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Light Interception

Generally, seasonal dry weight growth


of field crops is directly and linearly
related to the absolute amount of light
Crop Productivity and intercepted by green foliage (5, 6). This
relation usually holds whether the varia-
Photoassimilate Partitioning tion in intercepted light is achieved by
variation in incident light flux (7) or in
Roger M. Gifford, J. H. Thorne leaf cover of the ground due, for exam-
ple, to variation in time of planting.
W. D. Hitz, Robert T. Giaquinta Much of the impact of water supply and
nitrogen fertilizer on growth is via leaf
development and senescence and hence
via light interception. Thus it is of pri-
The concept that crop yield is deter- vironments and high planting densities, mary importance to ensure that crop
mined by a single limiting factor that, if were developed. genotype and management are such that
made nonlimiting, would give way to the Nevertheless, there remains potential the radiation of the growing season is
next most limiting factor has often been for further improvement in genetic yield intercepted as fully as possible. This
interpreted too literally. Even with re- potential of crops grown in fertile envi- requires minimizing the period of incom-
spect to environmental variables, it is ronments. While record farm yields do plete ground cover at the beginning and
true only in the extreme. A crop is rarely not in themselves represent genetic yield end of the season. The growing season is

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limited in its yield (or even its daily potential, the fact that average yield of usually circumscribed either by tempera-
growth rate) by a single environmental six major U.S. grain crops is only about tures too low for plant development or
factor. Indeed, that a successful crop is 20 to 35 percent of record yields (4) is by seasonal drought. During the period
adapted to its environment indicates that suggestive of a substantial improvement of full canopy cover, the leaf area per
no one factor is limiting. The progressive still to be achieved. unit of ground area (leaf area index)
increases in crop yields have been due to
improvements in numerous co-limiting
factors or phenomena, such as pest and Summary. The photosynthetic basis for increasing the yield of major field crops is
disease control by chemical and genetic examined in terms of improving the interception of seasonal solar radiation by crop
means; improved weed control by more foliage, the efficiency of conversion of intercepted light to photosynthetic assimilates,
effective and selective herbicides; in- and the partitioning of photoassimilates to organs of economic interest. It is concluded
creased supply of nutrients and water; that, in practice, genetic and chemical manipulation of light interception over the
better matching of the timing of crop life season and of partitioning offer the most potential for achieving further increases in
cycles to seasonal changes in the envi- yield. During the history of improvement of genetic yield potential of crops, increase in
ronment; closer matching of the crop's the partitioning of photoassimilates to harvested organs has been of primary
thermal requirement for development to importance.
the radiation regime; more timely and
efficient operations enabled by greater
mechanization; and increase in genetic Since most of the dry weight of plants ideally should not exceed that required
yield potential. consists of carbon compounds, the in- for full interception (8) or the crop will
Genetic yield potential has not been crease in harvested yield is intimately have committed photoassimilate to mak-
precisely defined. However, several ge- linked to changes in the photosynthetic ing noneconomic leaves that might have
notypes can be operationally ranked for fixation of carbon dioxide per unit of been invested in economic yield compo-
comparative genetic yield potential by land area and the subsequent partitioning nents. It can be necessary, however, for
growing them side by side in an experi- of this photoassimilate between harvest- peak leaf area index to exceed that need-
mental agricultural environment having ed and nonharvested portions of the ed for full interception at that time if this
near-optimal planting, water, and fertil- crop. However, photosynthesis and pho- ensures larger interception near the be-
izer regimes; effective control of pests toassimilate partitioning have not tradi- ginning and end of the season. Much
and diseases; lack of lodging and weath- tionally been explicit selection targets seasonal light is not intercepted by foliage
er damage; and a complete harvest. Al- for plant breeders. The photosynthetic in many crops (5, 6); further improvement
though average farm yields are well be- basis for increasing harvested yield in- in this area could be rewarding.
low the best experimental yields, steady volves maximizing (i) the amount of light For the season as a whole, increased
improvement in genetic yield potential intercepted by foliage, (ii) the conversion production of total crop dry weight,
has been found to contribute to increases efficiency of intercepted light to photo- whether it be achieved by greater light
in average yields where it has been ex- synthetic products, and (iii) the partition- interception or by greater efficiency of
amined. Seed yields of modern wheat ing of photoassimilate to the harvested light conversion due, say, to CO2 enrich-
and soybean cultivars are nearly 40 per- "economic sinks" (grains, tubers, sugar
cent greater than those of earlier culti- storage stem, and so forth). The authors are research scientists with E. I. du
vars when tested under comparable fa- A goal of crop physiologists is to un- Pont de Nemours & Company, Central Research
and Development Department, Experimental Sta-
vorable conditions (1). During the past derstand these component phenomena tion, Wilmington, Delaware 19898. Roger M. Gifford
40 years genetic yield potential of corn sufficiently to identify attributes that are was on sabbatical leave from the Division of Plant
Industry, Comrmonwealth Scientific and Industrial
hybrids increased about 50 percent (2) manipulable through management or by Research Organization, Post Office Box 1600, Can-
and peanuts nearly 100 percent (3) as chemical (plant growth modifiers) or ge- berra City, A.C.T. 2601, Australia. All correspon-
dence should be addressed to Robert T. Giaqumta,
modem genotypes, adapted to fertile en- netic means to increase crop yield. Research Manager, Agricultural Sciences.
24 AUGUST 1984 801
ment (9), is generally manifesttin im--- tory-of efforts to improve:photosynthetic culti-vars, released in Engiand du,ring a
proved economic yield (10). An;alysis of efficiency by breeding for various sub- period Pf 70 years (16) -e compared in
this correspondence between nelt overall components of crop photosynthetic CO2 Fig. 1. There was no trend in total shoot
carbon fixation per unit of grouind area fixation. These efforts have included dif- -dry weight yield when all cultiv8rs were
and yield can be taken a step fu rther by fusionally, biochemically, and photo- grown under the same fiekl conditions,
considering seasonally integrat' ;ed day- chemically determined steps. Several but grain yield had -increasedo 5 to 7
time net CO2 fixation by a fie-ld crop reasons-both physiological and meth- tons per hectare while HI tne-from 0.35
(night respiration excluded). T'his has odological-suggest why this approach to 0.5. Similarly, with a I,egum crop,
been done with soybean crops p1[anted at has not been successful (13). Important peanuts (3), the doubling of! podi yield
different densities and under different among these reasons is the complexity of was due primarily to increased HI rather
levels of shading (11) over 4 y(ears. A feedbacks in the crop photosynthetic than to increased total yield (Fig. 2),
broad linear relation was found 1between system. The hierarchy of regulations op- extra pods being produced- at the ex-
seed yield and seasonal daytime inet pho- erating over the full range of space and pense of vegetative plant parts (Fig. 3)
tosynthesis per unit of land areza. Many time from chloroplast membranes to (17). Similar patterns have been found
researchers have even sought to find field crop surface, and from less than for barley and soybeans (14).
relations between growth or yiield and nanoseconds for primary photochemical Such results concerning Othe impor-
net photosynthesis rates deternnined at events to months for seasonal growth tance of changes in dry -weight partition-
leaf, chloroplast, or enzymatic 1levels of appear to ensure that no single plant ing between organs- have focused atten-
organization, but they have n ot been attribute is rate limiting to CO2 fixation tion-on HI-as a specific selection criteri-
successful. for long, and that quantitative manipula- on. Although there must be an upper
tion of one attribute is compensated for limit to HI because of the-need for some
in time or space. So, although it is well investment in leaves and a robust stem,
Conversion of Intercepted established that total dry weight and it does not yet appear to have been
Light Photoassimilate
to economic crop yield can readily be in- reached in most crops. A limit of 0.62
creased by improving photosynthetic has been suggested for wheat (16). This
A typical rate of crop dry weiight pro- environment through CO2 or light en- compares with a value of about 0.5 for
duction per unit of seasonally initercept- richment in the field (9), it has not been best modem cultivars and 0.2 to 0.35 for
ed radiation (5, 12) is about 3 gr*ams per possible to improve yield by direct ge- traditional varieties. -Compared with
megajoule of light in the photossyntheti- netic or (nonsubstrate) chemical manipu- most photosynthetic- attributes, for
cally active wavelength band (40) to 700 lation of the photosynthetic system at which seasonally representative values
nanometers). There has been a Ilong his- levels of organization below that of leaf
canopy development. In fact, the pro-
. gressive increases in yield potential for _

15 _
crops such as wheat, barley, oats, and 0-
0

soybeans have not been associated with - 10


_-
14 0 0 increases in crop biomass. Similarly, in- C-.-
10
13 creased yields in cultivars of wheat, 'aas
o o
0fr

Oa
corn, tomato, and rice have occurred
O c 12 without any increase in relative growth
co._ rate of young plants (14). Over the his- 0

I l tory of improvement in genetic yield -

5I
c
potential of field crops, it has been the Q

0-
7 * partitioning of photosynthetic product 0
4
0
.* between economic yield and the rest of C
_
00
0
/ the plant ["harvest index" (HI) (14)] that c
6 0 has been of primary importance, even ._
co CL 3
'C
* though selection was not directed specif-
0
5 0
ically to that end. Harvest index, also 0.5
termed coefficient of economic yield,
.c
b. i 1 4~~~~~~~~~~~
- can apply to the ratio of harvested dry
0.5 [ weight to total aboveground dry weight MG 0.4
(shoot HI) or to the ratio of harvested
0.V
S
/ dry weight to above- plus belowground CD
0

0 0.4
- dry weight (plant HI). In the field, as- I 0.3
0
(D
0 0 sessing root dry weight can be extremely
difficult, so shoot HI is more commonly
0.3 used in agronomic studies. 0.2
1940 1960 1980
1900 1940 1 980 Cultivar introduction date
Cultivar introduction date Harvest Index Fig. 2. Comparative yield potential and HI for
Fig. 1. Comparative yield potential and HI for four major peanut cultivars from the southern
eight British winter wheat cultivars, plotted Improved HI was responsible for the United States, plotted against the year that
against the year that each cultivar was intro- grain yield potential increases among each cultivar was introduced. The cultivars
duced. The cultivars were grown in intensive- successively developed cultivars of the were grown in intensively managed experi-
ly. managed experimental plots at a high- mental plots in a favorable environment near
fertility site near Cambridge, England, in the major cereal species over the past centu- Gainesville, Florida, in the 1976 season.
1977-1978 season (16). ry (1, 14, 15). Eight major winter wheat [Adapted from W. G. Duncan et al. (3)]
802 SCIENCE, VOL. 225
in the field are difficult to obtain, HI -
simply measurable on a crop stand at the
end of the season without destroying the
nwxt generation of seed. Furthermore, in
pijing wheat, HI for spaced plants ap-
p&irs to be representative of the parame-
te fbor a community of plants (18).
Beders require easily measured selec-
tion criteria because of the large popula-
tions to be screened and the relative
difficulty of work in the field; they fre-
quently need to use spaced plants in the
early stages of new cultivar develop- 150
Days after planting
ment.
Recognition of the importance of parti- Fig. 3. Time course of total plant dry weight production ("total") and fruit growth ("pod") for
tioning of fixed carbon between alterna- the peanut cultivars grown in the study represented in Fig. 2. The cultivars are Dixie Runner
tive sinks in past improvements in genet- (released about 1943) and Early Bunch (1977). [Adapted from W. G. Duncan et al. (3)]
ic yield potential has led to much re-
search into the physiology and biochem- remain methodological uncertainties, tion or genetic engineering to suppress
istry involved. Figure 4B shows the main and figures based on other methods oxygenase activity while maintaining or
sinks for the gross quantity of carbon range as high as 50 percent (20). Since enhancing carboxylase activity. This
fixed in the leaves. It illustrates vividly the function of this apparently wasteful would have the double advantage of both
what a small proportion of carbon fixed partitioning is unknown, much research reducing the competitive effect of 02 at
is finally harvested. Figure 4A shows the has been directed at its reduction or the active site and reducing the photores-
typical fate of annual solar radiation inci- elimination by chemical or genetic piratory release of CO2. However, no
dent on crops. Carbon partitioning phe- means. one has been able to refute the argument
nomena start at the very point of carbon The photorespiratory pathway arises that the oxygenase reaction is a physio-
fixation with partitioning between the from an oxygenase activity possessed by chemically inevitable consequence of the
photosynthetic carbon reduction (PCR) ribulosebisphosphate carboxylase (21), carboxylase mechanism (23). Neverthe-
cycle and the photosynthetic carbon oxi- which catalyzes the primary CO2 fixa- less, recombinant DNA methodology
dation (PCO) cycle. They continue to be tion of photosynthesis. The substrate for provides a means for systematic manipu-
expressed in all aspects of carbon econo- both oxygenase and carboxylase activity lation of the amino acid composition of
my while harvestable yield is being gen- is the photosynthate intermediate ribu- ribulosephosphate carboxylase. This, to-
erated. For example, carbon is parti- lose-1,5-bisphosphate. This competition gether with investigation of the exact
tioned between starch storage in the between 02 and CO2 for the active site mechanisms of carboxylation and oxy-
chloroplast (for later mobilization) and in ribulosebisphosphate carboxylase re- genation, offers hope of creating an im-
immediate export into the mesophyll cell duces the gross rate of CO2 fixation (Fig. proved carboxylase/oxygenase ratio for
cytoplasm; between sucrose retention in 4B). A product of the oxygenase reaction crop species or at least of determining
leaf mesophyll and loading into the phlo- is phosphoglycolate. It is the subsequent why it is not possible to do so.
em for export; between retention in the multistep conversion of phosphoglyco-
phloem and unloading into growing late to phosphoglycerate, an intermedi-
sinks; between vegetative growth and ate required in the PCR cycle, that in- Starch Versus Sucrose
reproductive growth; and among com- volves release of photorespiratory CO2. Synthesis in Leaves
peting alternative sinks, such as root and This photorespiratory pathway also ac-
shoot, elongating wheat stem and ear complishes a partial recovery of carbon Early products of the PCR cycle in the
growth, or grains within an ear. Little is partitioned into phosphoglycolate. At- chloroplast are the triose phosphates,
known about the regulation of these pro- tempts to chemically inhibit phosphogly- phosphoglycerate, and dihydroxyace-
cesses. Given the numerous carbon par- colate metabolism to prevent the CO2 tone phosphate. These sugar phosphates
titioning steps that occur between pri- release have not been successful at in- are biochemically and spatially parti-
mary fixation of CO2 and final accumula- creasing net CO2 fixation: usually net tioned between two major biosynthetic
tion of a small fraction of the fixation fixation decreases instead (13). It seems pathways, one leading to the synthesis
product into harvested organs (Fig. 4B), that inhibition of any step in phosphogly- and retention of starch in the chloroplast
only a few aspects can be dealt with colate metabolism prevents a necessary and the other to sucrose synthesis in the
here. recycling of carbon back into the PCR cytoplasm. Up to 50 percent of the pho-
cycle, while the accumul4ted photorespi- tosynthetically fixed carbon can be allo-
ratory intermediates havve no capability cated either to starch or to sucrose de-
PCR Cycle Versus PCO Cycle of feedback regulation of the partitioning pending on several factors, including
between oxygenation and carboxylation plant species, environment, nutritional
Concurrent with photosynthetic car- of ribulosebisphosphate (22). This con- status, and developmental stage of the
bon fixation by the PCR cycle, the inter- clusion focused attention on the ratio of plant (24, 25). This partitioning is impor-
linked PCO cycle releases back to the carboxylase to oxygenase activity of ri- tant to plant growth because the forma-
atmosphere CO2 that was recently fixed. bulosebiphosphate carboxylase. Evi- tion of sucrose (the principal phloem
In C3 species the proportion of CO2 fixed dence suggesting that the ratio is not transport sugar in most crops) is a prime
by the PCR cycle that is partitioned back immutable has encouraged a search in determinant of carbon export from pho-
to CO2 by the PCO cycle is usually,found several laboratories for suitable manipu- tosynthesizing leaves and because leaf
to be 15 to 20 percent (19), but there lations of the protein structure by muta- starch is a major carbohydrate reserve
24 AUGUST 1984 803
that is mobilized to sucrose when current ose phosphates across the chloroplast the cytoplasm during sucrose synthesis
photosynthesis is low relative to sink envelope to the cytoplasm is stoichio- favors continued triose phosphate export
demand for photoassimilate, as occurs in metrically and obligatorily coupled in a from the chloroplast by counterexchange
low light or darkness (26) or, in the one-to-one counterexchange with inor- through the phosphate translocator.
longer term, when the leaves are senes- ganic phosphate (Pi) through this specific Thus, under conditions that favor su-
cing (27). translocator protein (28). In the cyto- crose synthesis, triose phosphates are
Dynamic and balanced partitioning of plasm, sucrose is synthesized from triose partitioned away from the starch biosyn-
the PCR-derived triose phosphates be- phosphates. Key enzymes involved are thetic pathway that resides in the chloro-
tween starch synthesis in the chloroplast fructose-bisphosphatase (FBPase) and plast. If sucrose synthesis in the cyto-
and sucrose synthesis in the cytoplasm sucrose-phosphate synthase (SPS) (29). plasm is reduced, triose phosphates re-
appears to be mediated by the levels of Sucrose synthesis is a phosphate-liberat- main within the chloroplast for starch
certain key metabolites and by the so- ing process (net reaction, 4 triose phos- synthesis. The resulting increase in
called phosphate translocator protein in phates + 3 H20 - 1 sucrose + 4 Pi). phosphoglycerate within the chloroplast
the chloroplast membrane. Export of tri- The liberation of inorganic phosphate in stroma (high phosphoglycerate to Pi ra-
tio) also favors starch synthesis by allo-
sterically activating the starch-synthesiz-
A ing enzyme adenosine diphosphate-glu-
cose pyrophosphorylase (30).
Studies on source-sink manipulations
of whole plants show that photosyntheti-
cally fixed carbon can be preferentially
ents (50 to 56)////f partitioned into sucrose available for ex-
port during periods of high sink demand
or retained by starch when sink demand
is low (31). However, in other plants,
export from photosynthesizing leaves
,oyveswron(60 se
o,//
to 7%~~ continues undiminished in response to a
rapid change in sink demand, at least in
4) the short term; the exported carbon ac-
5%)
cumulates in alternative sinks (32).
Fig. 4. (A) Fate of so- Starch synthesis and accumulation in
Ineffective absorption due to light saturatlion (20 to 40%) lar radiation incident leaves may be controlled indirectly by
over 1 year on a field the rate of sucrose synthesis. A growing
used for a typical body of evidence (29, 33) suggests that
grain crop in a tem- the FBPase and SPS are key regulating
perate agricultural
environment. (B) Par- enzymes in sucrose synthesis. As such,
titioning of gross pho- the activities of these enzymes, when
tosynthetic CO2 fixa- acting in coordination with the phos-
tion by a generalized phate translocator, may represent an im-
temperate grain crop.
B The values in paren- portant link between sink demand and
theses and relative rates of carbon partitioning into starch
width of the bars are and sucrose. For example, the level of
intended as guides to SPS in plants appears to be negatively
'iontopotential)~
X///,,,,,,,,,,,,,,,S,/////
the proportion of the
previous fractional correlated with the total starch content
flow remaining that is of leaves and with biochemical partition-
diverted into each ing of photosynthetic carbon into starch.
>OSe (1,51 to 20%) successive sink. For- Plants that form little starch, such as
aging by insects has wheat, barley, and spinach, have high
not been included be-
//////////////// cause of its extreme SPS activity compared to plants that
0 to 0variability. form large amounts of starch, such as
tobacco, peanuts, and soybeans. Intra-
specific differences in SPS activity and
carbon partitioning have been noted in
wheat (25). Recent studies of soybeans
XI0 toa 20%) 1,17.74, showed that altering the source-to-sink
ratio by partial defoliation, pod removal,
or changes in photosynthetic irradiance
zS/,,,,,,,,,,,,,,,,ble
pa rts (50 to 7 0%b'
. .........X at hoar,ves, ,3Z
caused changes within hours in extract-
~~~~Decayed before harvest M? able SPS activity and in starch and su-
crose synthesis (24, 34). These results
support the hypothesis that SPS activity
is important to starch-sucrose partition-
ing in leaves.
Regulation of FBPase is receiving in-
creased attention with the recent discov-
804 SCIENCE, VOL. 225
ery of fructose-2,6-bisphosphate (FBP) Utilization of the high-energy interme- Vegetative Versus Reproductive or
in plants. FBP plays an important regula- diates from respiration may be opera- Storage Growth
tory role in glycolysis and gluconeogene- tionally divided into that required for the
sis in animal liver (35). In plants the level processing of stored carbohydrate to The observed increase in HI for sever-
of FBP responds to changes in light, new growth and that required for main- al improved crop species reflects a shift
specific metabolites, sugars, and CO2. taining existing cells in a viable state from excessive vegetative development
That FBP is a potent inhibitor of cyto- (41). While it has been argued that the in traditional varieties to greater parti-
plasmic FBPase and sensitizes FBPase biosynthetic pathways that convert glu- tioning into fruits or other sinks for pho-
to the effects of FBP and Pi suggests that cose to the various lipids and nitroge- toassimilate, such as potato tubers or
it plays a key regulatory role in sucrose nous monomers required for growth are swollen storage roots, in modern culti-
biosynthesis (36). efficient (42), energy required for mainte- vars. The basis for this change can be
nance of existing cells may be as much as examined from two perspectives. The
50 percent of the overall respiration rate first concerns the timing and establish-
Catabolism Versus Anabolism in whole plants, and the utilization of this ment of large -numbers of fertile flowers
energy is poorly understood. If the con- or other storage organ initials. The sec-
Energy for growth and maintenance of tinuous breakdown and resynthesis of ond concerns regulation of transport and
plant structure and for ion uptake is existing cellular compounds (turnover) partitioning of current photoassimilate
derived largely from respiratory catabo- could be slowed, or if the energetic cost and prior reserves into these developing
lism ofphotosynthetically derived sugars of maintaining inter- and intracellular harvestable organs rather than into fur-
to CO2 and water (37). Up to 50 percent chemical and electrochemical gradients ther branching, rooting, or ineffective
of the net CO2 fixation by leaves of an across membranes could be reduced, flowering.
annual plant may ultimately be lost to the more carbon might be available for eco- For traditional varieties of species
plant by subsequent respiration. Crop nomic yield. from which seeds are harvested, such as
scientists have long questioned whether While improvement of respiratory effi- cereals and grain legumes, the number of
the partitioning of photosynthetically ciency may not have the potential for flowers formed and fertilized far exceeds
fixed carbon between biosynthesis very large yield increases, there is evi- the number that fill to mature seeds.
(anabolism) and respiration (catabolism) dence of increased plant growth rate and Despite having less reproductive redun-
could be shifted in favor of more biosyn- yield in association with decreased respi- dancy, modern high-yielding cultivars
thesis. Can respiratory efficiency be im- ration. In corn and tall fescue genotypes still have much fruitless flowering. In
proved, and if so, would it improve crop possessing high growth rates, low rates terms of yield components, however, the
yield? of leaf respiration were found (43). More improvement during the era of systemat-
Two possible routes to greater effi- directly, selection for intravarietal varia- ic breeding has mostly involved number
ciency in respiratory utilization of fixed tion in respiration rate of mature leaf of fruits harvested per hectare rather
carbon can be envisioned. Either the segments of perennial ryegrass readily than fruit size.
efficiency of conversion of stored carbo- gave lines with high or low respiration A key to high yield is the establish-
hydrate to adenosine triphosphate might rates. Measurement of forage yield under ment of a large number of seeds before
be increased or utilization of adenosine simulated cropping conditions in both their rapid filling commences. Barring
triphosphate for processes not strictly greenhouse and field studies (44) showed extraordinary weather or other calamity,
required for plant growth in the crop that the lines with low respiration rates once seed number has been established
environment might be reduced. had a consistent 6 to 13 percent greater mature yield has largely been predeter-
While bioenergeticists traditionally annual dry matter yield than the parent mined. The average mature weight per
have viewed respiration as an optimized population from which they were de- seed is a more conservative property of a
process under tight control, in plants rived. This increase came primarily from cultivar than is seed number per hectare.
there is an alternative terminal oxidase later summer cuttings in a continuous These generalizations can be illustrated
that transfers electrons from the cyto- cropping regime, when growth tempera- with wheat. Two weeks before pollina-
chrome oxidase chain to oxygen at ubi- ture was relatively high and the amount tion starts, a modern dwarf wheat has
quinone. This cyanide-insensitive alter- of root and stem tissue was large. As several times more partly developed
native oxidase is not coupled to adeno- such, it may indicate that some portion flowers than will set and fill grain (46).
sine triphosphate synthesis (38) and as of the maintenance respiration require- Each spikelet (that is, inflorescence
such appears to be wasteful of energy. ment was decreased in these lines. branchlet) in the central part of the spike
The pathway is found in many species, in The metabolic basis for this reduction can have nine to ten primordial florets.
both shoots and roots (39, 40), but does in respiration is not known, nor is there However, about two of these florets
not operate until the capacity of the any indication that yield increases asso- have ill-formed anthers'that render them
cytochrome oxidase system has been ciated with it would necessarily follow if incompetent to set grain. During the 2
exceeded or blocked after ubiquinone. genotypes with such reduced respiration weeks before pollination there is a col-
Considering the degree of engagement of were established in annual grain crops. lapse in floret competency, such that
the pathway in roots, it was calculated About half of the yield increase was typically only two or three florets will
that in wheat the carbon loss to that associated with an improved ability of actually set grain. This 60 to 70 percent
pathway was at least 6 percent of the the lines with low respiration rates to loss of competency to set grain appears
carbon in final grain yield (39). If a loss establish new leaf cover after defoliation to be closely related to the supply of
of such magnitude occurs and can be (45). So the yield enhancement from a photosynthetic assimilates at the time.
shown not to be associated with an es- reduction in respiration rate might not be Consequently, in the 10- to 20-day period
sential function, its elimination could significant in annual grain crops, which before pollination final seed number is
translate into a significant increase in the are not required to undergo multiple re- particularly sensitive to irradiance. Low
partitioning of carbon to economic yield. growth. light at that time can cause an irretriev-
24 AUGUST 1984 805
able loss of yield because fewer seeds mesophyll cells; (iii) intracellular com- occur at the carrier level or by a cell
are established (47). As a consequence of partmentation between cytoplasm and turgor-dependent process in which in-
this sensitivity of floret abortion to pho- vacuole; (iv) compartmentation between formation about the rate of unloading in
toassimilate supply in temperate cereals, the symplast (or intracellular volume) sinks is relayed instantly to the source as
CO2 enrichment to boost photosynthesis and apoplast (or extracellular "free a hydrostatic pressure change in the
of field crops before anthesis can raise space" in cell walls and intracellular whole transport network or by changes
final yield by increasing grain number spaces); and (v) accumulation of solutes in the rate of water entry into the sieve
per unit of ground area (48). By contrast, by the sieve element-companion cell elements (54).
CO2 enrichment after anthesis has a less- complex of the vascular tissue. The size, The sieve elements form a continuous
er effect on yield. distribution, and composition of these transport network throughout the plant,
Although the main component of vari- various pools varies with species and with numerous branches and anastomo-
ation in yield of wheat (and other spe- with translocation status of the plant. In ses. There is no evidence of one-way
cies) is the seed number per unit of soybean leaves, for example, there is a valves, so in principle any source leaf
ground area, mean seed weight can nev- preferential net accumulation of starch in can supply solutes to any sink without
ertheless vary somewhat by improved the second palisade mesophyll layer dur- leaving the sieve tube network. Experi-
photoassimilate supply (48, 49) and cer- ing the stage from flowering to early seed ments with radioactively labeled solutes
tainly differs among genotypes. Just as filling. This starch does not turn over show that in some species there are
kernel number is established before rap- diurnally. It is a longer term reserve, preferred routes from certain source
id grain filling gets under way, so is the being mobilized during the middle to late leaves to certain sinks but that selective
average potential size of the seed. This is stages of seed filling, when leaf photo- leaf or sink removal rapidly alters the
closely related to the mean number of synthesis has markedly declined (27). pattern of movement in most species (15,
cells per seed in other species as well as A portion of the sucrose synthesized 55). It seems unlikely that source leaves
cereals (50). Cell division in the starchy through FBPase and SPS in the cyto- have mechanisms to determine where
endosperm of wheat is virtually com- plasm is stored in the vacuoles. Kinetic their solutes are destined (56). General-
plete within 2 weeks after pollination studies (53) show that the cytoplasmic ly, the preferred channels of transport
(51). Once kernel number per unit of (or transport) sucrose pool has a much seem to be associated more with the
ground area and cell number per kernel faster turnover than the larger vacuolar least resistive vascular route between
are established, the filling of the grain pool, which is less available for immedi- source and sink (15).
usually proceeds rapidly (in about 4 to 6 ate export through the mesophyll toward Although the mechanism of long-dis-
weeks) to a substantially predetermined the veins. The vacuolar sucrose pool, tance transport has not been unequivo-
mean kernel size. From that perspective, exchangeable with the cytoplasmic pool, cally proven, the consensus is that there
by 2 weeks after grain set the partitioning is the first source for export during the is a bulk flow of solution along sieve
of photoassimilate appears to be largely night. Starch appears to be mobilized to tubes under the influence of a hydrostat-
regulated by the filling sinks themselves. sucrose at night only when the vacuole ic pressure gradient. This gradient is
The physiology behind such regulation pool is substantially depleted. maintained osmotically by regulated
has attracted much research: regulation The sieve element-companion cell loading of solutes into the sieve element-
of CO2 fixation rate per unit of leaf area complex of the phloem contains a much companion cell symplast in source re-
by sink demand; control over the or- higher concentration of sucrose than the gions and regulated unloading in sink
dered senescence of the leaf canopy by surrounding tissues. The partitioning regions. Measurement of sieve element
storage sinks; and regulation of the day- step leading to that high concentration is sucrose concentrations and gradients in
to-day partitioning of current photoassi- called phloem loading. The following sugarbeets, soybeans, and other species
milate between competing alternative sketch, based on detailed reviews (54), is showed them to be sufficient to generate
sinks. The last of these topics has been our currently favored view of how phlo- the necessary hydrostatic pressure gradi-
studied phenomonologically by estab- em loading occurs. ent (57). Long-distance transport seems
lishing principles of competition between The intricately reticulated network of unlikely to impose appreciable limitation
sinks of different sizes and distances veins in leaves ensures that no more than on the rate of transport from sources to
from the source (52). It is also being two or three cells need be traversed sinks even when partial incisions or re-
studied by tracing the mechanisms and between photosynthetic mesophyll cells strictions are made in the dominant
potential points of regulation of carbon and sugar-accumulating phloem cells. transport routes (15, 58)-alternative
compound flow between chloroplasts in Photoassimilates, mostly sucrose, travel paths appear to take over.
the leaves to uptake in cells of the devel- symplastically down their concentration The discussion so far suggests that
oping sink. gradients to the mesophyll cells close to photosynthesis and the mechanism of
the companion or phloem parenchyma phloem loading determines the amount
cells, where they are released without of photosynthetic assimilate made avail-
Carbon Transport from Source to Sink hydrolysis by a facilitated efflux mecha- able for translocation, whereas the
nism into an apoplastic solution of rela- mechanism and kinetics of unloading
Complementary to biochemical parti- tively low concentration. An energy-re- into, and associated uptake by, compet-
tioning between sucrose and starch is quiring active process then loads sucrose ing sinks, in association with relative
physical compartmentation of these into the phloem, creating a high sucrose distances between sources and sinks,
products in the leaf. Histochemical and concentration in the sieve tube symplast. determines the partitioning of loaded ma-
kinetic studies show at least five major This energetically "uphill" loading of terial in the short term.
types of photoassimilate compartmenta- sucrose appears to occur, at least in part, Less is known of the regulation and
tion in leaves: (i) differential starch stor- by a plasmalemma-bound, sucrose-spe- coordination of phloem unloading (solute
age among the different leaf cell types; cific carrier involving a sucrose-proton efflux from the phloem and interconnect-
(ii) different sucrose storage pools among cotransport mechanism. Regulation may ed tissues of the vascular bundles) than
806 SCIENCE, VOL. 225
of the subsequent uptake and assimila- mercially useful sinks. In grain crops developments through genetic engineer-
tion of solutes for growth and storage improving crop photosynthesis rate by ing, and although yield-enhancing chemi-
product formation in sink tissues. The environmental amelioration is most cals hold promise, the complexity of
diversity of sink types suggests that effective at increasing yield (by increas- yield and our lack of understanding of
there are several mechanisms of unload- ing the number of grains competent to plant physiology and development are
ing. fill) if effected before grain filling starts. such that the rational design of such
Unloading from the vascular bundles Increasing sink size (grain number per approaches for yield improvement is
can be through symplastic plasmodesma- hectare) by chemical or breeding meth- only in its infancy.
tal connections to growing cells, as in ods is likely to be an effective route to
pea and corn roots (59) and in young higher yields of seed crops; this will References and Notes
leaves (60), or unloading may be across a involve prevention of abscission or abor- 1. K. J. Frey, in Genetic Engineering for Crop
Improvement, K. 0. Rachie and J. M. Lyman,
cell membrane into the apoplast of the tion of flowers and young seeds while Eds. (Rockefeller Foundation, New York,
sink cells, as in sugarbeet tap roots (61) retaining the ability to fill these extra 1981), p. 15.
2. D. N. Duvick, Maydica 22, 187 (1977).
and in the storage stem of sugarcane sinks. 3. W. G. Duncan, D. E. McCloud, R. L. McGraw,
(62). In crop seeds solutes may first pass The rate of growth of established, de- K. J. Boote, Crop Sci. 18, 1015 (1978).
4. S. H. Wittwer, Science 188, 579 (1975).
symplastically from the phloem through veloping seeds seems to be determined 5. J. L. Monteith, Philos. Trans. R. Soc. London
Ser. B 281, 277 (1977).
one or more maternal seed coat tissues primarily by phenomena operating either 6. A. F. Hawkins, Outlook Agric. 11, 104 (1982).
before entering the apoplast of the em- at the stages of unloading of photoassi- 7. T. J. Johnston, J. W. Pendleton, D. B. Peters,
D. R. Hicks, Crop Sci. 9, 577 (1969); J. B.
bryonic sink. Furthermore, solutes (prin- milate into the extracellular solution sur- Schoper, R. R. Johnson, R. J. Lambert, ibid. 22,
cipally sucrose and amino acids) may rounding seed cells or accumulation and 1184 (1982).
8. One hundred percent light interception is im-
remain unaltered during unloading or, conversion to storage product of this practical. The leaf area index giving 95 percent
alternatively, be partially metabolized unloaded photoassimilate. However, if interception is termed critical leaf area index,
being that which for practical purposes gives
after (or during) unloading (63). HI is further increased, the ability of the maximum growth rate and is taken to constitute
full interception [R. W. Broughham, Aust. J.
The seed coat of the developing le- reduced photosynthetic surface per sink Agric. Res. 7, 377 (1956)].
gume seed is proving to be a convenient organ to supply the necessary photoassi- 9. D. B. Egli, J. W. Pendleton, D. B. Peters,
Agron. J. 62, 411 (1970); R. M. Gifford, in
system for studying unloading (64). In milate will be reduced, leading to a great- Photosynthesis, vol. 2, Carbon Metabolism and
that system, the phloem reticulates to er prospect for improvement in net pho- Plant Productivity, Govindjee, Ed. (Academic
Press, New York, 1983), p. 459.
varying degrees, depending on species, tosynthesis rate per unit of leaf area 10. This may not be true when attempts to increase
light interception by high-density planting are
throughout the seed coat, supplying as- being expressed in higher grain yield. made. For example, maize can suffer reduced
similates to the embryo across the apo- In leaves, partitioning of fixed carbon grain yield due to infertility in high-density
plantings; sugarbeets may have a reduced sugar
plast separating the two generations. Un- between its retention in the plant and its yield in plantings giving a maximum leaf area
loading from the seed coat appears to photorespiratory release is readily main- index greater than 3, even though total crop dry
weight may respond to a leaf area index of S [P.
involve an energy-dependent, carrier- tained by environmental change, but has J. Goodman, Agric. Prog. 20, 1 (1966)].
mediated process (65), rather than just so far defied attempts at genetic alter- 11. A. L. Christy and C. A. Porter, in Photosynthe-
sis, vol. 2, Carbon Metabolism and Plant Pro-
the passive leakage postulated earlier ation. The potential agronomic rewards ductivity, Govindjee, Ed. (Academic Press,
(15), despite a large downhill concentra- for success are so high, however, that New York, 1983), p. 499.
12. J. N. Gallagher and P. V. Biscoe, J. Agric. Sci.
tion gradient from sieve tube symplast to the remaining avenues in that endeavor 91, 47 (1978).
13. R. M. Gifford and C. L. D. Jenkins, in Photo-
embryo apoplast. This suggests that un- must be followed. Conversely, the ap- synthesis, vol. 2, Carbon Metabolism and Plant
loading may serve as a potential control parent scope for improving partitioning Productivity, Govindjee, Ed. (Academic Press,
New York, 1983), p. 419.
point in source-to-sink transfer of photo- of fixed carbon between carbon skele- 14. C. M. Donald and J. Hamblin, Adv. Agron. 28,
synthate and in intraplant competition tons for plant synthesis on the one hand, 361 (1976); L. T. Evans, in Genetic Engineering
of Plants, T. Kosuge et al., Eds. (Plenum, New
for photoassimilate. and substrate for respiration on the oth- York, 1983), p. 499.
er, is relatively small but appears to have 15. R. M. Gifford and L. T. Evans, Annu. Rev.
Plant. Physiol. 32, 485 (1981).
been effectively exploited in perennial 16. R. B. Austin et al., J. Agric. Sci. 94, 675 (1980).
17. Although total dry weight yield did not change,
Assessment and Conclusions ryegrass. It is yet to be seen whether this example of peanuts may in fact be indirect
some detrimental consequences follow evidence of an inadvertent increase in photosyn-
thesis energy fixation with successive cultivars.
In terms of carbon economy, the route or whether similar experience can be had This is because the energy content of unit nut
to increased commercial yield can be with annual crop species. dry weight (high lipid and protein) is higher than
that for unit dry weight of vegetative parts it
from either the carbon source (photosyn- The apparent success at improving replaced.
thesis) or the carbon sink (commercial ryegrass yield by selecting against ma- 18. R. A. Fisher and Z. Kertesz, Crop Sci. 16, 55
(1976).
product), but preferably both simulta- ture leaf respiration is surprising: the 19. D. T. Canvin, in Encyclopaedia of Plant Physi-
ology, M. Gibbs and E. Latzko, Eds. (Springer-
neously. High-yield cultivars and good more general experience in attempts to Verlag, Berlin, 1979), vQl. 6, p. 368.
management strategies are those that are use physiological and biochemical 20. A. Gerbaud and M. Andre, Plant Physiol. 64,
735 (1979); I. Zelitch, in Encyclopaedia of Plant
successful at maximizing the amount of knowledge to suggest selection criteria Physiology, vol. 6, Photosynthesis Two, M.
solar radiation intercepted seasonally by or chemical targets for improvement in Gibbs and E. Latzko, Eds. (Springer-Verlag,
Berlin, 1979), p. 353.
foliage without excessive investment of genetic yield potential has been one of 21. G. Bowes, W. L. Ogren, R. H. Hageman,
plant matter into vegetative rather than disappointment born of system complex- Biochem. Biophys. Res. Commun. 45, 716
(1971).
reproductive parts. In a given environ- ity. This complexity results largely be- 22. J. C. Servaites and W. L. Ogren, Plant Physiol.
60, 461 (1977).
ment, breeding has not so far been suc- cause yield is governed by numerous 23. G. H. Lorimer and T. J. Andrews Nature (Lon-
cessful at increasing yield through in- polygenic, organismic, and community don) 243, 359 (1973); T. J. Andrews and G. H.
Lorimer, FEBS Lett._90, 1 (1978).
creasing net photosynthesis rate per unit traits that have enormous plasticity as a 24. E. Silvius, N. J. Chatterton, D. F. Kremer,
J.
of photosynthetic tissue, but has been crop develops with multiple colimiting Plant Physiol. 64, 872 (1979).
25. S. C. Huber, Z. Pflanzenphysiol. 101, 49 (1981).
very successful at increasing the interor- factors-both metabolic and environ- 26. B. R. Fondy and D. R. Geiger, Plant Physiol.
gan partitioning of dry matter from un- mental. Although some claim that the art 70, 671 (1982).
27. V. R. Franceschi and R. T. Giaquinta, Planta
necessary vegetative parts to the com- of breeding is on the brink of substantial 157, 422 (1983).
24 AUGUST 1984 807
28. H. W. Heldt, C. J. Chen, D. Maronde, A. (1965); F. W. T. Penning de Vries, Neth. J. Scott-Russell [J. Exp. Bot. 15, 457 (1964)] is
Herold, Z. S. Stankovic, D. A. Walker, A. Agric. Sci. 22, 40 (1974). difficult to interpret without invoking destina-
Kraminer, M. R. Kirk, U. Heber, Plant Physiol. 42. D. K. McDermitt and R. S. Loomis, Ann. Bot. tion control by leaves.
59, 1146 (1977). 48, 285 (1981). 57. R. J. Fellows and D. R. Geiger, Plant Physiol.
29. M. Stitt, W. Wirtz, H. W. Heldt, ibid. 72, 767 43. G. H. Heichel, Photosynthetica 5, 93 (1971); W. 54, 877 (1974); D. R. Geiger, in Transport in
(1983). D. H.-nson, Crop Sci. 11, 334 (1971); R. J. Jones Plants, M. H. Zimmermann and J. A. Milbum,
30. J. Preiss and C. Levi, in The Biochemistry of and C. J. Nelson, ibid. 19, 367 (1979). Eds. (Springer-Verlag, New York, 1975), vol. 1,
Plants: A Comprehensive Treatise, vol. 3, Car- 44. D. Wilson, Ann. Bot. 49, 303 (1982);,_ and p. 395; D. B. Fisher, Planta 139, 19 (1978).
bohydrates: Structure and Function, J. Preiss, J. G. Jones, ibid., p. 313. 58. F. L. Milthorpe and J. Moorby, Annu. Rev.
Ed. (Academic Press, New York, 1980), p. 371. 45. M. J. Robson, ibid., p. 321. Plant Physiol. 20, 117 (1969).
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54, 201 (1974). Plant Physiol. 7, 169 (1980). (1975); R. T. Giaquinta, W. Lin, N. L. Sadler,
32. B. R. Fondy and D. R. Geiger, ibid. 66, 945 47. R. A. Fischer, Crop Sci. 15, 607 (1975); L. T. V. R. Franceschi, Plant Physiol. 72, 362 (1983).
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(1983). 49. R. A. Fischer and D. HilleRisLambers, ibid. 29, R. E. Wyse, ibid. 64, 837 (1979).
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Uyeda, Proc. Natl. Acad. Sci. U.S.A. 79, 4322 50. P. A. Brocklehurst, Nature (London) 266, 348 471 (1972).
(1982); M. Stitt, G. Mieskes, H.-D. Soling, H. (1977); D. B. Egli, Field Crops Res. 4, 1 (1981). 63. R. T. Giaquinta, in The Biochemistry of Plants:
W. Heldt, FEBS Lett. 145, 217 (1982). 51. A. D. Evers, Ann. Bot. 34, 547 (1970). A Comprehensive Treatise, vol. 3, Carbohy-
36. M. Stitt, R. Gerhardt, B. Kurzel, H. W. Heldt, 52. M. G. Cook and L. T. Evans, Aust. J. Plant drates: Structure and Function, J. Preiss, Ed.
Plant Physiol. 72, 1139 (1983). Physiol. 5, 495 (1978). (Academic Press, New York, 1980), p. 271.
37. In chloroplasts some photosynthetically derived 53. D. R. Geiger, B. J. Ploeger, T. C. Fox, B. R. 64. J. H. Thorne and R. M. Rainbird, Plant Physiol.
adenosine triphosphate and reduced nicotin- Fondy, Plant Physiol. 72, 964 (1983). 72, 268 (1983); P. Wolswinkel and A. Ammerlan,
amide adenine dinucleotide phosphate may be 54. R. T. Giaquinta, Annu. Rev. Plant Physiol. 34, Planta 158, 205 (1983); J. W. Patrick, Z. Pfan-
used directly. 347 (1983); L. C. Ho and D. A. Baker, Physiol. zenphysiol. 111, 9 (1983).
38. B. T. Storey, in The Biochemistry of Plants: A Plant. 56, 225 (1982); D. R. Geiger and R. T. 65. Sucrose concentrations in the apoplast of seeds
Comprehensive Treatise, vol. 2, Metabolism Giaquinta, in Photosynthesis: C02 Assimilation have been reported as 90 to 130 mM for Phaseo-
and Respiration, D. D. Davies, Ed. (Academic and Plant Productivity, Govindjee, Ed. (Aca- lus vulgaris [J. W. Patrick and R. McDonald,
Press, New York, 1980), p. 125; G. Laties, demic Press, New York, 1982), p. 345. Aust. J. Plant. Physiol. 7, 671 (1980)], 5 to 40
Annu. Rev. Plant; Physiol. 33, 519 (1982). 55. B. K. Singh and R. K. Pandney [Aust. J. Plant mM for soybeans (Glycine max) [A. B. Bennett
39. H. Lambers, Physiol. Plant. 55, 478 (1982). Physiol. 7, 727 (1980)] reported that chickpeas and R. M. Spanswick, Plant Physiol. 72, 781
40. _ _, D. Day, J. Azcon-Bieto, Plant Physiol. lack the ability to switch transport from one (1983)], and 10 to 50 mM for wheat (Triticum
72, 598 (1983). branch to another after selective defoliation. aestivum) [L. C. Ho and R. M. Gifford, J. Exp.
41. S. J. Pirt, Proc. R. Soc. London Ser. B 163, 224 56. Evidence obtained by J. Moorby and R. S. Bot. 35, 54 (1984)].

RESEARCH ARTICLE melt procedure. Purification of parasite


DNA is critical for these experiments
since one nucleated host cell per 100
parasites would result in approximately a
50 percent contamination due to differ-
Evolutionary Relatedness of ences in total genome size. Each prepa-
ration of parasite DNA was tested for
Plasmodium Species as Determined purity as described (see legend to Fig. 1).
Plasmodium falciparum DNA that had
by the Structure of DNA been analyzed previously (3) was used as
a control. Plasmodium falciparum para-
Thomas F. McCutchan, John B. Dame sites in continuous culture in human
erythrocytes in vitro (5) were nearly free
Louis H. Miller, John Barnwell of nucleated host cells. The P. falcip-
arum DNA was radiolabeled by nick
translation with either deoxyadenosine
triphosphate or deoxycytidine triphos-
Malaria parasites are classified in the closely related to rodent and avian ma- phate and the dG * dC content was deter-
genus Plasmodium. Historically, the larias than to other primate malarias. mined. The melting temperature (Tm) of
species were grouped according to the Further, our data allow us to suggest both deoxyadenosine- and deoxycyti-
hosts that they infected and then were which common characteristics of differ- dine-labeled DNA indicated a -dG * dC
subdivided according to morphological ent Plasmodium species are the result of content of 18 percent, consistent with
and biological characters (1, 2). Thus direct inheritance and which may be the the published figure (3). Plasmodium
Plasmodium species are classified into result of independently occurring but berghei DNA was extracted from infect-
primate, rodent, avian, and lizard malar- convergent events. ed mouse erythrocytes (6) and was fur-
ias. The implication is that the parasites ther purified by Hg2+CsSO4 or Hoechst
have evolved with their hosts and that dye CsCl gradients as shown below. The
there is greater relatedness among para- Analysis of Base Composition dG * dC content of the P. berghei DNA
sites in related hosts than those in hosts was found to be 18 percent. It had previ-
greatly separated in evolution. In the The deoxyguanosine deoxycytidine ously been reported to be 24 percent (4).
present article we examine this hypothe- (dG dC) content of DNA from P. fal- The difference probably can be attribut-
sis using analysis of base composition ciparum (3) and P. berghei (4) (18 and 24 ed to host DNA contamination in the
and organization of DNA from various percent, respectively) differs greatly previous study. Determination of the
species of Plasmodium. We find a major from that of the mammalian host (-37 dG * dC content of P. knowlesi, a malaria
exception to the classically derived orga- percent). We purified DNA samples
nization of the malarial evolutionary from P. falciparum, P. knowlesi, and P. H.Thomas F. McCutchan, John B. Dame, and Louis
Miller are in the Laboratory of Parasitic Dis-
tree. Surprisingly, P. falciparum, the berghei, tested them for host DNA con- eases, National Institutes of Health, Bethesda,
malaria of man that causes the most tamination, and then analyzed them for Maryland 20205. John Barnwell is in the Division of
Parasitology, New York University Medical School,
morbidity and mortality, appears more total dG * dC content by a DNA duplex New York 10010.
808 SCIENCE, VOL. 225

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