Journal of Biotechnology

& Crop Science Review

5(6): 32-40, 2016

Breeding hybrids and inbreds for temperature tolerance in maize

VP Mani, RS Khandelwal, GS Bist, KS Koranga
Received: 15 March 2016 Revised Accepted: 10 April 2016

ABSTRACT

The important breeding objective in any crop plants is to improve grain yield potential and stability of the cultivars including
in maize. Stability of performance becomes more important if crop is grown in less favorable environments. Tolerance to
abiotic stresses is in general and drought through cold and heat tolerance in particular is essential in crop plants, as plant
cannot alter an environmental stress external to itself. The effect and mechanism of all the three types of temperature stresses
vary with respect to survival, growth and development and physiological processes. So during planning of crop improvement
in open pollinated crops like maize for temperature tolerance through development of inbred and hybrids one must keep in
mind regarding mechanism of temperature tolerance. The improvements in vegetative growth and yield performance of any
of these crops will require selection of inbreds for hybrid development that have more efficient growth habits under
unfavourable stresses conditions.

Key Words: Drought, Hybrids, Inbreds, Maize, Resistance, Tolerance

INTRODUCTION

Temperature stress tolerance of a plant is an ability of
the plant to come in thermodynamic equilibrium with
extreme temperature fluctuations without suffering
injury. Hybrids or Inbreds with heat and cold stress
tolerance is able to prevent, decrease or repair the
injurious strain caused by the stress at a negligible
loss in the economic yield, provided proper and
scientific methods are followed. The heat and cold
stresses on plant have different susceptibility at
vegetative and reproductive phase.
In winter, the crop generally suffers cold stress at
germination especially in late sown conditions and
high temperature stress at reproductive phase during
grain filling period. During vegetative phase, the crop
plants may face chilling or frosting damage. Crops in
tropical and sub-tropical climates show varying
degrees of resistance to chilling injury. The plants
that are susceptible to chilling injury may harden in
VP Mani, RS Khandelwal ( ), GS Bist, KS Koranga
Vivekananda Parvatiya Krishi Anusandhan Sansthan (ICAR)
Almora 263601, Uttaranchal
Email: rskhandelwal@yahoo.com
the field, become more resistant and therefore capable
of surviving chilling temperatures. However, in
summer and rainy season the plant withstand higher
temperature stress at early vegetative phase and low-
temperature stress at reproductive phase. When the
tissues of the plant are frozen below a threshold
freezing temperature specific for that crop, it may
cause an irreversible freezing damage to the plant.
The development of inbred and hybrids that
avoid/tolerate freezing/chilling temperatures should
be targets of a plant breeder to sustain and increase
economic yield in crop plants under stress conditions.
Even though plants are categorized into six response
classes with respect to low temperatures (Levitt 1980)
but for a plant breeder, these six categories can be
aggregated into two broad groups based on nature of
stress, its physiological repercussions, the nature of
tolerance and the agronomic implications. These
groups include plants, which are chilling sensitive
and hardy plants.The most important breeding
objective in crop plants is to upgrade grain yield
potential and stability of performance. Stability of
performance is very important when crop is grown in

32

less favourable environments. Tolerance to abiotic
stresses is essential in crop plants, as plant cannot
alter an environmental stress external to itself.
Temperature Tolerance System
It is important to understand the system of inheritance
of temperature stress for any corp for its improvement
and development of hybrids and inbred in crop like
maize. Temperature stress includes chilling, freezing
and heat stress a crop has to withstand during its
vegetative as well as reproductive stage. The ability
of the plant to recover from the consequences of a
heat stress is important for the crop yield and
stability. Manipulation of regulatory processes that
are responsive to oxidase stress could enhance
chilling tolerance mechanism, while a precise model
for freezing tolerance is yet to be determined. The
genetic basis of inheritance of winter hardiness is
complex and polygenic in nature. Primarily, tolerance
to temperature stresses is largely non-additive.
However, the selection for SCA would allow the
recombination of temperature tolerance with other
agronomically desirable attributes. The effect and
mechanism of all the three types of temperature
stresses vary with respect to survival, growth and
development and physiological processes. So during
planning of crop improvement in open pollinated
crops for temperature tolerance through development
of inbred, scientist must keep in mind regarding
mechanism of temperature tolerance for all these
types. Many of the important crops around the world
are now cultivated in areas where temperature stress
is common. Therefore, improvements in vegetative
growth and yield performance of any of these crops
will require selection of inbreds for hybrid
development that have more efficient growth habits
under unfavourable stresses conditions (Greaves
1996). Before proceeding for developing inbred lines
or strains it is essential for a plant breeder to
understand the mechanism of temperature stress,
genetics of response of crop plant to different stress
conditions. While planning a breeding programme for
temperature stress tolerance, it is essential to identify
J of Biotech & Crop Sci (2016) 5(6): 32-40
the phenotypic characters that could assist a breeder
in successful implementation of the programme.
Heat Tolerance, its Mechanism and Genetic Basis:
Temperature higher than the optimal is considered as
heat stress that may be at vegetative growth or at
reproductive phase. At vegetative growth, the adverse
effect of high temperature may be on seedling
emergence, vigor and survival, while at reproductive
stage, the effects may be on process of fertilization,
pollen viability, stigma and style, ovules and post-
anthesis. At the whole plant level, heat stress causes
an acceleration of developmental stages, abortion of
seed development, and impairment of grain filling. At
the physiological level, high temperatures affect
major functions of plant cell, including
photosynthesis, energy metabolism, and translocation
of assimilates. Plant enzyme activities are
thermolabile, including RUBISCO (Weis 1981),
sucrose synthase (Rijven 1986), Catalase (Willekens
et al 1995) and superoxide dismutase (SOD) (Matters
and Scandalios 1986). Inhibition of these enzymes is
major cause of inactivation of CO2 fixation at high
temperatures. Heat stress severely inhibits plant
capacity to convert sucrose into starch. At molecular
level, the most prominent alterations caused by heat
stress in plant cell are modification of protein
synthesis, including synthesis of Heat Shocked
Proteins (HSPs) and antioxidant enzymes, and an
alteration of membrane composition and structure.
Genetic variation in heat tolerance for various
attributes exist in crop plants viz. germination,
growth during heat stress, growth recovery after heat
stress, photosynthesis, translocation, flowering and
seed set and stability of the cellular membrane. In a
6 x 6 diallel study in sweet corn, Williams et al
(1969) found that inheritance of recovery from a 6-hr
heat stock at 52OC behaved in partially dominant
nature. Inbred showing a high GCA for the trait
tended to produce more heat tolerant hybrids. In
another study on tomato, it was found that percent
normal flower and percent fruit set showed partial
dominance. Flower production and fruit set under
heat stress appear to be genetically independent
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J of Biotech & Crop Sci (2016) 5(6): 32-40
(Hanna et al 1983). Strong association between heat
tolerance and simple plant character cannot be
expected unless a genetic linkage is involved. Since
heat tolerance is largely a cellular manifestation,
selection in cell cultures presumably carries and
potential as a method for improving heat tolerance.
Genetic resources for heat tolerance are apparently
quite common within the normal breeding germplasm
of different crops. On the other hand, for a good
number of crop plants, the extent of existing genetic
variation in heat tolerance has a hardly been explored.
The various studies on the genetic variation in heat
tolerance reveal a number of genetic resources for
heat tolerance in several important crop plants.
Chilling Stress, its Mechanism and Genetic Basis:
Reduction in crop productivity by low temperatures,
called as chilling stress, whereby plants are exposed
to low temperatures essentially above 0 OC. Chilling
sensitive plants are typically tropical plants. Chilling
stress may be either at plant/organ level or at the sub-
cellular level. At plant level, chilling stress affects
seed germination, growth, fruit or seed set, economic
yield, pollen fertility and fruit quality. It leads to
reduced germination, poor seedling establishment,
stunted growth, wilting, chlorosis, necrosis, fruit or
seed set, pollen sterility etc. while at sub-cellular
level chilling affects membrane stability, chlorophyll
synthesis, photosynthesis, respiration and may
generate toxicity due to H2O2. In crop plants, chilling
injury results in poor seedling establishment, stunted
growth, wilting, chlorosis, necrosis, poor fruit set, etc.
Water stress is often observed in chill affected plants
and is largely localized at the root, as chilling of the
intact root results in wilting (Berry and Raison 1981,
McWilliam 1983, Christiansen and John 1981).
Some of the changes related to low temperature stress
include alterations in gene expression, composition of
proteins, lipids, carbohydrate, membrane properties,
solute leakage, mitochondrial respiration and
photosynthesis (Levitt 1980, Wang 1982, Markhart
1986, Guy 1990, Thomashow 1990, McKersie 1991,
Howarth and Ougham 1993, Smiranoff 1993, Foyer
et al 1994). Since low temperature induces oxidative
stress in tissues, chilling damage is partly attributed
to the effects of in-vivo-generated Reactive Oxygen
Species (ROS) in the cells. Kazemitabar et al (2003)
studied short term cold stress on rice seedlings and
found alteration to the total leaf protein, including
fragmentation of ribulose-1, 5-
bisphosphatecarboxylase RUBISCO). Physical
transitions of membranes from a liquid-crystalline
phase to a solid-gel phase were first suggested to be
the primary response of chilling-sensitive plants
subjected to low temperature stress (Lyons and
Raison 1970). Change in phase transition results in
increased leakiness of the membranes that ultimately
leads to a loss of campartmentation, collapsed
gradient and disrupted metabolism (Levitt 1980,
Wang 1982, Markhast 1986, Collings et al 1995).
Chilling tolerance was also linked with the extent of
lipid unsaturation in some plant species (Roughan,
1985, Hugly and Somerville 1992). Efforts to alter
the degree of unsaturation of membrane lipids have
resulted in improved chilling tolerance (Murata et al
1992, Kodama et al 1994, Moon et al 1995). Levels
of some of the nuclear encoded proteins, such as F 1-
ATPase, Cyt-oxidase, and molecular chaperones
(HSP 50 and HSP 60) were also reduced in the
mitochondria during chilling stress. The competence
and stability of mitochondria are important for plant
tissues to survive low temperatures especially during
early seedling growth. Because mitochondria are both
the source and a target of oxidative stress in seedling
subjected to chilling (Purtarulo et al 1991, Prasad et
al 1994, Purvis 1997), the functions of mitochondrial
proteins could be affected by chilling induced
oxidative stress. Chilling causes a decline in the
activity of cyt-oxidase and an increase in alternative
oxidase activity (Elthon et al 1986, Rybka 1989,
Prasad et al 1994). Genetic variation in chilling
tolerance has been revealed for various physiological
process such as photosynthesis and plasma-
membrane function as well as different plant
functions such as generation, growth seed set etc.
However, most of the information is available on
traits like seed germination and seedling
34

establishment under low temperature. Field
emergence of maize under early planting was
improved by recurrent selection at the rate of 84%
(Mock and Bakri 1976). In a maize population,
derived from a diallel mating system, primarily
additive genetic effects with a significant maternal
effect conditioned the emergence rate (Chapman
1984). The large genotype x environment interaction
revealed for emergence rate. In another study,
multiplicity of environmental factor that affects field
emergence of maize was reported (Unander 1984).
In a study of 56 reciprocal single crosses and parental
lines of maize, the nature of inheritance of cold
germination at 6OC and 8OC was found to be complex
with strong maternal effects (Pesev 1970). A possible
genotype x temperature in most likely at the basis of
conclusion made that selection for chilling tolerance
at germination must be performed at several low
temperatures. When selection was performed in
maize under different germination temperatures both
additive and dominance variances were found to
control the trait (Keim and Gardner 1984). Maternal
effect could not be ignored and the conclusion was
that selection under growth chamber condition did
not result in significant improvement of cold
tolerance at germination.
Crop establishment under condition of early planting
also involves chilling tolerance of the growing
seedlings. The question is raised whether cold
tolerance at germination is associated either
genetically or physiologically with cold tolerance of
the growing seedlings. In selection experiment
performed with adapted maize population, the rate of
cold emergence was not consistently or positively
correlated with seedling dry matter. Selection for cold
germination in the growth chamber resulted in only
little improvement in seedling vigour in maize. On
the other hand, significant positive genetic correlation
was revealed between seedling dry weight and vigour
and the total number of seedling emerged in the cold
(Keim and Gardner 1984). In nine tropical maize
populations, the rate of cold emergence was
J of Biotech & Crop Sci (2016) 5(6): 32-40
positively associated with seedling vigour (Stamp
1984). A positive association may therefore, exists
between cold germination and seedling vigour,
depending on the nature of the genetic material and
the environmental conditions under which selection is
perform. The question whether the association found
are genetic or physiological is unresolved. The
prevalence of dominance gene action for various
attributes of chilling tolerance in plants is manifested
and used in hybrids. Genetic resources for chilling
tolerance are to be found in the lower temperature
margins of the crops range of distribution. High
altitude races for various crop species were found to
possess relatively high levels of chilling tolerance.
While ample genetic variation for chilling tolerance
has been identified in well-adapted breeding
population, such as the case is for maize (mock and
Eberhart 1972), the use of exotic tolerance races of
the crop has been shown to offer good opportunities
for improving its chilling tolerance (Mendoza 1979).
The use of the wild relatives of crops has also been
attempted. Introgression of chilling tolerance from
such exotic germplasm has been successful in some
cases, such as the tomato.
Freezing Tolerance, its Mechanism and Genetic
Basis: The freezing causes 70 to 80 per cent of the
liquid water in the tissues are frozen as extra cellular
ice, resulting in cellular dehydration (Levitt 1980).
The abilities of organisms to modify the growth of ice
and to withstand extensive dehydration are key
elements of cellular survival. Freezing may cause
disruption in and/or alter the semi-permeable
properties of plasma membrane. This results in a loss
of solutes from the cells. Further, cells remain
plasmolyzed even after thawing. In addition, cells
with intact plasma lemma may take up excess water
and become unusually turgid. Thus, the freeze-thaw
cycle may create stress by affecting the structure and
function of plasma lemma, that depends on the
stability of protein and lipid components under
freezing stress. There are various components of
freezing tolerance like osmotic adjustment, amount of
bound water, plasma membrane stability, cell wall
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components and cold responsive proteins. For many
plants like Brassica cold acclimation is associated
with accumulation of soluble sugars in the cytosol,
especially sucrose (Fu et al 1999).
Numerous studies were devoted to the inheritance of
winter hardiness in the field, and conclusions were
drawn with respect to selection work. Complexity of
GxE interaction, leading to the low observed
heritability, was found. Marshall (1982) reviewed
some of the results on heritability in winter cereals.
He noted studies where high heritability was revealed
up to 93%, especially after years of consistent and
differential winterkill. He concluded that the high
estimates are unduly encouraging because they do not
reflect the whole spectrum of possible stresses that
occur in the field. Grafius (1981) concluded that the
inheritance of winter hardiness is complex and
polygenic in nature. Grafius (1981) noted for his own
work that from one year to the next year, the same
set of varieties has exhibited a correlation of 0.60
with regards to winter survival. Therefore, winter
hardiness, as a phenomenon measured in the field
environment, is apparently not a genetic entity.
Freezing tolerance in the cereals under controlled
freezing conditions was largely controlled by additive
(Sukla 1981) or largely by non-additive (Parodi et al.
1983), gene action. When actual improvement of
winter hardiness is sought, enough genetic variation
did not exist. Transgressive segregation for the trait
has to be revealed. In contrast, Limin and Flower
(1982) noted additive gene action with a few genes to
control freezing tolerance in their wheat crosses.
Marshall (1982) discussed transgressive segregation
for freezing tolerance in the cereals and its utilization
in the development of hardy varieties. Hard evidence
on genetic association between freezing resistance
and to the plant characters is limited, inspite of the
fact that such association are of great importance. The
immediate and preferred germplasm would naturally
be any cultivated forms that survive extreme winter
conditions. Such materials are likely to be found in
the extreme low temperature margins of the crops or
species geographical distribution. While very hardy
materials may be revealed within the cultivated
germplasm the available information shows that
transgressive segregation from hardy x hardy crosses
is rare. Genetic variation for freezing tolerance may
also be exists in non-hardy materials. Induced
mutations are another source of genetic variability for
freezing tolerance. The wild relatives of crops were
often considered as genetic resource for freezing
tolerance. The use of cell and tissues in selecting for
freezing tolerance is practically non-existent. The
complexity of plant freezing resistance would seem to
hinder any practical application of in vitro selection
methods.
HYBRID AND INBRED DEVELOPMENT
IN MAIZE
The pedigree method is most widely used to develop
inbred lines and consequently for hybrid development
in maize. The fixation of genes through inbreeding
can best be achieved through selfing followed by full-
sib mating and half-sib mating. Repeated selfing
helps in unmarking deleterious recessive genes,
which are selected against and advantageous genes
are retained. Selfing results in uniformity and loss of
vigour, therefore, it is important to select and test in
each selfing cycle. One generation of self pollination
results in same level of inbreeding as three
generations of full sib mating and six generation of
half-sib mating (Hallauer and Miranda 1988). A
slower approach of fixation of genes would be more
useful in development of inbred lines for characters
like temperature tolerance which are controlled by
polygenes thereby provide more opportunity for
selection. During phenotypic selection under stress
environments, selections may be carried out both
between and within progenies. As the inbreeding
continues, the differences between progeny increase
and those within progenies decrease. At initial stages,
more plants need to be selected giving more
opportunity for the desired genotype to progress
further for final selection at later generations. Each
generation need to be adequately sampled to include a
36

range of segregants. For two parents differing for 10
allelic pairs, the F2 population size is 1,048,576
individuals. Hence with large number of genes
involved in the temperature stress tolerance, the
sample size becomes very large. Practically such
large populations are difficult to handle. Those cases
where a number of sources for temperature stress
tolerance are available, it is practically preferred to
have a smaller sample size and handle a large number
of cross combinations. Bauman (1981) reported that
500 were the most common sample size. Dhillon et al
(1994) proposed the sampling of foundation plants
for inbreeding, as half-sibs rather than self. This
approach nearly quadruples the effective population
size and has other advantages. Tolerance to heat in
sunflower is an important abiotic stress in various
ecological zones that contributed significantly in
increasing seed and oil yields. Selection of self-
fertility is also important in addition to heat tolerance
among lines during inbreeding.
Back crossing method works best for highly heritable
characters and can make a good inbred even better.
However, for a complex trait the results are variable
(Duvick 1974, Geadelmann and Peterson 1978). The
success of this method depends upon number of
genes controlling the inheritance of temperature
tolerance trait and the effect of environment on
selection. The numbers of back crossing vary
depending upon recovery of the characters of
adaptable recurrent parent, selection during back
crossing, heritability of temperature stress tolerant
trait, diversity between recurrent and non-recurrent
parents and linkages. The aim of the maintenance of
inbred lines is to maintain it genetic constitution
without change in its homozygous form. Variations
are known to occur for mutations (Sprague et al.
1960; Russell et al 1963) as well as a definite trend
towards reduction in line performance when
maintained through both selfing and sib-mating
(Bogenschutz and Russell 1986). Hence, a regular
selection among and within progenies helps in
improving and maintaining inbreds for targeted trait,
improving vigour and other agronomic traits. The
J of Biotech & Crop Sci (2016) 5(6): 32-40
development and maintenance of inbred lines through
recurrent selection is the most effective method to
improve for abiotic stresses. Inbred lines are
improved by introgression of specific gene(s) from
identified donor germplasm for desired agronomic
characters. These genes can be available in distant
genera or species. The incompatibility barrier in
transfer of such genes from distant species/genera can
be overcome using cell and tissue culture techniques.
Development of genetically engineered plants
through genetic transformation holds great promise.
The transgenic inbred line with insecticidal Bt gene is
an example of commercialization of transgenic
technology.
The development of maize inbred line carrying a
synthetic gene encoding a truncated version of Cry
IA(b) derived from Bacillus thuringlensis for insect
resistance is an another example, expressed a high
level of insecticidal protein and showed resistance to
repeated infestation of corn borer in field conditions
(Koziel et al 1993). A number of successful efforts
have been done in development of transgenic inbred
lines in cotton, maize, groundnut, tobacco, tomato,
potato, cucumber against various biotic stresses at
near-commercial level. However very little
information is available on development of transgenic
inbred lines carrying genes with tolerance to
cold/heat at vegetative and/or flowering stage.
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