Syed Adeel Zafar, Amjad Hameed, Muhammad Amjad Nawaz, MA Wei, Mehmood Ali Noor,Muzammil Hussain, Mehboob-ur-Rahman
1 National Key Facility for Crop Gene Resources and Genetic Improvement/Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
2 Nuclear Institute for Agriculture and Biology (NIAB), Faisalabad 38000, Pakistan
3 Department of Biotechnology, College of Engineering Science, Chonnam National University, Chonnam 59626, Republic of Korea
4 Institute of Crop Sciences, Chinese Academy of Agricultural Sciences/Key Laboratory of Crop Physiology and Ecology, Ministry of Agriculture, Beijing 100081, P.R.China
5 State Key Laboratory of Mycology/Institute of Microbiology, Chinese Academy of Sciences, Beijing 100101, P.R.China
6 Plant Genomics & Molecular Breeding Laboratories, National Institute for Biotechnology and Genetic Engineering (NIBGE),Faisalabad 38000, Pakistan
Rice (Oryza sativaL.) is grown on around one 10th of the arable land (Wang and Peng 2017), and sustains the lives of three billion people (Krishnanet al. 2011). Major share of the rice production and consumption is centered in Asia(growing on ~90% acreage) (Kloti and Potrykus 1999; Datta 2004; Suh 2015). Rice is also a source of protein (~14%)and fat (2%) (Kennedy and Burlingame 2003). Rice is an attractive model plant species due to its small genome size(~440 Mb) (Bennetzen 2002), suitability for doing efficient transformation and genetic analysis (Hieiet al. 1994),availability of genome sequence of bothindicaandjaponicasubspecies and close genetic relationship with other cereals(Buell 2002). All these features made rice to be first choice for exploring its potential to the fluctuating climates (Jwaet al. 2006).
Climate change adversely impacts our agriculture and other resources including water, bio-diversity, etc. (Rasul et al. 2012; Afzalet al. 2015; Bakhtavaret al. 2015; Zafaret al. 2015; Fiazet al. 2016; Waqaset al. 2017). Escalating temperature (predicted to increase by 0.2°C per decade)would add 1.8 to 4°C at the end of this century (IPCC 2007). Most developing nations would be the major victim of emerging scenario largely because of lack of resources(Noor 2017) and information to the resource poor farming communities (Ahmadet al. 2016; Fiazet al. 2016). Thus it would be catastrophic to the low income farmers than that of the progressive growers.
Major source of changing the climate is the emission of greenhouse gases, result in increase in atmospheric temperature. Episodes of excessive heat occurred in the past and are estimated to recur more frequently at the fall of the 21st century (Semenov and Halford 2009). Climate change will suppress yields by 15–35% especially in Africa(Parryet al. 2007) and Asia, and 25–35% in middle East by the increment of 3–4°C (Ortizet al. 2008). Currently,most of the rice is grown in regions with prevailing optimum temperature (28/22°C), and any further change in average temperature will drastically impact the yield (Krishnanet al. 2011).
Heat stress (excessive heat) can cause irreversible damage(Wahidet al. 2007) by retarding the plant growth, metabolic activities, and pollen fertility and seed setting (Jagadishet al.2007; Xiaoet al. 2011), thus reducing the rice production(Wahidet al. 2007; Hasanuzzamanet al. 2013; Zafaret al.2017). In another report, it has been shown that excessive heat accelerates reduction in rate of photosynthesis,leaf area, reduces shoot and grain mass as well as seed weight, and water-use efficiency (Shah and Paulsen 2003).High temperature may impede the vegetative as well as reproductive stages (from emergence till maturity, Katiyar-Agarwalet al. 2003). However, booting and flowering are the most critical stages which may lead to complete sterility in rice (Shahet al. 2011).
Heat tolerance is usually coined with plants which can minimize the stress effects and produce acceptable economic yields at high temperature (Wahidet al. 2007). Like many other crop species, there is substantial genetic variations in rice germplasm exist which can thrive better under the prevailing high temperature environments (Shahet al.2011). The tolerance is addressed by making adjustments in various morphological, physiological, and biochemical traits in rice plant. Heat stress triggers the expression of certain genes and metabolites production - both together enhance the heat tolerance in plant (Hasanuzzamanet al.2013). Plants have evolved multiple mechanisms including escape, avoidance, or survival under high temperatures.These mechanisms impart short term avoidance or long term resisting adjustments. At cell level, tolerance processes including ion transporters, LEA proteins, factors participating in signaling cascades, osmolytes, antioxidant defense, and transcriptional control are essentially required to neutralize the stress effects (Rodríguezet al. 2005). Reduction in yield by inducing early maturity in hot environment is a part of an avoidance strategy under high temperature (Adamset al. 2001).
Modifications in plant architecture contribute significantly in heat stress avoidance. For instance, the cultivars with covered panicles are better tolerant to high temperature because of their ability to reduce the evaporation rate from anthers- reduced the spikelet sterility. Reduced evaporation rate results in swelling of pollens which is a crucial mechanism of anther dehiscence (Shahet al. 2011). In addition, the genotypes in which flowers open early in the morning have better heat tolerance utilizing the avoidance mechanism(Ishimaruet al. 2015; Bheemanahalliet al. 2017). Hence, the genetic variability for tolerance to heat in rice can be used as germplasm screening criteria (Ishimaruet al. 2015).
Temperature stress may significantly suppress the photosynthetic rate, hormone levels, membrane stability,respiration, the primary and secondary metabolites, etc.(Wahidet al. 2007; Bakhtavaret al. 2015; Ahmadet al. 2016;Waqaset al. 2017). For responding sudden heat shock, leaf position, cooling effect of transpiration and alteration in lipid constituents of membrane are more vital for plant survival(Rodriguezet al. 2005). A number of ionic and osmotic processes trigger the stress related signals which help in reviving the maintenance of damaged cellular proteins and membranes (Vinocur and Altman 2005). It is evident that the genetics of plant to compete high temperature is very complex. Among the physiological processes,photosynthetic rate is very heat sensitive which contributes in plant growth and yield. High photosynthetic rate at heading of rice is positively correlated with heat tolerance(Caoet al. 2003).Oryza meridionalisNg., a wild relative of the cultivatedO.sativa, maintains high photosynthetic rate,elongated leaf and maintains levels of protective proteins Hsp70, Hsp90, and Cpn60, all these attributes make it heat tolerant (Scafaroet al. 2010).
Heat shock triggers the synthesis of reactive oxygen species (ROS) in cellular organelles including mitochondria,endoplasmic reticulum, and peroxisomes, which damage their membranes and disrupt the internal cellular homeostasis.ROS also causes lipid peroxidation which may break the structure of cell membrane. For protecting membranes,various heat shock and other related genes synthesize several heat shock proteins, enzymatic and non-enzymatic antioxidants, and other osmoprotectants for maintaining the cellular homeostasis (Fig. 1). In rice, the tolerance to heat is linked with the production of high RNA content, strong antioxidative defense system, and less malondialdehyde content (Anjumet al. 2016) during meiosis (Caoet al. 2008).These mechanisms (synthesis of heat shock proteins)should be much more active at the sensitive growth stages of the plants so that damage by the excessive heat can be minimized (Maestriet al. 2002). In another study, it has been demonstrated that oxidative stress is frequently induced in rice leaves under high temperature environment(Fig. 1). In total, 48 heat responsive proteins identified in rice which were cataloged in classes related to energy and metabolism, regulatory actions and heat shock proteins.Four proteins corresponding to antioxidants can play role in heat tolerance (Leeet al. 2007). Also, the heat shock inhibits the protein synthesis, induces thermo-tolerance,increases the expression of heat shock proteins, and often results in apoptotic cell death. Heat shock also initiates the process of phosphorylation of proteins - involved in signaling the heat shock. These proteins are divided into three classes, of these two classes exhibit thermo-tolerance(Kimet al. 2002).
Antioxidants defense systemROS- very toxic compound for damaging the proteins, carbohydrates, DNA, and lipids,are produced abundantly in plants after their exposure to abiotic stresses. Ultimately the plant experiences oxidative stress (Sairam and Tyagi 2004; Xuet al. 2006). The ROS also play role in regulating expression of many genes- involved in controlling cell cycle, cell growth, programmed cell death(PCD), defense against pathogens, responses to abiotic stresses, and systemic signaling and development (Pandhair and Sekhon 2006; Gill and Tuteja 2010). For mitigating the damaging effects of ROS, plants synthesize antioxidants(Almeselmaniet al. 2006). Two types of antioxidants have been reported (enzymatic and non-enzymatic) which play roles in conferring tolerance to heat stress.
Enzymatic antioxidantsThese antioxidants are superoxide dismutase (SOD), peroxidase (POD), ascorbate peroxidase(APX), catalase (CAT), dehydroascorbate reductase (DHAR),glutathione reductase (GR), monodehydroascorbate reductase (MDHAR), glutathione-S-transferase (GST)glutathione peroxidase (GPX), and guaicol peroxidase(GOPX). However, increasing roles of GST, APX, and CAT in conferring heat tolerance as well as protection to ROS have been described in wheat cultivar (Ballaet al. 2009).Different antioxidant enzymes showed positive correlation with chlorophyll concentration in wheat plant cells while negative correlation was observed for membrane injury index at different growth stages (Almeselmaniet al. 2006).In another study, enhanced activities of SOD, GR, APX, CAT,and POD were observed at all growth stages in heat tolerant wheat cultivars while reduction in expression of POD, GR,and CAT was observed in heat sensitive cultivar PBW 343(Shewry 2007). The role of antioxidants in conferring tolerance to heat was compared inO.sativaandZea mays,and it was proved that the role of antioxidant defense system is evident in imparting tolerance to temperature stress(Kumaret al. 2012).
Recently, Hasanuzzamanet al. (2013) observed increased activities of APX, GR, GST, and GPX enzymes at different temperature regimes for different time intervals at seedling stage in wheat crop. These enzymes protect seedling from the oxidative stress induced after exposing them to high temperature. Generally, the elevation in temperature leads to enhanced production of antioxidative enzymes upto a certain temperature limit, and beyond this the production is reduced. High activity of APX has been identified in cytosol and chloroplast (Chen and Asada 1989)but has also been found in mitochondria (Andersonet al.1995). The SOD and APX enzymes are found in chloroplasts in soluble as well as in thylakoid-bound forms. The SOD converts the superoxide (produced on membrane surface)into H2O2followed by its detoxification by APX (Andersonet al. 1983). Thus these enzymatic antioxidants can be used as biochemical markers for heat tolerance in rice.
Non-enzymatic antioxidantsThese are ascorbic acid,phenolic compounds, glutathione, alkaloids, α-tocopherols,carotenoids, and non-protein amino acids. These are involved in protecting plants from oxidative stress (Pandhair and Sekhon 2006; Gill and Tuteja 2010). Ascorbic acid(vitamin C) detoxifies hydrogen peroxide and super oxide radicals (Duarte and Lunec 2005), and this compound is abundantly found in cytosol, vacuole, chloroplasts, and apoplastic space of leaf cells (Polleet al. 1990). Glutathione is another important antioxidant which can reduce the damage impact of oxidative stress (Chenet al. 2010). Also,thea-tocopherol (vitamin E) scavenges the single oxygen and lipid peroxides (Ognjanovi?et al. 2003). Carotenoids(zeaxanthin) are antioxidants which can quench singlet oxygen resultantly the plant is protected from oxidative damage (Zhang and Hamauzu 2004). High accumulation of all these antioxidants can be used as selection criteria selecting heat tolerant rice genotypes.
Fig. 1 A number of mechanisms as well as several compounds are produced after exposing to high temperature for rescuing rice plant out of the stress.
Heat tolerance is a complex trait- controlled by multiple genes at different growth stages of cereal crops (Maestriet al. 2002). At flowering stage, it behaves like polygenic traits in rice, hence making difficult to explore its genetics and utilize in breeding program (Zhanget al. 2009).Plants usually overcome such stresses by the coordinated expression of several genes in different pathways (Vinocur and Altman 2005). The expression analysis using microarray assay have shown that 73 genes can be induced by stress,of these 58 genes were novel (Rabbaniet al. 2003). A list of genes conferring heat tolerance in rice has been listed in Table 1.
Substantial progress has been made in several disciplines including plant molecular physiology and genomics- using this knowledge numerous strategies were designed to improve the complex trait like tolerance to heat (Koleet al.2015). Here we review several morpho-physiological,biochemical and molecular markers that are associated with heat tolerance in rice and can be used in future rice breeding programs to develop rice cultivars with brilliant genetics which can survive under high temperature stress (Fig. 2).
Table 1 Genes related to heat tolerance in rice
A number of morphological markers for heat tolerance(HT) such as high pollen fertility, long anthers, large basal dehiscence, and long basal pores have been identified in rice which can be used to screen the rice germplasm against heat stress (Shahet al. 2011). Similarly, number of spikelets per panicle, 1 000-grain weight, seed setting percentage, and grain yield were studied for screening rice germplasm to heat stress- significant reduction in all these traits were reported when exposed to high temperature(Caoet al. 2008). Thus, these attributes can be used as screening criteria (for heat tolerance) in classical rice breeding programs. Recently, opening of the spikelets early in the morning has been demonstrated as a useful criterion for selecting heat tolerant rice plants/genotypes(Bheemanahalliet al. 2017).
O.meridionalis, a wild species of rice, is a thermo-tolerant species as it maintains high net photosynthetic rate at elevated temperature. The high photosynthetic rate is sustained by the increased activity and stability of Rubisco- can be used as an important physiological marker for heat tolerance in rice (Scafaroet al. 2012). In a study, chlorophyll content in leaves whereas MDA content and electrolyte leakage in both leaves and roots increased under heat stress (Liu and Huang 2000) and can be efficiently utilized as physiological markers for heat tolerance. Similarly, leakiness of thylakoid membrane due to moderate heat stress is increased, and this can also be used as selection marker for high temperature tolerance (Sharkey 2005). Also, level of hormones, membrane stability, respiration, accumulation of primary and secondary metabolites, and water relations have been reported as important physiological parameters(Wahidet al. 2007) which can also studied for screening rice germplasm to excessive heat. Some other physiological attributes contribute to heat tolerance are leaf position,cooling effect of transpiration, lipid constituents of membrane(Rodríguezet al. 2005), and fluid content of membrane(Vinocur and Altman 2005).
AntioxidantsDifferent antioxidants such as SOD, POD,CAT, and APX can be used as biochemical markers for screening genotypes to heat tolerance (Almeselmaniet al.2006; Wahidet al. 2007; Hasanuzzamanet al. 2013).Several studies have elucidated the importance of these antioxidants in protecting against oxidative stress caused by high temperature (Ballaet al. 2009; Hameedet al. 2012).Similarly, non-enzymatic antioxidants also play active roles in conferring heat tolerance by protecting cellular organelles from ROS (Duarte and Lunec 2005; Chenet al. 2010). Thus these enzymatic as well as non enzymatic antioxidants can be used effectievly in screening rice germplasm for heat tolerance at early seedling stage.
Heat shock proteinsHeat stress is accountable for upregulation of numerous heat shock genes (HSGs)- encode HSPs (Zafaret al. 2016). These proteins protect cells from the injurious impact of high temperature (Changet al. 2007).Proteomic analysis showed elevated temperature regime could down-regulate proteins playing role in photosynthesis,energy and metabolism and up-regulating the resistance related proteins (Zhouet al. 2011). The HSPs can be classified into five unlike families in plants which are HSP20(or small HSP, sHSP), HSP60 (or GroE), HSP70 (or DnaK),HSP90, and HSP100 (or ClpB) (Swindellet al. 2007). Like many other crop species, response to heat stress in rice is very complicated. For instance, it involved the up and down regulation of various proteins including proteins involved in protection, biosynthesis and degradation of proteins, carbohydrate and energy metabolism and redox homeostasis (Zouet al. 2011). A HSP acts as molecular chaperons which repair stress-damaged proteins as well as protects cells from damage by stresses (Wanget al.2004). Heat tolerant rice over expressing the sHSP17.7 was developed through deploying transgenic approaches(Murakamiet al. 2004). Over expression of mitochondrial HSP70 (mthsp70) protects rice protoplasts from heat induced programmed cell death and ROS (Datet al. 1998),cosequecnlty it sustains the mitochondrial membrane potential and retards the synthesis of ROS (Qiet al. 2011).Importance of HSPs is increasing as their expression occur in nature, fluctuating number of genes are present in all species, and their expression and tolerance to stress are positively correlated (Feder and Hofmann 1999).
Malondialdehyde (MDA)Membrane lipid peroxidation in plants results from their exposure to heat stress that can be estimated by measuring the level of malondialdehyde(MDA, Anjumet al. 2016). Membrane damage is positively correlated to MDA level. Low MDA content, high RNA content and little ethylene synthesis are desirable traits for heat tolerance which can be useful biochemical markers in screening the rice germplasm for heat tolerance (Caoet al.2008; Zafaret al. 2017).
Fig. 2 Schematic diagram for studying the response of rice germplasm to excessive heat. HSPs, heat shock proteins; MDA,malondialdehyde; CMTS, cell membrane thermo-stability; RWC, relative water contents; QTLs, quantitative trait loci; SNP, single nucleotide polymorphism; InDel, insertion deletion; SSR, simple sequence repeat.
Marker-assisted selection (MAS) has been used to expedite the efficiency of plant breeding. A number of molecular markers have been used in MAS, however, simple sequence repeats (SSRs) and single nucleotide polymorphisms(SNPs) are being used extensively. The procedure was used to pyramid genes conferring resistance to biotic as well as abiotic stresses (Septiningsihet al. 2009; Das and Rao 2015; Shamsudinet al. 2016). For example,submergence tolerance was improved by deploying MAS strategy (Septiningsihet al. 2009; Luo and Yin 2013; Das and Rao 2015; Maet al. 2016). Similarly, tolerance to drought and salinity (Das and Rao 2015; Shamsudinet al.2016), insect (Das and Rao 2015) and diseases (Luo and Yin 2013; Das and Rao 2015; Maet al. 2016; Madhaviet al.2016) was improved using MAS in breeding. However,reports for improving tolerance to heat are scanty in rice(Langet al. 2015).
In the current scenario, SNPs have gained substantial popularity than that of SSRs due to their high abundance in rice genome. Several SNPs associated with tolerance to heat have been identified. Each marker has relatively small contribution due towards variance because of the complex nature of the trait. Hence it is important to introgress several markers-associated with several QTLs into a cultivar to improve its heat tolerance (Chenget al. 2012; Yeet al.2012, 2015a). Multiple QTLs conferring heat tolerance especially at flowering stage in rice have been mapped along with their associated markers (Chenget al. 2012; Yeet al.2012, 2015a). These markers can be deployed in initiating MAS for pyramiding genes to breed for high heat tolerance(Chenget al. 2012; Yeet al. 2012, 2015b). However, before application of these QTLs in MAS, it should be confirmed in subsequent populations after initial mapping for application to a wide germplasm (Yeet al. 2015a). Here we overviewed the identified QTLs and their markers conferring heat tolerance in rice (Tables 2 and 3).
It is always very challenging to evaluate plants for complex traits like heat tolerance under natural field conditions because of interaction of several other associated factors present in the open field. For example, heat and drought stresses occur simultaneously rather than heat alone, and usually their impact is more devastating at grain-filling period of cereals (Barnabáset al. 2008). It is therefore suggested that plants should be evaluated at various growth stages under controlled conditions. Different temperature regimes (35–48°C) were used for different durations to evaluate the rice germplasm (Jagadishet al. 2010; Weiet al. 2013; Fahadet al. 2016a; Mangrauthiaet al. 2016;Zafaret al. 2017). At seedling stage, rice is grown at normal temperature ((28±2)°C) for 2–3 weeks and exposed to high temperature ((45±2)°C) for 12 h. Then these plants were exposed to normal temperature (28°C) for 3 days(Zafaret al. 2017). Then these seedlings were evaluated for CMTS (cell membrane thermo-stability), RWC (relative water contents), MDA, and photosynthetic pigments like chlorophyll content and carotenoid (Zhouet al. 2011; Daset al. 2014; Zafaret al. 2017). In a different study, the plants were evaluated at booting (Fahadet al. 2016a, b) and anthesis stages (Jagadishet al. 2010), both these stages are signficantly reduced final yield. Plants were raised at normal temperature (28±2)°C from seedling until booting or anthesis, and were exposed to high temperature (38°C) for 6 h by transferring the plants in a growth chamber. Data regarding fertility percentage, seed setting rate, and other physiological assays were recorded to see variation for heat tolerance in rice germplasm (Wanget al. 2006; Jagadishet al. 2010; Daset al. 2014). Biochemical assays were also done to measure activities of various antioxidant enzymes like SOD, POD, CAT, APX, etc., which are associated with heat tolerance in rice (Wahidet al. 2007; Daset al. 2013).
Several genes and proteins respond to high temperature for conferring tolerance to excessive heat in rice (Katiyar-Agarwalet al. 2003; Murakamiet al. 2004; Sohn and Back 2007; Yokotaniet al. 2008; Wuet al. 2009; Qiet al. 2011;Weiet al. 2013; Mangrauthiaet al. 2016). A number of analyses representing the expression of genes can be undertaken to study the expression of various genes. For example, transcriptomic and proteomic profiles of the heat stresser stressed rice at multiple growth stages can be studied to observe differential response of genes. Thus the accessions-genotypes-cultivars expressing the genes conferring tolerance to high temperature can be selected(Jagadishet al. 2010; Mangrauthiaet al. 2016) for future gene cloning or breeding purposes. A gene (Athsp101)excised fromArabidopsis thaliana, and introduced in basmati rice cultivar Pusa basmati 1 (through transgenic approach)exhibited high tolerance to a fluctuating temperature regimes(Katiyar-Agarwalet al. 2003). Several efforts were made to develop thermo-tolerant transgenic rice by overexpressing or down-regulating genes derived from rice and other plantspecies (Zouet al. 2011).
Table 2 Identified and validated quantitative trait loci (QTLs) for heat tolerance in rice
The identified germplasm can be explored for studying the molecular mechanisms and can also be used for identifying DNA markers which can be used in markerassisted breeding. The use of DNA markers as diagnostic tools accelerates the breeding process (unlike traditional rice breeding practices). Thus the integration of modern genomic tools in breeding would lead to meet the future global food demand. The advent of next generation sequencing approaches made the deployment of these assays easy and cost effective in exploring the rice genome. The heat shock transcription factors (HSFs) have vital role in regulating heat stress response by controlling the expression ofHSPgenes(Chenet al. 2006; Zafaret al. 2016). In another study, 25HSFgenes in rice were identified which regulate the expression of HSPs (Guoet al. 2008). The identification of HSFs opened up new avenues for conducting future functional genomic studies. Recently, genome wide association studies(GWAS) helped in the identification of new QTLs controlling important traits including heat tolerance in crop plants with high accuracy with improved breeding value (Maet al. 2016;Lafargeet al. 2017). Several genes conferring tolerance to heat and other abiotic stresses at flowering stage have been identified in rice using GWAS which provides a strong basis to breed heat tolerant rice cultivars (Lafargeet al. 2017).
Table 3 Single nucleotide polymorphisms (SNP)/Insertion deletion (InDel) markers can be used for developing heat tolerance in rice
Climate change would challenge the sustainability of crop production. This impact can be minimized by developing thermo-tolerant rice cultivars - A user friendly approach.Earlier, substantial efforts were made to improve heat tolerance in rice by incorporating genes from other conventional genetic resources using traditional methods but the progress is relatively slow. In the age of modern genetics, it is possible to tap all the available phenotypic diversity contributing towards heat tolerance into the cultivated stuff through using high throughput phenotyping and genotyping techniques such as GWAS (Maet al. 2016;Lafargeet al. 2017) and genotyping by sequencing (GBS)(Spindelet al. 2013). The recent emergence of genome editing techniques like CRISPR-Cas9 and TILLING would further accelerate the rate of crop improvement for specific traits like heat tolerance. All these efforts would pave the way for initiating genomics-assisted breeding. However, an integrated approach using multiple techniques for improving complex traits like heat tolerance would be a more suitable route towards a swift success.
Increasing temperature would adversely threaten the global production of different crop species including rice. Plants cope such stresses by adapting various mechanisms in cells by altering gene expression as well as altering morphology and physiology of various parts. There is a need to explore these genes which are involved in conferring heat tolerance. Also, the genes from well-studied plant species can be transferred to rice for improving its tolerance to heat. Similarly, the available genetic diversity in rice (resequencing the available genetic resources) can be used in breeding through MAS or by MAS backcross breeding.Other approaches such as use of mutagens (chemicals)for altering the function of genes can also be used to improve the tolerance. The scope of the new genomic assay CRISPR-Cas9 should also be explored in rice for understanding the function of various genes conferring tolerance to heat. In the present scenario, bridging of conventional and genomic approaches for mitigating the heat stress is the most convincing approach for improving the genetics of the seed for heat tolerance.
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Journal of Integrative Agriculture2018年4期