Groundnut or peanut (Arachis hypogaea
L.), an annual legume, is an important oil and food crop. Global groundnut production has almost doubled, from 23.08 m tons in 1990 to 45.22 m tons in 2013, with an increase in cultivation area to 25.44 m ha from 19.75 m ha in the same period [1
]. Future demand projections indicate an increase in global demand for groundnut and its products. To meet the growing demand, groundnut is increasingly grown outside its traditional area of adaptation and beyond its natural growing seasons. Expansion of groundnut cultivation to non-traditional areas and/or seasons happens in regions of high profitability. This is evident in a non-traditional Northern part of India, where spring cultivation of groundnut is popular owing to economic returns. Groundnut is grown in about 5.0 m ha in India, of which 20% is cultivated in post-rainy season with an average yield of 1.8 t ha−1
more than the rainy season yield of 0.8 t ha−1
]. High-temperature adaptation of groundnut varieties is needed for cultivation in non-traditional areas and/or seasons.
Drought and high-temperature stress, and their combination, are important abiotic constraints of groundnut production in Asia and Africa. Yield loss to an extent of 1.7% in maize in Africa [3
] to 16% for soybean in the USA [4
] is expected with each degree rise in temperature beyond 30 °C. In the case of groundnut, an increase in mean air temperature of 2–3 °C is predicted to reduce groundnut yields in India by 23–36% [5
]. Vara Prasad et al. [6
] reported that heat stress during critical stages will affect the pod yield. Further, heat stress aggravates moisture stress, contributing to pod yield losses.
High-temperature stress affects several crops, including groundnut, but is not well understood [7
]. It is one of the major uncontrollable stresses affecting plant growth, development, and productivity [8
]. Understanding of trait responses under stress and non-stress environments is important to design a breeding program and develop improved cultivars suitable for stress environments. A few studies were carried out to elucidate heat-tolerance mechanisms in groundnut [10
], mungbean [11
], wheat [12
] and chickpea [13
]. Stress indices, mostly yield-based, are found to be reliable for screening genotypes for heat tolerance. Stress tolerance index (STI) is responsive to evaluate genotypes in stress and non-stress environments, and STI
has identified stress-tolerant genotypes in maize (Zea mays
]), mung bean (Vigna radiata
]), and common bean (Phaseolus vulgaris
Plant response to high-temperature stress is genotype-specific and varies with phenological stage of crop [17
], some specific physiological stages are more responsive to stress than others. Therefore, field tolerance of a genotype to heat stress is measured at several growth stages. Studies have shown that groundnut genotypes differ in sensitivity to temperature during both vegetative and pod growth [18
], and reproductive stages are more sensitive to stresses [21
]. Limited studies are available for screening of groundnut genotypes for high-temperature stress under controlled [10
] and field conditions [13
]. Screening of genotypes and understanding responses under field conditions is important to identify heat-tolerant genotypes. In the current study, variability for pod yield, yield parameters and physiological growth parameters are studied among groundnut genotypes under heat stress in field conditions, and heat-tolerant groundnut genotypes are identified.
The three test environments are represented as E1, E2 and E3. In E1, the flowering was spread over a period of 25 days with maximum temperature reaching up to 34 °C, except for three days (45, 52 and 53 days after planting (DAP)) when the temperature was 35 °C or above (Figure 1
a). In E2, on all the days of the flowering period, except five days (27, 28, 29, 30 and 43 DAP) the temperature was 35 °C or above for ca. 3–8 h in a day (Figure 1
b). The temperature in E1 varied from 28 °C to 36 °C, from 29 °C to 38 °C in E2, and 33 °C to 39 °C in E3. In E3, on all the days except two (32 and 33 DAP), the day temperature was 35 °C or above for ca. 5–8 h in a day (Figure 1
c). Duration of heat stress in E3 was 110 total hours, and 75 h in E2.
Individual ANOVA of three environments showed significant differences among the genotypes in heat-stress and non-stress environments for all traits, with an exception of crop growth rate (CGR) in E2, and sound mature kernel percentage (SMK) in E3 (Table 1
). Combined ANOVA over three environments showed significant differences for yield and physiological traits among groundnut genotypes, and among environments. However, genotype and environment interactions were significant for days to 75% flowering and days to maturity (Table 2
Variability among groundnut genotypes for yield and physiological parameters, and heritability estimates in a broad sense are summarized in Table 3
. The pod yield over three environments varied from 1483 to 6767 kg ha−1
, and harvest index from 24.6% to 65.2%. Days to 75% flowering (DF) of the genotypes varied from 35 to 50 days in the non-stress environment (E1), while in the heat-stress environment it varied from 31 to 39 days in E2, and 29 to 37 days in E3. Hundred kernel weight in heat-stress environment varied from 17 to 52 g, while it is higher, 27 to 59 g, in non-stress environment (E1). The oil content of the genotypes in heat-stress environment varied between 48.1% and 61.4% and in non-stress environment it was 48.6% to 58.8%. The crop growth rate (CGR) varied from 8.4 to 15.7 g m−2
in E2, and from 7.4 to 15.9 g m−2
in E3, compared to 5.7–14.6 g m−2
in E1. However, pod growth rate (PGR) was low in heat-stress environments, varying from 5.7 to 12.8 g m−2
in E2, and from 3.1 to 13.2 g m−2
in E3, compared to 4.9–13.4 g m−2
The coefficient of variation (CV) for pod yield in heat-stress and non-stress environments varied from 1.1% to 27.5%. The genotypes are categorized based on CV and presented in Table 4
. Stress tolerance index of groundnut genotypes under heat-stress environments and genotypes is categorized based on STI (Table 5
Flowering stage in groundnut is highly sensitive to high air temperatures of 35 °C and above, and results in pod yield reduction [25
]. The greatest sensitivity to hot days occurs from six days before to 15 days after flowering [6
]. Exposure to hot day temperatures of 35 °C and above continuously for six days relative to 28 °C reduced flower production by about 50% [26
]. Day temperature above 35 °C during reproductive phase reduces fruit set and, consequently, the number of pods and ultimately seed yield [26
]. In the present study, groundnut genotypes were exposed to different temperature regimes during flowering period, with increasing temperatures from E1 to E3 (Figure 1
In stress environments, E2 and E3, the genotypes were exposed to more than 35 °C temperature during flowering. Even after ca. 15–30 days of flowering, the air temperatures in E2 and E3 were higher than in E1. E1 was considered a stress-free environment as the maximum temperature was below 35 °C except for about eleven hours except on three days (on 45, 52 and 53 DAP) during flowering period. In E2, the temperature was 35 °C or above for 3–8 h in a day with a total of 75 h, and in E3, temperatures were 35 °C or above for 5–8 h in a day totaling to 110 h. Thus, both E2 and E3 represented heat-stress environments and severity of stress being higher in E3, compared to E2 (Figure 1
). Soil temperature is critical to pod formation and development, thus affecting pod filling and ultimately pod yield [28
]. In the present study, variability was not significant in average minimum and maximum soil temperatures in stress and non-stress environments. It varied from 17 to 33 °C in non-stress environments, while it was 21.7 to 37.5 °C in stress environments.
Combined ANOVA showed non-significant G × E interactions for pod yield and other physiological parameters (Table 2
), suggesting that genotypes responded in different ways in three different environments. The same was evident from the performance of the genotypes, wherein some genotypes showed a reduction in pod yield under heat stress, while others were either stable or recorded an increased pod yield. The observation suggests scope to identify groundnut genotypes that perform well in normal as well as heat-stress environments. Genotypic variation for pod yield [30
] for harvest index [33
] under high temperature among groundnut genotypes was associated with differences in botanical type. Our study involved two botanical types, var. hypogaea
(Virginia market class) and var. vulgaris
(Spanish market type) of Arachis hypogaea
but did show such an association.
High broad-sense heritability for pod yield, hundred kernel weight, oil content, harvest index, pod growth rate and crop growth rate in heat-stress and non-stress environments indicates the role of additive gene action in inheritance of these traits, and possible genetic gains through selection (Table 3
). Heritability was also high for days to 75% flowering and maturity duration, suggesting genetic gains through selection for these traits that may be useful in breeding early maturing varieties. Earlier studies reported high heritability for pod yield, harvest index [34
] and hundred kernel weight [36
] and moderate heritability for oil content [38
The influence of high temperature on flowering and maturity duration was profound among the groundnut genotypes. In non-stress environment, E1, the genotypes completed 75% of flowering in 35 to 50 days, while in heat-stress environments, they completed 75% flowering in 31 to 39 days in E2, and in 29 to 37 days in E3. Thus, under elevated temperature, groundnut genotypes complete flowering early, and matured early compared to non-stress environment. Similar to earlier observations [39
], early maturing genotypes that took 123 days in non-stress environment matured early by at least 18 days under heat-stress environments.
Pod and kernel yield of ca. 50% of the genotypes was reduced in heat-stress environments (E2 and E3), among which many genotypes recorded a pod yield reduction of up to 20% in E2, and over 20% in E3 (data not shown). Studies have shown that the reduction in pod yield at higher air temperatures is a consequence of the decrease in fruit set resulting from fewer pegs and pods [10
]. From controlled environment studies, Ketring [27
] showed that the numbers of pegs and pods were reduced by 33% by an exposure to a day temperature of 35 °C compared with 30 °C. Ntare et al. [24
], based on his field study, reported more than a 50% decline in pod yield when flowering and pod formation occurred at maximum temperature of 40 °C. Significant reduction in kernel mass due to heat stress to an extent of 45–46% was observed in heat-stress environments, E2 and E3 compared to non-stress environment, E1. It may be possible that kernel mass reduction, in part, may have contributed to pod yield reduction under heat stress, besides other factors.
The oil content of the genotypes in heat-stress and non-stress environment did not show variation. The oil accumulation in groundnut can be divided into three stages based on the phenotype, namely, the initial accumulation stage, the fast accumulation stage and the steady accumulation stage [42
]. Maximum oil accumulation in groundnut happens during the fast accumulation stage, which occurs towards the later part of seed development [43
]. In the present study, the maximum air temperature during late pod development stages is about 40 °C in all three environments and soil temperatures were also normal during entire pod developmental stages. Thus, to study the influence of heat stress on oil accumulation, it may be desirable to evaluate the genotypes by exposing them to varying temperatures of air and soil at late pod developmental stages. The reduction in duration of genotypes in the heat-stress environment did not show any effect on oil accumulation, suggesting the possibility of breeding early maturing varieties with high oil content.
The Crop Growth Rate (CGR) was high under heat-stress environments, E2 and E3, compared to non-stress environment, E1, indicating a greater accumulation of photosynthates at higher temperature. However, genotypic differences for CGR in the heat-stress environment indicate that the magnitude of response to heat stress is variable among genotypes. Pod Growth Rate (PGR) was low in heat-stress environments, E2 and E3, compared to non-stress environment, E1, indicating poor partitioning of accumulated photosynthates. Although groundnut accumulates higher photosynthates in response to high temperature, the partitioning of photosynthates is affected under high temperature, thus reducing the pod yield. However, the response of genotypes to CGR and PGR is variable under heat stress and did not follow a common trend. The heat-tolerant genotypes showed a marginal reduction in PGR under heat stress, suggesting the possible utility of PGR as a criterion to select high pod yielding genotypes for heat-stress environments. Earlier reports suggested that CGR and PGR may be useful to derive the partitioning factor (PF), which is the ratio of PGR to CGR, and PF was correlated with pod yield under heat-stress and water-deficit environments [30
] and PF was found to be one of the best indicators to screen heat-tolerant genotypes in Sahel environments [24
]. Harvest index of heat-tolerant genotypes did not vary much under heat-stress and non-stress environment, while in other genotypes, harvest index showed a reduction under heat stress. Under extreme heat stress, as in E3, there is a significant reduction in harvest index of heat sensitive genotypes from 33.2% to 24.6%.
3.1. Performance of Groundnut Genotypes under Heat Stress
Based on pod yield performance in heat-stress and non-stress environments, groundnut genotypes were categorized into three groups. The first group consisted of genotypes that were stable across heat-stress and non-stress environments, which implies that these genotypes are stable for pod yield under heat stress. The second group consisted of genotypes that showed an increase in pod yield in heat-stress environments, while the third are the heat-sensitive genotypes that recorded pod yield reduction under heat stress. Coefficient of variation (CV), one of the simplest parameters for determining stable genotypes [45
], was used in the present study.
Genotypes with a very low CV for pod yield are stable across environments. ICGV 06420 was identified as a stable genotype (CV of 1.1%) and its pod yield varied from 5089 to 5198 kg ha−1
in heat-stress and non-stress environments (Table 4
). The other stable genotypes, ICGV 87128, ICGV 87141, ICGV 97182, TCGS 1043 and ICGV 03042, recorded high pod yield varying from 3511 to 6192 kg ha−1
. The mean PGR of these genotypes in heat-stress environments, E2 and E3, varied from 0.25 to 3.1 g m−2
which was higher in comparison to non-stress environment, E1. Five genotypes, GJG 31, ICGV 87846, ICGV 03057, ICGV 07038 and GG 20, showed an increased pod yield by at least 9.0% under heat-stress environments as compared to non-stress environment. Pod yield increase of over 47% under heat stress was recorded by GG 20 and GJG 31. The mean PGR of these two genotypes in heat-stress environments, E2 and E3, is 0.65 to 3.6 g m−2
higher than in stress-free environment. Understanding the physiological mechanisms underlying increased accumulation of photosynthates and subsequent enhanced and/or efficient partitioning to the sink may be useful to develop promising groundnut genotypes for cultivation under heat-stress environments. The genotypes with an increase in yield under heat stress may have greater potential to be developed as heat-tolerant genotypes through breeding program. Ntare et al. [24
] reported genotypes with increased pod yield and partitioning factor under high temperatures as a consequence of high radiation-use-efficiency of these genotypes. On the contrary, pod yield reduction of ca. 18–26% due to high air temperature was reported [6
3.2. Heat-Tolerant and Superior Pod-Yielding Groundnut Genotypes
Stress tolerance index (STI) is associated with pod yield (r
= 0.9) under heat-stress environments, thus STI
is considered as a reliable parameter to identify heat-tolerant groundnut genotypes. Porch [16
], in their evaluation of heat tolerance indices, reported STI
and geometric mean as effective stress indices in common bean (Phaseolus vulgaris
) for selection of genotypes with good yield potential under heat-stress and non-stress conditions.
From the study, twenty-six groundnut genotypes with high STI
values ranging from 1.0–2.1 in E2 and E3 environments were identified as heat-tolerant genotypes. Heat stress-tolerant genotypes, ICGVs 97182, 01232, 07013, 07213, 89280, 00350, 03057, 06420, 02266, 03109, 06099, 07273, 00351, 07268, 06039, 07148, 03042, 05032, 07038, 05155, 06040, 07012, 06424, 07246, TG 37 and TAG 24, identified based on STI, also possess several other important traits. ICGV 00351 was released in India as a drought-tolerant variety [48
], and ICGV 00350 and TAG 24 were released for post-rainy season cultivation in Zone 5 of India. ICGVs 06040 and 06099 were identified as high kernel Fe- and Zn-containing lines [49
], and ICGVs 05155, 06420, 03057 and 03042 are high oil containing lines now in national level multi-location testing in India under the All India Coordinated Research Project on Groundnut.
Based on STI and superior pod yield performance, seven heat-tolerant genotypes, ICGV 07246 (5385–6761 kg ha−1), ICGV 03042 (5662–6192 kg ha−1), ICGV 06039 (5308–6041 kg ha−1), ICGV 07012 (5237–6761 kg ha−1), ICGV 06040 (5606–6767 kg ha−1), ICGV 06424 (4496–6597 kg ha−1) and ICGV 07038 (5206–6521 kg ha−1) were identified for use as varieties and/or in breeding programs as parents. In heat-tolerant genotypes, hundred seed mass was not reduced under heat stress as a consequence of the biological processes in these genotypes that enable efficient partitioning of photosynthates to pods even under heat stress. Thus, seed mass can also be used as selection criteria to select for superior pod-yielding genotypes under heat stress.