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CROP PHYSIOLOGY & METABOLISM

Sensitivity of Peanut to Timing of Heat Stress during Reproductive Development

^a Plant Environment Lab., Univ. of Reading, Dep. of Agriculture, Cutbush Lane, Shinfield, Reading RG2 9AD, UK

p.q.craufurd{at}reading.ac.uk

	ABSTRACT

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
Peanut (Arachis hypogaea L.) crops grown in the semi-arid tropics are commonly exposed to damaging hot temperatures of above 40°C. The objectives of this research were to identify the time(s) during reproductive development when hot days reduce yield, and to examine relations between flower production and sensitivity to heat stress. At start of flower bud initiation (21 d after planting, DAP) plants of the cvs ICGV 86015 and ICGV 87282 were grown either at 28/22°C (optimum temperature, OT) or at 38/22°C (high temperature, HT) or were reciprocally transferred at 3-d intervals between the OT to HT regimes and vice versa, until 46 DAP. Transferred plants remained in the new temperature regime for 6 d before being returned to their original regime. All plants were harvested at 67 DAP. In cv. ICGV 86015, transfers between 6 d before and 15 d after flowering (DAF) significantly (P < 0.001) affected total number of pegs (i.e., pegs and pods) and reproductive (peg and pod) dry weight, with the greatest effect occurring at 9 DAF. In cv. ICGV 87282, number of pegs and reproductive dry weights were also significantly reduced by transfers at 9 and 12 DAF. Heat stress had no effect on flower production or the proportion of pegs forming pods, but did significantly reduce the proportion of flowers producing pegs. Data presented suggest that it is heat stress during floral bud development that determines peg number.

Abbreviations: DAF, days after flowering • DAP, days after planting • HT, high temperature • OT, optimum temperature

	INTRODUCTION

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
PEANUT is an important oilseed and forage crop grown in many countries in the semi-arid tropics of Asia and Africa. Pod yields in the semi-arid tropics are poor, averaging only 800 to 900 kg ha^-1, compared with yields of >2500 kg ha^-1 in the USA (FAO, 1998). Peanuts grown in semi-arid tropical regions are often exposed to air temperatures above 40°C (ICRISAT, 1994). Heat stress and moisture stress have been identified as major constraints to productivity (ICRISAT, 1992). Furthermore, given the present trend of global warming, temperatures are likely to become even hotter (Houghton et al., 1990). It is important to identify heat-tolerant peanut cultivars for use in breeding programs, but the effect of heat stress is not uniform during all stages of the reproductive phase. To do so, it is necessary to understand the effects of the timing of heat stress on reproductive development and yield.

Temperature significantly influences the rate of development and growth of peanut (Leong and Ong, 1983). The optimum temperature range for vegetative and reproductive growth and development is between 25 and 30°C (Wood, 1968; Cox, 1979), although the precise optimum has not been determined for most processes (Williams and Boote, 1995). Day temperature 35°C decrease individual leaf area, reduce the numbers of pegs and pods, and result in lower pod yields (Ketring, 1984). Some of these adverse effects may be associated with pollen mortality, which occurs when temperature is 33°C (De Beer, 1963). Cultivars differ in their sensitivity to heat stress during both the vegetative and the reproductive phases (Nigam et al., 1994). Heat-tolerant cultivars have been identified in West Africa on the basis of their superior partitioning of dry matter to pods (Greenberg et al., 1992).

Although the reproductive phase is relatively more sensitive than the vegetative phase to heat stress in many crop species (Hall, 1992), no information is available on the effect of the timing of heat stress during reproductive development on peanut pod yield. Pod number is the end product of the number of floral buds that produce flowers, the proportion of those flowers that are fertilized and produce pegs, and the proportion of those pegs which develop into pods. Heat stress at any or all of these stages may reduce pod yield. For example, in common bean (Phaseolus vulgaris L.) and cowpea [Vigna unguiculata L. (Walp.)] plants are particularly sensitive to high night temperature during macro- and micro-sporogenesis, 6 to 8 and 6 to 12 d before anthesis, respectively (Ahmed et al., 1992; Gross and Kigel, 1994), and heat stress at these stages of development causes male sterility. Plants are also sensitive to heat stress at anthesis and in common bean the negative effects of heat stress at this stage are associated with the function of the gynoecium (Gross and Kigel, 1994). However, the post-fertilization and early seed development stages in common bean are more tolerant to heat stress than the pre-fertilization stages.

The objectives of this research were to identify the time(s) between floral bud initiation and pod initiation when day time high temperature stress causes the largest reduction in reproductive yield of cultivars representative of Spanish and Virginia botanical types of peanuts; and to examine the relation between the sensitivity to heat stress and flower production.

	Materials and methods

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
A reciprocal-transfer experiment was conducted during the summer months of 1996 in the controlled environment facilities at the Plant Environment Laboratory of the Department of Agriculture, The University of Reading, UK (51°27'N lat. and 00°56'W long.). The experiment involved moving plants reciprocally between optimum and high temperature regimes at different times and for a fixed period before returning them to their original temperature regime.

Environmental Conditions
The experiment was carried out in two adjacent polyethylene covered tunnels (poly-tunnels, 25 m long by 8 m wide by 3 m high at apex) aligned east-west, one maintained at an optimum day/night temperature of 28/22°C (OT) and the other at high day/optimum night temperature of 38/22°C (HT). The photo- and thermo-period in the poly-tunnels was 12 h d^-1 and the photoperiod was controlled by a manually operated blackout facility. Air temperatures were measured in each poly-tunnel with screened and aspirated copper constantine thermocouples positioned at the top of the plant canopy. Readings were taken at 10-s intervals and means for successive 10-min periods were stored with a data logger (Delta-T Devices Ltd., Cambridge, UK). Carbon dioxide was at ambient concentration, 360 µmol mol^-1, and relative humidity was maintained at 70 (±5)% through automatic sprinklers during the day. The poly-tunnels transmitted about 75% of the incoming photosynthetically active radiation (PAR) and photosynthetic photon flux (PPFD) density in both the poly-tunnels averaged about 500 µmol m^-2 s^-1 during the experimental period.

Cultivars and Plant Husbandry
One Spanish cultivar, ICGV-86015, and one Virginia cultivar, ICGV-87282, were used, the seeds of which were obtained from the ICRISAT Asia Centre located at Hyderabad in India.

Uniform seeds of each genotype were selected and treated with Apron Combi 453 FS ([methyn-(2-methoxyacetyle)-n-(2,6-xylyl)-DL-(alanite)] + [2-(thiazol-4-yl) benzimidazole: 2-(1,3-thiazol-4-yl) (benz-imidazole)] + [tetramethylthiuram disulfide: bis (dimethylthiocarbamoyl)disulfide]) (Ciba Agriculture, Cambridge, UK) as a precautionary measure against seed-borne diseases. They were pre-germinated on the moist filter paper in Petri dishes kept in the dark for 2 d at 25°C, until radicles became visible. The germinated seeds were planted on 6 June 1996 (DAP = 0), one per 15-L pot at a depth of 2.5 cm. The pots were covered with aluminum foil to reduce radiative soil heating. The rooting medium comprised of sand, gravel, vermiculite and loamless peat compost mixed in proportions of 4:2:2:1, by volume, respectively. A commercial controlled-release fertilizer (0.15 kg kg^-1 N, 0.10 kg kg^-1 P, 0.12 kg kg^-1 K, 0.02 kg kg^-1 MgO plus trace elements; Osmocote Plus, Scotts UK Ltd., Ipswich, UK) was incorporated into the mixture at the manufacturer's recommended rate of 5 g L^-1. Seeds were not inoculated with Rhizobium and plants were therefore wholly dependent on inorganic nitrogen. All pots were soaked with tap water and allowed to drain for 24 h before planting; thereafter they were irrigated as necessary through an automatic drip irrigation system.

All plants were healthy and there were no serious pest or disease problems. Release of predators (Phytoseiulus persimilis A.-Henriot) and foliar sprays of Torque (a.i. Fenbutatin Oxide) controlled a mild incidence of red spider mite (Tetranychus urticae Koch). Thrips (Thrips tabaci Lindeman) were controlled by release of the predator Amblyseius cucumeris Oudemans. Plants were also sprayed with Repulse (a.i. Chlorothalonil; 2,4,5,6-tetrachloro-1, 3-benzenedicarbonitrile) to prevent the occurrence of leaf spot (Cercospora sp.).

Reciprocal Transfer Treatments
From planting to 21 DAP, when the first flower buds were initiated, all plants were grown at OT. At 22 DAP, one-half of the plants were transferred to HT. Thereafter, plants were transferred at 3-d intervals from OT to HT, and from HT to OT, up to 46 DAP, giving a total of nine transfer treatments. Plants remained in the new temperature regime for 6 d (Wheeler et al., 1997) before being returned to their original regime, where they remained until harvest at 67 DAP (between R5 and R6; Boote, 1982). Plants were harvested at this stage, rather than at maturity, to ensure that the effects of the transfer treatments could be clearly defined (Wheeler et al., 1997). Plants remaining in the 28/22°C and 38/22°C environments from 22 to 67 DAP served as OT and HT controls, respectively. There were five replicate plants for the transfer treatments and 10 replicate plants for each control treatment.

Observations and Data Analysis
Durations (d) from planting to the appearance of first fully opened flowers (R1), and pegs (R2) were noted on all plants. The number of flowers that opened each day was determined until final harvest. The times of pod (R3) and seed (R5) initiation were determined from a destructive harvest in an adjacent experiment.

At the final harvest (67 DAP), plants were removed from each pot and separated into roots, leaves, stems, pegs, and pods. The numbers of pegs and pods per plant were recorded and roots were washed with water to remove the potting medium. The respective weights of roots, leaves, stems, pegs, and pods per plant were recorded after oven-drying these components to a constant weight for 3 d at 80°C. Total dry weight and pod harvest index, the ratio of pod to total dry weight (inclusive of senesced leaves and roots), were calculated from the weights of individual components. Total dry weight values were adjusted to allow for the oil content of the seeds (Duncan et al., 1978). Fruit-set was defined as the ratio of total number of pegs to total number of flowers, i.e., proportion of fertilized flowers. Pegs forming pods was defined as the ratio of total number of pods to total number of pegs, i.e., the proportion of fertilized flowers forming pods.

The 3-d moving averages of number of flowers produced per day during the period from first flowering until 42 DAF were calculated on the basis of the number of flowers produced per day. The respective number of flowers produced during the 6-d stress period and subsequently in the 6-d period following stress were calculated for all transfer treatments. Analysis of variance was used to compare these values with the number of flowers produced during the same period in the OT and HT controls. All data are expressed on a per plant basis unless otherwise stated.

The experiment was designed as a randomized block with added control. Each reciprocal transfer treatment was replicated five times and the controls were replicated 10 times in order to increase the precision of comparisons with the transfer treatments. The analysis of variance for all the variables was performed with Genstat 5 (Genstat 5 Committee, 1987).

	Results

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

 
The mean day and night temperatures (±SD) in the OT poly-tunnel were 27.9(±1.4)°C and 22.1(±1.2)°C, respectively; corresponding values in the HT poly-tunnel were 38.4(±1.1)°C and 22.3(±0.9)°C, respectively. There were significant effects of cultivar, temperature and transfers on all of the traits given in Tables 1 and 2 unless specific mention indicates otherwise.

The pattern of flower production over time was similar in both cvs (Fig. 1a and b) . The number of flowers opening each day increased until 24 or 27 DAF, when seeds started to grow (R5), and declined thereafter. The maximum number of flowers opening each day was greater in ICGV 86015 than in ICGV 87282, and so significantly (P < 0.001) more flowers were produced in ICGV 86015 (Table 1). Flower production had effectively stopped in ICGV 86015 by 40 DAF, while in ICGV 87282 more than 5 flowers d^-1 were still being produced at 42 DAF. There was no significant (P > 0.44) difference between culitvars in the proportion of flowers setting pegs (fruit-set), and so ICGV 86015 produced significantly (P < 0.001) more pods than ICGV 87282.

View larger version (22K): [in this window] [in a new window]   Fig. 1 Rate of flower production (number plant-1 d-1) over time (d) from first flowering in (a) the Spanish cv. ICGV 86015; and (b) the Virginia cv. ICGV 87282 grown continuously at 28/22°C and 38/22°C. Vertical bars are the SED for comparing the two temperatures. The stages R2, R3, and R5 show the appearance of first peg, pod and seed at 28/22°C, respectively

Effect of Reciprocal Transfers
Transferring plants for 6 d from OT to HT, or from HT to OT, had significant (P < 0.001 and P < 0.05, respectively) effects on the number of pegs and reproductive dry weights (Fig. 2) . When plants of ICGV 86015 were transferred from OT to HT, and vice versa, between 6 d before flowering and 15 DAF, the number of pegs was either significantly reduced (OT to HT) or significantly increased (HT to OT) relative to the respective controls (Fig. 2a). Transfers at 18 DAF had no significant effect on number of pegs. Irrespective of the direction of transfer to and from OT or HT, the effect of temperature increased with time of transfer until 9 DAF, which coincided with first peg appearance (R2). The effect of transfers on reproductive dry weights were similar to those on number of pegs; reproductive dry weights were significantly (P < 0.01) reduced or increased relative to their respective controls when the plants were transferred between start of flowering and 15 DAF.

View larger version (34K): [in this window] [in a new window]   Fig. 2 Effect of transferring plants of (a) the Spanish cv. ICGV 86015 and (b) the Virginia cv. ICGV 87282 from 28/22°C (OT) to 38/22°C (HT) and from 38/22°C to 28/22°C at different times relative to flowering on the number of pegs and reproductive dry weights. Horizontal dotted lines show the 95% confidence intervals for comparing the transfers with control (Con) means. Vertical bars show SEDs for comparing transfer means. The different stages of reproductive development R1, R2, R3 show the appearance of first flower, peg, and pod at 28/22°C, respectively

High temperature had a significant effect (P < 0.001) on the total flower number in the controls (Tables 2 and 3 , Fig. 1) and in the reciprocal transfer treatments (Table 3). High temperature increased flower production in the HT control and OT to HT transfer treatments and vice versa in the HT to OT transfer treatments. However, these changes in flower production only occurred in 6 d following transfers to HT or OT (P < 0.01) (Table 3); during the 6 d OT or HT stress period, temperature had no significant (P > 0.35) effect on flower production (Table 3).

	Discussion

TOP ABSTRACT INTRODUCTION Materials and methods Results Discussion REFERENCES

The reciprocal transfers clearly demonstrated that hot days imposed from 6 d before flowering until 15 DAF in ICGV 86015 and from 6 to 15 DAF in ICGV 87282, significantly reduced number of pegs and reproductive dry weights. The pattern of flower production and start of peg initiation was similar in both cultivars. The largest reduction in reproductive dry weight occurred at 9 DAF. This coincided with first peg appearance (R2), and the period when flower production rates in the initial 20 DAF in OT were near maximal. Given that flower production started to decline about the time seeds began to grow (R5), the end of the heat-sensitive period probably reflects the changing pattern of resource allocation between developing and growing fruits and vegetative growth (in ICGV 87282) and reproductive node initiation (Bunting and Elston, 1980).

The duration of the sensitive period was much shorter in ICGV 87282 than in ICGV 86015. This apparent difference in sensitivity was associated with slower rates of development and flower production in ICGV 87282. However, Virginia culitvars such as ICGV 87282 generally produce fewer, but larger fruits and the difference in the duration of the sensitive period probably reflects the different reproductive strategies of Virginia and Spanish types, rather than sensitivity per se. The remainder of the discussion will therefore focus on the more responsive Spanish cv. ICGV 86015.

The main effect of HT was on fruit-set, i.e., the proportion of flowers producing pegs. High temperature had no deleterious effect on flower production or on the proportion of pegs producing pods. These data therefore point towards fertilization as the processes most affected by HT in peanut. Fruit-set and fertilization have also be found to be particularly sensitive to HT in a number of other legumes, including cowpea (Hall, 1992; Ahmed et al., 1992) and common bean (Monterroso and Wien, 1990; Gross and Kigel, 1994). Detailed studies of individual flower buds and flowers have shown that the most sensitive stage of development to HT occurs at micro-sporogenesis, 6 to 8 and 10 to 12 d before anthesis in cowpea and common bean, respectively. High temperature at micro-sporogenesis causes low pollen viability, poor anther dehiscence, and hence male sterility. The reciprocal transfer treatments that started 6 d before flowering significantly reduced peg number (Fig. 1). These transfers ended at flowering and can therefore only have affected processes that occurred during floral bud development and before anthesis. In peanut micro-sporogenesis occurs 3 to 6 d before anthesis (Martin et al., 1974; Xi, 1991). Therefore, it seems highly likely that micro-sporogenesis in peanut is also sensitive to high temperature.

If floral buds at a stage 3 to 6 d before anthesis are sensitive to temperature, then exposure to HT at this stage (i.e., transfer from OT to HT) will result in male sterility and lower peg numbers. Conversely, floral buds exposed to OT at this stage (i.e. transfers from HT to OT) should set fruits normally and have greater peg numbers. To test this hypothesis, the total number of flowers opened in 6-d periods, at 3-d intervals, starting from 3 d before to 12 d after the start of each HT or OT reciprocal transfer treatment, were regressed against peg number at harvest expressed as a percentage of the control value. Transfers at 15 and 18 DAF were excluded, since after 12 DAF the direction of the response was reversed. The variances of these regressions were compared (Fig. 3) . The lowest variance for transfers from OT to HT and HT to OT was found for flower production starting 6 d after the start of the HT or OT treatment. These data show that variation in peg number was most closely associated with variation in flower production in 6-d period after exposure to HT or OT. Although the fate of individual flowers was not followed in our experiment, the number of flowers opening in the 6-d period after the HT or OT transfer treatment (Table 3) should reflect the number of floral buds exposed to HT or OT at 0 to 6 d before anthesis. These relations therefore confirm indirectly that it is floral bud development that is most sensitive to temperature.

View larger version (19K): [in this window] [in a new window]   Fig. 3 Variance (s2) of regressions of number of pegs relative to control values against the cumulative number of flowers opening in each 6-d period relative to start of temperature treatment in plants transferred (a) from 28/22°C (OT) to 38/22°C (HT) and (b) from 38/22°C to 28/22°C

View larger version (24K): [in this window] [in a new window]   Fig. 4 Relations between (a) the total number of pegs relative to 28/22°C (OT) control values and the number of flowers produced in the 6-d period following an episode of 38/22°C (HT) and (b) the total number of pegs relative to 38/22°C control values and the number of flowers produced in the 6-d period following an episode of 28/22°C

	ACKNOWLEDGMENTS

 
We thank the Felix Foundation and the Department of Agriculture, The University of Reading for financial support, and Messers K. Chivers, S. Gill, A. Pilgrim, and H. Dorji for technical assistance. Drs. T.R. Wheeler and Aiming Qi and Mr. V.G. Kakani produced valuable scientific comments during the preparation of the manuscript.

Received for publication October 19, 1998.

	REFERENCES

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