Physiological characteristics of
cassava tolerance to prolonged drought in the tropics: implications for
breeding cultivars adapted to seasonally dry and semiarid
environment.
ABSTRACT
The
paper summarizes research conducted at International Center for
Tropical Agriculture (CIAT) on responses of cassava to extended water
shortages in the field aided by modern gas-exchange and water-relation
techniques as well as biochemical assays. The aim of the research was
to coordinate basic and applied aspects of crop physiology into a
breeding strategy with a multidisciplinary approach.
Several
physiological characteristics/traits and mechanisms underpinning
tolerance of cassava to drought were elucidated using a large number of
genotypes from the CIAT core germplasm collection grown in various
locations representing ecozones where cassava is cultivated. Most
notable among these characteristics are the high photosynthetic
capacity of cassava leaves in favorable environments and the
maintenance of reasonable rates throughout prolonged water deficits, a
crucial characteristic for high and sustainable productivity. Cassava
possess a tight stomatal control over leaf gas exchange that reduces
water losses when plants are subjected to soil water deficits as well
as to high atmospheric evaporative demands, thus protecting leaves
from severe dehydration. During prolonged water deficits, cassava
reduces its canopy by shedding older leaves and forming smaller new
leaves leading to less light interception, another adaptive trait to
drought.
Though root yield is reduced (but much less than the
reduction in top growth) under water stress, the crop can recover
when water becomes available by rapidly forming new canopy leaves
with much higher photosynthetic rates compared to unstressed crops,
thus compensating for yield losses with final yields approaching
those in well-watered crops. Cassava can extract slowly water from deep
soils, a characteristic of paramount importance in seasonally dry and
semiarid environments where deeply stored water needs to be tapped.
Screening large accessions under seasonally dry and semiarid
environments showed that yield is significantly correlated with upper
canopy leaf photosynthetic rates, and the association was attributed
mainly to non-stomatal (anatomical/biochemical) factors. Parental
materials with both high yields and photosynthetic rates were identified
for incorporation into breeding and selection programs for cultivars
adapted to prolonged drought coupled with high temperatures and dry
air, conditions that might be further aggravated by global climate
changes in tropical regions.
INTRODUCTION
The
role of physiological research in crop improvement and cropping
systems management has recently been reviewed (El-Sharkawy, 2006b).
As a branch of basic science, plant physiological research has a
fundamental role in advancing the frontier of knowledge that is
essential for the better understanding of plants and their
interactions with surrounding biophysical environments. It also plays
a significant role in supporting other branches of science that deal
with the practical application of knowledge and in the development
of advanced technologies needed for improving biological systems in
general and agricultural productivity in particular. Crop physiology
deals with studying cultivated crops with the aim of increasing
productivity by enhancing the inherent genetic capacities of crops as
well as their adaptability to environments. To be effective in
realizing such a goal, physiologists have to work within
multidisciplinary research teams committed to a particular crop and/or
to multi-cropping systems (El-Sharkawy, 2005). Furthermore, to be
successful, the leader/manager of a multidisciplinary research team
should not tolerate potential rivalries between disciplines involved
nor the dominance of a particular discipline for research support and
funds.
Although
research conducted in laboratories and in controlled environments is
useful in elucidating a specific plant physiological characteristic
or mechanisms underlying certain biological processes and responses
to environmental factors affecting growth and productivity, by
themselves they are inadequate for creating some benefit to the
farmer (Evans et al.,1985; Kramer, 1980, 1981). Field research under
representative environments and in relevant cropping systems using a
broad genetic base must be conducted not only to verify findings in
laboratories and controlled environments but also to generate essential
information and insights concerning the real potential of crops under
natural conditions as well as their responses to a specific limiting
environmental factor (El-Sharkawy et al., 1965; El-Sharkawy, 1993,
2004, 2005, 2006a,b; Long et al., 2006).
El-Sharkawy (2004, 2005,
2006a,b) and Long et al. (2006) have shown that research based only
on potted plants grown in greenhouses and in controlled cabinets,
without the proper calibration in the field, is a waste of time and
resources since in most cases results cannot be extrapolated, or
simulated by crop modeling, to describe what may take place in
natural environments. Those authors concluded that field research is
the only valid ecosystem research in studying plant water relations
and crop photosynthesis in relation to productivity. Until recently,
the controlled-environment and greenhouse potted-plant scientists
(many of whom were members of national science academies) controlled the
plant photosynthesis and water relations research and often invoked
the misuse of the terminology "adaptation to stress" for "acclimation
to stress" to protect their domination over the public-funded
scientific establishment and to cover up their failure in
contributing to the early discoveries of the C4
photosynthesis and its implications for plant water use efficiency
(El-Sharkawy, 2005, 2006b; El-Sharkawy and Hesketh, 1965, 1986; Begonia
and Begonia, 2007). This is not a very good example to teach young
people about how science is done nor an efficient way to manage
public-funded research. Still, there is a need for good reviews of
field work similar to that reported on cassava research done in the
tropics (El-Sharkawy et al., 1989; El-Sharkawy and Cock, 1990;
El-Sharkawy, 1993, 2004, 2006a,b). Another good example of reviews of
field work in the tropics is the one on coffee research recently
published in the Brazilian Journal of Plant Physiology by DaMatta and
Ramalho (2006).
In
view of the ever increasing world human population, particularly in
developing countries (Sasson, 1990; Cohen, 1997), increasing demands
for food and feed in the coming few decades must be met by enhancing
agricultural outputs as well as conserving dwindling natural resources,
particularly arable lands and water. In developed and industrial
countries of the temperate zone, the gap between the potential
productivity of crops and actual yields had been largely closed aided
by advanced public and private research that has resulted in
improved technologies. On the other hand, in developing countries in
general, and in the tropics in particular, agriculture productivity is
still far below the potential. This situation will be further
aggravated in light of the recognized global climate changes that
might result in adverse effects on agricultural systems and food
security in developing countries (Rosenzweig and Parry, 1994; IPCC,
2006
The 2007 Nobel Prize for Peace was jointly awarded to IPCC and the
former USA Vice President Al Gore in recognition of their efforts in
raising public awareness of the implications of global climate
changes for environmental conditions and its consequent adverse
effects on agriculture, natural resources and ecosystems in general.
With few exceptions, agricultural research in tropical countries has a
short history and is inadequately supported by national financial
resources due to unfavorable agricultural policies. Furthermore, the
benefits from the so-called Green Revolution of the 1960's, supported
by international research on major cereal crops, were not equally
distributed among continents, countries and crops (Evenson and
Gollin, 2003). Moreover, the Green Revolution technologies were based
on developing high-yielding new cultivars that required expensive
production high-inputs, such as agrochemicals and irrigation facilities
that are beyond the reach of the many resource-limited small farmers,
particularly in the tropics.
Until
three decades ago, crops other than wheat, rice and maize, were not
included in the research agenda of the first two commodity-oriented
international agriculture research centers, i.e. the International Rice
Research Institute (IRRI) in the Philippines and the International
Maize and Wheat Improvement Center (CIMMYT, from the Spanish acronym)
in Mexico (Wortman, 1981). This situation was largely corrected by
the creation of more international research laboratories and centers
in Africa, Asia and Latin America dealing with various crops, ecosystems
and natural resources management. The International Center for
Tropical Agriculture (CIAT, from the Spanish acronym) in Colombia has
a world mandate for research on cassava, while the International
Institute of Tropical Agriculture (IITA) in Nigeria has a more
regional mandate. Research on cassava has received attention and
support from many developed countries and from various
research/development granting agencies. Before CIAT, with a very few
exceptions, cassava was a neglected crop as far as research was
concerned in tropical countries where the crop was normally
cultivated in marginal lands by resource-limited small farmers and
constitutes a main staple for food and feed for both rural and urban
habitants. Physiological information on cassava was, until recently,
scarce (Hunt et al., 1977; Cock et al., 1979; Cock, 1985).
The
cassava physiology section at CIAT conducted both basic and applied
research in coordination with a breeding program and took advantage
of the diverse genetic resources available within the extensive
cassava germplasm collection as well as the diverse environments within
Colombia where cassava is cultivated (El-Sharkawy, 1993; Madeley,
1994). The research covered a wide range of ecophysiological aspects
of the crop. Cassava was the first cultivated crop to be considered
as a C3-C4 intermediate species based on: (i)
atypical leaf anatomy including the presence of conspicuous
thin-walled bundle-sheath cells with large granal chloroplasts, which
are less developed than those in the typical C4 Kranz leaf
anatomy (e.g., El-Sharkawy and Hesketh,1965, 1986; Laetsch, 1974);
(ii) close physical association of chloroplasts with numerous
mitochondria and peroxisomes in bundle-sheath and mesophyll cells;
(iii) low photorespiration (as determined by CO2 release from illuminated leaves in a rapid stream of CO2-free air, less than 10% of net photosynthesis) and low CO2 compensation point (G = 20-30 cm3 m-3); (iv) ability to recycle all internal respiratory CO2 within
the palisade layer when abaxial stomata of amphistomatous leaves are
closed under a wide range of irradiances and temperatures; (v)
elevated activities of the C4 phosphoenolpyruvate
carboxylase (PEPC) in leaf extracts (10-30% of activities in maize and
sorghum); (vi) high percentage (30-60%) of 14C labeling in C4
dicarboxylic acids after 5-10 s exposure under illumination; (vii)
and immunological analysis and DNA hybridization of PEPC from cassava
and wild Manihot species against antibodies and ppc
probes from maize (El-Sharkawy and Cock, 1987a; Cock et al., 1987;
Riaño et al., 1987a,b; El-Sharkawy et al., 1989; El-Sharkawy and
Cock, 1990; Bernal, 1991; López et al., 1993; Aguilar, 1995;
El-Sharkawy, 2004, 2006a; El-Sharkawy and de Tafur, 2007). These
characteristics, collectively, underpinned the high photosynthetic
rate in normal air (PN > 40 µmol CO2 m-2 s-1) in high irradiances (> 1800 µmol m-2 s-1 of
PAR), high leaf temperature from 30 to 40 ºC, and in high
atmospheric humidities observed in cassava grown in favorable
environments (El-Sharkawy et al., 1992a, 1993).
Moreover,
leaf photosynthetic rates, as measured in the field, were
significantly correlated with both total biomass and root yield of a
wide range of cultivars grown across years and environments. The
relations were attributed mainly to nonstomatal (biochemical/anatomical)
factors (El-Sharkawy, 2004, 2006a). Cassava also tolerates prolonged
drought that often exceeded five months aided by partial closure of
stomata, deep rooting systems and small leaf canopy. These plant
traits make cassava a desirable and adaptable crop, as source for
food and feed, in the tropical regions that would be adversely
affected by global climate changes (Rosenzweig and Parry, 1994;
Kamukondiwa, 1996; El-Sharkawy, 2005; IPCC, 2006).
This
paper summarizes some research findings, published and unpublished,
on the responses of cassava to extended water shortages in the field
where physiological mechanisms and characteristics related to the
crop's tolerance to drought were sorted out. Moreover, the research laid
the foundations for selection and breeding of improved cultivars
adapted to prolonged drought normally encountered in seasonally dry
and semiarid environments.