5

Breeding for Heat Tolerance*Anthony E. Hall

Department of Botany and Plant Sciences,University of CaliforniaRiverside, California 92521

I. IntroductionII. Sensitivity to Heat of Different Stages of Plant Development and Plant Processes

A. Reproductive DevelopmentB. Germination and Seedling SurvivalC. Vegetative Growth and DevelopmentD. PhotosynthesisE. Heat Stability of MembranesF. Heat-Shock Proteins

III. Characterizing Production Environments to Determine the Extent to Which Heat isReducing Yield

IV. Genotypic Differences in Heat Tolerance. Inheritance. and Associations with OtherCharactersA. CowpeaB. Common BeanC. TomatoD. CottonE. RiceF. Chinese CabbageG. PotatoH. WheatI. General Observations

V. Selection Techniques and Breeding MethodsA. Selection TechniquesB. Breeding Methods

VI. Progress in Breeding for Heat Tolerance and ConclusionsLiterature Cited

I. INTRODUCTION

Relatively little effort has been devoted to breeding crop cultivars withheat resistance, even though many crop species can be damaged bytemperatures that are only moderately high, during specific sensitivestages of development. The breeding that has been conducted has, in

*This review is dedicated to Professor Otto Ludwig Lange. who conducted pioneeringstudies of plant heat tolerance in the Sahara Desert in Mauritania.

129Plant Breeding Reviews, Volume 10 Edited by Jules Janick

© 1992 John Wiley & Sons, Inc. ISBN: 978-0-471-57347-0

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several cases, been highly successful but not very well documented.Commercial breeders, understandably, rarely divulge successfulmethods such that they can be used by competitors. I have receivedvaluable advice from commercial plant breeders, but have decided thatgeneric reference to commercial approaches and successes is preferableto the use of personal communication citations. Cultivars of several cropshave been developed that have substantial heat tolerance, including:tomato (Lycopersicon esculentum Mill.); cotton, (Gossypium bar­badense L. and Gossypium hirsutum L.); and cowpea (Vigna unguiculataL. Walp.). The frequency of hot weather may increase in the future due toglobal climate change (Schneider 1989), and this change coupled withincreases in carbon dioxide concentration could substantially increasethe need for heat resistant cultivars (Hall 1990b).

Heat-resistant cultivars are defined as having higher yields, quality ofeconomic product, or greater plant survival under hot field conditionsthan standard cultivars. Two components contribute to heat resistance:(1) heat avoidance, in which tissues of plants subjected to high solarradia­tion or hot air have lower temperatures than control plants; and (2) heattolerance, whereby essential plant functions are maintained when tissuesbecome hot. The mechanisms of heat avoidance include: transpirationalcooling, leaf orientation and movement effects, differences in reflectionof solar radiation, and leaf shading of tissues that are sensitive to sun­burn. This review will give greater emphasis to breeding for heattolerance, but some of the opportunities and problems confrontingbreeding for heat avoidance will also be discussed.

An analytical approach to breeding for heat tolerance is presented. Iwill discuss the stages of plant development and plant processes that aremost sensitive to heat and are responsible for the reductions in yieldcaused by hot weather in production environments. This informationprovides a rational basis for evaluating heat-induced losses in yield fordifferent production environments, which is essential for determiningthe priority that should be given to breeding for heat tolerance in dif­ferent regions. Information on the plant processes that are most sensitiveto heat also facilitates the development of selection techniques thatdirectly address the factors responsible for yield losses. Effective selec­tion techniques are essential for discovering parental sources of heattolerance, conducting studies of inheritance, and combining traits thatconfer heat tolerance with the many other traits needed in cultivars.Information on inheritance can be used to develop effective breedingmethods. The overall effectiveness of different approaches for breedingfor heat tolerance is considered. A recent review of breeding for stressenvironments by Blum (1988) includes additional discussion andreferences pertaining to the physiology and genetics of heat resistance.

5. BREEDING FOR HEAT TOLERANCE

II. SENSITIVITY TO HEAT OF DIFFERENT STAGESOF PLANT DEVELOPMENT AND PLANTPROCESSES

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All plant processes are irreversibly damaged by heat if plants are sub­jected to sufficiently hot temperatures for sufficiently long duration. Forplant breeding, it is important to know the stages of plant developmentand plant processes that are most sensitive to heat and whether high dayor high night temperatures are most injurious. Insights into heat-sensitivestages and processes have been gained by subjecting plants to differenttypes of heat stress during different stages of development. The sensi­tivity of-specific plant processes to heat stress has been evaluated by com­paring genotypes with differences in tolerance to heat. These studieshave demonstrated that several crop species are sensitive to heat duringreproductive development. Because the fruit or the seed often are theeconomic product, these heat stress effects can substantially influenceproductivity.

A. Reproductive Development

Different stages of reproductive development can be damaged by hotweather, including: floral bud development, seed and fruit set, andembryo, seed, and fruit development. Research with cowpea will beexamined first, because of the comprehensive information available forthis species. Research with other species, including common bean(Phaseolus vulgaris L.), tomato, cotton, rice (Oryza sativa L.), wheat('friticum aestivum L.), maize (Zea mays L.), and sorghum [Sorghumbicolor L. (Moench)], will be examined to evaluate the generality of thesensitivity to heat of specific reproductive processes, and any species dif­ferences that are present.

1. Floral Bud Devel()pment. For cowpea, sensitivity to heat during floralbud development depends upon the photoperiod. Under hot long-dayconditions, specific cowpea accessions initiate floral buds, but the budseither abort or exhibit suppressed development, and hence no flowers areproduced (Dow EI-Madina and Hall 1986; Patel and Hall 1990). In con­trolled environments with a daylength of 14 h and day temperature of33°C, moderately high night temperatures of 24°C caused completesuppression of floral buds, whereas development was normal at 20°C(Ahmed 1992). This heat stress response only occurs in long days, andstudies with red and far-red light treatments during the night demon­strated that it may involve the phytochrome system (Mutters et a1. 1989b).The quality of light (red/far-red ratio) during the day also can

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influence reproductive responses to heat stress. Future studies of heatstress effects on reproductive development should not ignore the pos­sibility of photoperiod interactions, because these interactions wouldinfluence the relevance of the studies to different natural environments.The extent of heat-induced floral bud suppression has not been estab­lished for cowpea in different commercial production environments. But,suppression can be complete in extremely hot, long-day field environ­ments (mean daily maximum and minimum temperatures of 41°/24°C),where susceptible genotypes produce virtually no flowers (Patel and Hall1990).

Considerable abortion of floral buds has been observed in hot long-dayconditions in kidney-type common beans (Shonnard 1991). Studies inwhich kidney beans were transferred between a hot growth chamber(35°/24°C day/night) and a cooler growth chamber (25°/15°C day/night)demonstrated that flower buds were sensitive to heat 1-2 weeks prior toflower opening (G. C. Shonnard, unpublished data). Transfer studieswith cowpea have demonstrated that 15 or more days of high nighttemperature during the vegetative stage can suppress the development ofall floral buds on the main stem (Ahmed 1992). High night temperaturesalso caused abscission of floral buds in snap-type common beans underlong days (Konsens et al. 1991). However, the authors argued that podproduction was not constrained by floral bud abscission because highnight temperatures also promoted branching and production of floralbuds. Floral bud abscission could reduce the synchrony of pod produc­tion and this would reduce economic yield with mechanized harvesting.Hot long-day conditions also promote branching in cowpea, but podproduction is delayed and substantially decreased due to the abortion offloral buds on the main stem. Similarly, in a study characterizing fruitproduction in tomato under hot (33°/23°C day/night temperatures) short­day (12 h) conditions, Levy et al. (1978) observed that as many as 66% offlower buds abscised and commented that it would cause drastic reduc­tions in fruit yield of cultivars grown for a single harvest.

There have been relatively few studies of high temperature effects onearly floral bud development, and it is possible that many dicotyledonousplants experience late or reduced flowering due to this effect of heatstress. In general, the impact on fruit or seed yield of stress-inducedreductions in flower production will depend upon the magnitude of thereductions, that is, in relation to the natural tendency of the species toproduce more flowers than could be supported as fruit by thephotosynthetic capacity of the plant.

2. Fruit and Seed Set. Reductions in percent pod set could be respon­sible for much of the heat-induced reductions in seed yield by cowpea

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under field conditions (Nielsen and Hall 1985b), and high night tempera­tures are particularly damaging (Warrag and Hall 1983, 1984a,b). Lowpod set under high night temperatures in growth chambers (33°/30°Cday/night) has been associated with reduced pollen viability andindehiscence of anthers (Warrag and Hall 1984b). Artificial pollinationwith pollen from plants grown under optimal temperatures (33°/22°Cday/night) demonstrated that pistil viability was not influenced by highnight temperatures that caused zero pod set in naturally self-pollinatedplants (Warrag and Hall 1983). Some progress has been made towardsunderstanding the mechanisms of male sterility resulting from high nighttemperatures in cowpea. Studies in which plants were subjected to 6-daypulses of high or optimal night temperatures demonstrated that indi­vidual flower buds are sensitive to heat 9-7 days before flower opening(Ahmed et al. 1992). This period is just after meiosis of the pollen mothercells, and during this time degeneration of tapetal tissue was observed inheat-stressed plants. Field studies with heat-sensitive and heat-tolerantcowpea genotypes indicated that heat injury was associated with inhibi­tion of proline accumulation in pollen and greater accumulation ofproline in anther walls (Mutters et al. 1989a). The degeneration of thetapetal tissue was responsible possibly for the lack of transfer of prolinefrom the anther walls to the pollen. For tomato, pollen collected during ahot season (daily maximum and minimum temperatures of 31°/24°C) had43% lower proline concentration and 73% lower germination than pollencollected during a cooler season (daily maximum and minimum tempera­tures of 23°/13°C), and there was a highly significant correlation betweenpercent germination and proline concentration (Kuo et al. 1986b). Fertilepollen of cowpea has a high concentration of proline (3-4% on a freshweight basis) (Mutters et al. 1989a). Proline is thought to protect pollenfrom heat stress during germination [Zhang and Croes 1983a), and con­tribute to protein SYnthesis during pollen tube elongation (Zhang andCroes 1983b). Other insights into the mechanisms of heat-induced malesterility in cowpea are provided by evidence for partial effects ofphotoperiod and phytochrome mediation [Mutters et al. 1989b). Percentpod set was higher in hot short-day conditions compared with hot long­day conditions, but was still much lower than under optimal tempera­tures. Evidence for circadian regulation of sensitivity to heat, which isalso consistent with phytochrome mediation, was provided by theobservation that high temperatures late in the night substantially reducepod set, while high temperatures early in the night had no effect (Muttersand Hall 1992). Apparently, in interpreting possible effects of hotweather on fruit or seed set, it is important to consider the time of day andstage of floral development when heat stress occurs, and thephotoperiod.

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Common bean exhibits some similarities in pod set response to heatwith cowpea. Pod set in snap bean was substantially reduced by highnight temperature (27°C), whereas high day temperature (32°C) hadsmaller and less consistent effects (Konsens et al. 1991). Plants were sen­sitive to high night temperatures during sporogenesis (about 10 daysbefore anthesis), and anthers failed to dehisce and pollen grains had lowviability, but ovule development was unaffected (T. Kigel and M. Dfir,unpublished report). Pod set in snap beans also is sensitive to hightemperatures at four to two days before anthesis, and artificial crossesdemonstrated that the pollen was damaged (Dickson and Petzoldt 1989a;Monterroso and Wein 1990). Some genotypic differences in ability to pro­duce parthenocarpic pods under hot conditions have been observed insnap bean.

Tomato responses to heat stress, as reviewed by Stevens and Rudich(1978), Kuo et al. (1979) and Dpena et al. (1987), appear to be more com­plex than those of cowpea but with some similarities. The classicalstudies of Went (1945) established that night temperature is a criticalfactor in fruit set in tomato with optimal night temperatures beingbetween 15°-20°C. Stamens are particularly sensitive to high tempera­tures 9-4 days before anthesis during the stages of meiosis, and just aftermeiosis when the microspores are released from the tetrad (Iwahori1965). Lack of anther dehiscence may be a major factor in low fruit set forsome tomato genotypes, and it was associated with an absence ofendothecium formation in the anther (Rudich et al. 1977). Excessive styleelongation and exertion of the stigma through the mouth of theantheridial cone is another major response to high temperatures intomato, which prevents normal pollination (Rick and Dempsey 1969).Fertilization is not essential to fruit set in tomato; however,parthenocarpic fruits are reported to have inferior quality in most cases(Stevens and Rudich 1978).

The roles of plant hormones in fruit set in tomato under high tempera­tures have been reviewed by Kuo et al. (1986a). Apparently, the system iscomplex with auxins, gibberellins, cytokinins, ethylene, and abscisicacid influencing fruit set. The authors concluded that hormonal treat­ments were not yet available that would enable tomatoes to produce high­quality, normal-seeded fruits under hot conditions. H. C. Wein hasproposed that sprays with ethephon [(2-chloroethyl)phosphonic acid]may be used to detect cowpea genotypes that are less prone to flowerabscission (Wein and Summerfield, 1984). Under hot or warm long-dayconditions, sprays of ethephon reduced pod-set, whereas sprays withchemicals, which inhibit ethylene synthesis (aminoethoxyvinylglycine)or action (Ag+), enhanced pod-set in both heat-tolerant and heat-sensitivecowpea genotypes (Hamed EI-Saed and A. E. Hall, unpublished data).

5. BREEDING FOR HEAT TOLERANCE 135

Ethephon treatment reduced pod set to a similar or greater extent in theheat-tolerant genotype than the sensitive genotypes under either hot ormore optimal temperatures. Consequently, ethephon sprays may not beeffective in detecting cowpea genotypes with ability to set pods under hotconditions. Ethephon sprays have also been considered in screening forheat tolerance during fruit set in tomato (Villareal and Lal, 1979), but Ihave not discovered reports showing that the technique is effective.

Field studies with cotton, in which different night temperatures wereimposed, demonstrated that the number of bolls per unit shoot freshweight can decrease with average night temperatures greater than 20°C(Gipson and Joham 1968). Cotton grown in the southwestern deserts ofthe United States at low elevations can be subjected to extremely hightemperatures (daily maximum and minimum air temperatures of 43° and27°C). Boll set in these conditions has been negatively correlated withnight temperatures for the preceding 10-day period (Fisher 1973). Heat­induced boll shed was associated with lack of anther dehiscence, and theanthers contained few pollen grains (Fisher 1975). Some cytoplasmicmale-sterile cottons exhibit indehiscence of anthers when they are sub­jected to hot weather 15 to 16 days before anthesis (Meyer 1969). Heatstress 15 h prior to anthesis also can reduce pollen viability in cotton, andguidelines have been developed concerning methods for evaluatingpollen viability (Barrow 1983). The in vivo method based upon sec­tioning styles to determine the number of pollen tubes penetrating thelower style regions was shown to be an effective method, because it wascorrelated with seeds set per boll. Neither pollen germinability (either insitu on stigmas or in vitro) nor staining with tetrazolium red orAlexander's stain detected the initial expression ofheat-induced damage.The fluorochromatic test has been widely used to measure pollenviability, and while it may provide a reliable measure of pollen ger­minability, it may not detect heat-induced reductions in pollen vigor(Shivanna et a1. 1991), which could determine if pollen tubes reach ovulesand fertilization occurs.

Monocotyledonous plants also exhibit sensitivity to heat duringreproductive development. In a review of the responses of sorghum toheat stress, Peacock and Heinrich (1984) reported that Ogunlela (1979)found floret development to be inhibited by a 5°C increase in nighttemperature, such that the number of seed/panicle was reduced by 30%.In rice, high day temperatures caused indehiscence of anthers andimpaired pollen germination, but high day temperatures at anthesis wereeven more damaging (Yoshida et a1. 1981). These results led the authors tosuggest that heat resistance could be enhanced by selecting genotypesthat initiate anther dehiscence earlier in the morning when diurnaltemperatures are minimal. The second stage where heat caused sterility

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in rice occurs 9 days before anthesis, and coincides with the end ofmeiosis or just after it. Day temperature effects at anthesis also have beenreported for maize. Studies with excised tassels subjected to heat demon­strated that temperatures above 32°C can reduce pollen germination ofmany genotypes to levels close to zero (Herrero and Johnson 1980).

For all of the species that were discussed, pollen development and/ortransfer were particularly sensitive to heat stress. In most cases, highnight temperature was more damaging than high day temperature, andthe most sensitive development stage occurred just after meiosis and atthe release of the microspores from the tetrad. Heat-induced enhance­ment of out-crossing would have been expected to result in strong selec­tion pressure against heat-induced male sterility. Apparently, pollendevelopment represents a weak link in the ability of plants to withstandhigh temperatures. The persistence of sensitivity to heat during floraldevelopment may have been due to pleiotropic relations with otherprocesses for which there were strong positive selection pressures. Incowpea, sensitivity to heat during floral bud development is associatedwith the phytochrome system, which also regulates time of flowering.Natural selection and selection by farmers in the Savanna zone of WestAfrica, where cowpea was domesticated, would have favored genotypeswith photoperiod regulation of flowering; this may explain why manyaccessions from this region do not have the type of heat tolerance asso­ciated with insensitivity to photoperiod (Patel and Hall 1990).

3. Embryo, Seed, and Fruit Development. Pods of different cowpeagenotypes produce 9-20 ovules with many cultivars having 15; but theyrarely produce this many seeds per pod. Under optimal conditions, two­thirds of the ovules may produce seed, whereas with high night or highday temperature they produce fewer seeds per pod, and high daytemperatures have been shown to cause embryo abortion (Warrag andHall 1983). For most cowpea genotypes, it is the ovules at the blossom endof the pod that do not produce seed when the plants are subjected tostresses.

For dry bean-type common bean. Shonnard (1991) established that podfill (the proportion of ovules that produce seed) is particularly sensitive toheat under both hot field conditions and in hot growth chambers. Theheat-induced reductions in pod fill could be due to reduced fertilization orincreased embryo abortion. Heat reduces the number of seeds producedper pod in snap beans and, in contrast to cowpea, it is the ovules at theblossom end of the pod that have the greatest probability of producingseed when the plants are subjected to heat (Dickson and Petzoldt 1989a).Studies in which snap beans were subjected to one day of heat stress(32°/27°C day/night temperatures) at anthesis had a much higher level of

5. BREEDING FOR HEAT TOLERANCE 137

embryo abortion (43%) and unfertilized ovules (20%) compared to con­trol plants at 22°117°C day/night temperatures (24% abortion and 6%unfertilized ovules) (J. Kigel and M. Dfir, unpublished report). In addi­tional treatments, exposure of plants with young pods (lor 3 days old) to 5days at 32°/27°C did not affect seeds/pod or pod development. Theauthors interpreted the latter results as showing that the plants toleratedexposure to hot temperatures during early embryo and endospermdevelopment. For tomato, heat imposed 1 to 3 days after anthesis causedflowers to not set seeds or fruits due to ovule abortion or degeneration ofendosperm or retardation of proembryo development (Iwahori 1966).

For cowpea, seeds produced under extremely hot field conditions canhave asymmetrically twisted cotyledons and, for some genotypes, browndiscoloration of the seed coats. Controlled environment studies demon­strated that high day temperatures (but not high night temperatures) canresult in asymmetrically twisted cotyledons (Warrag and Hall 1984a).Field studies with plants exposed to different night temperatures (Nielsenand Hall 1985b) demonstrated that with higher night temperatures,progressively larger proportions of seed had brown discoloration of seedcoats. These heat-induced effects were not associated with changes ingerminability, but the brown discoloration of the seed coats would sub­stantially reduce consumer acceptability.

Hot conditions accelerate seed and fruit development. Accelerateddevelopment may not be related to heat-induced physiological lesions butcould still result in reductions in seed or fruit yield (reviewed by Blum1988). For cowpea, the period of pod development (days from anthesis tomature dry pod) exhibits a linear negative relation with night-timetemperature (Nielsen and Hall 1985b). Pods of plants subjected to dailyminimum temperatures of 16°C took 21 days to develop, whereas pods ofplants subjected to 26°C took only 14 days to develop. Consequently,under high nighttime temperatures, much less photosynthate would beavailable to individual pods during their development, and individualseed weight is often less under higher night temperatures. In addition,with higher temperatures, the rate of nodal development and number ofinflorescences produced per day can be increased, in some cases,resulting in a further reduction in the balance of photosynthetic source toreproductive sink. Analyses of wheat performance over a large range ofenvironments demonstrated that higher temperatures can reduce theduration of the spike development period, and the subsequent reductionin numbers of kernels per spike can reduce grain yields (Fischer 1985).High temperatures during the booting stage in wheat can also result ininfertile pollen and low grain set (Dawson and Wardlaw, 1989), whereashigh temperatures occurring at later stages of development cause reduc­tions in grain filling (Wardlaw et al. 1989a,b).

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B. Germination and Seedling Survival

Inadequate crop stands severely limit the productivity of crops, such aspearl millet, Pennisetum americanum L. (Leake) (Soman et al. 1987) andsorghum (Peacock 1982), in tropical environments. Soil seed-zonetemperatures can exceed 45°C in these environments and substantiallyreduce seedling emergence independently of drought effects (Wilson etal. 1982; Soman and Peacock 1985). Soman and Peacock (1985) haveshown that measurements of germination in constant temperatureincubators are not necessarily relevant to the field where soil tempera­tures vary diurnally. They have observed that certain sorghum lines,which fail to germinate in incubators at 40°C, will germinate and emergewhen sown in soil at the same mean temperature. For cowpea, theopposite response has been observed; seed will germinate over a largerrange of temperatures in incubators at constant temperatures than willemerge under field conditions (Dirk Rodriguez and A. E. Hall, unpub­lished data). Depth of sowing can also be critical. For cowpea in soil at35°C, Warrag and Hall (1984a) observed 100% emergence when seed weresown at 2.5 cm depth but only 46% emergence when seed were sown at5.0 cm depth. Depth of sowing had little effect on emergence at 25° or30°C. Onwueme and Adegoroye (1975) also observed less emergenceunder heat stress for seeds sown deeper in the soil, and that seeds ofcowpea were most sensitive to heat stress during the first day aftersowing. Germination of lettuce (Lactuca sativa L.) exhibits similar sensi­tivity to high soil temperatures during early stages. Soil temperaturesgreater than 25-33°C inhibit germination of lettuce seed, but the sensi­tive stage only persists for 7-12 h after the seed begins imbibing water(Borthwick and Robbins 1928). Consequently, the extent of inhibitiondepends upon the time during the day when seeds are sown and beginimbibing water in relation to diurnal changes in temperature in the seedzone. In contrast, wheat seed may be more tolerant to high temperaturesduring the initial 9-12 h of imbibition than during the following period(Abernethy et a1. 1989): For sorghum, the detrimental effects of hightemperatures on seedling emergence and survival are associated withreduced embryo protein synthesis (Ougham et a1. 1988) and reductions incarbohydrate translocation to roots due to heat girdling of the base of theshoot (Peacock et a1. 1990). The latter effect could be particularly impor­tant, because soil surface temperatures can reach very high levels inexcess of 60°C (Peacock 1982).

c. Vegetative Growth and Development

Potato (Solanum tuberosum L.) is normally grown in cool environ­ments, but there is considerable interest in growing it in more tropical

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conditions (Mendoza and Estrada 1979; Chandler Jr. 1983). When shootsare subjected to high night temperatures, irrespective of the soil tempera­ture, tuber fonnation is inhibited with greater effects under long days(Went 1957). Hot soil can also prevent tuber development irrespective ofthe air temperature (Reynolds and Ewing 1989a). The authors suggestedthat the induction of leaves to develop the tuberization signal can beinhibited by high shoot temperatures, whereas the expression of thesignal can be blocked by high soil temperature. There are interactionsbetween night temperature and photoperiod, with respect to tuberiza­tion, which vary among potato gennplasm (Mendoza and Estrada 1979).Other processes, such as ability of seed tubers to sprout and partitioningof carbohydrates under high temperatures, can influence heat tolerance(Ewing et al. 1987).

The heading type of Chinese cabbage (Brassica campestris spp.pekinensis Rupr.) is nonnally grown in cool environments, and as withpotato, there is interest in growing it in more tropical conditions(Chandler Jr. 1983). Most cultivars of Chinese cabbage do not form denseheads if average daily temperatures are greater than 25°C (Opena et al.1987). Comparisons of heat-tolerant and heat-sensitive cuItivars indi­cated that head formation at high temperatures is associated with aspectsof plant water relations. Plants of tolerant and sensitive genotypes pro­duced similar amounts of dry matter under high temperatures, suggestingthat heat tolerance is not associated with maintenance of photosyntheticcapabilities (Kuo et al. 1988).

D. Photosynthesis

Heat-induced reductions in photosynthesis could influence seedlingsurvival or reduce yields through effects on vegetative or fruit growth.The net uptake of carbon dioxide decreases at high daytime tempera­tures commonly experienced in natural environments (Berry and Bjork­man 1980). Initially, the decreases are reversible, but with high enoughtemperatures irreversible damage occurs. The water-splitting compo­nent of photosystem II may be particularly sensitive to heat (Berry andBjorkman 1980); however, the threshold temperatures required to causeirreversible damage were quite high (greater than 40°C for a speciesadapted to cool seasons and greater than 50°C for a species adapted to hotconditions). The extent to which irreversible damage occurs tophotosynthetic systems in hot crop production environments can beevaluated by measuring chlorophyll fluorescence (e.g., variable fluores­cence Fv).

Wheat genotypes were subjected to high temperatures (32°27°Cday/night) compared with moderate temperatures (22°17°C day/night) as

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seedlings or from anthesis to maturity (AI-Khatib and Paulsen 1990).High temperature decreased mean photosynthetic rates 32% and 11%,mean Fv 42% and 11%, and mean total biomass 32% and 15% in seedlingand more mature plants, respectively. Wheat genotypes also were shownto differ in the extent that hot growth chamber conditions reduced Fv, butgenotypic rankings were not consistent in hot growth chamber and fieldconditions (Moffat et a1. 1990b). For the data to be relevant to the adapta­tion of wheat to hot field environments, it may be necessary to makemeasurements of Fv on the flag leaves of field-grown plants during grainfilling, in which case the data may exhibit extreme nongenetic variability.Clones of potato that had been selected for yield in hot environmentsexhibited greater heat tolerance with respect to chlorophyll fluorescenceproperties than clones adapted to cooler environments (Smillie andHetherington 1990).

Several mechanisms enable leaves to avoid heat stress. In environ­ments conducive to high rates of transpirational cooling, leaves may be asmuch as 10°C cooler than air (Pearcy et a1. 1972; Upchurch and Mahon1988) or even more (Lange 1959). For Pima cotton, it has been shown thatcultivars bred for increased boll set and yield in hot environments, alsocan exhibit enhanced stomatal conductance and photosynthetic capacity(Cornish et a1. 1991b). The advanced cultivars with higher stomatalconductances had lower leaf temperatures. The extent to which thehigher gas exchange rates are contributing to the higher heat resistanceand yields of the advanced cultivars is not clear. The reported dif­ferences in leaf temperature were not large. Measurements in field plotsgave maximum differences of 3°C in the afternoon (Cornish et aI. 1991a),and under large-scale field conditions the differences may be evensmaller Uarvis and McNaughton 1986). The advanced lines with higherphotosynthetic rates also had smaller leaves, such that thephotosynthetic output per leaf was less in the advanced lines and, there­fore, would not explain their heat resistance (Cornish et a1. 1991a). Thisseries of studies with Pima cotton is unique in that it is the first docu­mented case where breeding has indirectly resulted in what appear to beconsistent genotypic differences in stomatal conductances, which arepositively correlated with yield. A possible explanation is that the selec­tion procedure resulted in greater earliness, in addition to greater heattolerance during pod set, and that the earliness was associated withgreater stomatal conductance, and the greater yield was associated withthe heat tolerance. Leaves of some species exhibit reversible movementsduring the day, which can contribute positively or negatively to heatavoidance. In cotton and well-watered cowpea, leaf movements tend toincrease radiation loading, which increases leaf temperatures. In con­trast, for droughted cowpea, leaf movement reduces radiation loading

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and can reduce leaf temperature as much as 5.5°C (Shackel and Hall1979). Leaf pubescence may enable leaves to avoid potentially lethal hightemperatures through increases in reflectance (Ehleringer 1980).

Heat avoidance mechanisms of leaves either require an abundantwater supply for evaporative cooling or they act through reductions inradiation load, which could reduce photosynthesis in some circum­stances, but not others. Small organs have temperatures that are similarto the air, because their thermal boundary layer resistances are low, espe­cially with moderately high wind speeds.

E. Heat Stability of Membranes

Many studies have been conducted on the effects ofheat on membrane­related processes. The most sensitive of the reactions of photosynthesisto high temperature are associated with membranes, and it was proposedthat qualitative changes in lipid properties may playa central role indetermining sensitivity to both low (chilling) and high temperatures(Berry and Raison 1981). The development of rapid tests for membranethermostability based upon electrolyte leakage from leaf disks resulted inmany studies identifying species and genotypic differences in heattolerance (Sullivan et al. 1977). There have been reports of either associa­tions or absence of correlations between genotypic differences inmembrane thermostability based upon leaf disk assays and plant per­formance under hot conditions. A significant correlation was obtainedbetween grain yield and heat tolerance determined during a period ofmaximum heat stress in the field for 15 sorghum hybrids (Sullivan andRoss 1979). The hybrids were made from crosses among five linesselected for heat tolerance and three commercial lines, which were usedas female parents. Blum (1988) has provided a comprehensive review ofresearch using leaf disk assays for thermostability including some inter­esting unpublished data by Blum and Sullivan. They measured growthrate of 19 landraces of sorghum and pearl millet grown at variousday/night temperatures causing different levels of heat stress. Theymeasured membrane thermostability of the same genotypes grown atoptimal temperatures and heat hardened for 24 h at 40°C prior tosampling. A positive, significant association was observed betweengrowth rate and membrane stability for plants grown at 32°/44°Cday/night temperatures, but not for plants grown at lower (30o/40°C] orhigher temperatures (34°/46°C). This suggests that the leafdisk assay mayonly provide an indication of membrane thermostability under specificconditions of heat stress.

Studies by Chen et al. (1982) indicate a possible association betweengenotypic differences in heat stress based upon leaf disk assays and fruit

142 ANTHONY E. HALL

set. They chose two cultivars of tomato that differ in heat toleranceduring fruit set, and two cultivars each of soybean, snap bean, and potatothat had been reported to differ in yield under hot conditions. A correla­tion was found between heat killing time for leaf disks under specificconditions and the performance of the same genotypes under hot fieldenvironments described by other scientists. The genotypic differenceswere expressed only in plants that had been heat acclimated (at tempera­tures of 2: 35°C for 2: 6 h) and with leaves of olderbut not younger plants.They also established that heat-induced damage as measured by theability of plant tissue to reduce 2 ,3,5-triphenyl tetrazolium chloride (TTCtest) gave similar results as damage measured by the extent of electrolyteleakage. The extent of the association betweenheattolerancebased uponability to set fruits under hot conditions and heat tolerance based uponmembrane thermostability or the TTC test as measured with leaf disks isnot known. A large number of snap bean and dry bean cultivars ofcommon bean were studied under hot phytotron, greenhouse, and fieldconditions. Genotypic differences in heat killing time based upon the leafdisk assay for electrolyte leakage were not associated with genotypic dif­ferences in pod set or yield in any of these environments. The authorssuggested that sensitivity of pollen development to high night tempera­ture may not be related to membrane stability (T. Kigel and M. Ofir,unpublished report). Many studies have been conducted over many yearswith the leaf disk assay for heat stability of membranes (reviewed byBlum 1988). It is still not clear, however, whether this assay is consis­tently associated with plant characters that confer adaptation in hotenvironments, such as seedling survival, plant growth, fruit set, or seedyield. Photosynthetic responses to heat stress were studied with commonbean genotypes that differ in heat tolerance as measured with the leafdisk assay for ion leakage (Chaisompongpan et al. 1990). The photo­synthetic apparatus was more sensitive to heat than the plasmalemma asdetermined with the leaf disk assay. For the six genotypes that werestudied there was no association between heat tolerance as measured bythe leaf disk assay and either O2 evolution or chlorophyll fluorescence.

Recently reported studies indicated some potential for using themembrane thermostability test for incorporating useful heat toleranceinto winter wheat. Relative injuryas measured byelectrolyte leakage wassignificantly correlated for genotypes assayed as seedlings and atanthesis, when appropriate hardening and test protocols were used(Saadalla et a11990b). Parental cultivars and F5 genotypes were evaluatedin three field environments with high temperatures during grain filling(Saadalla et al. 1990a). The genotypes were classified into three groupsbased upon the membrane thermostability test: heat tolerant, inter­mediate, and sensitive. The heat-tolerant genotypes had significantly

5. BREEDING FOR HEAT TOLERANCE 143

higher kernel weight and volume weight of kernels (a measure of kerneldensity) than the heat-sensitive genotypes in all three field environ­ments, and the intermediate class was intermediate for these traits. Thesestudies indicate that the membrane thermostability test applied toseedlings may be effective for selecting wheat genotypes with heattolerance during grain filling. In contrast, for tomato genotypes with dif­ferences in heat tolerance during fruit set, heat tolerance was not asso­ciated with membrane thermostability of leaves, but it was associatedwith membrane thermostability of anthers (C. G. Kuo, personal com­munication 1991). Apparently, the effectiveness of membrane thermo­stability assays can depend on the tissue used in the assay in relation tothe type of heat tolerance that is needed to improve plant adaptation.

F. Heat-Shock Proteins

Since the classical studies of Yarwood (1961), which demonstrated thatleaves subjected to high temperatures (50°C) for short periods (15-30 sec)tolerated high temperatures (55°C) longer than untreated leaves, therehave been many molecular studies of heat-shock responses. The reviewby Sachs and Ho (1986) describes the unique heat-shock proteins (HSPs)that can be induced by heat-shock treatment of plants. They commented,however, "that a well-defined role for any of the plant HSPs has not yetbeen elucidated." Substantial progress has been made since 1986, but asimilar statement was made in 1988 (Schoffl), and it may still be valid(Vierling 1991). Lin et al. (1984) demonstrated that soybean seedlingsexposed to 40°C for 2 h produced HSPs and could grow when subjected to45°C for 2 h; however, plants transferred directly from 28 to 45°C did notproduce HSPs and could not grow. In addition, it has been shown thatHSPs may accumulate under hot field conditions in soybean (Kimpel andKey 1985) and cotton (Burke et al. 1985) for droughted plants but not forirrigated plants. Two wheat genotypes were studied, which differed incellular thermal tolerance as measured by TTC reduction by leaf disks(Krishnan et al. 1989). The studies demonstrated that the genotype withthermal tolerance produced unique HSPs, which were not produced bythe heat-shocked sensitive genotype. The genotype with cellular thermaltolerance also exhibits less heat-induced foliar senescence than the sensi­tive genotype (H. Nguyen, personal communication 1991). Two sorghumlines that differ in susceptibility to heat during germination were studiedby Ougham and Stoddart (1986). Both lines did not produce HSPs inresponse to heat-shock during very early stages of germination, and itwas proposed that this may account for their sensitivity to heat duringthese stages. However, the heat-tolerant line produced HSPs earlier in

144 ANTHONY E. HALL

the germination process and acquired greater heat tolerance during theseedling stage than the heat sensitive line. These results have beenextended in subsequent studies with sorghum and pearl millet (Howarth1989). Associations have not been reported between genotypic dif­ferences in heat tolerance during reproductive development and produc­tion of HSPs. This lack of association may be explained by two phenom­enon. First, floral bud and pollen development can be very sensitive tomoderately high night temperatures (24°-27°C), which are probably toolow to cause the induction of heat-shock proteins. Secondly, pollen maynot have the ability to synthesize HSPs, as appears to be the case withmaize (Cooper et a1. 1984), and this tissue is moderately sensitive to heat(Herrero and Johnson 1980). It is possible that the extreme sensitivity ofplants to heat stress during reproductive development and sources ofgenetic tolerance that are available are not related to the HSP phenom­enon. Cowpea genotypes with contrasting heat tolerance duringreproductive development (Patel and Hall 1990) have been examined byseveral laboratories and, to date, no differences in HSPs have beendetected among them. In a recent review, Vierling (1991) stated that"there is no clear evidence that HSPs contribute to these genetically deter­mined differences in heat tolerance"-referring to research with manycrop species.

III. CHARACTERIZING PRODUCTIONENVIRONMENTS TO DETERMINE THE EXTENT TOWHICH HEAT IS REDUCING YIELD

Establishing the priority that should be given to incorporating heattolerance, as part of a breeding program, requires an estimate of theextent to which heat is reducing yield. Thermal regimes are complex,consequently, it is useful to know which stages of plant development aremost sensitive to heat. If heat is inhibiting seedling emergence, then soiltemperature in the seed zone during the first few hours after inhibition ofwater may be the most critical factor. If seedlings emerge but do notsurvive, then soil surface temperature may be critical, because it canreach levels much higher than air temperature and cause stem girdling.Seed zone and soil surface temperatures are strongly influenced byrain orsprinkler irrigation through evaporative cooling. Irrigation managementmethods may make it unnecessary to develop cultivars that are heattolerant during germination. When lettuce seed are sown in hot condi­tions in Imperial Valley, California, they often are sown into dry soilduring the day and then sprinkle irrigated in the early evening. In thisway, imbibition of water and subsequent early stages of germination that

5. BREEDING FOR HEAT TOLERANCE 145

are sensitive to heat (Borthwick and Robbins 1928) take place during thenight in soil that has been cooled by evaporation. In addition,thennodonnancy in lettuce seed may be overcome by osmotic priming for24 h in aerated 1.5 MPa polyethylene glycol at 18°C (Valdes etaI. 1985).

For potato, it is important to quantify the extent to which high soil orhigh shoot (during the day or night) temperatures are inhibiting tuberiza­tion and other processes (Ewing et a1. 1987). The system used by Dreyer eta1. (1981) to impose different soil temperatures under field conditions,which consists of heating cables and differential thermostats, would beuseful for quantifYing soil temperature effects.

Where vegetative growth is substantially reduced by heat, themaximum daytime temperatures of leaves or apical meristems may becritical. Leaf temperatures can be substantially different from airtemperature and depend upon plant water supply and the extent of trans­pirational cooling. This may explain why heat-shock proteins have beenobserved in the leaves of dryland crops but not in irrigated crops growingin the same field (Burke et al. 1985; Kimpel and Key 1985). This issue iscomplicated further by the possibility of cultivar differences in stomatalconductance, as appears to be the case for Pima cottons (Cornish et al.1991b). These cultivars could exhibit differences in the extent to whichleaf temperatures are cooler than air temperatures, but the effect willdepend upon a complex of factors influencing leaf energy balanceincluding leaf size and wind speed. It has been proposed that leaftemperatures of crop plants may deviate from the optimal range forenzYme function most of the time (Burke et a1. 1988). This conclusion,however, is based upon consideration of the temperature dependence ofonly one enzYme, and deeper analysis is warranted.

High day temperatures can result in high rates of water loss and waterstress. In this case, damage to plant functions could be due to either directeffects of high tissue temperatures or indirect effects of water stress, andit is difficult to separate them. This issue could be important with crops,such as Chinese cabbage, where heat tolerance may depend upon plantwater relations (Kuo et al. 1988). Sullivan and Ross (1979) discussed theproposition that selecting for heat tolerance may improve adaptation todrought. The rational for this proposal was that drought and heat stressoften occur together, and that tolerance'to heat could be easier to screenfor than resistance to drought, because heat stress is easier to control thandrought stress. It is likely, however, as was pointed out by Sullivan andRoss (1979), that heat and desiccation tolerance involve differentmechanisms.

Progress has been made in quantifYing the influence of heat stress onreproductive development in natural environments. Climatologicalstudies (reviewed by Dale 1983) have shown that maize yields in the

146 ANTHONY E. HALL

United States can be negatively correlated with accumulated degrees ofdaily maximum temperatures above 32°C in July and August. Grainyields decreased 63 kg/ha for each 5.5°C accumulated above 32°C. Thesensitive period may coincide with silking. Clearly, it is important toknow the stages of reproductive development that are most sensitive toheat. Cotton, cowpea, common bean, and tomato are extremely sensi­tive to high night temperature during early stages of floral development.An experimental system was developed to directly evaluate the effects onyield of higher nighttime temperatures under field conditions (Nielsenand Hall 1985a). In this system, thermally insulated plastic sheets wereplaced over frames covering cowpea plants in the field during the night.Fans and heaters within the enclosures and differential thermostats wereused to raise air temperatures 4,8, or 12°C above ambient during thenight. The plastic sheets were removed during the day so that all treat­ments were exposed to the same daytime conditions. When higher night­time temperatures were imposed for one month beginning at earlyflowering, linear decreases in grain yield were observed of 4.4%/oC(Nielsen and Hall 1985b). These studies demonstrated that the high night­time temperatures occurring in the summer in hotter parts of the south­western United States can substantially reduce pod set and grain yield ofcowpea. Implications of these results for the tropics where nighttimetemperatures are very high (Nielsen and Hall 1985a) are complicated byinteractions with photoperiod. The field studies were conducted underdaylengths of 13.5 to 14.5 h. Controlled environment studies have shownthat high night temperatures may be less damaging to pod set under daylengths of 11 to 12 h. In tropical areas where cowpea are grown,daylengths may vary from 14 to 12 h during the growing season, depend­ing upon the latitude and sowing date. It is clear that photoperiods mustbe considered when evaluating the impact of hot weather on grain yield ofcowpea. The same effects may occur with some other crops whosedevelopment is influenced by photoperiod.

Heat tolerance in wheat was evaluated by growing the same cultivarsduring a cool or a hot season under irrigation (Shpiler and Blum 1991).The authors concluded that heat strongly reduced kernel number perspike but it is likely that, in addition to temperature differences, therewould have been other differences in environment between the twoseasons. In natural environments, variation in temperature can beaccompanied by variation in solar irradiance. For intensively managedwheat, Fischer (1985) observed that the number of kernels/m2 (K) waspositively correlated with solar radiation (19 kernels/MJ) and negativelycorrelated with average temperature (-40f0/oC). He developed an overallmodel for the combined effects in which K was linearly correlated withthe ratio of intercepted solar radiation to mean daily temperature above a

5. BREEDING FOR HEAT TOLERANCE 147

threshold of 4.5°C during the 30 days preceding anthesis. Phytotronstudies indicated grain yield reductions in wheat of 3 to 4% for eachincrease in temperature of 1°C above a mean daily temperature of 15°C(Wardlaw et al. 1989b). Linear models of this type can be used to estimateaverage yield losses expected from average temperature data for specificenvironments. There are likely to be cases, however, where the yieldresponse to temperature is not linear, and where extremely high tempera­tures cause catastrophic losses. Prediction of yield losses for thesecircumstances may require the development of stochastic models, whichuse information concerning the probabilities of hot weather of differenttypes, and the responses of plants to these different heat stresses.

For fruit trees, predicting effects of heat stress on economic yield iscomplex in that reductions in number of fruit can be beneficial bydecreasing the work involved in thinning to increase fruit size, unless thelevel of fruit drop is catastrophically high, which can occur when navelorange trees with young fruit are subjected to hot weather. High tempera­tures also can result in decreased quality of fruit. Studies have beenconducted with sweet cherry in which temperatures were varied by con­trolled heating with infrared lamps, overhead irrigation, or location. Theproportion of sutured fruit increased with increases in temperatureduring July in the year prior to flowering (S. Southwick and K. Shackel,unpublished data). Presumably, there are early stages of floral buddevelopment, where cherry is sensitive to high temperatures.

IV. GENOTYPIC DIFFERENCES IN HEATTOLERANCE, INHERITANCE, AND ASSOCIATIONSWITH OTHER CHARACTERS

A. Cowpea

The reproductive responses to high temperature of contrasting cowpeaaccessions have been evaluated under long days in an extremely hot fieldenvironment (PatelandHall 1990) and underboth short and long days inaglasshouse with high night temperatures (P. N. Patel and A. E. Hall,unpublished data). Photoperiod must be included in classifying cowpeaaccessions for heat tolerance because some reproductive processes areless sensitive to heat under short days. Cowpea accessions have beenclassified into two broad groups. The accessions contained in the firstgroup (group one) are "classical" day neutral accessions because thenodal position, where the first floral bud is initiated, is not influenced byphotoperiod. The accessions in the second group (group two) are

148 ANTHONY E. HALL

"classical" short-day plants, because with photoperiods longer thancritical values either the plants remain vegetative, or the first floral budsare initiated on higher nodes. Accessions in group one are also early,because they initiate floral buds on the second to sixth node on the mainstem.

Group one accessions have been classified into three major subgroups.The first subgroup contains a small number of accessions and breedinglines that have substantial heat tolerance. They exhibit near-normalfloral bud development, flower production, and pod set in both hot long­day and hot short-day environments. The second subgroup of group onecontains a small number of accessions and breeding lines that havepartial heat tolerance. They exhibit near-normal floral bud developmentand produce many flowers in both hot long-day and hot short-dayenvironments. But they exhibit no pod set under hot long-day conditionsand intermediate pod set in hot short-day environments. Inheritancestudies indicated that the difference in pod set between subgroups oneand two involve at least two recessive genes (ph and ph) conferring heattolerance during early periods of pod set and with a photoperiod interac­tion (P. N. Patel and A. E. Hall, unpublished data), and a dominant gene(Ha) conferring heat tolerance during later periods of pod set (Marfo andHall 1992). In the latter studies, narrow-sense and realized heritabilitieswere similar but low (0.24-0.29), although segregation patterns indi­cated the presence of a single major gene due to substantial environ­mental influences on pod set. The third subgroup of group one containsaccessions that exhibit suppressed floral bud development under hotlong-day conditions and they do not produce open flowers. Inheritancestudies indicated that a major dominant gene (Ptd is mainly responsiblefor the heat-induced floral bud suppression with an absolute effect ofphotoperiod, because floral bud development is normal under hot short­day conditions. Studies with red and far-red light indicated that compo­nents of the phytochrome system responsible for classical short-dayphotoperiod sensitivity, as manifested in group two accessions, are alsopresent in the heat-sensitive accessions in subgroups two and three ofgroup one accessions (Mutters et al. 1989b). Ability to produce substan­tial numbers of flowers and pods under hot long-day conditions requiresthe presence of a set of recessive genes (pt1 , pt2 , p~) and a dominant gene(Ha). Multiple forms of phytochrome are present in plants (Smith andWhitelam 1990; Thomas 1991), and it is tempting to speculate that thedominant Pt genes and the basic photoperiod gene(s} differentiatinggroups one and two control the synthesis of different forms ofphytochrome. One of the accessions with considerable heat toleranceduring floral bud development and pod set TVu 4552 is sensitive to heatduring seed development and produces a discolored seed coat. This

5. BREEDING FOR HEAT TOLERANCE 149

cosmetic defect is due to a single dominant gene (Hbs), and no linkage wasobserved between it and the gene (Ptl ) governing heat sensitivity duringfloral bud development (Patel and Hall 1988). Group two cowpea acces­sions exhibit classical short-day sensitivity to photoperiod, and under hotlong-day conditions they either do not initiate floral buds or the buds arecompletely suppressed. Under short-day conditions these accessionsexhibit differences in the nodal position of the first floral bud and in theirheat tolerance during early floral bud development and pod set.

Cowpea is the only species in which comprehensive studies have beenconducted of heat stress X photoperiod interactions. However,phytochrome-mediated photoperiod effects have been shown to occur inmost crop species; consequently, heat stress effects on many crop plantsmay be influenced by photoperiod.

B. Common Bean

A photoperiod X temperature interaction is present in common beanthat influences time of flowering (Wallace 1985) and is similar to theresponses observed in cowpea (Dow EI-Madina and Hall 1986). Conse­quently, it is possible that some heat stress effects on common bean alsoare influenced by photoperiod. Genotypic differences in heat toleranceduring reproductive development have been observed in snap beansunder long- and short-day conditions (Dickson and Petzoldt 1989a) and indry beans under long-day conditions (Shonnard 1991). For the snapbeans, narrow-sense heritabilities for pod set were low (0-14%) and withsome dominance for heat tolerance. From another study with snap beans,Bouwkamp and Summers (1982) concluded that heat tolerance asmeasured by pod production may be simply inherited involving one ortwo genes but with some epistasis and dominance. The studies with drybeans (Shonnard 1991) indicated that heat tolerance during floral buddevelopment and seed set may be complex, with substantial additiveeffects and some epistatic gene action and dominance and strongenvironmental effects. Realized heritabilities for floral bud developmentand seed set under hot conditions were 36% and 22%, respectively. Forone heat-tolerant parent and set of crosses, a single dominant gene forindeterminate growth habit was highly correlated with heat toleranceduring floral bud development, but the author (Shonnard 1991) pointedout that some plants may have escaped hot weather in the field nursery. Insubtropical field conditions where large seasonal or weekly changes intemperature can occur, it is difficult to screen plants for heat toleranceduring reproductive development, especially where individual genotypesexhibit different dates when flowering begins.

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C. Tomato

ANTHONY E. HALL

Thousands of tomato accessions have been screened for fruits percluster under hot conditions at the Asian Vegetable Research andDevelopment Center, Taiwan (AVRDC), and less than 1% were found tobe heat tolerant (Villareal and La11979; Opena et al. 1989). Villareal andLal (1979) presented a list of 39 tomato accessions with high fruit-setunder hot conditions. Genotypic differences in number of fruit per clusterhave been related to differences in premature abscission of floral buds,stigma exsertion, antheridial cone splitting, and pollen sterility (Levy etal. 1978). Some studies indicated that sensitivity to heat caused by stigmaexsertion is simply inherited with major effects of a few dominant genes(Rick and Dempsey 1969; EI Ahmadi and Stevens 1979b), although the F1

from a cross using different parents indicated that stigma exsertion underheat was recessive (Levy et al. 1978). The heritability of low stigma exser­tion was sufficiently high in all three studies, so that the authors wereable to conclude that breeding for this character should be efficient andeffective. A diallel study was conducted with six cultivars exhibitingsome heat tolerance with respect to flower production, lack of stigmaexsertion, fruit set, and seed set (EI Ahmadi and Stevens 1979a,b). Theauthors concluded that the specific combining ability of the differentparents should be used to breed genotypes that have high levels of the dif­ferent traits conferring heat tolerance. A seven-parent diallel has beenstudied under hot conditions at AVRDC (Opena et al. 1987). Fruit set andantheridial cone splitting were negatively correlated, and some parentsexhibited high general combining ability for desirable traits, but withsome effects due to specific combining ability indicating the presence ofgenes with additive effects and some genetic interactions. Studies byShelby et al. (1978) indicated that fruit set can be conferred by a fewmainly dominant genes with moderate broad-sense heritability (54%) butvery low narrow-sense heritability (8%). In early studies at AVRDC(Villareal and La11979), inheritance of fruit set was continuous with lowheritability (5-19%), but more recent studies demonstrated that heattolerance can be conferred by a small number of major genes, which arelargely recessive (Opena et al. 1989). Apparently, heat tolerance duringfruit set in tomatoes can be conferred by either recessive genes ordominant genes depending upon the parents used in the cross, and thereare large environmental effects.

Some of the tomato cultivars developed for short-season, coolerenvironments have heat tolerance during fruit set (Stevens 1979), andsome chilling tolerant genotypes of snap beans also have heat tolerance(Dickson and Petzoldt 1989b). This unexpected phenomenon may beexplained by either the presence of genes that generally improve fruit set

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under a range of conditions, or that there is a genetic linkage or pleio­tropy between heat tolerance and earliness, which has been observed incowpea (Patel and Hall 1990). Heat tolerance, as measured bychlorophyll fluorescence, was found to be positively correlated withchilling tolerance for potato clones but not among wild potato species(Smillie and Hetherington 1990).

D.COttOD

Differences in heat tolerance are present in Pima cultivars of cotton,which are associated with the ability to set bolls at low nodal positionsunder high night temperatures (Feaster and Turcotte 1985). Selectionunder hot conditions was found to produce lines that performed well in abroader range of environments than selection under cooler conditions(Feaster et a1. 1980). Similar observations have been made on uplandcottons in the southwestern United States.

E. Rice

Genotypic differences in heat tolerance have been detected in rice inwhich there was a highly significant correlation between the percentageof florets setting seed and the number of pollen grains per stigma (Yoshidaet a1. 1981; Mackill et a1. 1982). The heat-tolerant lines also had higherpollen shedding under more optimal temperatures than the heat-sensitivelines. A six-parent diallel experiment was conducted with these lines,which indicated that general and specific combining ability effects forheat tolerance during grain set were significant. The heritabilities for heattolerance in the diallel cross were 76% for the broad-sense heritability and71% for the narrow-sense, indicating that most of the genetic variation isadditive (Yoshida et a1. 1981). Inheritance of heat tolerance was studied inmore detail with two contrasting parents from the diallel experiment byMackill and Coffman (1983). The broad-sense heritabilities for number ofpollen grains per stigma and percent filled grains were high (84% and69%, respectively). The phenotypic and genetic correlation coefficientsbetween the two traits were 0.58 and 0.65 respectively. This indicates thatselection for high pollen shedding could be effective in increasing heattolerance in terms of percent filled grains. The segregation of F2 plants forpollen grains per stigma indicated that this aspect of heat tolerance isrecessive and controlled by several genes. Progeny values for percentfilled grains did not segregate in the same manner as pollen grains perstigma. There was no dominance evident for percent filled grains and thedifferences among parents and the F1 were not as distinct as in the case ofpollen grains per stigma. This indicates that additional genes were

152 ANTHONY E. HALL

influencing percent filled grains. Heat tolerance in rice, as measured bypercent filled grains, may be associated with earliness (as was observedwith cowpeas), but it was not associated with cold tolerance (Yoshida etal. 1981).

F. Chinese Cabbage

Research at AVRDC has detected genotypes of Chinese cabbage thathave the ability to produce a compact head under hot conditions, and thisaspect of heat tolerance is conferred by a single recessive gene (Opena etal. 1987).

G. Polato

Clones of white potato with ability to produce substantial yields oftubers under hot conditions have been detected and developed throughresearch at AVRDC (Chandler Jr. 1983) and at the International PotatoCenter, Peru (Mendoza and Estrada 1979). A large number of accessions(319) of 59 tuber-bearing species of Solanum were screened for heattolerance (Reynolds and Ewing 1989b). Six accessions from four specieswere shown to tolerate heat between 30 and 40°C in terms of shoot andtuber growth.

H. Wheat

Genotypic differences in heat tolerance were observed among 21spring wheat cultivars growing under hot, irrigated field conditions(Shpiler and Blum 1991). Heat tolerance was associated with high kernelnumber per spike. For winter wheat, genotypic differences have beendetected in chlorophyll fluorescence (AI-Khalib and Paulsen 1990;Moffat et al. 1990a) and membrane thermostability (Saadalla et al. 1990b)under hot conditions. A diallel study involving six parents indicated thatinheritance of chlorophyll fluorescence characteristics is complex withboth nuclear and cytoplasmic effects and interactions (Moffat et al.1990b). A phytotron was used to evaluate heat tolerance during graindevelopment of 66 wheat cultivars (Wardlaw et al. 1989a) The authorsconcluded that a wider assessment of genetic variation was needed ifresponse to high temperature was to be incorporated into a breedingprogram.

I. General Observations

Genotypes with morphological traits, which confer heat toleranceduring reproductive development, have been detected in cowpea,

5. BREEDING FOR HEAT TOLERANCE 153

common bean, tomato, cotton, and rice. Where the most extensivescreening has been reported (for tomato and cowpea), the proportion ofaccessions with high levels of heat tolerance was low <1%). Heattolerance during reproductive development involves a small number ofgenes that are mainly recessive, and is associated with earliness incowpea and rice (and possibly tomato).

Little progress has been made in detecting genotypic differences inphysiological traits, such as photosynthesis, chlorophyll fluorescence,membrane thermostability, or production of heat shock proteins, that arerelated to adaptation. This lack of success is due to a combination offactors: the small number of accessions that have been screened forphysiological traits, inconsistencies in genotypic rankings, variationsdue to experimental protocols, and difficulties in interpreting the resultsof the screens with respect to their relevance to either physiological oryield-limiting processes. Some new approaches may be needed for theuse of physiological traits in screening for heat tolerance, and this will bediscussed in the next section.

v. SELECTION TECHNIQUES AND BREEDINGMETHODS

A. Selection Techniques

For crops that are sensitive to heat during reproductive developmentand with no obvious limitation in supplies of photosynthate, selection formorphological flowering and fruiting traits can be effective in increasingoverall heat tolerance. Flowering or pod set of cowpea can be totallyinhibited by moderately high night temperatures, which have only smalleffects on photosynthesis and vegetative growth; raising carbohydratelevels by growing plants in elevated CO2 concentrations does not enhanceflowering or pod set in these hot conditions (Ahmed 1992). It is also likelythat there are hot conditions where fruit set in tomato, cotton, and othercrops is limited by lesions in reproductive development, which are notdue to shortages of photosynthate.

Choice of field environments can influence the ability to reliably detectmorphological characters conferring heat tolerance and any inadvertentnatural selection of characters that influence other aspects of plant per­formance. Selection in hot production environments has been effective inPima cotton (43°/27°C, daily maximum and minimum temperatures,Feaster and Turcotte 1985), upland cotton, and tomato (programs of PaulLeeper, Texas Agricultural Experiment Station, Weslaco, and AVRDC,Taiwan, Villareal and LaI1979). In other cases, field-screening nurseries

154 ANTHONY E. HALL

have been used that are hotter than commercial production environ­ments, such as with cowpea (42°/24°C average daily maximum andminimum temperatures, Hall and Patel 1990) and common bean (35°/17°Caverage daily maximum and minimum temperatures, Shonnard 1991).The use of extremely hot environments has the advantage that discreteand strong heat stress effects occur, which can be detected easily and con­sistently from year to year. It has the disadvantages that selection forgeneral agronomic traits may not be possible or advisable, and thatinadvertent natural selection can occur for traits that may not be desirablein commercial production environments.

Specially designed glasshouses may be useful for screening for heattolerance, because they do not have the problem of variation in tempera­ture, which can make field screening inefficient, especially in sub­tropical zones. In this case, it is important to know whether day or night(or soil) temperature is most damaging. For cowpea, a glasshouse withhigh night temperatures (30°C) but moderate day temperatures (34°C)elicits strong heat stress effects. A greenhouse environment has beenproposed for screening tomato for heat tolerance (35°/26°C day/nighttemperatures, Stoner and Otto, 1975) and used by Berry and Uddin (1988).The extent to which these glasshouses can and should be used forscreening during the off-season, depends upon the extent of heat stressand photoperiod interactions, and the ability of the glasshouse system tomaintain appropriate temperatures without shading, which could causeartifacts (Villareal and LaI1979). For crop species with root systems thatare sensitive to heat stress, it maybe advisable to use soil beds in the glass­house rather than pots. The temperatures of soils beds are buffered,whereas pots track air temperatures more closely and can overheat andproduce artifactual responses, which may not occur under fieldconditions.

The morphological reproductive traits used in screening should beeasily observed and readily quantified in an unambiguous manner. Fruitset may be an important trait, but counting the number of flowers pro­duced can be laborious and may not be necessary. For cowpea, number ofpods per peduncle provides an estimate of pod set (Marfo and Hall 1992),because the number of effective flowers produced per peduncle is 4 in awide range of cultivars and commercial production environments.Similarly, the number of fruits per cluster may be effective in tomato(Villareal and LaI1979). Where temporal variation in hot weather occursin field nurseries, it is useful to use similar nodal positions for evaluatingfruit set, and screening is most effective when the genotypes that arebeing evaluated have similar earliness. Where genotypes with substan­tial differences in dates of first flowering are being compared, it may beuseful to conduct experiments in separate nurseries containing materials

5. BREEDING FOR HEAT TOLERANCE 155

with similar earliness. For cotton, the first nodal position at which plantsset bolls has been used in selecting for heat tolerance (Feaster andTurcotte 1965), and a highly significant genotypic correlation wasobserved between lint yield and first fruiting height in hot environments(Feaster and Turcotte 1985). This approach may also select for earlinessor lack of heat-induced abortion of floral buds.

Where specific combining effects are present, or heritability for fruitproduction is low, it may be effective to screen for several morphologicaltraits conferring heat tolerance (EI Ahmadi and Stevens 1979b; Hall1990a; Hall and Patel 1990). In this manner, a gross trait is subdivided intoa set of traits that may be simply inherited. For cowpea, these traits wouldinclude production of first floral buds at a desirable nodal position (levelof earliness), absence of floral bud abortion, high number of pods perpeduncle, and absence of embryo abortion, cotyledon twisting and seedcoat browning. For tomato, absence of floral bud abortion, stigma exser­tion and antheridial cone splitting, and high numbers of fruit per clusterand seed per fruit would appear to be important. It would also be neces­sary to avoid undesirable negative correlations that may occur betweenyield components, such as number of fruit per cluster and fruit size orintensity of fruiting and overall reproductive duration. For environ­ments and crop species where reproductive development is much moresensitive to heat than photosynthesis and the capacity of the plants to pro­duce carbohydrates, the negative correlations between yield compo­nents may not be strong.

For crops and environments where the photosynthetic system isdamaged by heat, such as with wheat during grain filling (in someenvironments), it is necessary to consider the ratio of the supply of carbo­hydrates to the reproductive sink. This is critical in studies of landraces,which often produce relatively few seeds that are well-filled even whensevere stresses occur during seed filling. In a study of the responses ofspring wheat cultivars to heat, Harding et al. (1990) concluded thatdiminished source activity and sink capacity may be equally important inreducing productivity. In cases where it has been established that heatstress is limiting yields through effects on photosynthesis, it may be pos­sible to screen for morphological traits. For example, genotypic dif­ferences in rate of leaf senescence have been detected in sorghum,soybean, and cowpea. Measurements of photosynthetic rates are notvery suitable for screening because of the considerable variation withincanopies and with time and due to environmental effects. Measurementsof stable carbon isotope composition C3C/12C) of leaves may produceuseful evaluations of stress effects on photosynthetic systems. Leafcarbon isotope composition is influenced by photosynthetic and stomatalproperties with low carbon isotope discrimination being associated with

156 ANTHONY E. HALL

low CO2 concentration within leaves and high water-use efficiency(Farquhar et al. 1982). The advantages of carbon isotope compositionmeasurements are that they provide an estimate of photosyntheticproperties integrated over the time when the carbon was fixed, and theycan be sampled with modest effort and then processed in the off-season.For cowpea, genotypic differences in carbon isotope composition werefar more consistent (and more heritable) than genotypic differences inCO2 assimilation rates (Hall et al. 1992). Cowpea genotypes differing inleaf senescence also exhibited significant differences in carbon isotopecomposition (Gwathmey and Hall 1992) in conditions where it wouldhave been extremely difficult to detect any significant differences in gasexchange due to variability among the leaves undergoing senescence.Chlorophyll fluorescence properties would also appear to be moresuitable for screening for stress effects than photosynthetic rates, wherethey reflect both time-integrated damage to the photosynthetic systemand time-integrated effects on photosynthetic rates. Different chloro­phyll fluorescence properties have been used in screening; Moffat et al.(1990a) and many other workers used variable fluorescence, whereasSmillie and Hetherington (1990) used the maximum rate of the increase ininduced chlorophyll fluorescence. Presumably, the most effectiveparameter for screening should be determined empirically. The same con­sideration applies to the use of membrane thermostability tests basedupon electrolyte leakage from leaf disks. Experimental protocols must bedeveloped, and tissues must be chosen that permit selection for theprocess or processes that limit plant adaptation and yield. Indirect selec­tion for photosynthetic traits may be achieved by selecting for morpho­logical characters. Based upon studies of heat stress effects on leaf andear photosynthesis, Blum (1986) has proposed that a large amount ofawns should enhance adaptation of wheat to environments that becomehot and dry at the end of the season.

When screening for heat tolerance during vegetative growth, it isnecessary to consider the influences of alternative sinks for carbo­hydrates. A screening protocol has been developed for potato (Reynoldsand Ewing 1989b) in which the plants are subjected to hot conditions withlong days (18 h) to minimize tuber induction. In this way, heat tolerancewith respect to shoot growth can be evaluated with minimal complica­tions due to variable levels of tuberization. Accessions exhibitingvigorous shoot growth under these conditions are then subjected to hotconditions with short days to permit evaluation of tuberization.

Where heat stress is most damaging during seed germination and emer­gence, stressful field nurseries can be created by applYing materials, suchas charcoal dust, to the soil surface to increase soil temperature (Wilson etal. 1982) or by choosing very hot seasons and locations. Alternatively,

5. BREEDING FOR HEAT TOLERANCE 157

special controlled environment systems can be used in which infraredlamps subject the soil surface and emerging seedlings to high tempera­tures (Soman and Peacock 1985). A method has been proposed forscreening seed germination at high and low temperatures based uponmeasurements at four temperatures (Ellis et al. 1987), but it may be moreeffective for defining minimum rather than maximum temperature limits(Covell et al. 1986). Seedling germination responses appear particularlysuitable for evaluating the roles of specific heat-shock proteins, becausegenotypic differences in HSPs have been reported in seedlings that areassociated with heat tolerance (Ougham and Stoddart 1986; Howarth1989). They are also appropriate for applying genetic engineeringstrategies (Schoffl 1988) to increase heat tolerance, because seedlingsystems are easy to manipulate and can be evaluated quickly.

B. Breeding Methods

A pedigree breeding backcross approach has proved to be effective inincorporating heat tolerance during reproductive development into purelines of cowpea (Hall and Patel 1990). This approach may have somegeneral value for cases where heat tolerance is only available in exoticmaterials and is conferred by several major genes. In this approach,simple and triple crosses were made among complementary sets ofparents that exhibited heat tolerance during different stages of reproduc­tive development and desirable agronomic characters. In some cases, abackcross was applied to the F1 using the most productive but heat­sensitive cultivar that was available. The first segregating generation wasscreened as single plants in very large populations (1000s) in an extremelyhot field environment. Individual plants that exhibited abundantflowering, high numbers of pods per peduncle, adequate seeds per pod,and adequate seed quality were selected. This proved to be effective infixing several traits that are conferred by recessive genes (insensitivity tophotoperiod, lack of floral bud abortion, partial heat tolerance during podset, and absence of seed coat browning). An additional cycle of selectionhas been practiced with F2 -derived families at more advanced genera­tions to incorporate traits, such as aspects of heat tolerance during podset, which exhibit substantial environmental variation and appear toinvolve at least one major dominant gene. Small numbers of progenies areleft by this time, and it is possible evaluate rows of the F2 -derived lines toselect lines that have uniformly high pod set and other desirable charac­ters. The heat-screening nursery is too hot to permit effective selectionfor some agronomic characters, and a replicate set of these lines isscreened in a commercial production environment during the same year.Observations are made in both nurseries, and final plant selections are

158 ANTHONY E. HALL

made in the commercial production environment. Commercial cultivarswere backcrossed to these selections, and the cycle was repeated.Screening for disease resistance has been conducted in interveninggenerations, e.g., F3). Performance testing is conducted in a series of pre­liminary, advanced, and then multilocation trials with material that hassufficient stability and appropriate agronomic characters. This last stepis critically important because heat tolerance during reproductivedevelopment is only useful if it results in improvements in yield or qualityof the economic product in commercial production environments.Performance testing is conducted in several locations over several yearsbecause of the variability that occurs in the timing and intensity of hotweather.

The AVRDC breeding programs have used a pedigree breedingapproach with some backcrossing to develop improved tomatoes and, inrecent years, have emphasized the development of hybrid cultivars ofboth tomato and Chinese cabbage (Opena et al. 1987). For processingtomatoes, recurrent selection for specific combining ability has beenused to combine different components of heat tolerance during reproduc­tive development in a single cultivar (Stevens 1979).

For self-pollinating species where the main lesion from heat stress ismale sterility, there is the possibility of using this effect to cause out­crossing and transfer of favorable alleles by the pollen. A populationimprovement scheme could be envisaged in which a population ofagronomically desirable but heat-sensitive genotypes is planted in rowsalternating with rows of heat-tolerant genotypes in an extremely hotenvironment. Where appropriate, beehives could be placed in the nurseryto enhance the level of cross-pollination. Plants would be selected fromthe population rows, seed would be bulked and resown the following yearwith alternating rows of heat-tolerant parents sown using seed producedin an environment where outcrossing is low. After several cycles of massselection, the best individuals could be selected from the populationrows, tested for homozygosity in the extremely hot environment in theabsence of pollinators, and then evaluated in the yield-testing program orused as parents in a pedigree breeding program.

Possibilities exist for using selection among male gametophytes, asindicated by studies of chilling tolerance in wild and cultivated tomatoes.Tanksley et al. (1981) obtained evidence for genetic control of chillingtolerance that was due to postmeiotic gene expression in pollen. Studieswith artificial pollination using mixtures of pollen from a chilling­tolerant and a chilling-sensitive species demonstrated that differentialselection occurred at the gametophyte level in response to low tempera­ture (Zamir et al. 1981). They also demonstrated that the fertilizationability of pollen from the chilling-tolerant parent is determined, in part,

5. BREEDING FOR HEAT TOLERANCE 159

by genes expressed by the haploid genome (Zamir et al. 1982). Morerecently, Zamir and Gadish (1987) demonstrated an association betweenpollen selection under low temperatures and a sporophytic trait,enhanced root growth under chilling conditions. This supports thehypothesis that the sporophyte and gametophyte of higher plants rely, inpart, on a common set of structural genes (Tanksley et al. 1981). Dicksonand Petzoldt (1989a) provided information that is relevant togametophytic selection for heat tolerance. They subjected F1 plants (from9 crosses among 11 snap bean genotypes that exhibit heat toleranceduring pod set) to heat stress or to more optimal temperatures. In 6 out ofthe 9 progenies, a higher proportion of F2 plants exhibited heat tolerancewhere the F1s had been subjected to heat stress. Presumably, the heatstress imposed a selection pressure on the pollen produced by the F1

plants, which resulted in higher proportions of F2 plants exhibiting heattolerance. Where heat tolerance during early stages of floral develop­ment is conferred mainly by recessive genes, F1 plants tend to have lowseed production when heat stressed. An alternative approach would be togrow the F1 plants under optimal temperatures, and then to make artifi­cial crosses using pollen from the F1 plants to the emasculated flowers ofplants growing under hot temperatures. A simpler but more artificialprocedure would involve growing F1 plants under optimal temperaturesand subjecting excised flowers to heat stress and then using them to polli­nate plants growing under optimal temperatures. Vigor of pollen can bereduced by subjecting it to 38°C for several hours; the amount of reduc­tion depends on the species (8hivanna et al. 1991). Pollen selection couldbe effective for detecting rare variants, because there are thousands ofpollen grains in one flower. But it may be less appropriate for incorporat­ing heat tolerance than conventional breeding methods where simplyinherited traits are present.

VI. PROGRESS IN BREEDING FOR HEATTOLERANCE AND CONCLUSIONS

The success that has been achieved in breeding for heat tolerance hasbeen documented only for a few cases. Commercial breeding companies,understandably, cannot divulge their methods to potential competitors.Four improved cultivars of Pima cotton (Feaster and Turcotte 1976, 1984)and six germplasm lines (Turcotte et al. 1991) have been bred with selec­tion for boll set on low nodal positions under high temperature fieldconditions. 'Pima 8-6', which was released in 1983, was estimated to havea yield advantage of 69% over the original 'Pima 8-1' (the dominant cul­tivar from 1955 to 1961) in hot environments and 27 to 43% in cooler

160 ANTHONY E. HALL

environments (Feaster and Turcotte, 1985). Average yields of Pima andupland cotton were compared for 6 counties in Arizona over a 30-yearperiod (Kittock et a1. 1988). Pima cotton lint yields increased substan­tially more than the upland cotton lint yields (particularly in hotterenvironments), as improved Pima cultivars were released over the 30­year period. The authors concluded that about 50% of the 30-year lintyield increase of Pima cotton in hot environments resulted from theincreased heat tolerance of the improved cultivars. They also point outthat upland cottons had greater heat tolerance than these Pima cottons,especially in earlier years. The success of the commercial breeding pro­grams for upland cotton cultivars for the extremely hot environments ofthe southwestern United States was probably also partially due to incor­poration of heat tolerance during boll set.

Breeding programs that put selection pressure on the extent of poddingin an extremely hot, long-day environment in northern India have pro­duced cultivars of edible-pod vegetable cowpeas (Patel and Singh 1984),which have been shown to have substantial heat tolerance (Patel and Hall1986, 1990). A pedigree breeding/backcross program was conducted byP. N. Patel in which dry grain cowpeas were selected for heat toleranceduring reproductive development in an extremely hot environmentduring the summer in Imperial Valley, California (Hall and Patel 1990).Advanced lines developed by the program will set significant numbers ofpods in this environment, whereas the available cultivars set very fewpods. For example, in this very hot environment the grain yields of theadvanced lines were about six-fold greater than the yields of the mostproductive California cultivar, which was used as the recurrent parent inthe crosses (Hall and Patel 1987). One of these advanced lines (#518) hadgreater heat tolerance during reproductive development than the linesused in the original crosses, which indicates that alleles conferring heattolerance were obtained from both parents. Progress has been made incombining heat tolerance with the other traits needed in dry grain cowpeacultivars for California. Hot weather occurred at early flowering during arecent advanced yield trial at the Kearney Agricultural Center, which islocated in the center of the commercial production region in California.Five advanced lines with heat tolerance ranked highest in yield in thistrial out of 16 entries with 15-26% higher yield than the cultivar used asthe recurrent parent in their breeding (Hall et a1. 1990). The objective ofthe cowpea breeding program is to develop cultivars that have higher andmore stable yields than current cultivars over the range of temperaturesexperienced during the summer in the San Joaquin Valley of California.The breadth of adaptation of the heat-tolerant lines is being evaluated bymultilocation and multi-year yield tests.

For tomato, the heat-tolerant 'Saladette' was bred by Paul W. Leeper by

5. BREEDING FOR HEAT TOLERANCE 161

selecting for fruit set under the hot summer conditions of the Lower RioGrande Valley in Texas. Since this time, 'Saladette' and other heat­tolerant genotypes (Stevens 1979) have been used as parents in breedingprograms. Several commercial breeding programs in California havedeveloped improved tomato cultivars by incorporating heat toleranceduring reproductive development. The approach usually consisted ofsubjecting segregating material to hot or extremely hot field or green­house environments and selecting for high fruit and seed set. The AsianVegetable Research and Development Center in Taiwan has focused onimproving the heat tolerance of vegetable cultivars for the tropics, wherenight temperatures are high. Heat-tolerant cultivars of tomato weredeveloped by selecting for fruit set under hot conditions (Villareal and Lal1979), and of Chinese cabbage by selecting for production of a firm headunder hot conditions (Opena et al. 1987). AVRDC (Chandler Jr. 1983) andCIP (Mendoza and Estrada 1979) have developed heat-tolerant clones ofpotato.

Most of the progress made in breeding heat-resistant cultivars has beenachieved by incorporating heat tolerance during reproductive develop­ment through selection for morphological characters, such as fruit set, inhot field nurseries. Inheritance studies indicate that different aspects ofheat tolerance during reproductive development are conferred by majorgenes, which are either recessive or dominant, and substantial progresshas been made using pedigree breeding methods. Breeding for heattolerance by selecting for morphological traits has been successful inseveral crop species (e.g. cotton, tomato, and cowpea), and there are noindications that progress can be enhanced for these species by selectingfor physiological or molecular traits. The use of physiological criteria inscreening for heat tolerance may be more appropriate for cases whereheat stress is reducing economic yield through reductions inphotosynthesis (e.g., in wheat and potato). In these cases, there may besome value in screening for chlorophyll fluorescence properties,membrane thermostability, or possibly stable carbon isotope composi­tion, but the values of these screening procedures have not been ade­quately demonstrated, and screening for morphological traits, such asawns or delayed leaf senescence, should not be ignored.

Approaches based upon heat-shock proteins are not yet recommendedfor practical breeding programs. Cropping systems where high tempera­tures inhibit germination and seedling establishment (e.g., sorghum andpearl millet in West Africa) may provide opportunities for developingnovel approaches to improving heat tolerance through the manipulationof heat-shock proteins. Overall, inadequate effort may have beendevoted to breeding for heat tolerance through selection formorphological characters associated with reproductive development, in

162 ANTHONY E. HALL

relation to the potential improvements in crop yields and yield stabilitythat could be achieved. Increases in frequency of hot weather and carbondioxide concentrations due to global climate change may increase theneed for heat-resistant cultivars in the next century.

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