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Chapter 15

Breeding Cowpea for Future ClimatesAnthony E. Hall

Introduction

Global climates are changing, and since plantbreeding programs typically operate within timeframes of decades, it is appropriate to begindesigning cultivars adapted to future climates.Cowpea breeding strategies are examined thatcould solve heat-stress problems and exploit anopportunity that may result from global climatechange. An established feature of global cli-mate change is the continuing increase in atmo-spheric carbon dioxide concentration ([CO2]).Plants with the C3 photosynthetic system, suchas cowpea, potentially should exhibit increasesin photosynthesis with increases in [CO2]. Priorto 1900, however, plants were subjected to low[CO2]s between 180 and 300 μmol mol−1 for atleast 220,000 years (Barnola et al. 1987; Jouzelet al. 1993) and plants may still be adapted tothese conditions. The extent to which plants withC3 photosynthesis are adapted either to current[CO2]s of about 380 μmol mol−1 or the dou-bling of [CO2] expected to occur in the futureis not known. Plant traits that might enhance theresponse of photosynthesis by cowpea to ele-vated [CO2] are discussed. Global warming ofa few degrees Celsius has been predicted to oc-cur as a consequence of the increases in [CO2]and other gases that absorb infrared radiation in

the earth’s atmosphere (Kerr 1986). Greater in-creases in night temperature than in day temper-ature were observed in some locations for severalyears after 1950 (Kukla and Karl 1993), whichhas particular significance to breeding cowpeato tolerate heat. More recent data indicate, how-ever, that from 1979 through 2004, similar in-creases occurred in both the 24-hour minimumand 24-hour maximum temperatures (Vose et al.2005). Possible interactive effects on cowpea ofglobal warming and increases in [CO2] are ex-amined. Problems arising from changes in hy-drologic conditions due to global climate changeare not considered because these problems mightbe solved by changes in crop management meth-ods. This review builds on reviews by Hall andAllen (1993) and Hall and Ziska (2000) who ex-amined breeding strategies for all crops in thetwenty-first century by providing additional andmore recent information on cowpea.

Cultivated cowpea (Vigna unguiculata L.Walpers) has been divided into five cultivargroups based mainly on pod, seed, and ovulecharacteristics (Pasquet 1999). Cultivars in thesegroups are grown to produce dry grain (includ-ing blackeye peas or blackeye beans), fresh peas(including southern peas), edible pods (includ-ing bush-types and members of cultivar groupSesquipedalis, which also are known as yardlong

Crop Adaptation to Climate Change, First Edition. Edited by Shyam S. Yadav, Robert J. Redden, Jerry L. Hatfield,Hermann Lotze-Campen and Anthony E. Hall.c© 2011 John Wiley & Sons, Ltd. Published 2011 by John Wiley & Sons, Ltd.

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BREEDING COWPEA FOR FUTURE CLIMATES 341

beans, long beans, Asparagus beans, or snakebeans), and hay. Cowpeas are grown as warm-season-adapted annuals in tropical and subtropi-cal zones (as defined by Hall 2001) in all coun-tries in sub-Saharan Africa and in Asia, SouthAmerica, Central America, the Caribbean, theUnited States, and around the MediterraneanSea. In subtropical zones, temperatures are onlysuitable for growing cowpea in the summer,whereas temperatures often are suitable year-round in tropical zones. Most of the world’scowpea production takes place in tropical ar-eas of sub-Saharan Africa with about 11 millionhectares under cultivation (Singh et al. 2002).The main production is in the Sudan Savannazone of West Africa (especially in Nigeria) butwith substantial production also in the semi-arid Sahelian zone, which stretches across Africafrom Senegal in the west to the Sudan in the east.Outside of Africa, major cowpea production oc-curs in tropical areas of Brazil and Asia, and sig-nificant subtropical zone production takes placein the United States and South Africa (Singh et al.2002).

Adaptation to elevatedatmospheric [CO2]

Under optimal temperatures, photosyntheticrates of cowpea increase substantially with short-term increases in [CO2] (Hall and Schulze 1980)similar to other C3 species. Doubling [CO2] hasincreased grain yield of grain legumes by 54% atintermediate temperatures (Kimball 1983). Forthe only study reported for cowpea (Ahmed et al.1993a), pod yield was 45% greater for plantsgrowing at 700 μmol mol−1 [CO2] comparedwith 350 μmol mol−1 [CO2]. This study wasconducted with plants in pots in growth cham-bers with moderate light levels (530 μmol photonm−2 s−1). Grain yield of cowpea growing undersunny field conditions might increase more than45% with a doubling of [CO2], providing tem-peratures and rooting conditions are optimal. Butwill current cowpea cultivars be well-adapted to[CO2]s of 700 μmol mol−1? Cowpea like other

C3 species was subjected to [CO2]s between180 and 300 μmol mol−1 for at least 220,000years prior to 1990. The characteristics of theenzyme involved in the initial fixation of CO2

in C3 plants, ribulose bisphosphate carboxylase,may not have changed very much during this pe-riod (Morell et al. 1992). However, it is likelythat low [CO2] resulted in evolutionary modifi-cations to whole-plant processes, such as a highratio of photosynthetic source tissue to carbohy-drate sink tissues, that would not be well-adaptedwith [CO2]s of 700 μmol mol−1 where potentialrates of photosynthesis are greater. Plants with ahigh ratio of photosynthetic source to carbohy-drate sink tissue would have low values of harvestindex (the ratio of grain dry matter to total shootdry matter at harvest). Natural evolution tends tofavor plants with competitive canopies that alsohave low harvest indexes. Consequently, it is notsurprising that the new cultivars of grain cropsdeveloped by plant breeders for optimal condi-tions have tended to have progressively greaterharvest indexes (Gifford 1986). Selecting for fur-ther increases in harvest index may be effectivein increasing grain yield in future environmentswith higher [CO2]s.

In some cases, downregulation of photosyn-thetic capacity has occurred when plants wereexposed to high [CO2]s for long periods or grownunder high [CO2]. Downregulation of photosyn-thetic capacity was apparent in cowpea grownat 700 μmol mol−1 [CO2] compared with plantsgrown at 350 μmol mol−1 [CO2] (Ahmed et al.1993a). This downregulation could have been ei-ther a consequence of the artificial growth con-ditions or it may indicate that current cultivars ofcowpea are not well adapted to elevated [CO2].Down regulation of photosynthesis has been at-tributed to feedback mechanisms that operatewhen the supply of carbohydrates from photo-synthesis exceeds sink demands for carbohy-drates (Allen 1994). However, as Arp (1991)pointed out, strong downregulation of photo-synthesis mainly has been observed in elevated[CO2] experiments, like the one with cowpea,where plants were grown in small pots that would



342 CROP ADAPTATION TO CLIMATE CHANGE

have resulted in a much smaller root sink forcarbohydrates than occurs in most natural soilconditions.

Adaptation to global warming

Stressful high temperatures that reduce the grainyields of cowpea already occur in some trop-ical and subtropical production zones. Conse-quently, heat-tolerant cowpea cultivars are use-ful today (e.g. Ehlers et al. 2000) and likely willbe even more valuable in the future. The website www.plantstress.com has a section on cropbreeding for heat tolerance and has much in-formation on cowpea. Breeding for heat toler-ance with all crops was reviewed by Hall (1992,1993). This review emphasizes cowpea and pro-vides some more recent information. Much ofthe information on cowpea response to heat wasobtained in a subtropical zone. This informationwill be discussed first followed by a discussion ofits relevance to tropical zones where most cow-peas are cultivated. Then, information obtainedin tropical zones will be discussed.

Heat stress effects in subtropical zones

What stages of plant growth and developmentare most sensitive to heat and are responsiblefor the reductions in grain yield that occur?

For cowpea, and many other crops, reproduc-tive stages are very sensitive to heat, while thevegetative stage is very tolerant to high temper-atures (Hall 1992, 1993, 2004). Most cowpeacultivars tested grew rapidly and produced abun-dant shoot biomass under irrigation in one of thehottest crop production environments on earth(during the summer in the low elevation desert insouthern California with mean daily max/min airtemperatures of 41/24◦C and long days varyingfrom 14 hour 50 minutes at sowing to 14 hour16 minutes after 30 days). However, many ofthese cultivars did not produce flowers and vir-tually all of those that did produce flowers did notproduce any pods (Patel and Hall 1990; Ehlersand Hall 1996). Several reproductive stages are

damaged by heat but low pod-set is most closelyassociated with reductions in grain yield and willbe discussed first.

What aspect of hot weather is responsiblefor reductions in pod-set?

Early studies with well-irrigated cowpeas sownat different dates and years showed variationsin grain yield between 2000 and 4000 kg ha−1,which were positively correlated with variationsin number of pods per m2 and negatively cor-related with high temperatures expressed as de-gree days for air temperatures above 35◦C for30 days after the appearance of floral buds (Turket al. 1980). However, in subsequent growthchamber studies, neither high day temperaturenor moderate drought caused a reduction in pod-set, whereas, very high night temperature causedplants to have no pod-set (Warrag and Hall1984a, 1984b). A definitive study was conductedin which plants in the field were subjected to dif-ferent higher night temperatures during flower-ing. This was achieved by enclosing large plotswith plastic covers placed over plants at sun-set (Nielsen and Hall 1985a). Inside the coveredareas, there were fans, heaters, and differentialthermostats that increased air temperatures pre-set numbers of degrees above the outside ambientair temperature. Plastic covers were removed atsunrise and fans and heaters were switched offsuch that the daytime environment was not in-fluenced by the treatments. For plots having fivemean minimum nighttime temperatures varyingfrom 15◦C to 26.5◦C, there was a linear decreasein grain yield from 2.8 to 1.4 t ha−1, and a lineardecrease in pod-set from 62% to 32% (Nielsenand Hall 1985b; Hall 1993). This represented a4.4% decrease in grain yield per degree Celsiusincrease in nighttime temperature above a thresh-old daily minimum night temperature of 15◦C.In a subsequent correlations study using con-trasting field environments, cowpea exhibited a13.6% decrease in grain yield per degree Celsiusincrease in average daily minimum night temper-ature above 16◦C during early flowering (Ismail




and Hall 1998). In this study also the decreasesin grain yield were mainly due to decreases inpod-set.

What is responsible for the reductions inpod-set caused by high nighttime temperature?

Low pod-set was associated with low pollen via-bility (Warrag and Hall 1984b), and some geno-types that were very sensitive to heat also hadlow anther dehiscence (Mutters and Hall 1992).Artificial pollination studies demonstrated thatpistil viability was not affected by high nighttemperatures (Warrag and Hall 1983). Recipro-cal transfers of plants between growth chamberswith high or optimal night temperatures demon-strated that the stage of floral development mostsensitive to heat stress occurred 9–7 days beforeanthesis (Ahmed et al. 1992). This is after meio-sis, which occurs 11 days before anthesis andabout the same time that the tetrads are releasedfrom the microspore mother cell sac (Warragand Hall 1984b; Ahmed et al. 1992; Mutters andHall 1992). Premature degeneration of tapetaltissue and lack of endothecium formation wereobserved, which could have been responsiblefor the low pollen viability, low anther dehis-cence, and low pod-set under high night tem-peratures (Ahmed et al. 1992). Tapetal tissueplays an important role in providing nutrients todeveloping pollen grains and its premature de-generation could thereby stunt pollen develop-ment. Mutters et al. (1989b) demonstrated that,at pollen maturity, heat-sensitive cowpea geno-types contained lower concentrations of prolinein pollen than heat-tolerant cowpea genotypesunder hot conditions, but similar levels as heat-tolerant genotypes under more optimal tempera-tures. Pollen development, membrane functionand germination, and pollen tube growth arethought to require high levels of proline. Mutterset al. (1989b) proposed that heat injury duringfloral development of sensitive cowpea geno-types may be due to reduced translocation ofproline from anther walls and tapetal tissue todeveloping pollen. Tapetal malfunction has been

considered to be the causal mechanism of muchof the cytoplasmic and genetic male sterility oc-curring in plant species (Dundas et al. 1981;Nakashima et al. 1984).

Why is pod-set in cowpea sensitive to highnight temperature when much highertemperatures occur in the day?

Growth chamber studies demonstrated that pod-set of cowpea is sensitive to heat during thelast 6 hours of the night but not during the first6 hours of a 12-hour night (Mutters and Hall1992). Sensitivity of pod-set to heat is greater un-der long days than short days, and the responsesto red light during long nights, far-red light af-ter long days, and far-red then red light afterlong days indicate that this is a phytochrome-mediated photoperiod effect (Mutters et al.1989a). Phytochrome-mediated events have a de-gree of circadian control, and Mutters and Hall(1992) hypothesized that there is a physiologi-cal process in pollen development that is undercircadian control and only occurs during the latenight. Note that the sensitive period may stretchinto the early morning in that in growth cham-ber studies under moderate night temperatures,greater reductions in pod-set were observed witha very high day temperature than with a high daytemperature (Warrag and Hall 1983). For a heat-sensitive process that is under circadian control,natural selection would favor plants in which theprocess takes place during the coolest part of thediurnal period, which is the late night and earlymorning.

What other reproductive responses aresensitive to high temperatures?

Under long day and very hot field conditions,some cowpea genotypes produced floral buds,but they did not produce any flowers (Patel andHall 1990). Prior to discussing growth cham-ber studies of floral bud suppression by heat,it is important to note that it depends on lightquality and does not occur in some hot growth




chamber conditions. Floral bud development wasarrested by high night temperature and long daysonly in growth chambers that had red (655-665nm)/far-red (725-735 nm) ratios of 1.3 or 1.6but not in chambers with a higher R/FR ratioof 1.9 (Ahmed et al. 1993b). Note that growthchambers that mainly use either fluorescent ormetal-halide lamps can have a high R/FR ra-tio and often have been used in plant growthstudies. Few tungsten lamps were used in thesestudies because even though they produce muchFR, they have the undesirable features of pro-ducing much heat and relatively few photosyn-thetically active photons. Also note that sunlighthas a low R/FR ratio of 1.2 above the canopyand an even lower ratio within dense canopies.The suppression of floral bud development underlong days with high night temperatures appearsto be a phytochrome-mediated photoperiod ef-fect except that a night-break of red light duringa long night did not result in floral bud suppres-sion (Mutters et al. 1989a). Suppression of floralbuds under long days occurred under hot nightsbut was greater under the combination of hotnights and very hot days (Dow El-Madina andHall 1986). Transfer and heat-pulse experimentsdemonstrated that plants did not have a particu-lar stage of development where they were verysensitive to high night temperature but that theduration of heat experience may be critical for thesuppression of floral bud development (Ahmedand Hall 1993). Two weeks or more of consec-utive or interrupted hot nights during the firstfour weeks after germination caused completesuppression of the development of the first fivefloral buds on the main stem (Ahmed and Hall1993). The minimum daylength required to elicitheat-induced suppression of floral bud develop-ment may be as short as 13 hours, including civiltwilight. Days that are longer than this minimumoccur in all subtropical and some tropical zonesduring the cowpea growing season. It should benoted that genotypes of cowpea with “classical”sensitivity to photoperiod do not produce flo-ral buds under long days. Under inductive shortdays and high night temperatures a cultivar with

“classical” sensitivity produced floral buds, andthe buds were not sensitive to heat and devel-oped normally and produced flowers (Mutterset al. 1989a).

Different cowpea genotypes have pods thatproduce 9–20 ovules, with many cultivars having15, but they rarely produce these many seeds perpod. Under optimal conditions, the average num-ber of seeds per pod is about two-thirds of themaximum possible number. In short-day green-house conditions, 17 sensitive cowpea genotypesexhibited an average reduction in number ofseeds per pod of about 50% in hot comparedwith moderate night temperatures (Ehlers andHall 1998). In long-day conditions, cowpea alsoexhibited reductions in numbers of seeds per poddue to either hot night temperatures (Nielsenand Hall 1985b) or hot day temperatures (Warragand Hall 1983). For virtually all cowpea geno-types, it is the ovules at the blossom end of thepod that do not produce seed when plants are sub-jected to heat and other stresses. An exceptionis the important genotype TVu4552, which hasstrong heat tolerance during floral bud develop-ment and pod-set, but a tendency to not producethe first seed at the peduncle end of the pod. Thisgenotype also exhibited brown discoloration ofthe seed coat when subjected to high night tem-peratures in subtropical field conditions (Nielsenand Hall 1985b). This seed-coat browning can re-sult in consumer dissatisfaction with the qualityof the grain. The important thrip-resistant cow-pea TVx3236 also exhibits unpleasant seed-coatbrowning when grown in tropical regions wherenight temperatures are high. High day tempera-tures caused seed to have asymmetrical cotyle-dons and more wrinkled seed coats but the ger-minability of the seed was not affected (Warragand Hall 1984a).

What sources of heat tolerance duringreproductive development are availablein cowpea?

Accessions of cowpea from different coun-tries were screened for heat tolerance during




reproductive development in an irrigated lowelevation desert, summer environment in Cal-ifornia with very hot (mean daily maxi-mum/minimum air temperatures of 41/24◦C)long-day (14 hour, 50 minutes at planting to14 hour, 16 minutes after 30 days) conditions.Only 3 out of 268 accessions were found to haveheat tolerance during both floral bud develop-ment and pod-set and abundantly produce flow-ers and pods in these conditions: two dry-grainbush types from Nigeria, Prima, and TVu4552,and one edible-pod bush type from India (Pateland Hall 1990). Many of the accessions (71) ex-hibited heat tolerance during floral bud develop-ment, abundantly producing flowers but did notset any pods. A genotypic classification of cow-pea based on responses to heat and photoperiodhas been developed (Ehlers and Hall 1996). Thisclassification can help breeders choose geno-types with appropriate juvenility, photoperiodresponse, and heat tolerance for breeding pro-grams to serve different subtropical and tropicalproduction zones. Out of 20 accessions studied,two had heat tolerance during grain developmentunder short days, exhibiting the maintenance ofmany seeds per pod: TN88-63 a grain type fromNiger and B89-600 a grain type from Senegal(Ehlers and Hall 1998).

What is the inheritance of heat tolerance andhow can this information be used in breeding?

Sensitivity to heat during floral bud developmentappears to be phytochrome-mediated. Toleranceto heat during floral bud development appearsto be conferred by a single recessive gene whenusing either Prima or TVu4552 as a heat-tolerantparent (Hall 1993). Heat tolerance during earlyfloral bud development has been effectively se-lected during the first generation (e.g., F2) byselecting individual plants that abundantly pro-duced flowers when subjected to hot, long daysduring the first month after germination.

Sensitivity to heat during pod-set appears tohave at least two components one of which isphytochrome mediated. Segregation of heat tol-

erance during pod-set was consistent with thehypothesis that some heat tolerance during pod-set is conferred by a single dominant gene in bothTVu4552 and Prima (Marfo and Hall 1992). Al-though it is likely that at least one more gene isinvolved in conferring more complete heat toler-ance during pod-set. In addition, there were largeenvironmental effects on pod-set, and narrow-sense heritability was only 0.26 while realizedheritability was only 0.27 (Marfo and Hall 1992).Not surprisingly, at least two cycles of family se-lection with advanced generations subjected tohot, long days have been required to incorpo-rate substantial levels of heat tolerance duringpod-set.

While breeding for heat tolerance during pod-set has been effective in southern California, ithas taken several cycles of selection, and mostbreeders in other regions have not had idealscreening environments. This led to a search forphysiological features that are associated withheat tolerance during pod-set. Several researchgroups evaluated the heat-tolerant lines and theheat-susceptible lines developed by the Univer-sity of California, Riverside, to see if they dif-fered in heat-shock proteins, but no differencesin heat shock proteins were found.

An indirect screening technique was evalu-ated, involving percent electrolyte leakage fromleaf tissue sampled at the end of the darkperiod following incubation at high tempera-tures as a measure of membrane thermostability(Ismail and Hall 1999). Genotypes with heat tol-erance during both floral development and pod-set exhibited less leaf electrolyte leakage thaneither genotypes with susceptibility during bothearly flowering and pod-set or genotypes havingheat tolerance only during floral development(Ismail and Hall 1999).

On the basis of earlier research, leaf elec-trolyte leakage had been proposed as a methodfor screening for tolerance to heat and otherstresses (Blum 1988). More recent work withcowpea by Thiaw and Hall (2004) will be de-scribed in detail because this was the first timethat leaf electrolyte leakage had been related




to a process, pod-set, that contributes to heatresistance, which is the ability of a cultivar to pro-duce more grain yield than other cultivars in hotenvironments. A further refined leaf electrolyteleakage technique was developed and used ina definitive selection experiment that demon-strated a close association between heat toleranceduring pod-set and slow leaf electrolyte leakage.Leaf discs were sampled during the predawn pe-riod from plants in the vegetative stage. Leafdiscs were rinsed and then incubated in deion-ized water in a test tube for 6 hours in the pres-ence of aeration at 46◦C with a cover to minimizeevaporation. Electrical conductivity of the solu-tion was then measured. The test tube containingthe leaf discs was covered again and then placedin boiling water for 45 minutes to kill the cellsand then incubated at 46◦C for 18–24 hours toallow most of the electrolyte to diffuse out of theleaf discs into the solution. A second measure-ment of electrical conductivity was taken and thepercentage leakage was calculated based on thefirst and second measurements. A heat-sensitivecultivar, CB5, and a heat-tolerant breeding line,H36, were used as parents in a selection experi-ment. In breeding H36, CB5 had been crossedwith TVu4552, a heat-tolerant accession, andthen backcrossed with CB5. Several generationsof selection had been conducted for ability toproduce flowers and set pods in an extremelyhot, long-day environment producing line 518-2.Then, line 518-2 had been backcrossed to CB5,and segregating progenies had been selected forheat tolerance in several generations, as was donein developing 518-2, producing line H36. LineH36 was shown to consistently have less leafelectrolyte leakage (average of 52%) than theheat-sensitive cultivar CB5 (average of 68%) intests over a range of environments with opti-mal or extremely hot temperatures and long orshort days. Line H36 and CB5 were reciprocallycrossed and produced F1 seeds that were plantedto produce F2 seeds, from which two popula-tions were developed. Thirty-two lines were di-vergently selected based on low (16) and high(16) leaf electrolyte leakage with plants grown

in optimal temperatures and long days in growthchambers in both the F2 and F3 generations andthen advanced by single-seed descent for twogenerations. One hundred and six lines were di-vergently selected based on high pod-set (66)and low pod-set (40) in an extremely hot, long-day field environment in the F2 generation andthen advanced by single-seed descent for threegenerations. Both populations were evaluated inthe F6 generation for their ability to set pods andproduce grain in an extremely hot, long-day fieldenvironment and a very hot, long-day glasshouseenvironment. In both environments, the 66 linesselected in one generation for pod-set and the16 lines selected in two generations for low leafelectrolyte leakage had greater pod-set and grainyield than either the 40 lines selected for lowpod-set or the 16 lines selected for high leafelectrolyte leakage. In both environments, highlysignificant negative correlations were obtainedbetween leaf electrolyte leakage and number ofpods per peduncle and grain yield using datafrom both populations. Realized heritabilities ofleaf electrolyte leakage were 0.28–0.34, and thegenetic correlation between leaf electrolyte leak-age and pod-set was −0.36. This provides a valuefor the indirect realized heritability for enhancingpod-set by selecting for leaf electrolyte leakageof 0.10–0.12. The value of 0.10–0.12 is smallerthan the realized heritability for direct selectionfor pod-set of 0.27 reported by Marfo and Hall(1992). Despite the low indirect realized heri-tability value, indirect selection for pod-set us-ing leaf electrolyte leakage may have value inbreeding programs. Selection for leaf electrolyteleakage could be effective with plants grown inmoderate or hot temperatures and long- or short-day environments. Therefore, it can be used inboth summer field nurseries and in glasshousesin off-seasons, and it would be particularly use-ful in regions where extremely hot, long-day en-vironments are not available for use in directselection for heat tolerance during pod-set.

The heat-induced seed-coat browning of theheat-tolerant accession TVu4552 constrains itsuse as a parent in breeding. Genetic studies




demonstrated, however, that this detrimental traitappears to be conferred by a single dominantgene and is not linked to the recessive geneconferring heat tolerance during floral bud de-velopment (Patel and Hall 1988). Also, insteadof using TVu4552 as a parent, breeders cannow use lines developed at the University ofCalifornia, Riverside, such as H36 mentionedpreviously, which was bred by crossing TVu4552with CB5 and followed by extensive backcross-ing with CB5, and it does not have the seed-coatbrowning trait.

The heat-tolerant accession Prima has anundesirable trait involving leakage of purple pig-ment from its blackeye during cooking or can-ning. Effective simple tests are available to elim-inate genotypes with this trait (Hall et al. 1997).Also, instead of using Prima as a parent, breed-ers could use lines developed at the Univer-sity of California, Riverside, such as the culti-var California Blackeye 27 (Ehlers et al. 2000),also called CB27, which had both Prima andTVu4552 as parents and has substantial heattolerance.

What progress has been made in breedingcultivars with heat tolerance for subtropicalzones, and what positive and potential negativeeffects are associated with the heat-tolerancegenes?

Heat tolerance of plant processes is of commer-cial value only if it results in a cultivar havingheat resistance, which is higher grain yields com-pared with other cultivars in hot environments.In addition, a heat-resistant cultivar should havesimilar or greater grain yields than current cul-tivars in moderate-temperature environments. Aheat-resistant cultivar, CB27, that has these de-sirable traits has been bred for use in California(Ehlers et al. 2000).

Breeding CB27 took many years. VariousCalifornia blackeye cultivars and lines were in-tercrossed and then crossed with both Primaand TVu4552. Heat tolerance was incorporated

by selecting progeny with ability to produceflowers and set pods over several generationsin extremely hot, long-day field nurseries. Un-desirable traits, such as heat-induced seed-coatbrowning and pigment leaking from the blackeye, were removed and additional resistances todiseases and pests were incorporated.

Breeding for heat tolerance can now proceedmore quickly. CB27 and lines such as H36, whichhave both heat tolerance and many desirableagronomic traits, can be used as heat-tolerantparents. A rapid breeding procedure is availableto incorporate heat tolerance. Make the cross andsubsequently subject a large F2 generation to anextremely hot, long-day field environment in thesummer and select plants with abundant flowerproduction and pod-set. This will fix heat toler-ance during floral bud development in virtuallyall selected lines. Note that if an extremely hot,long-day field nursery is not available, a summerglasshouse that has high night temperatures andlong days could be used. However, glasshousesusually can accommodate fewer plants or aremore expensive to operate (per plant screened)than field nurseries. During the fall and winter,there would be two possibilities. If the heat-tolerant parent had less leaf electrolyte leakageunder heat stress than the heat-susceptible par-ent, then select plants with low leakage duringthe F3 and F4 generations with plants growingin moderate-temperature glasshouses and shortdays. If this option is not possible, then simplyadvance two generations by single-seed descent.During the second summer, grow replicate fam-ilies of the F5 generation in the extremely hot,long-day field nursery (or glasshouse with highnight temperature) and in parallel nurseries toscreen for agronomic traits. Note that selectionfor grain quality traits is particularly importantin cowpea breeding. Choose families that haveabundant flower production and pod-set, andalso suitable agronomic traits in parallel nurs-eries, and select the best individual plants fromwithin these families. In the following fall andwinter, advance two generations in moderate-temperature glasshouses and short days or in




an off-season field nursery. Finally, in the thirdsummer, performance test selected F8 lines inseveral hot, long-day, commercial production en-vironments.

For any trait used in plant breeding, it is im-portant to determine whether it has any associ-ated traits that are either beneficial or detrimen-tal. The positive and potential negative effectsof heat-tolerance genes in cowpea have beenevaluated (Ismail and Hall 1998). Six pairs ofcowpea lines either having or not having heattolerance during reproductive development butwith similar genetic backgrounds were grown ineight field environments with average night tem-peratures ranging from cool (17◦C) to very hot(28◦C). Heat-tolerant lines had greater first-flushgrain yields in hot and very hot environmentsand similar yields as heat-susceptible lines incooler environments. In hot environments, theheat-tolerant lines had greater pod-set and har-vest index, and dwarfing due to shorter main steminternodes and reduced vegetative shoot biomasswhen compared with heat-susceptible lines. Theheat-tolerant lines were semidwarfed in all envi-ronments where they were tested, ranging frombeing cool to very hot with the greatest dwarf-ing in the hotter environments. These semidwarflines were compared with genetically similarheat-sensitive standard-height lines at three dif-ferent row spacings in four field environmentswith moderate temperatures (Ismail and Hall2000). Average grain yield of standard-heightlines did not respond to row spacing. Semidwarflines produced greater grain yield than standard-height lines at narrow row spacing in soil condi-tions that promoted moderate to vigorous earlyplant growth. The lower grain yields of thestandard-height lines were due to impaired repro-duction when competition for light was strong.Plant morphological relations with heat tolerancewere studied with three heat-susceptible lines,three lines with heat tolerance during both flo-ral bud development and pod-set, and three lineswith heat tolerance during early floral bud de-velopment but heat sensitivity during pod-set(Ismail and Hall 1999). The three lines with

complete heat tolerance were dwarfed, while thethree completely heat-susceptible lines were tall.One of the lines with heat tolerance only duringearly floral development was dwarfed, whereasthe other two lines were tall. These data in-dicate that dwarfing is caused by a gene thathas genetic linkage with the gene responsiblefor heat tolerance during early floral bud de-velopment, a linkage that can be broken, andmay not be associated with heat tolerance duringpod-set.

Reproductive activity of cowpea can be char-acterized by two flushes of pod production sep-arated by a period of two weeks when lit-tle or no flowering occurs (Gwathmey et al.1992). Cowpea growers in the southern SanJoaquin Valley of California often manage thecrop to accumulate two flushes of pods (Halland Frate 1996). Grain yield from the secondflush depends on the extent of plant death due tosoil pathogens after the first flush is completed(Ismail and Hall 1998). Heat tolerance can in-crease first-flush grain yield but may reduce plantsurvival after the first flush is completed (Ismailand Hall 1998). A delayed-leaf-senescence(DLS) trait has been discovered, which enhancesthe extent of plant survival after the first flushin senescence-inducing soils, thereby enhancingsecond-flush grain yield but with a tendency toreduce first-flush grain yield (Gwathmey et al.1992). Four sets with ten lines each were bredwith +/− DLS and +/− heat tolerance and eval-uated in contrasting field environments to test forinteractions between the DLS and heat-tolerancetraits (Ismail et al. 2000). The heat-tolerance traitincreased first-flush grain yield in very hot en-vironments and only slightly enhanced the ten-dency for premature plant death in non-DLS lineswith no effect on lines having the DLS trait.In senescence-inducing soil conditions, the DLStrait greatly increased plant survival and second-flush grain yield, and only caused a small re-duction in first-flush grain yield. Consequently,the DLS and heat-tolerance traits can be effec-tively incorporated into cowpea and would havebeneficial effects on grain yield in the specific




circumstances where they are effective with onlysmall detrimental interactive effects.

Five bush-type edible-pod cowpea cultivars(750, 754, 779, 868, and 1552) were bred atthe Indian Agricultural Research Institute, NewDelhi, India (Patel and Singh 1984). Whenevaluated in an extremely hot, long-day nurs-ery in subtropical California, they exhibited heattolerance during floral development and pod-set(Patel and Hall 1986). In a performance trial con-ducted in a moderately hot, long-day field envi-ronment, their green-pod yields varied between25 and 28 tons ha−1, whereas the US cowpeacultivar Snapea yielded only 13 tons ha−1 anda snapbean (Phaseolus vulgaris) cultivar, Con-tender, gave green-pod yields of only 6.7 tonsha−1 (Patel and Hall 1986). The heat-tolerantedible-pod cowpea cultivars also have a semid-warf habit.

Can cowpea be planted early such that itescapes heat at early flowering?

In principle, early-sown cowpeas that flowerearly could escape the high night temperaturesthat occur in the summer. Current cowpea cul-tivars cannot be sown too early in the spring,however, because they are sensitive to chillingand require a minimum soil temperature greaterthan 18◦C if they are to emerge adequately(Ismail et al. 1997). In addition, the cool nighttemperatures of spring in subtropical zones causecowpeas to develop slowly, and the earliest flow-ering cultivars take about 60 days from sowing tofirst flowering in cool conditions. Some progresshas been made in breeding cowpeas with chillingtolerance during emergence. On the basis of stud-ies with contrasting lines in chilling field condi-tions, Ismail et al. (1997) proposed an additivemodel in which chilling tolerance during emer-gence is conferred by the presence of a specificdehydrin protein in the seed (positive single genenuclear effect) and the extent of electrolyte leak-age from seed under chilling conditions (nega-tive maternal effect) as a measure of membranethermostability. Tests with backcross materials

and molecular genetic (Ismail et al. 1999) andinheritance studies (Ismail and Hall 2002) sup-ported the hypothesis that the dehydrin proteinconfers an increment of chilling tolerance undersingle nuclear gene inheritance. The dehydrinprotein effect was shown to be independent ofthe seed electrolyte leakage effect (Ismail et al.1999). The maternal electrolyte leakage effectwas shown to persist in subsequent generations,indicating it is a nuclear-inherited seed-coat trait(Ismail et al. 1999). Four large sets of cowpealines were screened for the presence of the dehy-drin and for electrolyte leakage from seed underchilling conditions (Ismail and Hall 2002). Thedehydrin was present in many landraces (59%out of 140) that evolved in subtropical zonesaround the Mediterranean Sea where soils oftenare cool during emergence. Surprisingly, how-ever, the dehydrin also was present in most of thetropical accessions (88% out of 59). Only threeout of 61 US cultivars, which had been developedin subtropical zones where soils can be cool,contained the dehydrin protein. Many lines withthe dehydrin protein in their seed are availablefor use in breeding. This trait can be screenedin individual seeds using an immunoblot assayof a chip taken from a cotyledon in a mannerthat does not harm the germination of the seed(Ismail et al. 1999). Genotypes that have sim-ilar slow electrolyte leakage from seeds at lowtemperature as the chilling-tolerant line 1393-2-11 were identified. Heat tolerance during pod-set appears to have some dependence on mem-brane properties, and chilling tolerance duringemergence may depend on different membraneproperties. Consequently, it could be hypothe-sized that it might not be possible to combinethese traits. This does not appear to be the casein that lines have been bred at the University ofCalifornia, Riverside, which have both chillingtolerance during emergence and heat tolerance atpod-set. In germplasm screening studies, no as-sociation was seen between heat tolerance duringemergence, chilling tolerance during emergence,and heat tolerance during flowering (El-Kholyet al. 1997).




Heat stress effects in tropical zones

Detecting heat stress effects on cowpea grownin tropical zones can be difficult due to the nu-merous pests and diseases that damage floralbuds, flowers, pod-set, and developing seeds andpods (Hall et al. 1997). The six pairs of cowpealines with differences in heat tolerance during re-productive development in subtropical environ-ments (Ismail and Hall 1998) were evaluated byfield studies in three locations in the tropical Sa-vanna zone of northern Ghana and three environ-ments in the tropical Sahelian zone of Senegal(Hall et al. 2002). Average daily minimum tem-peratures one week prior to the start of floweringin these tropical zones varied between 21◦C and26◦C, which is much higher than the thresholdminimum night temperature of 17◦C for caus-ing damage to pod-set, indicated by the studiesof Ismail and Hall (1998) in subtropical zones.With the higher night temperatures experiencedin these studies, the heat-tolerant lines developedin California experienced even greater dwarfingthan had occurred in the subtropical zone. In allof the six trials in West Africa, however, therewas no significant difference in grain yield be-tween the averages of the six heat-tolerant linesand the six heat-susceptible lines (Hall et al.2002). In a study that included two more trialsin Senegal, similar results were obtained, and itwas demonstrated that the grain yields of the Cal-ifornia lines were much less than those of well-adapted local cultivars (Cisse 2001). The con-trasting performances of the two sets of lines maybe partially explained by the longer daylengthsexperienced by the plants in Californiacompared with West Africa. Growth chamberstudies had shown that high night tempera-tures can be more damaging to cowpea in long-day than in short-day conditions (Mutters et al.1989a). However, growth chamber studies alsoshowed that high night temperatures can substan-tially reduce pod-set under short days (Muttersand Hall 1992). The heat tolerance of contrastingcowpea lines have been evaluated in glasshouseswith high night temperature and either long or

short days (Ehlers and Hall 1998). Heat-tolerantCalifornia lines had much greater grain yieldsthan heat-susceptible California lines under hot,long-day conditions as had been observed underhot, long-day field conditions in California. Incontrast, in hot, short-day glasshouse conditions,the heat-tolerant and heat-susceptible lines hadsimilar very high grain yields. In West Africa,under hot, short-day field conditions, these twosets of lines gave similar grain yields, but theywere moderate. The moderate levels of grainyield may be explained by the fact that theseCalifornia lines are not well-adapted to WestAfrica. For example, the California lines are toodwarfed in tropical night-temperature conditionsand they are highly susceptible to wet and drypod rots and insect pests. On some occasions,in West Africa, the heat-tolerant California lineswere observed to produce many pods but mostof the pods shriveled due to attacks by pests anddiseases. Screening studies have indicated thatvery high temperatures can damage reproduc-tive development of cowpea in short-day tropi-cal conditions (Singh et al. 2002). A set of 102breeding lines was evaluated in field conditionsat the IITA, Kano Station, from March to Maywhen days were short and temperatures rangedfrom 24◦C to 27◦C at night and from 38◦C to42◦C during the day. Most of the lines exhibitedmuch flower abscission and produced few or nopods with the most susceptible lines not produc-ing pollen. These heat-susceptible lines had pro-duced high yields during the regular croppingseason (July to October) when day and nighttemperatures were cooler. Out of the 102 lines,only four lines were found that had heat toler-ance in that they produced normal pollen andhad good pod-set and high grain yields in theMarch–May field screening. One of the heat-tolerant parents, TVu4552, used to produce theCalifornia heat-tolerant lines, was also evaluatedin this extremely, hot short-day tropical field en-vironment and was found to have high pod-setand grain yield. The other heat-tolerant parent,Prima, has been shown to have heat-tolerance inshort days in growth chamber studies (Craufurd




et al. 1998). The genes in Prima, TVu4552, andthe California lines that confer heat toleranceduring pod-set may be able to enhance pod-setunder tropical conditions, but they need to becombined with additional genes that confer lo-cal adaptation, such as resistance to various pestsand pod rots. The effects of these genes on grainyield may not be as large in hot, short-day trop-ical environments as has been observed in hotsubtropical zones. Some other lines observedto produce high grain yields under hot, short-day conditions by Ehlers and Hall (1998) andSingh et al. (2002) might prove to be more effec-tive parents for providing heat tolerance undertropical conditions, since they already are well-adapted to certain regions in tropical Africa. Theheat-tolerance traits of importance in hot tropi-cal zones include ability to set pods and abilityto maintain many seeds per pod as exhibited byB89-600 from Senegal and TN88-63 from Niger(Ehlers and Hall 1998). There may be a negativecorrelation between these two yield components,however, lines B89-600 and TN88-63 did havelarge grain yields as well as many seeds per podin hot, short-day conditions.

In another approach for developing heat-tolerant lines for tropical zones, Marfo crossedtwo cultivars from Ghana, Sumbrisogla, andVallenga, with two heat-tolerant lines developedat the University of California, Riverside, 518-2 and 148-1, which had TVu4552 and Prima assources of their heat tolerance. He screened seg-regating populations in an extremely hot, long-day field nursery in California, selecting for abil-ity to produce flowers and set pods. He thenscreened the selections in northern Ghana foragronomic traits, subjected them to multiloca-tion performance trials, and selected and releasedtwo cultivars (Padi et al. 2004a, 2004b). Froma breeding standpoint, this approach was effec-tive, but it is not known whether the two newcultivars have any heat tolerance that is effectivein Ghana.

Empirical selection for grain yield in hot re-gions of tropical Africa has produced some cul-tivars (and lines) that glasshouse studies under

short days with high night temperatures (Ehlersand Hall 1998) indicate have some heat toler-ance (e.g., Mouride, B89-600, TN88-63, 58-57,and Suvita 2) and some cultivars that do not (e.g.,Melakh, N’diambour, KN-1, and Sumbrisogla).Apparently, selection for grain yield in hot re-gions of tropical Africa does not necessarilyincorporate heat tolerance, but it has producedsome cultivars that may be useful donors ofheat-tolerance traits. The heat-tolerant cultivarshave good vegetative vigor and have producedlarge grain yields in the Sahelian zone, espe-cially Mouride (Cisse et al. 1995). In additionto having high pod-set, B89-600 and TN88-63have the ability to maintain many seeds per pod.

Empirical selection for high pod yield innorthern India under very hot, long-day fieldenvironments produced bush-type cultivars ofedible-pod cowpeas that were shown to haveheat tolerance during floral bud development andpod-set (Patel and Hall 1986). Some of theselines have performed well in tropical conditionsin Tanzania (Patel et al. 1982). Consequently,these lines may be useful sources of heat toler-ance when breeding bush-type edible-pod cul-tivars for both subtropical and tropical zones.They may not be useful sources of heat tolerancefor the Sesquipedalis edible-pod cultivars thatare extensively used in Asia because of largedifferences in growth habit. The Sesquipedaliscultivars have a vining habit with very long podsand are grown on trellises, while the heat-tolerantcultivars are semidwarfs with a bush habit andshort pods.

Interactive effects of increases inatmospheric [CO2] and global warming

If heat stress effects on reproductive develop-ment of cowpea are caused by heat-induced re-ductions in carbohydrate supply, elevated [CO2]might reduce the heat stress effects through in-creases in photosynthesis. In contrast, if heatstress directly affects reproductive development,then the reduction in demand for carbohydratecould make plants less responsive to elevated




[CO2] due to negative feedback effects on pho-tosynthesis. These contrasting hypotheses weretested in a study in which three cowpea linesdiffering in heat tolerance were subjected to twolevels of [CO2], 350 or 700 μmol mol−1, and twoday/night temperatures, 33/20◦C or 33/30◦C, ingrowth chambers with long days and plantsgrowing in pots (Ahmed et al. 1993a). Under350 μmol mol−1 [CO2] and intermediate nighttemperature (20◦C), all lines set substantial num-bers of pods, whereas at high night temperature(30◦C), one completely heat-sensitive line didnot produce flowers, the partially heat-sensitiveline produced flowers but did not set pods, andthe heat-tolerant line abundantly set pods. Withelevated [CO2] and high night temperature, thecompletely heat-sensitive line still did not pro-duce flowers, the partially heat-sensitive line pro-duced many flowers but still did not producepods, and the heat-tolerant line produced 43%more pods than at ambient [CO2]. These resultsdo not support the hypothesis that heat stresseffects on reproductive development are causedby a shortage of carbohydrates, and direct mea-surements of carbohydrates in tissues supportedthis conclusion. With elevated [CO2] and inter-mediate night temperature, the heat-tolerant lineproduced 50% more pods than it did at ambi-ent [CO2] and 58% more pods than the heat-sensitive lines did at elevated [CO2] and inter-mediate night temperature. The overall resultsare consistent with the hypothesis that heat stressis directly affecting reproductive development inheat-sensitive lines, making them less respon-sive to elevated [CO2]. A completely unexpectedand important result was the fact that the heat-sensitive line was more responsive to elevated[CO2] under intermediate as well as high nighttemperatures. This result is consistent with theobservation that the heat-tolerance genes causecowpea plants to be semidwarfed with higherharvest indexes in intermediate as well as hottemperatures (Ismail and Hall 1998, 2000). Ap-parently, the heat-tolerance genes are enhancingthe reproductive-sink demand of cowpeas grow-ing under a range of temperatures. Consequently,

by developing cowpeas with greater heat toler-ance during reproductive development, it maybe possible to breed cultivars with greater grainyield response to elevated [CO2] under interme-diate or high night temperatures. This importantconclusion is based on the results from only onestudy with only three cowpea lines growing inpots in growth chambers (Ahmed et al. 1993a).More studies of [CO2] × temperature interac-tions are needed with a larger number of cowpealines and, if possible, they should be conductedunder field conditions.

Conclusions

For subtropical zones, effective methods andbreeding lines that will facilitate breeding cow-pea for future climates have been developed. Acowpea cultivar and various lines that are heattolerant during floral bud development and pod-set have been bred, and they may also be moreresponsive to elevated [CO2] in terms of grainyield. This cultivar and the lines are semidwarfsand appear to be most effective when grown atnarrower row spacing than is the current prac-tice. Edible-pod cowpea cultivars that have heattolerance and abundantly produce pods in hotenvironments have been bred. They also havea semidwarf habit. Cowpea cultivars that haveheat tolerance during reproductive developmentand also are more vegetatively vigorous thanthe semidwarfs should be bred. This might beachieved by using, as a parent, one of the linesthat was identified as having heat tolerance dur-ing floral bud development, no dwarfing, and ad-equate vegetative vigor. Vegetatively vigorous,heat-tolerant cultivars would be useful in manyparts of the subtropical zone and in the tropi-cal zone. However, the high reproductive sinkto photosynthetic source hypothesis predicts thatvegetatively vigorous heat-tolerant cultivars maynot be as responsive to elevated [CO2] as theheat-tolerant semidwarfs, but more tests of re-sponses to elevated [CO2] by contrasting cowpeacultivars are needed to more comprehensivelytest this hypothesis.




For tropical zones, the main priorities for cow-pea breeders should be to breed for resistances tocurrent biotic stresses, especially in West Africa,where there is the major area of cowpea produc-tion. In West Africa, there are many insect pests,and some diseases, that damage floral buds, flow-ers, pod-set, and grain and pod development.Once resistances to the major insect pests anddiseases have been pyramided into cultivars, itwould be appropriate to begin breeding for heattolerance. One objective would be to breed heat-tolerant cowpeas that also have adequate vegeta-tive vigor. The most effective donors of heat tol-erance for tropical zones should be determined,including evaluating lines identified as havinghigh pod-set, numbers of seed per pod, and grainyield in hot, short-day field and glasshouse en-vironments that also are vegetatively vigorous.Possibly, lines with heat tolerance during floralbud development should be avoided since thistrait may have little value in short-day tropicalenvironments and may be associated with dwarf-ing through close genetic linkage in some geno-types. In tropical zones, the useful heat-toleranttraits include high pod-set and maintenance ofmany seeds per pod. Ideally, breeding and selec-tion for these traits should be conducted in theregion where the cultivar will be grown. If anyparents differ in leaf electrolyte leakage underheat stress, this test should be used to try to in-corporate heat tolerance during pod-set becausedirect selection for high pod-set can be difficultin much of West Africa due to the presence ofseveral biotic stresses that influence pod-set. Ef-fective field selection for pod-set and many seedsper pod might be possible during the croppingseason in the Sahelian zone, where there usuallyare fewer pests and diseases of cowpea than inthe wetter Savanna zones. Also, field selectionfor pod-set and for many seeds per pod might beeffective in the dry season, with irrigated plants,in locations and times when temperatures canbe very high, such as Kano, Nigeria, betweenMarch and May. In these field nurseries, pestsand diseases that damage reproductive devel-opment should be controlled or it may not be

possible to detect differences in heat tolerancereliably.

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crop adaptation to climate change (yadav/crop adaptation to climate change) || breeding cowpea for...

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