig 1A) It is significant that senescence in maize tended to occur

first in the lower leaves, which are least active in supplying photosynthate

to the grain (Eastin, 1969)

Because senescence is irreversible, it reduces the potential for vegetative recovery after rain and consequently it may inhibit grain production It

is not clear to what extent the drought-induced senescence of desiccated leaves of cereal grains represents a mechanism by which the plants shed transpiration surface, or a sacrifice of carbohydrates and nitrogen com- pounds in the senescing leaves for the sake of grain formation and the maintenance of growing points If the latter is the case, senescence of leaves may be necessary for continued crop development under desiccating condi- tions that are severe enough to restrict photosynthesis

Time (days since s t a r t of desiccation)

FIG 6 Leaf senescence during grain-fill in maize that was desiccated by withhold- ing water from the soil after pretreatment under two humidity conditions See Fig

1 for details of the experiment 0 , High vapor pressure ( V P ) pretreatment; 0, low

VP pretreatment

PHYSIOLOGY OF WATER DEFICITS IN CEREAL CROPS 17

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

REFERENCES Acevedo, E., Hsiao, T C., and Henderson, D W 1971 Plant Physiol 48, 631-636 Asana, R D., and Basu, R N 1963 Indian 1 Plant Physiol 6, 1-13

Beevers, L., and Hageman, R H 1969 Annu Rev Plant Physiol 20, 495-522

Biscoe, P V 1972 1 Exp Bot 23, 930-940

Boyer, J S 1968 Plant Physiol 43, 1056-1062

Boyer, J S 1969 Annu R e v Plant Physiol 20, 351-364

Boyer, J S 1970a Plant Physiol 46, 233-235

Boyer, J S 1970b Plant Physiol 46, 236-239

Boyer, J S 1971a Plant Physiol 47, 816-820

Boyer, J S 1971b Plant Physiol 48, 532-536

Boyer, J S 1973 Phytopathology 63, 466472

Boyer, J S., and Bowen, B L 1970 Plant Physiol 45, 612-615

Brevedan, E R., and Hodges, H F 1973 Plant Physiol 52, 436-439

Brix, H 1962 Physiol Plant 15, 10-20

Chang, T T., Loresto, G C., and Tagumpay, 0 1974 Sabrao 1 6, 9-16 Claassen, M M., and Shaw, R H 1970a Agron J 62, 649-652

Claassen, M M., and Shaw, R H 1970b Agron 1 62,652-655

Croy, L I., and Hageman, R H 1970 Crop Sci 10,280-285

Deckard, E L., Lambert, R J., and Hageman, R H 1973 C r o p Sci 13, 343-350

Eastin, J A 1969 Proc 24th Annu Corn Sorghum Res C o n f Amer Seed Trade

Frank, A B., Power, J F., and Willis, W 0 1973 Agron 1 65, 777-783

Fry, K E 1970 Plant Physiol 45, 465-469

Fry, K E 1972 C r o p Sci 12, 698-701

Goode, J E., and Higgs, K H 1973.1 Hort Sci 48, 203-215

Greacen, E L., and Oh, J S 1972 Nature (London), N e w Biol 235, 24-25

Hsiao, T C 1973 Annu Rev Plant Physiol 24, 519-570

Husain, I., and Aspinall, D 1970 Ann Bot (London) [N.S.] 34, 393-408

Jordan, W R., and Ritchie, J T 1971 Plant Physiol 48, 783-788

Keck, R W., and Boyer, J S 1974 Plant Physiol 53, 474479

Kerr, J P., McPherson, H G., and Talbot, J S 1973 Proc Aust C o n f Heat Mass

Kirkham, M B., Gardner, W R., and Gerloff, G C 1972 Plant Physiol 49, 961-962

Kozlowski, T T., ed 1968 “Water Deficits and Plant Growth,” Vols 1 and 2 Aca-

Kozlowski, T T., ed 1972 “Water Deficits and Plant Growth,” Vol 3 Academic

Kramer, P J 1969 “Plant Water Relationships.” McGraw-Hill, New York

McCree, K J 1974 Crop Sci 14,273-278

McCree, K J., and Davis, S D 1974 Crop Sci 14, 751-755

Mederski, H J., and Jeffers, D L 1973 Agron 1 65, 410-412

Meyer, R F., and Boyer, J S 1972 PIanta 108, 71-87

ASS Publ NO 24, pp 81-89

Transfer, Ist, 1973 Sect 3, pp 1-8

demic Press, New York

Press, New York

PHYSIOLOGY OF WATER DEFICITS IN CEREAL CROPS 23

Miller, E C 1938 “Plant Physiology.” McGraw-Hill, New York

Morilla, C A., Boyer, J S., and Hageman, R H 1973 Plant Physiol 51, 817-824

Moss, G I., and Downey, L A 1971 Crop Sci 11, 368-372

Nelson, C J., Asay, K H., Horst, G L., and Hildebrand, E S 1974 C r o p Sci

Nir, I., and Poljakoff-Mayber, A 1967 Nature (London) 213, 4 1 8 4 1 9

Passioura, J B 1972 Aust 1 Agr Res 23, 745-752

Plaut, 2 1971 Plant Physiol 48, 591-595

Plaut, Z., and Bravdo, B 1973 Plant Physiol 52,28-32

Potter, J R., and Boyer, J S 1973 Plant Physiol 51, 993-997

Ritchie, J T., and Burnett, E 1971 Agron J 63, 56-62

Salter, P J., and Goode, J E 1967 “Crop Responses to Water a t Different Stages

Schneider, G W., and Childers, N F 1941 Plant Physiol 16, 565-583

Singh, T N., Aspinall, D., and Paleg, L G 1973 Aust I Biol Sci 26, 77-86

Slayter, R 0 1969 “Physiological Aspects of Grain Yield” (J D Eastin et al.,

eds.), pp 53-83 Amer SOC Agron and Crop Sci SOC Amer., Madison, Wisconsin

14, 26-28

of Growth.” Commonw Agr Bur., Farnham Royal, Bucks, England

Stewart, C R 1971 Plant Physiol 48, 792-794

Terry, N., Waldron, L J., and Ulrich, A 1971 Planta 97, 281-289

Upchurch, R P., Peterson, M L., and Hagan, R M 1955 Plant Physiol 30, 297-303

Wardlaw, I F 1967 Aust J Biol Sci 20, 25-39

Wardlaw, I F 1969 Aust J B i d Sci 22, 1-16

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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

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)

ENZYMES ACCUMULATED IN SOIL 27

zymes have a real significance in the biological cycles of elements? Do

these enzymes contribute to soil fertility and to the creation of conditions favorable for the nutrition of higher plants?

A comprehensive review dealing with this problem has not appeared

in the literature Only a preliminary report was published (Kiss et al.,

1971) The present paper is a more detailed review of the literature con- cerning the biological significance of the enzymes accumulated in soil The principal method by which this problem is studied is based on the comparison of substrate transformations in soil samples permitting micro- bial proliferation with those in which microbial proliferation is prevented

A general examination of the pertinent experimental results described in

the literature makes it evident that the enzymes accumulated in soil d o have a biological significance as they participate in the biological cycles

of elements They play a very important role in the initial phases of the

decomposition of organic residues and of the transformation of some min- eral compounds, and under unfavorable conditions for the proliferation

of microorganisms

I I Role of Accumulated Soil Enzymes in the Initial Phases

of the Decomposition of Organic Residues and of the

Transformation of Some Mineral Compounds

1 Hydrolysis of Sucrose

Hofmann and Seegerer (1950) and Kuprevich (1951 ) were the first

to demonstrate that hydrolysis of sucrose in soil takes place in the presence

of toluene Thus, it is clear that soils contain invertase These investigators did not, however, compare the hydrolysis of sucrose in the presence and

in the absence of toluene Such a comparison was later made by Kiss (19.58~) It was found that during the first 4 hours of incubation there was no significant difference in the intensities of saccharolysis measured

in the presence or in the absence of toluene Consequently, hydrolysis of sucrose was catalyzed by the accumulated invertase which existed in the soil samples before incubation Chromatographic and manometric results

of Bose et al (1959) indicate that the accumulated invertase causes

sucrose hydrolysis in soil at a much higher rate than the rate at which the proliferating microorganisms can oxidize the hydrolytic products, glu-

cose and fructose

In experiments in which the incubation time was longer (24 hours), Peterson and Astaf'eva (1962) and Galstyan (1965a, 1974) observed that