Phenology , Growth and Yield of Three Wheat ( Triticum aestivum L . ) Varieties as Affected by High Temperature Stress

Wheat is the most important cereal in the world. However, due to an increasing trend of rising temperatures around the world, wheat may be exposed to greater thermal stress in the near future. Therefore, the identification and development of suitable wheat varieties is an important step to resolve this threat to production and to achieve high yield, even under high temperature stress. In this context, phenology, growth and yield of three elite varieties of wheat (‘Gourab’, ‘BARI Gom-25’ and ‘BARI Gom-26’) were evaluated under two sowing conditions: optimum (sown on November 15) and late heat stress condition (sown on December 27). All wheat varieties, when sown late, faced severe temperature stress that significantly affected phenology, growth and finally yield. Taking into consideration phenological variation, dry matter (fresh and dry weight) partitioning and grain yield, variety ‘BARI Gom-26’ performed better both in optimum and late heat stress, followed by ‘BARI Gom-25’; ‘Gourab’ performed the least. On the basis of heat tolerance parameters [relative performance (RP) and heat susceptibility index (HSI)], ‘BARI Gom-25’ (RP-79%; HSI-0.7) was the best performing variety followed by ‘BARI Gom-26’ (RP-74%; HSI-0.9) under heat stress while ‘Gourab’ (RP-61%; HSI-1.3) was sensitive to heat.


Introduction
Accounting for a fifth of humanity's food, wheat is second after rice as a source of calories in the diets of consumers in developing countries and is first as a source of protein (Braun et al., 2010).Wheat is an especially critical "staff of life" for the approximately 1.2 billion "wheat-dependent" to 2.5 billion "wheat-consuming" poor-men, women and children-who live on less than $US 2/day (FAOSTAT, 2010).The International Food Policy Research Institute (IFPRI) projections indicate that the world demand for wheat will rise from 552 million tons in 1993 to 775 million tons by 2020, and 60% in total by 2050 (Rosegrant et al., 1997;Rosegrant and Agcaoili, 2010).At the same time, climate change-induced temperature increases are likely to reduce wheat production in developing countries (where around 66% of all wheat is produced) by 20-30% (Esterling et al., 2007;Lobell et al., 2008;Rosegrant and Agcaoili, 2010).The IPCC (2007) noticed that global climate change (GCC) will have a major impact on crop production.
Regarding agriculture and food security, overall crop yield (wheat, maize and rice) could decrease in South Asia by up to 30% by the end of this century (compared with an increase as much as 20% in East and South East Asia) (Anonymous, 2012).In cereal production alone, the most conservative climate change projections suggest a mini-mum decline of 4-10% across South Asia.In Bangladesh, rice production could fall by 8% and wheat production by 32% as early as 2050 (Anonymous, 2012).CIMMYT-ICARDA (2011) estimated that 20-30% of wheat yield losses will occur by 2050 in developing countries as a result of an assumed temperature increase of 2-3°C on a global scale, but these yield losses will not be fully compensated by yield gains in high latitude regions, estimated at 10-15% (OECD-FAO, 2009).
The annual mean temperature of Bangladesh is 25.75°C, which is expected to rise about 0.21°C by 2050 (Karmakar and Shrestha, 2000).The Organization for Economic Cooperation and Development (OECD) (2003) estimated a rise in temperature of 1.4°C by 2050 and 2.4°C by 2100 in Bangladesh.Islam (2009) estimated, from 34 meteorological climate sites in Bangladesh, that temperature increases over the past 100 years-for all Bangladesh-of 0.62°C (maximum) and 1.54°C (minimum) occurred in February.Poulton and Rawson (2011) reported that temperature in Bangladesh increased over the past two decades by 0.035°C/year.If this trend continues, temperatures will have increased 2.13°C more than 1990 levels by 2050.
Substantial losses in rain-fed wheat are also anticipated: studies in India suggest that a 0.5°C rise in winter temperature would reduce wheat yield by 0.45 tones/ha while a similar rise in temperature of > 2.5°C would reduce non-irrigated wheat and rice farm revenue by 9-25% The obtained results showed that the drought tolerant varieties 'Katya' and 'Zlatitza' had higher levels of these proteins, especially RBP and Clp proteases.(Anonymous, 2012).The Intergovernmental Panel on Climate Change (IPCC) estimates that by 2050, there will be changing rainfall patterns with increasing temperatures, flooding, droughts and salinity that would cause rice production to decline in Bangladesh by 8% and wheat by 32%, against 1990 as the base year (CCC, 2009).
Several research findings noticed that temperature below (<10°C) or above (>25°C) the optimum (12 to 25°C) alter phenology, growth and development and finally reduce the yield of existing Bangladeshi wheat varieties (Hakim et al., 2012;Hossain et al., 2009Hossain et al., , 2011Hossain et al., , 2012aHossain et al., , 2012bHossain et al., , 2012c;;Nahar et al., 2010;Rahman et al., 2009).Thus, heat is the greatest threat to food security in Bangladesh where wheat is the second most important food grain and where population is rapidly increasing (Indexmundi, 2011).The IPCC ( 2007), CIMMYT-ICARDA (2011), CGIAR (2009) and OECD (2003) reported that world wheat production will decrease due to global warming and developing countries, like Bangladesh, will be highly affected.Heat stress in wheat can be mitigated in two ways: heat management or the development of heat-tolerant cultivars.Breeding for cultivars that are tolerant to postanthesis high temperature stress is an effective strategy to overcome this problem.There is a concerted effort by researchers around the world to develop stress (heat and drought)-tolerant cultivars (Tab.1).As a sub-set of this global effort, and in the light of future global warming forecasting for the country, Bangladeshi researchers, including our group, are also trying to develop heat-tolerant wheat varieties.Therefore, the study was conducted to identify heat-tolerant and -susceptible wheat varieties from existing varieties for future breeding programmes.

Experimental site
The study was conducted at the experimental field of the Wheat Research Center (WRC), Dinajpur, Bangladesh during November, 2010 to April, 2011.The area falls under the Old Himalayan Piedmont Plain designated as Agro Ecological Zone 1 (FAO/UNDP, 1988).It is situated in northern part of Bangladesh and geographically, the area lies between 25°38ʹ N, 88°41ʹ E and 38.20 m above sea level.The soil is sandy-loam and strongly acidic (pH ranges from 4.5 to 5.5) (WRC, 2009).

Treatments and design
Three existing elite wheat varieties ('Gourab' , 'BARI Gom-25' and 'BARI Gom-26') from WRC, Bangladesh were used as experimental materials.The characteristics of these varieties are presented in Tab. 2. Their performance was evaluated under two growing environments: the first was an optimum sowing (OS) environment (sown on 15 November) while the other was a post-anthesis heat stressed environment i.e., late sowing (LS) (sown on 27 December).The experiment was conducted in a randomized complete block design (RCBD) with a split plot arrangement and three replications.Sowing dates comprised the main plot and elite varieties of wheat comprised the subplot.

Experimental procedure
Before sowing, seeds were treated with Provax-200 WP, a seed-treated fungicide containing Carboxin and Thiram.Research conducted at the WRC ( 2009) indicated that Provax-200 WP is a perfect match for controlling fungi in Bangladesh soil, for achieving excellent seed germination and for protecting wheat cultivars from fungal attacks during the seedling stage.This fungicide is marketed by Hossain Enterprise CC Bangladesh Ltd., an agrochemical company engaged in crop protection and seed treatment, in association with Chemtura Corp., USA.Seeds were sown at 120 kg/ha.Unit plot size was 1.6 × 4 m [4 m long 8 rows and row to row distance 20 cm (i.e., 9.6 g seeds/ row)].Fertilizer was applied at doses recommended by the WRC: 100-27-40-20-1 kg/ha of N (nitrogen), P (phosphorus), K (potassium), S (sulfur), and B (boron).Twothirds of N and a full amount of the other fertilizers were applied as a basal amount during final land preparation.The remaining N fertilizer was applied immediately after the first irrigation [21 days after sowing (DAS)].Second and third irrigations were applied at booting (47 DAS) and grain-filling (78 DAS) stages.Intercultural operations were done properly according to treatments.

Data collection and their procedure
The crop was harvested plot-wise at full maturity according to treatments.Sample plants were harvested separately from an area of 3 × 1.2 m (i.e., 3 m long middle 6 rows), avoiding border effects.The harvested sample crop of each plot was bundled separately, tagged and taken to a threshing floor.The bundles were thoroughly dried un-

Results and discussion
Temperature is a modifying factor in all stages of wheat development including germination, tillering, booting, ear emergence, anthesis and maturity since it can influence the rate of water supply and other sub strates necessary for growth, but varies with plant species, variety and phenological stages (Wahid et al., 2007).Under high temperature, the crop completes its life cycle much faster than under normal temperature conditions (Fischer, 1985;Hakim et al., 2012;Hossain et al., 2009Hossain et al., , 2011Hossain et al., , 2012aHossain et al., , 2012bHossain et al., , 2012c;;Nahar et al., 2010;Rahman et al., 2009).Delayed planting in a sub-tropical region such as Pakistan, India, Bangladesh, etc. reduced plant height, DH, days to maturity and the duration of grain filling and ultimately reduced yield and yield components (Din and Singh, 2005;Mahboob et al., 2005).

Days to germination
Low temperature is one of the most important environmental parameters of late-sown wheat in sub-tropical environments.Chakrabarti et al. (2011) conducted a field experiment in India and found that air temperature <15°C was not suitable for the growth and development (germination, seedling stand establishment and tillering) of spring wheat.Timmermans et al. (2007) reported that seedling emergence and establishment in Solanum sisymbriifolium, when planted late, were negatively affected by low temperature during germination.At the time of our present research, the maximum temperature during the germination period was >26 to 28°C, sometimes nearing 30°C, while the minimum temperature was between 12 and 13°C, in OS.However, at LS, the average maximum and minimum temperatures were near 23 and 10°C, and der bright sunshine until fully dried, then weighed and threshed.
Heat tolerant data of relative performance (%) and heat susceptibility index were calculated by following equations.Relative performance (RP%) for yield was calculated as described by Asana and Williams (1965) and was expressed as a percentage: If HSI < 0.5, the crop is highly tolerant to high temperature stress, if HSI > 0.5 < l.0, it is moderately tolerant, and if HSI > 1.0, it is susceptible to high temperature stress.
Temperature data was recorded regularly by HOBO U12 Family of Data Loggers (MicroDAQ.com)at the meteorological station, WRC, Dinajpur, Bangladesh and is presented in Fig. 1.
Data was analyzed using MSTAT-C (Russell, 1994).Treatment means were compared for significance by the least significant difference (LSD) test at p= 0.05.

Days to booting
Reproductive phases like booting, fertilization and gametogenesis (8-9 days before anthesis) are most sensitive to high temperature in various plants (Foolad, 2005;Tarchoun et al., 2012), as also observed with our present research findings, which noted that DB of the three evaluated varieties were significantly different in OS and LS.Among the varieties 'BARI Gom-26' took the most time for booting while 'Gourab' took the least time under both OS and LS (Fig. 3).In LS, required DB was reduced the most, by 14% in 'BARI Gom-26' and the least in 'BARI Gom-25' by 4%.Hakim et al. (2012) evaluated 20 wheat cultivars in same agro-climatological conditions and noticed that the life span of all wheat cultivars were reduced in LS due to high temperature stress (> 25°C) at the reproductive stage.sometimes minimum and maximum temperature ranged between 8-9°C and 20-19°C, respectively (Fig. 1).The required DG was earlier when temperature was higher (in OS) but germination was later in LS due to low temperatures (Fig. 2).This claim is supported by Fig. 1 and previous results reported by Hossain et al. (2011Hossain et al. ( , 2012c)), who conducted a field experiment in Bangladesh and noted that low temperature (<10°C) at the germination stage delayed the time taken for grain to germinate.Significant differences in DG were found among the three varieties with respect to OS and LS.Among them, 'BARI Gom-25' took more time to germinate in LS than other varieties, closely followed by 'Gourab' .On the other hand, 'BARI Gom-26' took least time to germinate.In OS, all three varieties took statistically similar time to germinate (Fig. 2).In our study, the required DG increased by 50% in 'BARI Gom-25' followed by 38% in 'Gourab' and 25% in 'BARI Gom-26' in LS, due to low temperature stress.

Days to ear emergence/heading
The developmental stage in which the spike or ear partially or fully appears to emerge from its enclosing sheath is also called ear emergence or heading (Acevedo et al., 2002).However, the time taken for the spike or ear to emergence from the enclosing sheath is entirely dependent on growth conditions.In our study, the three varieties evaluated needed most time for heading in OS and less time in heat stress (LS) (Fig. 5).Among them, 'BARI Gom-26' and 'BARI Gom-25' took statistically similar and longest time while 'Gourab' required the least time to reach heading due to heat stress in LS (Fig. 1, 5).Due to heat stress, the reduction in required DH was highest in 'BARI Gom-26' (25% reduction) and lowest in 'Gourab' (14% reduction).Hossain et al. (2011Hossain et al. ( , 2012bHossain et al. ( , 2012c)), Nahar et al. (2010), Rahman et al. (2009) and Ubaidullah et al.

Days to first visible awn
Growth chamber and greenhouse studies suggested that high temperature is most deleterious when flowers are first visible and sensitivity continues for 10-15 days (Foolad, 2005).In our present findings, due to heat stress in LS, all three evaluated varieties had a shorter life span than OS, which ultimately affected final GY (Fig. 1, 4 and 10).Both in OS and LS, 'BARI Gom-26' and 'BARI Gom-25' took more time than 'Gourab' to reach the first visible awn.Under high temperature stress, the required DFAV was reduced by 14% in 'BARI Gom-26' and by 8% in 'BARI Gom-25' .Nahar et al. (2010) also observed a decrease in the life span of wheat varieties in LS but not in OS, due to high temperature stress; in their study, maximum temperature at vegetative and reproduction stages were 25 to 27°C and 30 to 32°C, respectively.differences.'BARI Gom-26' and 'BARI Gom-26' took more but statistically similar time both in LS and OS while 'Gourab' took less time to reach anthesis.In LS, all three varieties showed a reduced life span to complete anthesis due to heat stress.Among them, 'BARI Gom-26' took less time (21% reduction) than 'Gourab' (10% reduction) to reach anthesis (Fig. 6).Hakim et al. (2012) also noticed that 20 wheat cultivars took 14 to 19% less time in LS than OS to reach days to flowering, due to high temperature stress (> 25°C).

Days to physiological maturity
The DPM of wheat cultivars varies due to inherent differences between cultivars (Shahzad et al., 2007), but is influenced by different environmental conditions (Spink et al., 1993).They also observed that delayed sowing shortens the duration of each developmental phase due to (2006) also observed that delayed sowing in wheat shortened the duration of each developmental phase due to a rise in temperature.They also reported up to 23 days difference between OS and LS for heading.Al-Karaki (2012), investigating 16 wheat cultivars in a Mediterranean climate, showed long pre-heading periods, followed by short periods and high rates of grain filling to avoid terminal drought and high temperature stress (25-31°C).Among them, 'Waha-1' , 'Omrabi-5' and 'Massaa-1' were tolerant to stress (drought and high temperature).

Days to anthesis/flowering
The main developmental stage when yellow anthers are clearly visible on spikes is termed anthesis or flowering (Acevedo et al., 2002).In the present experiment, it was found that all three varieties showed a different duration to reach anthesis, both in LS and OS, due to temperature

Days to harvest maturity
Environmental factors affect the number of days required to reach or achieve different growth stages in wheat, but that this varies with genotype due to their different genetic makeup (Araus et al., 2007).In the present study all 3 varieties matured earlier in LS than in OS.Among them, 'Gourab' matured earlier both in OS and LS while the two other varieties needed statistically more time to mature, 'Gourab' finally yielding lower GY (Fig. 8,10).The temperature during the grain-filling or grain-maturing period was near 22°C in OS and >30°C in LS, which ultimately forced the life span to become complete (Fig. 1).There is also a similarity between this result and that of a 2-year study by Ubaidullah et al. (2006) in which heading, grain filling and grain maturity were 23, 3 and 29 days earlier a rise in temperature.This observation is similar to that of our present research findings.In our research, DPM of all three varieties decreased significantly from OS to LS (Fig. 7).Among the 3 tested varieties, 'BARI Gom-26' and 'BARI Gom-25' were statistically similar but took the most time to reach PM in both OS and LS while 'Gourab' needed fewer days.However, in LS, all 3 varieties had a reduced life span from germination to physiological maturity.Among them, 'BARI  less time to reach PM than 'Gourab' which needed 15% less time as a result of heat stress during this period of LS (Fig. 7).Hakim et al. (2012); Hossain et al. (2011Hossain et al. ( , 2012b, c) , c) and Rahman et al. (2009) also observed that LS shortened the duration of each development phase due to high temperature stress at the reproductive stage.

Grain yield
Sowing time is the most important for temperaturesensitive cereals such as wheat, barley, sorghum, etc., but the time of planting and their effectiveness on a plant varies from region to region.In Kansas, USA, planting during OS encourages tillering during fall and spring, reduces competition among tillers, and promotes a high harvest index (HI).Early planting causes excessive tillering, increases competition, and leads to a low HI.LS wheat decreases tillering during fall and spring and causes tillers that develop during spring to be small with a low HI (Thiry et al., 2002).In Bangladesh, early wheat faces high temperature stress at the vegetative stage and LS wheat is affected at two stages: germination by low temperature stress (<10°C) and at the reproductive stage by high temperature (>25°C), which ultimately affects GY (Hossain et al., 2011;2012c).Every 1°C rise in temperature above the optimum (15°C) reduces yield by 3-4% per spike (Wardlaw et al., 1989a(Wardlaw et al., , 1989b)).
In our present study, all 3 varieties were highly affected by heat stress in LS than in OS, which finally drastically reduced GY.Among the 3 varieties, 'BARI Gom-26' produced statistically highest GY both in OS and LS, followed by 'BARI Gom-25' while 'Gourab' produced least GY.However, the rate of reduction varied from genotype to genotype.Among 3 varieties, 'Gourab' (39% yield reduction in LS) was highly affected by high temperature stress in LS than 'BARI Gom-25' (21% yield reduction in LS) and 'BARI Gom-26' (26% yield reduction in LS) (Fig. 10).In our research, fluctuations in weather conditions (Fig. 1) were reflected in phenology, crop growth and development (Fig. 2 to 9) and ultimately GY (Fig. 10), which is common to several crops (Martiniello and Teixeira da Silva, 2011).Previous research findings also indicated that high temperature significantly decreased all traits, especially GY (by 46.63%), 1000-kernel weight (by 20.61%) when wheat was sown late than when sown normally due to heat stress during LS.Due to heat stress in LS, 19% less time was required to reach DHM in 'BARI Gom-26' and 'BARI Gom-25' and 16% less time in 'Gourab' .Nahar et al. (2010) also observed a reduction in the number of required days to maturation in LS due to high temperature stress.

Fresh weight and dry weight
Under optimal conditions, 80 to 90% of the carbohydrates translocated to the wheat grain are assimilates from current photosynthesis and 10 to 20% from the plant's reserve (Spiertz and Vos, 1985).However, under stress conditions such as drought and high temperature, crops do not translocate carbohydrates to grain because in this situation the crop basically survives without production (Hall, 2001) or resource allocation (Martiniello and Teixeira da Silva, 2011).Hasan and Ahmed (2005) conducted a field experiment in Bangladesh (sub-tropical climate) and found that post-anthesis heat stress (>26°C) reduced maximum dry matter accumulation due to a reduction in wheat kernel dry matter, mirroring our experimental results.In LS, all 3 tested varieties were highly affected by heat stress, expressed as a reduction in dry matter (FW and DW) and GY (Fig. 9; 10).For these parameters, 'BARI Gom-26' performed better, followed by 'BARI Gom-25' while 'Gourab' performed worst in LS.Due to heat stress in LS, the highest reduction in FW and DW was 40 and 37% in 'BARI Gom-26' , followed by 'BARI Gom-25' (29 and 36%) and the least reduction was 25 and 32% in 'Gourab' (Fig. 9).Ahamed et al. (2010) evaluated 5 existing wheat varieties of Bangladesh under two growing conditions (optimum and late) and showed that dry matter partitioning and production in all 5 varieties was affected at LS due to heat stress (30 to 32°C), resulting in reduced GY.From the above results and discussion, due to high temperature stress in LS, duration of life cycle stages of our tested wheat varieties was reduced.OS (i.e.optimum sowing on November 15) resulted in better performance of all varieties than late sowing (i.e., LS on December 27).From overall performance (phenology, growth, yield and heat tolerance parameters), 'BARI Gom-25' and 'BARI Gom-26' were considered to be the best performing varieties under heat stress while 'Gourab' was found to be sensitive to heat.
grain yield of a genotype under a stress environment Y p = mean yield of the same genotype under a stressfree environment X = mean Y of all genotypes X p = mean Y p of all genotypes

Fig. 2 .
Fig. 2. Days passed to germination of 3 wheat varieties sown under optimum and very late conditions.Mean (±SD) was calculated from three replicates for each treatment.Bars with different letters are significantly different at p≤0.05 (LSD test)

Fig. 4 .
Fig. 4. Days passed to the first visible awn of 3 wheat varieties when sown under optimum and very late conditions.Mean (±SD) was calculated from three replicates for each treatment.Bars with different letters are significantly different at p≤0.05 (LSD test)

Fig. 6 .
Fig. 6.Days passed to anthesis of 3 wheat varieties when sown under optimum and very late conditions.Mean (±SD) was calculated from three replicates for each treatment.Bars with different letters are significantly different at p≤ 0.05 (LSD test)

Fig. 8 .
Fig. 8. Days passed to harvest of 3 wheat varieties when sown under optimum and very late conditions.Mean (±SD) was calculated from three replicates for each treatment.Bars with different letters are significantly different at p≤ 0.05 (LSD test)

Fig. 10 .
Fig. 10.Grain yield of 3 wheat varieties when sown under optimum and very late conditions.Mean (±SD) was calculated from three replicates for each treatment.Bars with different letters are significantly different at p≤ 0.05 (LSD test)

Fig. 11 .
Fig. 11.Relative performance (%) and heat susceptibility index of 3 wheat varieties in very late heat stress condition, as compared with optimum sowing Tab. 1.Recent studies related to heat, drought and low temperature stress, primarily in wheat, from different countries around the world Lukacs et al. (2008)sensitivity indices over 2 years, the bread wheat cultivars 'Yayla-305' , 'Gerek-79' , 'Dagdas-94' and 'Bolal-2973' werefound to be more drought-tolerant than the other cultivars.Bagci et al. (2007)Argentina Wheat, barley and Triticale Wheat, barley and a triticale cultivar were evaluated in three season under three thermal condition: control and two timing of heating before anthesis and found stem elongation stage is most sensitive to high temperature stress (yield reduction 46%)Ugarte et al. (2007)Hungary Wheat 'GK-Elet' and 'Mv-Emese' Pot culture experiment in growth chamber indicated that 'Mv-Emese'was good drought stress tolerance than GK-EletLukacs et al. (2008)Bulgaria Two drought tolerant wheat ('Katya' 'Zlatitza') and two sensitive 'Sadovo' and 'Miziya')