Responses to prolonged mid-season water stress: Research
at CIAT (Connor et al., 1981; Porto, 1983; El-Sharkawy and Cock,
1987b) has shown that cassava tolerates a relatively long period of
drought once the crop is established. In these studies, using a
limited number of varieties, a stress period of 2-3 months was
imposed 3-4 months after planting. The crop was later allowed to
recover from stress for the rest of the growing cycle with the aid of
rainfall and supplementary irrigation.
Figure 1
presents the relationship of yield with the seasonal average leaf
area index (LAI) for four contrasting varieties, as affected by a
prolonged mid-season water stress conducted in two separate field
trials (El-Sharkawy and Cock, 1987b). The highest reference (100%)
yields were 19 t ha-1 dry root for CM
507-37 under nonstressed conditions over 345 d in Experiment I (El-Sharkawy and Cock, 1987b) and 11.2 t ha-1
for M Col 22 under non-stressed conditions for 306 d in Experiment
II (Connor et al., 1981). Compared with the control, the final root
yields of the stressed crop were increased in vegetative vigorous
varieties (e.g., M Mex 59); were reduced in less vigorous types
(e.g., M Col 22); and slightly reduced or remained unchanged in
varieties with intermediate vigor (e.g., the parent M Col 1684 and
the its hybrid CM 507-37). These responses were closely related to leaf
area characteristics (i.e., peak LAI and leaf area duration over the
growing cycle), and to patterns of photoassimilate partitioning
between top growth (stems and leaves) and storage roots. The vigorous
types responded positively to stress because top growth was reduced
and the harvest index was increased, whereas the less vigorous types
responded negatively because leaf area was drastically reduced to
levels below optimal LAI for root yield (El-Sharkawy and Cock, 1987b).
The stability of root yields in intermediate types under both
favorable and stressful environments stemmed from an ability to
maintain leaf area near optimum during a major part of the growing
cycle. Also, the relationship between leaf area and storage root
yield is very important when cassava is subjected to a cold period
coupled with water shortages in the subtropics where leaf area is
reduced. Under these conditions, the crop requires a second warm-wet
cycle for leaf area recovery and for attaining higher yields (Sagrilo
et al., 2006). A similar ideotype approach was followed in studying
tolerance to water stress in various crops including winter and
spring wheat, maize, sorghum, millets, cowpea and coffee (Kirkham,
1980, 1988; Kirkham et al., 1984; Blum and Sullivan, 1986; Blum and
Pnuel, 1990; Bolaños and Edmeades, 1993a,b; Bolanños et al., 1993;
Whan et al., 1993; Richards, 2000; Hall, 2004; DaMatta and Ramalho,
2006). This information on the mode of response to water shortages is
fundamental for a cassava breeding strategy and points to the need
for selecting different plant types for different environments, a
strategy later adopted by CIAT and IITA, (Hershey and Jennings, 1992;
El-Sharkawy, 1993; Iglesias et al., 1995; Iglesias and Brekelbaum,
1996) and by national cassava programs, as in Brazil (Fukuda et al.,
1992-1993). 
Nevertheless,
CIAT researchers needed to know to what extent cassava can tolerate a
more prolonged period of water stress imposed at an earlier stage of
growth. They also needed to simulate, as closely as possible, the
common cassava-farming practice of planting cassava near the end of a
rainy season, letting it pass through a long period of no rain, and
then allowing it to recover in a second wet cycle. This objective was
addressed using larger group of varieties.
Responses to prolonged early water stress: In the 1987-1988 season, eight cassava varieties (Table 1) were planted in a field drainage lysimeter (the total area, including borders, was about 3000 m2)
at the CIAT research station at Santander de Quilichao, Cauca
Department, Colombia, on 25 November 1987. Planting density was 12 500
plants ha-1 in ridge, plot size was 25 m2 and
there were four replications per variety and treatment. Plants were
adequately fertilized and the plots were kept weed-free manually.
Because of rainfall deficits in December 1987 (94 mm) and January
1988 (81 mm), three irrigations were applied to ensure cassava
sprouting and establishment. Two months after planting, before
imposing the stress, supplementary irrigation was applied to bring the
soil-water content to near field capacity within the 2.3-m soil
depth. The available soil water within the 2.3-m profile of the
experimental site was about 250 mm (between -0.03 and -1.5 MPa). Half
of the experimental area was covered with white plastic sheets to
exclude rainfall from day 60 to day 180 after planting. At this stage
of growth, cassava had less than 0.8 LAI and less than 2 t ha-1
total dry biomass, with no visible storage roots (Connor et al.,
1981; Porto, 1983; CIAT, 1987-1989; El-Sharkawy and Cock, 1987b;
Pellet and El-Sharkawy, 1993, 1997). During the stress period of four
months, the control plot received about 540 mm of rain, together
with three heavy irrigations within the first and second month, to
compensate for the rainfall deficits in that period.
The total amount of water received by the control plot in four
months was greater than the potential evapotranspiration at the
Quilichao Experiment Station (about 4.2 mm d-1). In the
stressed plots, water was removed manually immediately after
rainfalls and any cracks in the plastic sheets were sealed. The
plastic cover was removed during the first week of June 1988. By the
end of the stress period, the total water extracted from 2.3 m soil
depth ranged among varieties from 168 to 200 mm. From 1 June to 20
October, the total rainfall was 656 mm. Supplementary irrigation to both
the stressed and control plots was applied twice in June, July, and
August to compensate for the low rainfall during that period. The
total rainfall received from planting to harvest was 1406 mm in the
control and 865 mm in the stressed plots.
During the stress period, field measurements of leaf gas exchange, both CO2 uptake and H2O loss, were made with a portable, infrared CO2 analyzer (LI-COR model LI-6000) on single, attached, upper canopy leaves at solar radiation greater than 1000 µmol m-2 s-1
of PAR. These measurements were normally made between 0900 and 1300 h
once a week within the first two months, and once every two weeks
within the last two months of stress. Light interception, leaf water
potential, and soil water content were also monitored. Final harvest
was made on 20 October 1988 (11 months after planting) and the total
standing biomass, root yield and dry matter contents of roots were
determined.
Table 1
summarizes data of final standing total biomass, root yields,
harvest index, and dry matter contents of storage roots. In the
control plot, the total dried biomass ranged (in round figures) among
varieties from 23 to 38 t ha-1 , fresh roots from 42 to 60 t ha-1, dried roots from 14 to 21 t ha-1;
dry matter contents from 32% to 39%; and the harvest index from 45%
to 71%. In the stressed plot, the ranges were (again in round
figures) 18 to 28 t ha-1 for total biomass, 41 to 59 t ha-1 for fresh roots, 14 to 19 t ha-1 for dried roots, 30% to 38% for dry matter contents, and 62% to 76% for harvest index.
There
were notable varietal differences in response to stress. Fresh and
dried-root yields were decreased by stress in the parent M Col 1684,
whereas they increased in its hybrid CM 507-37. Previous studies with
these two genetically related varieties (CM 507-37 is a hybrid between
M Col 1684 and M Col 1438) have shown that CM 507-37 is more
vegetative vigorous and leafy (El-Sharkawy and Cock, 1987b,
El-Sharkawy et al.,1992b). In other varieties, the yields were
relatively unchanged, except for CM 2136-2, where dried-root yields
decreased notably, mainly because of reduction in dry-matter contents
from 35.5% to 31.1%.
Compared
with the control, water stress across all varieties caused a
reduction in total biomass by 12%, no change in fresh root yields, a
reduction in dried-root yields by 3.4%, a reduction in dry matter
contents by 3.3%, and an increase in the harvest index by 10%. These
data clearly demonstrate cassava's ability to tolerate prolonged
water stress when it is induced gradually at an early stage of
growth. Furthermore, the crop is able to recover and compensate, in
terms of economic yields, from the adverse effects of stress. In
areas with intermittent rainfall and with long periods of drought,
cassava should produce reasonably well, providing good crop management
(e.g., weed control and adequate fertilization) is practiced and
cassava is grown in deep soils with good water-holding capacity.
The physiological mechanisms that underlie cassava's tolerance of severe water stress are illustrated by data in Tables 2 and 3 and Figures 2, 3 and 4. The capacity of cassava leaves to fix atmospheric CO2, a basic process for dry matter accumulation, during the stress period was 80% of that in the control (Table 2, Figure 2).
This indicated that the photosynthetic process in cassava is not
greatly inhibited by prolonged stress, an advantage that many other
field crops do not have.
A
second and important physiological mechanism of cassava leaves is
their ability to partly close their stomata in response to water
stress. For example, in the experiment, there was an average 43%
reduction in leaf conductance to water vapor in stressed plots (Table 2) and consistent reduction over the stress period, compared to the control (Figure 3).
The partial closure of stomata enabled cassava leaves to maintain,
to some extent, the midday leaf water potential at levels comparable
with those of cassava leaves in the control plot. Leaf water potentials
at 1400 h across all varieties were -1.13 and -1.12 MPa for the
control and stressed leaves, respectively (Table 3). This is another comparative advantage for cassava in dry areas, compared to other crops with poorer stomatal control.
In
addition to its beneficial effect by preventing severe leaf
dehydration, and consequently preventing impairment to photosynthetic
capacity of the leaf, the partial closure of stomata reduces water loss
through transpiration (Figure 4), thereby maximizing water-use efficiency, WUE (i.e., the amount of CO2
fixed per amount of water transpired). Across all varieties, there
was 39% increase in intrinsic leaf water use efficiency (PN /gs) in stressed crops over the control (Table 2).
A
third and equally important physiological mechanism that enables
cassava to withstand severe water stress is its ability to maintain a
predawn leaf water potential comparable with that of unstressed
cassava. In the experiment, leaf water potentials at 0600 h across
all varieties were -0.39 and -0.40 MPa for the control and stressed
plants, respectively (Table 3).
This was partly achieved by reducing total leaf area (as indicated by
the 31% reduction in light interception in the stressed plot, Table 2), thereby reducing total canopy transpiration, and by slow withdrawal of water from the deeper layers of the soil profile (Figure 5)
(Connor et al., 1981; Porto, 1983; CIAT, 1987-1989; El-Sharkawy and
Cock, 1987b; El-Sharkawy et al., 1992b; de Tafur et al., 1997a;
Cadavid et al., 1998; El-Sharkawy, 2006a). During water stress,
cassava fine roots extend for more than 2 m into deeper, wetter soil
from where cassava can extract between 20% and 40% of its total water
uptake (CIAT, 1987-1989; El-Sharkawy et al., 1992b). This is of
paramount importance in areas with bimodal rainfall patterns and
those with one short-wet annual period where excess water percolates
deeper in soil profile and, hence, it could be extracted during long
dry periods.
Also,
it is possible that the phenomenon of "hydraulic lift" [i.e.,
nocturnal uptake of water from deeper wet soil layers that is
transported and then released from fine roots into dryer top soil
layers; see, for example, Mooney et al. (1980), Richards and Caldwell
(1987), Caldwell and Richards (1989), Dawson (1993), Squeo et al.
(1999)] occurs in cassava since predawn water potential in
water-stressed plants always remained as high as in well-watered
plants. This might be the case because the majority of fine roots
exist in the top 0.40 m and a fewer portion of roots penetrate deeper
layers (Connor et al., 1981; El-Sharkawy and Cock, 1987b) where a
substantial water extraction occurs (Figure 5).
Water uptake from upper layer (0.40 m) continued during long period
of water stress with decreasing patterns over time (Figure 5;
El-Sharkawy et al., 1992b, de Tafur et al., 1997a, El-Sharkawy,
2006a), thus indicating the existence of available water in this
layer. Another characteristic that might be implicated in cassava
tolerance to prolonged water stress is the obligate association with
vesicular-arbuscular mycorrhizal fungi (VAM) (Howeler and Sieverding,
1983; Sieverding and Howeler, 1985). Among 20 cassava cultivars
growing in large pots outdoors, the percent infected root length
under stress varied from ~50 to ~90%, and these values were highly
correlated with total plant root length across cultivars (r = 0.955, P <
0.001) (Sieverding et al., 1985). There is some evidence that
plant-VAM associations may confer tolerance to water stress,
particularly in species with low fine root density (Hayman, 1980; Nelsen
and Safir, 1982; Ellis et al., 1985; Safir, 1985; Augé et al., 1987;
Khalvati et al., 2005). Compared to cereal crops, cassava has a
sparse fine root system and the extensive fungal hyphae-network in
the soil may increase water absorption capacity of infected roots. By
using a new split-root hyphae system in barley plants under
well-watered and water-stressed conditions in growth chamber,
Khalvati et al. (2005) found that water was transported from the
fungi hyphae to barley root compartment under water stress, as compared
to non-hyphae treatment. VAM-infected plants suffered less (relative
to non-infected plants) from water stress in terms of leaf elongation
rate, leaf turgor pressure, stomatal conductance and photosynthetic
rate. These parameters indicate a better plant water status in
VAM-infected plants.
A
fourth mechanism underlying tolerance to drought is the ability of
cassava to compensate partly for previous losses in dry matter
production, due to water stress, by an increase in leaf canopy area
(El-Sharkawy and Cock, 1987b; El-Sharkawy et al., 1992b) and by
higher photosynthetic rates in the newly developed leaves after
recovery, as compared to the unstressed plants (Figure 6)
(El-Sharkawy, 1993, Cayón et al., 1997; de Tafur et al., 1997a;
El-Sharkawy, 2006a). These higher photosynthetic rates in new leaves
of previously stressed cassava were associated with higher leaf
conductances, higher nutrient contents, as well as with stronger sinks
for carbohydrate in storage roots (Cayón et al., 1997).
Not
only can cassava tolerate long periods of soil water deficits aided
with the above-mentioned inherent mechanisms, but it can also react
to changes in atmospheric humidity (Figure 7)
(Connor and Palta, 1981; El-Sharkawy and Cock, 1984, 1986, 1990;
El-Sharkawy et al., 1984, 1985, 1989; Cock et al., 1985; Berg et al.,
1986; El-Sharkawy, 1990, 1993, 2004, 2006a; Oguntunde, 2005,
Oguntunde and Alatise, 2007). Cassava leaf stomata are sensitive to
air humidity, irrespective of soil water content; they close rapidly
in dry air when evaporation is high under field conditions, which may
be translated into high leaf water potential. This mechanism enables
cassava to maximize its WUE during periods of prolonged drought. When
air humidity is high (e.g., early in the morning and during rainy
periods), the stomata remain open. Thus, in a humid atmosphere and in
the presence of soil water deficits, cassava leaves remain
photosynthetically active and the crop can produce well; for example,
in the Pacific coast of Ecuador, cassava produces 8 to 12 t ha-1
of fresh roots with only 400 mm of rainfall in 3-4 months. In that
region, the intensity of solar radiation is low because of cloudy
skies and, hence, evaporation is low. A similar situation occurs in
the Pacific coast of Peru where rainfall is very low but there is an
intense fine mist that persists for hours, allowing stomata to remain
partly open and the leaf to actively fix CO2 at a lower rate of transpiration. Thus, WUE at the leaf level (CO2 uptake per H2O
loss) and at the crop level for the whole growing cycle (dry matter
produced per total water loss) are maximized in this case. Cock et al.
(1985) found that increasing air humidity by fine misting from 1000 h
to 1500 h, in a large cassava field experimental plot that was kept
wet via irrigation and protected from wind drift by hedge rows of
tall elephant grass at the CIAT Experiment Station, Palmira, Valle
Department, Colombia, resulted in both higher leaf photosynthesis and
higher root yields than in the adjacent unmisted plot that was
equally irrigated. Moreover, leaf photosynthetic rate was significantly
and positively correlated with air humidity, indicating stomatal
reactions to air humidity even in a wet soil (Figure 8).
Coupled
with stomatal sensitivity to air humidity is the strong leaf
heliotropic response that allows leaves to track solar radiation
early in the morning and late afternoon when the leaf-to-air water vapor
deficit (VPD) is low. At midday when solar elevation is high and VPD
is greatest, cassava leaves bend downward (i.e., leaf drooping
movement) irrespective of soil water content and leaf turgor pressure
(El-Sharkawy and Cock, 1984; Berg et al., 1986). The net result of
these two leaf movements is to maximize light interception and total
canopy photosynthesis when WUE is greatest, and to minimize light
interception when WUE is least.
In
the present trial, the four months during which soil water stress
was imposed coincided with a rainfall peak (total rainfall in April
and May 1988 at Quilichao was 400 mm). During April and May 1988, the
last two months of the stress period, the photosynthetic rates of the
stressed plants were 60% to 70% of those in the control plants (Figure 2).
This remarkable photosynthetic activity of the stressed cassava can
be attributed partly to the favorable effects of high humidity which
kept the stomata partly open (Figure 3).
It may be concluded that cassava is extremely tolerant (or
resistant) to prolonged drought because of multiple-inherent
morphological, structural and physiological plant traits that allow
the crop to obviate the negative effects of severe water stress.
The
same trends in responses to extended water deficits imposed at early
(2-6 months after planting), mid-season (4-8 months after planting)
and terminal (6-12 months after planting) growth stages were observed
in a 3-yr field trial with four contrasting cultivars that differed
in their vigor (CIAT, 1992, 1993; Caicédo, 1993; El-Sharkawy et al.,
1998; El-Sharkawy and Cadavid, 2002; El-Sharkawy, 2006a). Across
cultivars there were no significant differences in root yield among
water regimes, but there were significant differences among cultivars
indicating genotypic x treatment interactions (P <0.01) (Table 4).
Similar responses were observed in the Sudan Savanna zone of Nigeria
using variation in the soil-water table as a variable for water
availability (Okogbenin et al., 2003). These findings support the
sound breeding strategy for developing cultivars for specific ecozones
(Hershey and Jennings, 1992; El-Sharkawy, 1993; Iglesias et al., 1995;
Jennings and Iglesias, 2002).
Plant
ecophysiologists have proposed a sort of "classification/
terminology" scheme based on mechanisms underlying plant adaptation
to water deficits (for more information see for example, Levitt,
1980; Turner, 1986; Ludlow and Muchow, 1990). According to Turner
(1986), plants that are able to endure long periods of water
shortages while maintaining a high tissue water potential are called
drought tolerant. Cassava may fit among these types of plants.
Nevertheless, Alves (2002), working with indoor-grown plants, found
no significant accumulation of solutes and osmolytes in mature
cassava leaves, and, hence, no occurrence of osmotic adjustment (for
more information, see http://www.generationcp.org/vw/Download/ARM_2005/SP3_Alves.pdf).
This finding further confirms that cassava stomatal control over
plant water relations is the predominant defense mechanism protecting
the leaf from severe dehydration, and, hence, it can be considered a
stress avoidance mechanism (El-Sharkawy, 2006a). Similar stomatal
reactions to atmospheric and soil water deficits that strongly
control water use, often coupled with deep rooting systems, were
observed in drought-tolerant cultivars of other tropical perennial
trees/shrubs as in Coffea arabica and C. canephora (Hernández et al., 1989; Pinheiro et al., 2005; DaMatta and Ramalho, 2006).
The
discussed above plant traits and mechanisms that underlie cassava
tolerance to prolonged drought have further implications for the
possible expansion of adaptable cassava cultivars into marginal lands
and under adverse climatic conditions. As a potential food and feed
crop for the tropical and subtropical regions most likely affected by
global climate changes, cassava will probably become an important
food-security source in developing countries where there are severe
food shortages (Rosenzweig and Parry, 1994; Kamukondiwa, 1996;
El-Sharkawy, 2005; IPCC, 2006). Rosenzweig and Parry (1994) pointed
out that cereal crop production in the tropics and subtropics will
possibly decrease in the near future because of global climate
changes, hence, food shortages would be further aggravated in these
regions.
Selection for drought tolerance in cassava for seasonally dry and semiarid environments in Colombia
The
physiological research, as discussed above, laid the foundation for
improving the cassava genetic base, and for selection for drought
tolerance in seasonally dry and semiarid environments where a
significant portion of cassava production occurs (El-Sharkawy, 1993;
Iglesias et al., 1995). A large group of cassava from the core
germplasm collection was screened for leaf photosynthesis and
productivity in seasonally dry and semiarid environments in Colombia.
Evaluation of core
germplasm for productivity and photosynthesis in seasonally dry
environmenst at the southwest Andean mountains of Colombia: In
the 1986-1987 growing season, 127 CIAT cassava accessions, including
cultivars, land races and breeding lines were screened on a private
farm in the Patia Valle, Cauca Department, Colombia (600 m a.s.l.,
latitude 2º09'N, longitude 77º04'W, mean annual temperature 28ºC with
little seasonal variation, average atmospheric humidity about 70%).
The soils in Patia Valley are heavy clay, and the farm was under
continuous pasture grasses, mainly Panicum maximum, for the last 25 years. The trial was planted at a population density of 15,625 plant ha-1 on
23 October 1986, with adequate fertilization. The site received
about 700 mm of rain in 309 d, but from December 1986 to April 1987,
the rainfall was much less than the potential evaporation which was
greater than 5 mm d-1. The Patia Valley, lying between the
central and western Andes mountains, is characterized by two wet
periods (October-December and March-June), and with high solar
radiation of about 22 MJ m-2 d-1. The 1986-1987
season was particularly dry, with no rainfall recorded from June to
August. The trial was harvested on 26 to 27 August 1987.
Measurements
of single-leaf gas exchanges were made with a portable infrared gas
analyzer (LI-COR model LI-6000) using central lobes of upper canopy
leaves on several occasions between February to June 1987. At this
stage of crop growth, LAI was near its peak, and storage root bulking
rate was greatest, and, hence, both carbon source capacity and
root-sink demand were near optimal. Measurements were always made
from 0900 to 1300 h when the solar irradiance exceeded 1000 µmol m-2 s-1
of PAR. Leaf water potential was determined with the standard
pressure chamber technique (Scholander et al., 1965) on lobes from
the same leaves used for gas exchange. Values for leaf water
potential ranged from -1.0 to -1.5 MPa, across varieties and
measurement dates. Nitrogen, phosphorus and potassium contents were
also determined on the same measured leaves (El-Sharkawy et al., 1990).
Across all
accessions, both fresh total plant biomass and dried root yield were
highly significantly and positively correlated with average leaf
photosynthetic rate, and the correlation was higher in the high and
medium top weight varieties than in the low top ones. These results
indicate that, on the one hand, at high level of light interception
(i.e., near optimum LAI in high and medium top weight), there was a
direct relationship between productivity and leaf photosynthesis. On
the other hand, at lower light interception because of lower than
optimal LAI in the low top genotypes, the relation is weaker and
light interception appears to be the predominant factor in
determining productivity. Thus, when both canopy light interception and
root-sink demand for carbohydrate are not limiting, productivity
correlates well with leaf photosynthesis, as measured in the field
(El-Sharkawy and Cock, 1990; El-Sharkawy et al., 1989, 1990).
Sixteen
clones were selected from the many screened accessions on the basis
of their high-yield performance, and were planted on 13 April 1988,
in another adjacent private farm in the Patia Valley, and at a
population density of 10,000 plants ha-1. A split-block
design with four replications was used to allow for two fertilization
treatments, i.e., (1) without fertilization; (2) with 50, 100 and
100 kg NPK ha-1. The size of the plot per clone was 25 m2.
The crop received about 950 mm of rain during the growing cycle of
308 d, with 560 mm out of the total rainfall occurring in October and
November 1988, which resulted in a significant amount of water
runoff. On 14-16 February 1989, the nine central plants per plot were
harvested to determine biomass and root yield weight. Measurements
of single-leaf gas exchanges were made only once per day on 29 August to
7 September 1988, with an LCA-2 portable infrared gas analyzer
(Analytical Development Co., UK) that operates in an open-end system,
in contrast to the LI-COR 6000 that operates in a closed fashion
system. Across all blocks and fertilizer treatments, 35 fully
expanded upper-canopy leaves were measured per cultivar. A small leaf
chamber (Parkinson Broad Leaf Model) was clamped over the middle
portion (6.25 cm2 leaf surface area), in contrast to the
4-L leaf chamber used with the LI-COR closed system where the whole
lobe of cassava leaf was measured for gas exchanges. All measurements
were made from 0800 to 1300 h with solar irradiance exceeding 1000
µmol m-2 s-1 of PAR. Normal air with 320 ± 10 µmol mol-1 CO2 was drawn from above canopy using a vertically mounted 4-m glass-fiber probe connected to a pump.
Since
no significant fertilizer effects were observed in root yield and
gas exchange rates, data were pooled. Average root yields were higher
than those in the 1986-1987 preliminary screening trial, and this
was mainly attributed to the higher rainfall in 1988-1989, as well as
to the smaller group of selected high-yielding clones. The mean dry
root yield among the 16 cultivars ranged from 15 to 27 t ha-1, indicating the high yield potential in cassava when grown in near optimal environments. In this trial with nearly 9000 m2 land including borders, the overall average dry root yield harvested from the whole area exceeded 20 t ha-1.
Despite
differences in rainfall between the two growing seasons, the leaf
photosynthetic rates measured in 1986-1987 season were highly
significantly and positively correlated with the dry root-yield of
the 1988-1989 season (Figure 9).
Furthermore, average leaf photosynthetic rates, as measured only
once with the LCA-2 in the 1988-1989 season, was significantly
correlated with rates measured over a more extended period of time in
the 1986-1987 season with the LI-COR closed system (Figure 10). The dry root yield and the average leaf photosynthesis of the 1988-1989 season crop were also significantly correlated (Figure 11).
These data clearly demonstrate the consistent relation over years
between upper canopy single-leaf photosynthesis, as measured in the
field, and productivity in cassava.
The
relation between leaf photosynthesis and productivity was mainly due
to nonstomatal factors (i.e., due to biochemical/anatomical leaf
characteristics), as demonstrated by the negative significant
correlation between yield and intercellular CO2 concentration (Ci)
(El-Sharkawy et al., 1990). This conclusion is further substantiated
by the significant positive correlation between yield and
photosynthetic nitrogen-use efficiency (PNUE = CO2 uptake/ unit total leaf nitrogen, Figure 12).
Leaf anatomical characteristics that may affect the amount and
distribution of photosynthetic machinery can play a significant role
in leaf photosynthesis. But since yield is significantly correlated
with PNUE, it appears, therefore, that biochemical factors affecting
photosynthesis, such as activities of photosynthetic enzymes, are
more important in this case. Leaf photosynthetic rates of various
cassava varieties subjected to water stress in the field were
significantly and positively correlated with the activity of the C4 enzyme PEPC activity in extracts of the same measured leaves (El-Sharkawy, 2004). Table 5
(El-Sharkawy et al., 2008) presents correlation coefficients and
regressions between yield, photosynthetic characteristics, and PEPC
activity in 18 varieties selected from the preliminary trial in
Patia. There were significant correlations between yield,
photosynthetic characteristics and PEPC activity. Such activity was
highly significantly correlated with PN and PNUE. Moreover, PEPC activity in cassava was much greater than that observed in typical C3 plants and about 10-30% of the activity in typical C4
species such as maize and sorghum (El-Sharkawy et al., 1989;
El-Sharkawy and Cock, 1990; El-Sharkawy, 2004, 2006a). Also, it is
possible that differences in leaf photosynthesis within cassava
germplasm could be due partly to differences in characteristics of
the C3 enzyme, Rubisco. Paul and Yeoh (1987) reported wide variation in kinetic properties of cassava Rubisco. Values of Km (CO2) for 16 cassava varieties ranged from 7.8 to 14.0 µM CO2, while Km
(RuBP) values ranged from 7.5 to 24.8 µM RuBP. Wide variation was
also found in activities of Rubisco among cassava genotypes (López et
al., 1993; El-Sharkawy, 2004, 2006a). Thus, selection for high
photosynthetic rates and high enzyme activity would be beneficial for
breeding improved cassava varieties, particularly under drought
conditions. Molecular biologists, along with plant breeders,
physiologists and biochemists, should participate in screening for
genetic variation in photosynthetic characteristics and in
identifying potential genotypes as a genetic source for crossing in
breeding programs. Interdisciplinary/interinstitutional collaboration
should enhance progress and ensure efficiency in science output,
and, hence, increase the benefit/cost ratio of research.
Evaluation of core germplasm in both seasonally dry and semiarid environments in northern coast of Colombia:
Two field trials were conducted during the 1992-1993 season in two
locations at the northern coast of Colombia using two groups of
cassava clones selected from the CIAT core germplasm. One trial was
conducted on a private farm at Santo Tomas, Atlantic Department (14 m
a.s.l., latitude 10º57'N; longitude 74º47'W). At this site the mean
annual rainfall of 830 mm is 50% of the mean annual pan evaporation
of 1650 mm, with a rainy period from May to November and a dry period
from December to April. The soil at the site is sandy (>80% sand)
with low water holding capacity, very low in organic matter and low
in nutrients. The second trial was conducted at a site of a religious
school for the native young students (Aremasain) near Riohacha,
Guajira Department (4 m a.s.l., latitude 11º32'N; longitude 72º56'W).
At that site the mean annual rainfall of about 560 mm is 25% of the
mean annual pan evaporation of 2300 mm. The rainfall distribution
pattern in this region is characterized by a short rainy period from
September to November, a dry period from December to April, and a
second low-rainfall period from May to August. The soil in that site
is sandy (> 80% sand) with low water holding capacity, very low in
organic matter and nutrients. In both trials, no chemical fertilizer
was applied.
Healthy
stem cuttings (20 cm long) of the tested cultivars were planted on 25
September 1992 (Santo Tomas, Atlantic) and on 19 September 1992
(Riohacha, Guajira) on flat places of disked land at a 1 m by 1 m
distance and in 5 x 5 m plots with four replications in a randomized
complete-block design. The eight central plants from each plot were
harvested for determination of yields on 4 August 1993 (Riohacha) and
5 August 1993 (Santo Tomas).
Under the above-mentioned stressful environments, average oven-dried root yield was 6.7 t ha-1 at the seasonally dry location (yield ranged among cultivars from 5.8 to 7.6 t ha-1), whereas at the semiarid location overall average yield was 2.3 t ha-1 (yield ranged among cultivars from 0.4 to 3.3 t ha-1).
These levels of productivity, without fertilization and with severe
prolonged drought, illustrate again the high adaptability of cassava
to adverse atmospheric and edaphic conditions. Moreover, the crop not
only survived but also produced reasonably well, where other major
staple food crops like tropical cereals would not be able to compete
with cassava. The most drought-tolerant tropical cereals such as grain
sorghums and millets (Blum and Sullivan, 1986) perhaps would fail to
produce under the semiarid conditions experienced in these trials.
Nevertheless, because of the severe shortage of rainfall in the
semiarid environment, root dry matter content was lower (less than
30%) than in seasonally dry environments. In practice, however, such
as in northeastern Brazil with mean annual rainfall less than 700 mm,
the crop is allowed to go into a second wet cycle that leads to higher
yields as well as higher root dry matter content.
Measurements
of leaf gas exchanges were made with an LCA-2 portable infrared gas
analyzer during several days from February to March, 1993. All
measurements were made on upper canopy leaves (four leaves per
cultivar per replication with a total of 16 leaves) between 0800 h and
1200 h local time with a solar irradiance higher than 1000 µmol m-2 s-1.
Measurements were taken during the dry period 4-5 months after
planting at air temperatures within the leaf cuvette ranging from 29
to 37ºC, depending on time and date of measurements. This range of
temperatures is near the optimum for photosynthesis in cassava as
measured under controlled laboratory conditions (El-Sharkawy and
Cock, 1990; El-Sharkawy et al., 1992a).
Overall
average photosynthetic rates across cultivars were much higher at
the seasonally dry site than at the semiarid one, with the highest
rates observed early in the morning and the lowest at midday (Figure 6)
(de Tafur et al., 1997b). Leaf conductance to water vapor showed the
same trend, indicating the striking effect of air humidity on stomatal
opening as previously observed under controlled laboratory conditions
(El-Sharkawy and Cock, 1984, 1986; El-Sharkawy et al., 1984, 1985).
These photosynthetic rates are much lower than the maximum rates
(above 40 µmol CO2 m-2 s-1) that are
normally observed in field-grown cassava in wet soils and with high
atmospheric humidity (El-Sharkawy et al., 1992a, 1993). However,
compared with other field crops, cassava is more photosynthetically
active under severe prolonged drought, an advantage that underlies
its remarkable productivity and ability to endure harsh environments.
Thus, it is beneficial to select for higher photosynthetic capacity,
combined with other desirable plant traits such as longer leaf life
(better leaf retention and duration, Lenis et al., 2006) and deeper
and extensive fine root systems in order to enhance growth and yield
in dry areas.
In both
environments, dry root yield was highly significantly and positively
correlated with average leaf photosynthetic rate (Figure13, r2 = 0.76, P <
0.01) (CIAT, 1995; de Tafur et al., 1997b). Moreover, dry root yield
was highly significantly and negatively correlated with Ci (Figure14, r2 = 0.82, P <
0.001, de Tafur et al., 1997b), indicating that the relation is due
mainly to nonstomatal factors controlling leaf photosynthesis (i.e.,
biochemical/anatomical factors). These results corroborate other
findings in humid and sub-humid/seasonally dry environments, as
discussed above (El-Sharkawy et al., 1990, 1993; Pellet and
El-Sharkawy, 1993; El-Sharkawy, 2006a). The results also point to the
importance of utilizing genetic variations in photosynthetic enzyme
characteristics as selection criteria in cassava breeding, particularly
for improved genotypes targeted for dry environments. The C4
PEPC, in particular, plays a significant role in cassava
photosynthesis, when the numerous abaxial stomata close in hot-dry
environments. Under this situation, PEPC recycles respiratory CO2, and, hence, dissipates excess solar energy and obviates photoinhibition of the photosynthetic process.
Breeding for drought tolerance in cassava under the semiarid conditions of northeastern Brazil: Besides
being, for millennia, the main geographical site for the origin of
cassava, the center for its genetic diversity and for its
domestication (Allem, 2002), Brazil is the largest cassava producer
in Latin America. According to FAOSTAT (1999) (cited by Henry and
Hershey, 2002), the 1999 area harvested under cassava in Brazil was
about 1.54 million ha, about 21% less than that in 1990 and the total
fresh root production was 20.2 million tons (12.7 % of world 1999
estimated production of about 158 million tons). The estimate of root
yield across the country was 13.1 t ha-1 for 1999, slightly higher than that in 1990 (about 12.6 t ha-1).
On the one hand, one reason behind the decrease in acreage, and
consequently the reduction in total production, was the pattern of
decreasing cassava cultivation in the most favorable environments in
southern Brazil (El-Sharkawy, 1993). On the other hand, in the more
marginal regions of the semiarid northeastern Brazil, the area under
cassava production expanded rapidly and now may account for more than
50% of the total Brazilian production. This trend strengthened the
importance of improving the genetic base of cassava, and for breeding
new cultivars more adapted to the severe water stress conditions
prevailing in that region. This objective was further strengthened by
the knowledge of cassava's inherent potential for drought tolerance
and the newly acquired basic physiological information and insights
about the mechanisms underpinning such tolerance.
In
late 1980 and early 1990, breeding efforts at CIAT were further
integrated with the Brazilian national institutions involved in
cassava research, mainly the federal research organizations of EMBRAPA
and CNPMF, with headquarters at Cruz das Almas, Bahia State (Fukuda
et al., 1992-1993). Also, collaboration with IITA, Nigeria, took
place at the same time. As the crop physiologist at CIAT, I
participated, along with CIAT breeders and the Brazilian national
cassava team, in the initiation of a research project for cassava
breeding in northeastern Brazil that was supported by the International
Fund for Agricultural Development, Rome (El-Sharkawy, 1993). Based on
the available meteorological data, four relevant sites were
pre-selected for screening cassava germplasm in northeastern Brazil,
namely: (1) Itaberaba, Bahia (270 m a.s.l., latitude 12º31'S). At
this site, mean annual rainfall is about 718 mm, with a continuous
rain throughout the year, but with two wet cycles. From January to
April total rainfall is about 332 mm. There is a shorter wet cycle from
November-December with a total rainfall of 200 mm. The rest of the
year is considered dry as the monthly rainfall oscillated between 20
to 40 mm, which is far below the potential evaporation. (2) Quixadá,
Ceará (179 m a.s.l., latitude 4º57'S). At this site, mean annual
rainfall is about 677 mm, with only a four-month wet cycle (from
February to May) with a total rainfall of 542 mm. The rest of the
year is extremely dry, as monthly rainfall oscillated between zero to 45
mm. (3) Petrolina, Pernambuco (376 m a.s.l., latitude 9º22'S). At
this site, mean annual rainfall is about 400 mm, with monthly
distribution (mm) as follows: 50 in January, 78 in February, 92 in
March, 43 in April, 7 in May, 4 in June, 2 each from July to
September, 9 in October, 45 in November, 64 in December. This site is
the driest among the pre-selected sites, as illustrated by the
pattern of rainfall distribution. (4) Araripina, Pernambuco (816 m
a.s.l., latitude 7º32'S). This site is the wettest among the
pre-selected sites with mean annual rainfall of about 820 mm. The
rainfall distribution pattern is very similar to that in Petrolina,
but with the three wetter months having a total rainfall of 422 mm
(January 114, February 134, March 174). The rest of the year was
considered dry, as indicated by the monthly rainfall distribution
that oscillated between zero and 63 mm. The soils in these sites are
sandy with low water holding capacity in addition to being very low
in fertility.
Cassava
germplasm (500 clones) originating from northeast Brazil and the
north coast of Colombia was initially screened at these four sites
for yield, harvest index, root dry matter content, cyanogenic glucosides
level (expressed in total hydrocyanic acid, HCN, concentration in
storage root parenchyma) and resistance to mites. In general, in the
1991-1992 growing season, cassava at all sites suffered from a more
severe drought than normal, with total annual rainfall less than 200
mm in Petrolina, less than 500 mm in Araripina, less than 360 mm in
Quixadá. Only at Itaberaba was rainfall about 853 mm, more than
normal (Fukuda et al., 1992-1993). Despite these harsh environments, a
large number of accessions persisted and produced, while some failed.
Better drought-adapted clones established full canopy after four
months and retained leaf area up to eight months after planting
(Fukuda et al., 1992-1993; El-Sharkawy, 1993). In Table 6
the results of the preliminary screening trials as overall averages
of the four sites are summarized. Several accessions of Brazilian
origin were selected with good yield potential that ranged from 13 to
18 t ha-1 fresh roots with mean 25% dry matter. Harvest
index ranged from 0.45 to 0.55. There was tolerance to prolonged
drought, as indicated by better leaf retention and duration during
most of the cropping cycle. Low HCN content was in root parenchyma,
and they ranged from 53 to 100 mg kg-1 fresh root, which
are acceptable levels for fresh root consumption. Mite resistance
scores ranged from 3.3 to 2.7, based on a visually assessed scale from 5
(highly susceptible) to 1 (highly resistant).
These
preliminary trials laid the foundations for a further expanding of
the breeding project based on a scheme for producing hybrids via
crossing among various selected clones with a range of desirable
traits under semiarid conditions (Fukuda et al., 1992-1993). Further
on-farm trials involving farmers in the process of evaluation of
breeding materials have resulted in a few selected genotypes with
higher yields, compared to local checks (Table 7).
When left for a second wet cycle in semiarid low-rainfall locations,
fresh yields more than doubled (from an average yield of 14 t ha-1 at 12 months to 35 t ha-1
at 18 months). The dry matter contents in fresh roots increased from
25% at 12 months to 35% at 18 months, which led to more than
three-fold increases in dry root yields (from an average of 3.5 t ha-1 at 12 months to 12.2 t ha-1
at 18 months). Farmers adopted some of these improved genotypes and
started multiplying planting material even before being officially
released. In these semiarid environments drought-tolerant grain crops
such as sorghum and millets (Blum and Sullivan, 1986) will fail to
produce as much, indicating the comparative advantages of cassava.
This research is a remarkable example of
interdisciplinary/interinstitutional collaborative efforts that serve
the needs of some of the poorest farmers in the tropics.
Consequently, a follow-up collaborative research project supported by
the CGIAR Generation Challenge Program was conducted by EMBRAPA/CNPMF,
Brazil, CIAT, Colombia, IITA, Nigeria, and Cornell University, USA
(see: http://www. generationcp.org/vw/Download/Competitive_ Grant_ Proposals/3_ALVES.pdf).More than 20 new genotypes tolerant to drought were selected (see: http://www. generationcp.org/vw/Download/ARM_2005/SP3_ Alves.pdf).
