High Temperature Stress Tolerance in Maize
High Temperature Stress Tolerance in Maize
High Temperature Stress Tolerance in Maize
(2019) 62:93-102
DOI 10.1007/s12374-018-0350-x
REVIEW ARTICLE
Abstract Maize, third most important staple cereal crop across necessary for the rainfed crops since climate of these regions
the globe, has been threatened with different environmental is very fragile, seriously affecting crop production and
constraints including heat and water deficit stress. Higher productivity. With increasing understanding of biochemical
environmental temperatures negatively affect the most at pathways and mechanisms that contribute to plant stress
anthesis, silking and grain filling reproductive phenophases. response, it has become evident that many of these responses
The situation is further complicated by the variable climatic lead to universal protective mechanisms which are activated by
events, resulting in gradual and sometimes sudden increase salt, drought and temperature and other signaling pathways.
in environmental temperature followed by irregular rain Among the various abiotic stresses, drastic temperature
frequency and intensity, and thus posing a serious threat to fluctuations are very common during plant growth and
global food security. To meet the ever increasing food development. High temperature stress especially during
demand there is an urgent need to develop climate resilient reproductive phenophase is becoming a major area of concern
maize varieties and the goal can be achieved by exploiting for plant scientists under fast changing climatic scenario,
the pertinent physiological, biochemical and molecular affecting crop production and productivity worldwide. High
mechanisms. By introducing certain modifications, together temperature stress induces cellular changes leading to
these mechanisms can help us to combat the negative impact overproduction of reactive oxygen species (ROS) which
of high temperature stress. This review encompasses many damages nucleic acids, proteins and lipids eventually
of such physiological and molecular approaches which may consequential cell death. Anti-oxidative stress metabolism in
help in mitigating the adverse effects of heat stress on maize plants comprising of enzymatic and non-enzymatic antioxidants
yield. Molecular, biochemical and physiological knowledge imparts stress tolerance by scavenging or detoxification of
available in domain that may be employed in breeding excess ROS. Better understanding of all the intricacies of
approaches to develop heat tolerant maize genotypes, has anti-oxidative stress metabolism will help in designing
thoroughly been discussed. appropriate strategies to develop crop plants with enhanced
high temperature stress tolerance.
Keywords: Antioxidants, Climate change, Heat stress, New approaches are being developed to manipulate
Maize, Photosynthesis expression of functionally related classes of genes by
maneuvering signaling pathways of abiotic stress and
characterization and cloning of transcription factors that regulate
Introduction the expression of many genes that could contribute to stress
tolerance (Ma et al. 2016).
Diverse environmental challenges pose a serious threat to Maize (Zea mays L.) is one of the most versatile emerging
food production for the burgeoning human population. C4 crop having wider adaptability under varied agro-climatic
Development of genotypes with enhanced abiotic stress is conditions across the globe. Globally, maize is known as
queen of cereals because it has the highest genetic yield
potential among the cereals. It is cultivated on around 177
*Corresponding author; Sushil Kumar Yadav
million hectares worldwide (FICCI 2014) and production
Tel : +91-9492042651; 91-40-24530161
E-mail : [email protected] during 2016-17 was 1067.21 million tonnes. Despite of its
94 J. Plant Biol. (2019) 62:93-102
global reach United States is the highest maize producing temperatures. World has witnessed excessive heat events
region (377.5 million tonnes). As per the 2014 FAOSTAT previously and there are predictions of their recurrence more
data, India with 42.3 million tonnes is the fourth largest frequently in coming decades (Semenov and Halford 2009).
maize producing country. It is the third most important food As per model studies it is estimated that sudden extreme
crops after rice and wheat in India and one of the fastest environmental events will suppress agricultural yields. On an
growing crop commodity. It can be consumed in a variety of average escalation of 3-4°C in environmental temperature,
ways by both human and animals. Maize can be used for the there will be a reduction of 25-35% in crop yield in Middle
production of ethanol, animal feed, cooking oil, syrups, East (Ortiz et al. 2008) and 15-35% in Africa and Asia (Ortiz
starch and many other useful products. Nutritionally maize et al. 2008). Currently, maize is mostly grown in regions with
contains around 24% carbohydrates, 18% protein and 7% prevailing 18-27°C optimum temperatures. However, it can also
fat. It is also a good source of phosphorus, magnesium, be grown at 33-38°C with optimum yield. Temperatures
manganese, zinc, copper, iron, Vitamin A, B1, B2, B6, C, E, beyond 38°C will drastically impact the economic yield of
Niacin, Folate and Pantothenic Acid. In addition to its maize (Koirala et al. 2017).
nutritional, industrial and agronomic importance maize is an
attractive model plant species. In comparison to other cereal
model plants, maize model has been studied most thoroughly Heat Stress
and been a model plant for genetic studies over the past one
century. A vast range of maize characteristics, a huge collection Heat stress (enough high temperature for a certain period)
of mutant stocks, large heterochromatic chromosomes, can induce irreversible damage to crop plants growth and
extensive nucleotide diversity, and genic co-linearity within economic yield (Wahid et al. 2007; Fahad et al. 2017). High
related species, have made it a keystone species for genetic, temperature can alter metabolic events at cellular level and
cytogenetic, and genomic studies (Strable and Scanlon pollen dehiscence, pollen fertility, silk emergence and stigma
2009). All these attributes made maize to be the prime choice receptivity, seed setting and grain filling (Xiao et al. 2011),
for identifying its potential to the variable climatic variables. ultimately reducing the grain yield. Excessive heat also
causes the reduction in net photosynthesis, leaf area, reduced
biomass accumulation and 1000 seed weight (Shah and
Climate Variability Paulsen 2003; Cheikh and Jones 2006). Environmental
temperatures higher than optimal may impede both vegetative
Sudden changes in environmental conditions adversely as well as reproductive growth. However, reproductive stage
impact the agriculture productivity. Prominent among these (anthesis, silking, grain filling and seed set) is the most
environmental factors include rainfall and water, light, sensitive stage which eventually lead to complete sterility
temperature, relative humidity, air and wind. Other abiotic and kernel abortion in maize (Shah et al. 2011).
components, including topography and soil also influence
plant growth and development. High temperature influences
all plant growth processes such as photosynthesis, respiration, Mechanisms of Heat Tolerance
transpiration, breaking of seed dormancy, seed germination,
protein synthesis, and translocation. At high temperatures the Stress/heat tolerance is the ability of plants which can
translocation of photosynthate is faster so that plants tend to evade the negative impacts of high temperature and produce
mature faster. Climatic variability leads to abrupt changes the economic yields at par or near to that of normal
rise in temperature (predicted rate expected is 0.2-0.4°C per conditions (Wahid et al. 2007). Tolerance may vary from
decade) and is likely to add 1.8 to 4°C in present day species to species and even genotype to genotype within the
temperature by the turn of this century. Significant coherent species. In cereal crops including maize substantial genetic
increasing trends in mean temperature were observed in variations exists which can sustain and produce during
Southern states of India (Rathore et al. 2013). The major unfavorable environmental temperature events (Shah et al.
threat of variable climate is to developing countries due to 2011; Jat et al. 2016). Unlike motile organisms, plant tolerance
scarcity of resources (Noor 2017) and unavailability of real is achieved by a number of morpho-physiological, biochemical
time weather information to the poor farming communities and molecular adjustments. At cellular level high temperatures
(Ahmad et al. 2016; Brown et al. 2018). Variable climate trigger the expression of certain genes and increase the
would be more disastrous for marginal and lower income accumulation of certain metabolites which may enhance the
farmers as compared to progressive and rich farmers. heat enduring ability of plants and thus heat tolerance
Greenhouse gases are the main and major culprit of (Hasanuzzaman et al. 2013). Being sessile in nature plants
changing the climate, especially for the increase in atmospheric have evolved several mechanisms ranging from escape to
J. Plant Biol. (2019) 62:93-102 95
avoidance for survival under unfavorable environmental dehiscence at early morning confers heat tolerance by avoidance
conditions and so for heat stress (Fig. 1). These mechanisms mechanism in rice (Ishimaru et al. 2015; Bheemanahalli et al.
operate both at whole plant level and cellular level. At whole 2017). Therefore, morphological variabilities available in
plant level, early maturation, changing leaf angle, leaf thickness, maize germplasm can be used as screening indices.
leaf wilting and the like are the stress avoiding strategies. Heat stress may alter several physiological processes viz.
While at cellular level, adjustment processes include ion membrane fluidity, net photosynthesis, respiration rate, osmolytes
transporters, LEA proteins, factors participating in signaling accumulation, hormone levels and so on (Wahid et al. 2007;
cascades, osmolytes, antioxidant defense and transcriptional Waqas et al. 2017). Plants have different strategies to cope with
control (Rodríguez et al. 2005). sudden and acquired heat stress. For sudden temperature
shoot up; leaf angle, leaf cooling by transpiration and
Morpho-physiological Adaptations adjustments in membrane lipid composition and distribution are
more vital for plant survival (Rodriguez et al. 2005). Apart
Stress avoidance primarily achieved by inducing certain from this, a number of ionic and osmotic adjustments, induced
changes in plant architecture. For instance, the maize genotypes stress related signals may trigger damage control processes
with high leaf wax, lower leaf angle, compact tassel and (Vinocur and Altman 2005). Heat tolerance in total is a very
lower cob angle are better suited for high temperature stress complex phenomenon which involves several individual events
conditions because of their ability to reduce direct sunlight as well as events in conjugation. Among the physiological
exposure and the evaporation rate. Reduced evaporation rate adaptations, maintaining photosynthetic rate at optimum even
in anthers may result in bulging of pollens, a very crucial under high temperature stress is the key physiological
phenomenon for anther dehiscence (Shah et al. 2011). Pollen process that contributes to heat tolerance. Higher rate of
96 J. Plant Biol. (2019) 62:93-102
photosynthesis is directly correlated with economic yield and Stress tolerance is an inclusive and complex mechanism,
hence enhanced heat tolerance. A report by Yadav and regulated by several genes at multiples stages during the
coworkers (2015) suggested that high photosynthetic rate, plant growth (Maestri et al. 2002). Like other cereals, in maize
maintenance of maximum quantum yield PSII photochemistry also heat tolerance seems to be regulated by a polygenic system,
(Fv/Fm), cell membrane stability and lowering the leaf therefore difficult to exploit its genetics for developing heat
temperature collectively contribute to heat tolerance in maize. tolerant genotypes. Thirunavukkarasu et al. (2017) has reported
total number of 174 drought-responsive genes in maize when
Biochemical and Molecular Adaptations exposed to moisture stress and their co-expression studies
revealed a very vital correlation between several adaptive
High temperatures induce several metabolic events at cellular events, each one representing a specific biological function.
and sub-cellular level. These events may involve production
of ROS and oxidative stress. Oxidative stress is the metabolic
stage when production of ROS become more than their Strategies for Improving Heat Tolerance
neutralization. ROS production occurs at several sub-cellular
sites including chloroplasts, mitochondria, peroxisomes, It is evident from the literature that substantial progress has
cellular and sub-cellular membranes. ROS are highly reactive in been made in individual disciplines like, plant physiology,
nature and cause damage to membranes, proteins, nucleic molecular biology, metabolomics and genomics. By integrating
acids. Membrane lipid peroxidation is the most destructive knowledge from these individual domains, strategies can be
and damaging effect of ROS reaction. Peroxidation of designed to improve heat tolerance in the already existing
membrane lipids increases membrane fluidity and leakage genotypes and introduce it in the sensitive ones.
of cellular fluid. This disrupts the cellular homeostasis and Transcription factors that regulate functionally related
eventually cell death. Plants have developed an excellent genes could be attractive targets for such investigations,
mechanism widely known as anti-oxidative defense system since they may also function in regulating quantitative traits.
to protect them from ROS damage. Anti-oxidative defense Transgenic manipulation of such transcription factors should
system includes both enzymatic and non-enzymatic antioxidants. help us understand more about multigene regulation and its
Enzymatic antioxidants include SOD, POD (APx/GPx), relationship to tolerance.
CAT, GR and non-enzymatic antioxidants are comprised Several morphological, physiological, biochemical and
mainly of tocopherols, β-carotene, ascorbic acid, glutathione molecular markers known to be associated with high
and polyphenols. temperature tolerance in maize which can further be used for
developing genotypes with advanced capabilities to thrive Biochemical Indices for Heat Tolerance
and yield better under higher environmental temperatures
(Fig. 2). Antioxidants
al. 2000) and sHSPs (Heckathorn et al. 1998). small towards the variance because of the trait complexity.
Therefore it is important to introgress several markers
Osmolytes associated with several QTLs into a cultivar to improve its
tolerance against heat stress (Messmer et al. 2011; Rodríguez
In response to unfavorable environmental events, plants et al. 2013; Frey et al. 2015). Multiple QTLs conferring heat
activate some adaptive mechanisms and the increased tolerance especially at reproductive stage in maize have been
production of osmolytes is most important and one of the mapped along with their associated markers (Frey et al.
well-studied mechanism. These osmolytes may include 2016). These markers can be deployed in initiating MAS for
sugar molecules, proline, glycine betaine and trehalose under pyramiding genes to breed for heat tolerance.
heat as well as other abiotic stresses. Several studies showed
that the plants having less ability to accumulate these
molecules were found to be sensitive to high temperature Approaches for Evaluating Heat Tolerance
stress (Rasheed et al. 2011; Yadav et al. 2016). These results
were further supported by the studies where exogenous Physiological and Biochemical Approaches
application of osmolytes like proline and glycine betaine
reduced the level of oxidative stress and improved the Genotypic evaluation for heat stress under field conditions
accumulation of soluble sugars thus protected the plants has always been challenging task because heat is often
from deleterious effects of heat stress. accompanied with moisture stress conditions. For better
understanding of heat tolerance in maize, the evaluation
Molecular Markers for High Temperature Tolerance studies should be performed at different growth stages under
controlled conditions so that the associated factors may not
Conventional breeding has made substantial progress in influence the findings. It is evident that each developmental
developing heat tolerant crop varieties. However, the stage in plants life cycle shows differential sensitivity to heat
genetics of heat tolerance in cereal plants is poorly understood. stress. As compared to reproductive stage, vegetative stage
Several studies focusing on the effect of heat stress on in maize life cycle is less sensitive to high temperature. In a
reproductive characters like, pollen viability, silk receptivity, study under field conditions Yadav and coworkers (2015)
pollen germination, pollen tube growth, grain weight, grain reported that high temperature during vegetative stage promoted
filling and post-anthesis leaf senescence, seed set and quality the growth of vegetative plant parts but affected yield-related
traits such as dent-flint kernels in maize. In maize, five and parameters. Higher temperatures during vegetative growth
six QTLs those regulate pollen heat tolerance (quality and improved net photosynthetic rate resulting in higher total
pollen tube growth) have been identified with a high heritability. stover yield at maturity. This yield reduction could be
However, the pollen tests were performed in vitro and might because of reduced pollen viability and source to sink supply
not be representative of the situation in vivo (Frova and Sari- of photosynthates. Another study by Yadav and coworkers
Gorla 1994). In a study on adult maize under heat stress Frey 2016 on maize seedlings reported a significant decrease in
et al. (2016). identified 11 QTL including 2 loci for heat membrane stability, chlorophyll fluorescence and chlorophyll
tolerance with respect to grain yield. Furthermore, they have concentration under extended heat stress and sudden heat
identified six heat-tolerant and 112 heat-responsive candidate shock. In another study by Tiwari and Yadav (2016), differential
genes co-locating with the previously mentioned QTL. Similarly, response of antioxidative enzymes under heat stress in maize
maize varieties tolerant to drought and salinity (Ribaut and during reproductive stage was reported. Different antioxidant
Ragot 2006; Luo et al. 2017), insect (Samayoa et al. 2015) enzymes; SOD, CAT, APX and POD were found to be
and diseases (Willcox et al. 2002; Wisser et al. 2011; Hurni associated with heat tolerance in maize. Tiwari and Yadav
et al. 2015; Maschietto et al. 2017) were developed by using (2017) reported the role of ascorbate-glutathione cycle in
marker assisted selection (MAS) in breeding. More detailed providing tolerance to maize against heat stress at reproductive
information for maize QTLs can be explored at http:// stage.
www.maizegdb.org and http://www.plantstress.com. However,
reports for improving tolerance to heat stress in maize are not Genetic and Molecular Approaches
very common.
Simple sequence repeats (SSR) and single nucleotide Several heat responsive genes and proteins have been
polymorphisms (SNPs) both are widely used in MAS. SNPs reported in maize. A number of gene expression studies can
are more commonly used markers because of their abundance be undertaken to confirm role of heat responsive genes.
in genome. Many SNPs associated with heat tolerance in Transcriptomic and proteomic profiles of the heat stressed
maize have been identified. Each one contributing small- maize at multiple growth stages can be studied to observe
J. Plant Biol. (2019) 62:93-102 99
differential response of genes. Thus the genotypes expressing minimized by developing heat tolerant crop cultivars possessing
the genes conferring tolerance to high temperature can be multiple abiotic stress tolerance. It needs concerted efforts to
selected for future gene cloning or breeding purposes (Jagadish develop new crop varieties possess tolerance to major abiotic
et al. 2010; Mangrauthia et al. 2016). Constitutive expression components via breeding or genetic modification.
of the Nicotiana PK1 gene enhanced moisture stress Earlier, substantial efforts were made to develop heat
tolerance in maize (Shou et al. 2004). In another transgenic tolerant maize by incorporating genes from other conventional
approach, bacterial RNA chaperones conferred moisture genetic resources using traditional methods but the progress
stress tolerance in maize plants (Castiglioni et al. 2008). has been relatively slow. In the age of modern genetics, it is
Transgenic maize with enhanced ZmVPP1 expression exhibits possible to tap all the available phenotypic diversity contributing
improved drought tolerance (Wang et al. 2016). Transgenic towards heat tolerance into the cultivated material through
maize over-expressing OsMYB55 led to activation of stress- using high throughput phenotyping and genotyping techniques
responsive genes and enhanced heat and drought tolerance such as GWAS (Ma et al. 2016; Lafarge et al. 2017) and
(Casaretto et al. 2016). Several attempts were made to genotyping by sequencing (GBS) (Spindel et al. 2013). The
develop heat-tolerant transgenic maize by manipulating recent emergence of genome editing techniques like
(over-expression/down-regulation) genes of recognized relevance CRISPR-Cas9 and TILLING would further accelerate the
isolated from different crop species including maize. rate of crop improvement for specific traits like heat
The already screened germplasm can be explored for tolerance. All these efforts would pave the way for initiating
studying the molecular mechanisms and used for identifying genomics assisted breeding to have genotypes with desired
genetic markers which further can be used in marker assisted characteristics. However, an integrated approach using
breeding. The use of genetic markers as diagnostic tools multiple techniques for improving complex traits like heat
accelerates the breeding process. Thus the integration of tolerance would be a more appropriate route towards a swift
modern genetic engineering practices in traditional plant success.
breeding would lead to develop maize varieties suitable for
future growing environments to meet the increasing global
food requirements. Rapid progress in next generation Conclusion
sequencing approaches has made the whole process more
easy and cost effective. During the regulation of heat stress Escalating global environmental temperature due to changing
response in plants, heat shock transcription factors (HSFs) climate would adversely affect the agriculture production
play a very vital role. HSFs control the expression of HSP across the globe. Plants have evolved several adaptive
genes (Chen et al. 2006; Zafar et al. 2016). 25 HSF genes in mechanisms to cope with such environmental stresses. These
rice were identified which were observed to regulate the strategies may involve several metabolic adjustments, gene
expression of HSPs (Guo et al. 2008). The identification and expression and morpho-physiological alterations. There is a
characterization of HSFs has opened up new avenues for need to explore and characterize genes which are involved in
conducting future functional genomic studies. Recently, conferring enhanced heat/multiple abiotic stress tolerance.
genome wide association studies (GWAS) has helped in the Genes and transcription factors from other plant species,
identification of new QTLs controlling important traits identified for enhancing multiple abiotic stress tolerance can
including heat tolerance in crop plants with high accuracy for be employed for improving its intrinsic tolerance in maize
improved breeding value (Ma et al. 2016; Lafarge et al. which is a vital cereal crop grown under very fragile
2017). Several genes conferring tolerance to heat and other environments. Similarly, the available genotypic variability
abiotic stresses at flowering stage have been identified in in maize (re-sequencing the available genetic resources) can
maize using GWAS which provides a strong basis to breed be exploited for breeding purpose by means of MAS or by
heat tolerant maize genotypes (Lafarge et al. 2017). MAS backcross. Other approaches like use of mutagens
(chemicals) for altering the gene function can also be given
a try for improving tolerance. Possibility of use of advanced
Future Perspectives genomic assay CRISPR-Cas9 should also be explored in
maize for understanding the function of various genes conferring
Prominent environmental factors which affect crop growth multiple abiotic stress tolerance and high temperature stress
and development include rainfall and water, light, temperature, in particular. Interface of conventional and modern genomic
relative humidity, air and wind. Amongst these drought and approaches for mitigating environmental stresses would be
high temperature pose a serious threat to sustainable crop the most credible approach for enhancing the high temperature
production. The negative impacts of climate change can be stress tolerance in crop plants including maize.
100 J. Plant Biol. (2019) 62:93-102
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