Euphytica73: 151-166,1994 .

151© 1994 Kluwer Academic Publishers . Printed in the Netherlands .

Present status and future strategy in breeding faba beans (Vicia Faba L .) forresistance to biotic and abiotic stresses

D. A. Bond', G . J. Jellis', G. G. Rowland2 , J. Le Guen3 , L. D . Robertson', S . A. Khalil 5 &L. Li-Juan6'Plant Breeding International Cambridge, Maris Lane, Trumpington, Cambridge CB2 2LQ, UK; 2Crop Develop-ment Centre, University of Saskatchewan, Saskatoon, Saskatchewan, S7N OWO Canada ; 3Station d'Ameliorationdes Plantes, INRA, Le Rheu, France ; 4Genetic Resources Unit, ICARDA, P O . Box 5466, Aleppo, Syria ; 5FieldCrop Research Institute, Research Section, Agricultural Research Center, P O . Box 12619, Giza, Egypt, and 6FabaBean Germplasm and Breeding, Zhejiang Academy of Agricultural Sciences, Hangzhou, China

Key words : Vicia faba, faba bean, breeding, biotic stress, Abiotic stress, Botrytis, Ascochyta, Uromyces, Orobanche,drought, frost, high temperatures, resistance

Abstract

Progress is being made, mainly by ICARDA but also elsewhere, in breeding for resistance to Botrytis, Ascochyta,Uromyces, and Orobanche ; and some lines have resistance to more than one pathogen . The strategy is to extendmultiple resistance but also to seek new and durable forms of resistance . Internationally coordinated programs areneeded to maintain the momentum of this work .

Tolerance of abiotic stresses leads to types suited to dry or cold environments rather than broad adaptability,but in this cross-pollinated species, the more hybrid vigor expressed by a cultivar, the more it is likely to toleratevarious stresses .

Introduction

Faba bean is a valuable protein-rich food that has sus-tained large human populations and provides an alter-native to soybean meal for animal feed in temperateregions, but the total area in the world is declining(3 .7 m ha in 1979-81 to 3 .2 m in 1989), partly due tounreliable yields .

It is a plant that is capable of heavy yields butis sensitive to stress, and because of economic pres-sures, growers are increasingly reluctant to take therisk of poor returns from the crop . The contributionthat plant breeding is making towards the alleviationof this problem was recently reviewed by Robertson &Saxena (1993), but in this paper we have taken reportsfrom seven authors covering a wider geographical areafrom which we hope to provide an overview of the sta-tus of breeding for resistance to stress and to discusshow strategies may develop .

The biotic stresses that we examined included themajor pests and pathogens ; also the effect of stress onorganisms that are normally beneficial to faba beans .Abiotic stresses were mainly to do with the effect ofextremes of temperature and humidity .

The aim was also to consider the impact of changesthat are occurring in breeding objectives, such as nutri-tional quality and in breeding methods, on the plant'sability to tolerate stresses . Though each stress wasexpected to vary in importance among the regions, afinal goal of this review was to try to identify commonproblems and strategies to tackle them, particularlywhere international collaboration might lead to a morespeedy solution than parochial endeavors .

First, each type of stress was considered for someof the regions where it is known to have importance .Authors have first hand experience of faba beans inUK, France, North Africa, the Middle East, China,

1 52

Fig. 1 . Generally recognised centres of diversity and sources of chocolate spot resistance . 40 putative centre of origin ; • secondary centres ofdiversity ; o sources of chocolate spot resistance ; • • • ancient region of cultivation of V.faba ; 0 region of winter hardy types .

North America, and countries in the ICARDA sphereof influence .

Biotic stresses

Chocolate spot (Botrytis fabae and B. cinerea)

This has been for many years one of the mostwidespread and potentially devastating diseases of fababeans. Yield losses can be heavy where luxuriant veg-etative growth and a humid microclimate allow thefungus to go into its aggressive stage . Thus, it is mostfrequently reported from humid regions such as theNile Delta, Yangtse valley, rainy coastal areas of theMediterranean, and the more oceanic climate of west-ern France and western UK .

In view of this, it is remarkable that the most con-sistently resistant accessions (ICARDA lines BPL 710and BPL 1179) have come from close to a mountain-ous region in Ecuador (Figure 1) where there havebeen only about 300 years for resistance to evolve . Weattribute this to wide general genetic variation intro-duced by Spanish settlers, adaptation to extremely var-ied environments within short distances due to alti-tude, frequent gene exchanges by insect pollinators andmovement of peoples, and natural screening for resis-tance in the more humid of those environments . Fur-

ther collections from the same region have been mademore recently and new sources of resistance obtained(Hanounik & Robertson, 1988) .

The resistance of the original source (ILB 938 =BPL 1179) (Table 1) was first confirmed in the NileDelta and, after crossing there to the local cultivarGiza 3, has now been transferred to locally adaptedmaterial and released as "Giza 461" . Diallel crosses inEgypt indicated that dominant, additive, and reciprocalgene effects for resistance were stable over a number ofyears. ICARDA has also successfully transferred BPL710 resistance into other well adapted genetic stocks,including a Moroccan base, and to alternative planttypes like determinate habit and independent vascularsupply .

However, the transfer of BPL 710 type resistanceinto the more widely divergent backgrounds of Frenchand English winter hardy faba beans is proving moredifficult and a slower process . The genotype BPL 710is resistant when spring sown in France or Englandand in all other ICARDA locations, but differences insusceptibility among winter beans in those two coun-tries are much less reproducible (Table 2) . Lines thatappear resistant as seedlings or when the disease isnon-aggressive are often susceptible as adult plantsor in the presence of aggressive Botrytis (Figure 2) .Detached-leaf test data do not always correlate withfield observations (Harrison, 1981 ; Tivoli et al., 1986) .

Table 1 . Sources of resistance to major pathogens

153

Disease orpest

Source (underline = highly resistant) Origin

Chocolate BPL 110, 112 UKspot BPL 261,266 Greece

BPL 710, 1179, ILB 3025, 3026, 2282 EcuadorBPL 1196 SpainBPL 1278 SyriaBPL 1821, 1763 EthiopiaL83114, L82003, L82009 ICARDA*

Ascochyta

Zhehiang 41 LAO, Qi Dou No . 2, Lu-Xiao-Li-Zhong

BPL 74

China

Iraqblight BPL 230, 365 Morocco

BPL 460, 465, 471, 472 LebanonBPL 818 EthiopiaBPL 266 GreeceBPL 646, 2485, ILB 752, L83118, 3120, 3124 ICARDA*L8 3125, 3127, 3129, 3136, 3142, 3149, 3151, 3155 ICARDA*L83156,2001,31818-1 ICARDA*Quasar, Line 22429H

UKFrance

Rust BPL 7,8 JordanBPL 260, 261, 263 GreeceBPL 309 TurkeyBPL 406, 417, 427, 490 SpainBPL 484 UruguayBPL 524 JapanBPL 533 USABPL 539, Qi Dou No . 282-15563

ChinaCanada

BPL 552 IranBPL 554, 567, 571, 573, 576, 588, 604, 610 EgyptBPL 627 AlgeriaBPL 649, 663, 665, 667, 680 TunisiaBPL 640,643 UKBPL 702 Sudan

Stem BPL I, 10, 11, 12 Jordannematode BPL 21, 23, 26, 27, 40 Syria

BPL 63,88 IraqBPL 183 Afghanistan29H France1827, 1698, 1696, 84, 154 ICARDA*

BYMV BPL 1584, 1567, 2875, 1592, 1530, 1541, 1581 ICARDA*1597,1351,1363,1366,1371

1 54

a

6

4

2

0

Disease score (0-9)

0 10 20

30

40

50Days (day 1 • first score)

Line 335 -'- Line 224

* ICARDA: Lines selected by ICARDA

60

Fig. 2 . Scores for Botrytis infection after inoculation of two inbredlines at Cambridge, UK.

Defoliation due to infection is not always related tospread from lesions, extent of crop damage in the fieldcan be more a consequence of the amount of sporula-tion on fallen and senesced leaves that re-infect greenplants than of rate of disease spread in the live canopy(Gondran, 1975) .

The effect of chocolate spot can, however, be ame-liorated by breeding for (a) early flowering so thatmost pods are set before the disease goes aggressive(cv Punch escapes some chocolate spot in UK thisway), (b) slow leaf senescence, (c) open canopy or (d)resistance to predisposing factors such as frost or virusdamage. Inbreeding often uncovers greater suscepti-bility than in existing populations, so a high level ofheterozygosity should be maintained .

The BPL 710 resistance is thought to be quanti-tative rather than qualitative (Robertson & Saxena,1992) and additive with some dominance (El-Hady

70

Mohamed, 1988) so it is not surprising that it is diffi-cult to transfer all the genes concerned to widely differ-ent backgrounds. Up to 21 other sources of resistancehave been identified by ICARDA and there are threegenotypes from China with some resistance (Table 1)but most of these do not have as high a level of resis-tance or have been shown to be susceptible in certaincountries (Halila et al ., 1990). Existence of races ofB.fabae has been proposed on the basis of the reactionof five differentials in seven Mediterranean countriesbut confirmation is needed from tests of all sources ofinoculum on the putative differentials in the same envi-ronment because quantitative resistance is often highlyinfluenced by environment .

On limited evidence BPL 710 resistance seemsdurable, and other sources have incomplete resistanceor field resistance so the future strategy should be strictmonitoring of durability of resistance, and the main-taining of bean cultivars as mixed populations whichrarely challenge the pathogen .

Ascochyta blight (Ascochyta fabae)

Average yield losses due to Ascochyta (5 to 50% inPoland, Zakrweska, 1986 ; 7.5 to 41% in Czechoslo-vakia, Ondrej, 1991) are less than for Botrytis butAscochyta can spread under cooler and drier condi-tions, and can be seedborne, so resistance is importantnot only to reduce biotic stress but also to avoid quar-antine and (in the UK) seed certification problems .

Resistance has been found in wider backgrounds,results of tests more positive and reliable (Table 2),and the situation on races clearer than with Botry-tis. In addition to 24 sources of resistance listed by

Table 1 . Continued

Disease or Source (underline = highly resistant) Originpest

Orobanche Giza 402, BPL 241 Egypt2830,18105,2210,18009,18035,18049 N. Africa15-2-5,(402 x INIA 06) x 402 N. AfricaChiaro TL GreeceBaraca Spain

Aphids BPL 23 ICARDA*Rastatt GermanyLine 14 UK

Table 2 . Ranking of five lines, out of a group of 10, for resistance to chocolatespot and Ascochyta at Rennes (1 = resistant)

Disease

Chocolate spot

Detached leafspots after 15 h

spots per hscore after 6 days

Plants in pots

young plantflowering stage Yr 1

flowering stage Yr 2Field assessment

disease scoreflower damage Yr 1

flower damage Yr 2

Ascochyta blightAdult plant

leaf (Year 1)stem (Year 1)

leaf (Year 2)

% damaged stems (Yr 2)% damaged pods (Yr 2)

Young plantleaves (Year 1)

pods(Year1)Flowering stages

leaves (Year 1)pods (Year 1)

ICARDA (Hanounik & Robertson, 1988; and Table 1),lines with good resistance have been found in adaptedmaterial in France (Line 29H), England ("Quasar"),and in Poland ("Fioletowy" and "Czyzowskich" seeZakrzewska, 1986) .

Thus there are fewer places where resistance needsto be transferred between diverse types . However, useof the ICARDA lines, especially BPL 471, 460, 74and 2485, has already been made in various countriesand at ICARDA with the objective of combining resis-tance with improved plant architecture (Robertson &Hanounik, 1987 ; Hanounik & Robertson, 1989). Also,as there is evidence of differential interactions betweenfaba bean genotypes and isolates of A. fabae(Hanounik& Robertson,1988, 1989 ; Halila et al ., 1990; Rashid etal ., 1991), there is a possibility of a breakdown in resis-tance and therefore a need for more than one sourcein each breeding program . Some European breeders,

1 55

for example, are therefore adopting a strategy of utiliz-ing resistance found in Mediterranean as well as localcultivars. BPL 471 is thought to carry a broad basedgeneral resistance compared with a narrow based resis-tance in BPL 818 (Hanounik & Robertson, 1989) . Butdurability of the present best sources of resistance alsoneeds constant monitoring .

Resistance has been observed in tannin-free as wellas tannin-containing cultivars but a suggestion that seedtransmission may be more frequent in tannin-free cul-tivars requires investigation (Jellis et al ., 1991) .

Rust (Uromyces fabae)

Though previously considered of secondary impor-tance because the disease appeared late in the life ofthe host plant, recent estimates of yield loss are up to80% in China and 27 to 32% in UK (Yeoman et al .,

29H Bourdon Soravi 3 .33 48B

10 5 6 8 9

9 3 8 10 7l 7 2 9 10

9 4 8 4 52 7 3 10 9

6 7 1 9 10

9 2 3 10 59 2 3 10 5

8 1 5 3 9

3 4 6 8 93 4 7 8 10

3 4 6 8 10

2 4 7 6 101 4 6 7 10

2 4 6 9 8

2 4 5 9 10

2 4 9 10 82 8 9 3 10

156

1987; Dobson & Giltrap, 1991) . Appearances of thedisease earlier in the season in northwest Europe havebeen associated with the introduction there of earliermaturing cultivars .

Race-specific resistance controlled by major geneswas established by Conner & Bernier (1982) andRashid & Bernier (1986), and only one of 65 linesselected by them (Line 82L-15563-1) was rated asresistant in the field in Syria (Hanounik & Robertson,1988) .

The postulate of Conner & Bernier (1982) that aquantitative form of resistance ("slow rusting") wouldbe more durable than race specific immunity has sofar been upheld. Most of the resistant lines bred byICARDA (Table 1) probably have this slow rustingtype of resistance. Thus, unless facilities are availablefor continuous study and prediction of races before theyappear in nature, the best strategy is to utilize lines withproven field resistance . BPL 261, for example, is beingused in crosses in Europe.

Downy mildew (Peronospora fabae)

This was not seen to any extent until about 1985,but now occurs in most faba bean trials in northwestEurope . Clear genotypic differences in susceptibilityexist with, for example, Marts Bead being resistantand Troy susceptible . Little breeding is being done buta basis for improvement exists .

Foot rot (Fusarium solani and other Fusarium spp .)and wilt (F. oxysporum)

These diseases are soilborne so yield losses maydepend on the frequency of faba beans in the rota-tion . In China, where foot rots and wilts are next inimportance after Botrytis (Liang, 1989), it was esti-mated that Fusarium foot rot was responsible for 6%loss in the first year of faba bean but 38% loss with con-tinuous beans . In general, the extent of damage is ofteninfluenced by concurrent abiotic stresses like waterlog-ging, soil compaction, heat, and drought . However inRussia "Burshtyn 56" was reported resistant (Yartiev,1976), and tolerance was reported in Germany for ahomozygous line, KK13, selected from the Austrian cvKornberger Kleinkornige. KK13 is being used in jointEEC-program crosses . Yield of tannin-free genotypesis low in the presence of Fusarium infection (Link &Hempel, 1992), and the tannin-free member of somenear isogenic pairs is more susceptible to Fusariumspp. than the tannin-containing member, especially in

stressed soil conditions like low temperature and highmoisture (Kantar, 1992) . On the other hand, resistancecan also be selected in zero-tannin lines (van Loon etal ., 1989; Pascual Villalobos & Jellis, 1990) .

Inbreeding in populations can often reveal lines thatare significantly more susceptible than the mean ofthe population . Thus a method of maintaining existingtolerance of stress and of Fusarium is to breed cultivarswith a good level of heterogeneity and which displayheterosis .

Stem rot (Sclerotinia trifoliorum and S . sclerotiorum)

This is a major stress factor only when other susceptiblecrops occur frequently in the rotation. In the UK, winterfaba beans are affected only by S. trifoliorum (Jellis etal ., 1990) but infections of S. sclerotiorum on springfaba beans restrict entry of rapeseed, linseed, and peain the rotation .

In Greece, damage has been serious enough to pro-mote a breeding program . Resistance has been report-ed in Lines KU 189, 190, and 191 (Podimatas, Pers .comm. 1990). But more investigations are needed torelate laboratory tests to field observations .

Viruses

There are a large number of viruses contributing to biot-ic stress and it would be almost impossible to breed forresistance to all of them . Annual average yield losses inGermany were estimated as 8% (Schmidt, 1984) . Inci-dences were : bean yellow mosaic virus (BYMV) 13%,pea enation mosaic virus (PEMV) 5%, bean leaf rollvirus (BLRV) 3%, and the seed and weevil transmit-ted viruses, true broad bean mosaic virus (TBBMV),and broad bean stain virus (BBSV), about 0.5%. Sim-ilar incidences were reported in Poland (Blaszczak &Fiedorow, 1979) ; but, in France and the UK, BLRV isrelatively more important.

ICARDA found two accessions from Afghanistanto be resistant to BLRV (BPL 756 and 758), and fourlines with resistance to BYMV (BPL 1351, 1363,1366,and 1371) (Robertson & Saxena, 1993 ; and Table1). Two other independent sources of resistance toBYMV were reported by Rohloff & Stulpnagel (1984) .Schmidt et al . (1986) described a line that combinesresistance to 11 strains of BYMV with some resistanceto Aphis fabae, while Schmidt et al . (1989) wrote of aline with resistance to both BYMV and PEMV (Table3) . In the UK, the common cultivars have varied sig-nificantly in frequency of plants infected with BLRV,

Maris Bead and Wierboon being among the more resis-tant (Lawes et al ., 1983). No resistance to the seedtransmitted viruses is known, so care has to be takenwith quarantine .

In many countries viruses are not damaging oftenenough to warrant priority in breeding programs . Themain strategy is to attempt to combine resistance tothe common viruses with resistance to another majorstress factor.

Stem nematode (Ditylenchus dipsaci)

The giant faba bean race is important in Morocco andcould be in other countries if control over crop rota-tions and checking for seed infection is relaxed . TwelveICARDA lines have some resistance (Hanounik etal ., 1986 ; Robertson & Saxena, 1993), and this wasconfirmed for BPL 1696 and 1827 and FLIP 84-154(Caubel & Leclercq, 1989) but only the French INRAline, 29H, has a high level of resistance (Caubel & LeGuen, 1992) . This is controlled by a single gene and isinherited maternally through 29H cytoplasm .

Breeding may commence in France, while Moroc-co should utilize ICARDA sources of resistance, butotherwise control will mainly be by clean seed (quar-antine in countries where the nematode does not exist)and long rotations .

Broomrape (Orobanche crenata)

Orobanche is a major stress factor in many Mediter-ranean countries . Resistance of "Giza 402" (Nassibet al ., 1982) has proved useful in upper Egypt whereBotrytis is not a problem, but because Giza 402 issusceptible to Botrytis and is unadapted to the west-ern Mediterranean region other sources of resistanceto Orobanche are being sought . Also resistance ofGiza 402 has been partly attributed to late floweringand late stimulation of O. crenata to germinate (Kheiret al ., 1989), or to low root biomass (Khaled & El-Bastewesy, 1989), so different mechanisms of resis-tance are required .

Screening in Morocco resulted in BPL 2830 beingrated as resistant, but progress is most likely amongselections from crosses of the best from the Spanish(Cubero et al ., 1988) and from the Egyptian programse.g ., (402 x INIA 06) x 402 (Robertson & Saxena,1992) or the cross VF 1071 (402 derivative) x "Bro-cal" which gave the resistant cv Baraca (Cubero et al .,1992). Several of these are proving to be resistant inSpain, Morocco, Algeria, and Syria though with lower

6

5

4

3

2

0

= Faba bean yield

I

ama -18032-2 18049-6 15-2-5 18029-2 16049-6 18029-3 15-3-6

Variety

(ICARDA FLIP Annual Report 1990)

Fig, 3. Performance of Orobanche-resistant lines in a naturallyinfested field in Morocco .

resistance to O. foetida in Tunisia (Hanounik et al .,1992; Kharrat et al ., 1992). In Morocco none of the13 lines tested in 1989/90 and 1990/91 averaged morethan 1 .2 shoots or 2 .2 g of shoots per host plant com-pared with 8.9 and 18.7 g respectively for the control,"Aquadulce". This difference was reflected in a muchhigher yield for the selected lines (Figure 3) . Anotherpossible source of resistance is "Chiaro TL', a cultivarthat was significantly less susceptible than 11 others inGreece (Karamanos & Avgoulas, 1989) .

Mutation breeding (with gamma rays and EMS)also produced some resistance which appeared to beunder polygenic control (Hussein et al ., 1988) but fur-ther single plant selection was necessary in the sameway that it was among populations collected in Egypt.BPL 241 was resistant but other bean lines were tol-erant of only some Orobanche accessions (Radwan etal ., 1988) .

Inheritance of the Giza 402 type of resistance isstrongly additive so the most appropriate breedingmethod is recurrent selection following intercrosses ofselected F2 or backcross plants from original resistant xsusceptible crosses (Cubero et al., 1988). Strict controlof pollination and continuous selection are necessaryto prevent dilution of the resistance . However, effec-tive use of the present resistance to Orobanche alsoinvolves integration with other control measures likeplanting date and herbicides . Susceptible cultivars haveto be sown late, e.g ., January, to avoid Orobanche, andthereby suffer a yield loss, but a resistant cultivar couldbe sown at the normal, early high-yield producing date(Figure 4) . In Morocco in 1991, resistant lines had less

0\\\0\ No shoots/host plant

1 57

1 58

Table 3 . Examples of Multiple Resistance

* I = Botrytis, 2 = Ascochyta, 3 = Uromyces, 4 = Alternaria,5 = Peronspora, 6 = Ditylenchu s, 7 = Aphis craccivora, 8 = A . fabae,9 = BYMV, 10 = PEMV, 11 = Fusarium, 12 = Orobanche R = resistant

need of herbicide to give their maximum yield thandid the susceptible control (Figure 5) . A combinationof herbicide, resistant cultivar, early sowing date andappropriate plant density are likely to give the highestyield .

Aphids (Aphis fabae, A . craccivora)

Oi1.1 .,

W °1,06-a- vqu-1,01

Orobanche/plant

Faba bean plants are under considerable stress once500

sap-sucking aphids start to multiply . Insecticides arerelatively inexpensive so resistance breeding has notreceived priority. However, it may be needed whereaphicides are uneconomic or prohibited .

Host-aphid relationships are complex leading todifficulties in assessing resistance (Klinghauf, 1982); Fig. 4 . Effect of planting date and genotype on Orobanche infesta-for example, "Bolero" was clearly more resistant than

tion and yield .

"Diana" at 20 °C but not at lower temperatures (Zebitzet al ., 1988). Nevertheless, the resistance of "Rastatt"to A. fabae (Muller, 1968) and also one of its deriva-

The yield of untreated resistant lines, however, was lesstives, Line 14, (Bond & Lowe, 1978) was established .

than that of susceptible lines treated with aphicides .In Egypt, over 1000 lines were screened for resis-

tance to A . craccivora and 36 classified as resis-

dbn .V7

o, .1 . .cn.-•6.w.m . G7 orowe.n.-wo66-~- Vi .16•bw .ulc .

4- y1.10-,1006

Pathogen/Pest*Lines 1 2 3 4 5 6 7 8 9 10 11

12

L82003 R RL82005 R R RL82006 R R RL82007 R R RL82010 R RL82013 R R

BPL 261 R RBPL 1179 R R R RQi Dou 2 R R29H R RBPL 23 R R RBPL 26 R R

88123 R R

8810 R R

8817 R R

Schmidt 1989Schmidt 1986Nadwislanski R R

RRR

R

R

18105

Yield - a pray

O orobanche - .pray

Fig . 5. Effect of herbicide and genotype on Orobanche infestationand yield .

tant. Plastic house screening against A. fabae in Syriarevealed 5 resistant lines . BPL 23 was resistant to bothaphid species and to stem nematode (Table 3). Otherswere resistant to an aphid and also to Botrytis (Bisharaet al ., 1989). The yielding ability of these lines in thepresence and absence of aphids needs to be measuredbut, if good, the way is open to develop a strategy ofmultiple resistance that includes aphid resistance .

In the long term, when biotechnology has advancedto the stage of transferring genes from other Viciaspecies, the aim should be to utilize the very highlevels of resistance to aphids in wild relatives (Birch,1985) .

Weed competition

Where herbicides are not applied, or are only partlyeffective, weed competition can be a major stress thatlimits yield of faba beans . Breeders can contribute byproviding cultivars that are vigorous enough to com-pete with weeds . In particular, shading by an early-closing canopy can much reduce growth of late germi-nating weeds when early weed growth has been con-trolled by pre-sowing cultivations or by non-persistentherbicides .

The most competitive cultivars are usually largerseeded than others within their botanical group and areheterotic due to being in a hybrid or composite pop-ulation. Weed competition is often worst in low plantdensities of pathways and perimeters of fields, so a cul-tivar needs to tolerate high plant densities without therisk of yield loss . This implies good resistance to dis-eases, especially chocolate spot, that spread rapidly athigh plant densities, and also good autofertility in case

Aquadulce

Yield - no *prey

Orooanche - no spray

18035

bees cannot penetrate the dense canopy at floweringtime.

Pollination

Robertson & Saxena (1993) pointed out that stressaffects pollinators which in turn affect yield and vig-or of bean stocks . The answer is to breed autofertilecultivars which can set seed independently of bee visi-tation but which, given the opportunity, can also crosspollinate and maintain vigor .

There are a number of sources of autofertility (Han-na & Lawes, 1967; Poulsen, 1980 ; Robertson & El-Sherbeeny, 1988) and it is well known that most Fthybrids are more autofertile than their parents (Drayn-er, 1959; Holden & Bond, 1960; Salih & Ali, 1989 ;Link, 1990) . The latter type is almost impossible tofix in an inbred line. The process of transferring thefixable types of autofertility, those that are thought tobe controlled by relatively few genes, is hampered bythe need to distinguish plants in segregating popula-tions that carry the fixable genes from those that areautofertile because of general heterosis . For this reasonprogress is slow but some breeding programs are nowachieving improvements in autofertility .

Symbiosis with Rhizobium

Ineffective strains of R. leguminosarum could causestress to faba bean plants . Fortunately most strains infaba-bean growing areas are effective but there maybe stress in soils where V faba has not been grownbefore. Interaction between faba bean line and Rhizo-bium strain has been demonstrated (Lawes et al ., 1978)and improvement in Rhizobium for nitrogen fixationhas been induced (Shukkla et al ., 1986) but translat-ing these results into practice depends on stability andcompetitiveness of new strains (even if they are suitedto a particular faba bean genotype) in the field .

The importance of Rhizobium to V. faba wasdemonstrated by the yield benefits, up to 14%, obtainedby insecticidal control of Sitona larvae that feed on theRhizobium nodules (Bardner et al ., 1982) . Thus thisis another way in which stress can be relieved but weknow of no resistance to Sitona .

1 59

160

Abiotic stresses

Drought

The faba bean plant requires a large amount of waterto support its erect stem and retain turgor in its fleshyleaves. It is therefore prone to drought stress but, whererainfall is fairly predictable, adaptation to a dry cli-mate has been associated with a plant architecture thatcan minimize this stress . For example, the continentalclimate of eastern Europe, including Austria, favorstall late maturing types like "Gobo", "Erfano" and"Frinebo". These sometimes lodge and suffer muchflower-drop on fertile soils with higher rainfall in west-ern Europe where short, early types are now more pop-ular. However, drought stress can severely limit yieldsin seasons when rainfall is lacking in regions that arenormally wet . Then the short early types suffer most .Care is needed in extrapolating this conclusion to oth-er environments . Whereas Van Noel (1985) in Hollandconcluded that drought tolerance was lower in earlylines, Ricciardi (1989b) wrote that early genotypes arebetter adapted to drought stress in Italy . Determinatehabit reduces excessive growth in wet conditions buthas not been associated with any drought tolerance .However, as autofertility of moderately autofertile cvsis reduced during drought (Stoddard, 1986), improve-ments in intrinsic levels of autofertility might amelio-rate effects of drought .

Breeding is mainly a matter of testing advancedlines under dry conditions and aiming for maximumwater use efficiency at given plant densities and rowspacing (Robertson & Saxena, 1993) . Water use effi-ciency is not as good as in pea, so there is need forimprovement, and recurrent selection in random mat-ing populations is being practiced in Canada . Droughtstress is common in spring faba bean in northern Chinaand any part of the Mediterranean area where it cannotbe avoided by early sowing .

In seeking drought resistance, breeders can eitheraim for drought avoidance or tolerance (Van der Wal,1981). Drought avoidance is not only selecting forrapid early growth but can be approached by extendingthe root system or by saving water through stomata]control . True drought tolerance is in plants that canendure low internal water potential, e.g., by dehydra-tion tolerance or osmoregulation . Osmotic adjustmentwas considered to account for drought-tolerance dif-ferences at the Centre for Plant Breeding and Repro-duction Research at Wageningen in 1987, and Soja etal. (1988) found that screening seedlings in nutrient

solution with variable osmotic stress correlated withyield under stress in the field .

Direct observations on root growth have beenmade through transparent tubes (El-Shazly & Warboys,1989) and thick roots found to be associated with rapidwilting (Harrewijn & van Norel, 1986) . Other tech-niques are to control water in field plots and monitorwater potential with lysimeters or to construct a binthat gives a gradient for rooting depth and select geno-types that can tolerate shallow rooting (Van der Wal,1981). However, in some soils, rooting volume can bemore closely related to drought tolerance than rootingdepth .

Stomatal size and frequency vary among genotypes(Nerkar et al ., 1981) and stomata] density can be neg-atively correlated with yield under stress conditions(Ricciardi, 1989a) though not always (Ricciardi &Steduto, 1988). Metabolic markers of drought toler-ance being investigated at Rennes, France, includethe role of proline accumulation in DOPA (3,4-dehydroxyphenylalanine) degradation . This is estimat-ed from leaf discs in polyethyleneglycol and NaCI solu-tion .

For arid conditions there is a role for fundamen-tal research as well as breeding. Though differencesamong present genotypes exist, heritability is oftenlow (Nanda et al ., 1988) and inbreeding depressionresults in lower yields in stress conditions (Milews-ka, 1988). So far as conclusions can be drawn, ILB1814, 80S43856, and 80L90121 were reported as hav-ing good water use efficiency (Robertson & Saxena,1993), JV-37 performed well in stress conditions (Nan-da et al., 1988), while Nadwislanski and Mazur weredrought tolerant in Poland (Tomashevski & Yanushe-vich, 1975) .

Waterlogging

Excess water on autumn sown beans is common insouthern China and this results in damage to the crop .Elsewhere it is sometimes associated with excessivesoil consolidation which can cause up to 48% yieldloss (Dawkins & Brereton, 1984) . We know of no cul-tivar tolerance to waterlogging ; the problem is bestapproached through resistance to foot rot (Fusariumspp. and Pythium spp .) and interpollinating popula-tions that have the vigor to penetrate poorly structuredsoil .

Low temperatures

Frost on seedlingsThere are three distinct areas where V faba is autumnsown and which differ in degrees of hardiness for thecommonly grown cultivars .(a) England, northern France and a very small amount

in Germany . Cultivars tolerate about - 18°C .

(b) Southern and western France, and northern Spainwhere cultivars are earlier maturing but less hardy,tolerating about - 12 °C .

(c) Mediterranean countries with a cultivar toleranceof about - 6° C, distinguishing them from Africancultivars with almost no frost tolerance .

Most spring sown European and Chinese cultivars fallin category (c) or (b) . There are also differences in frostresistance among cultivars in the Mediterranean area,Aquadulce, "ILB 3187" and "3188" being among themost hardy (Herzog & Saxena, 1988) but they are notas hardy as the majority of cultivars in areas (a) and(b) .

Breeding for improved hardiness in area (a) hasbeen attempted but the very hardy "Cote d'Or"(France) is very susceptible to Botrytis and the veryhardy "Hiverna" and "Webo" (Germany) are suscepti-ble to Ascochyta . Large scale breeding would be need-ed to combine hardiness with disease resistance .

More promising is the improvement in hardiness ofthe early maturing cultivars in category (b) by cross-ing with the hardy late maturing cultivars of category(a) . In addition, selection in populations from cross-es of French cultivars from area (a) by winter pop-ulations from Spain, Greece, and Italy has producedrecombinants that have the hardiness of "Soravi" and"Bourdon", yet are 15 to 20 days earlier. These resultswere obtained under controlled conditions . Some ofthe effort involved in exposing lines to controlled lowtemperatures, or in waiting for real winters, could beavoided because 64% of the genotypic variation in frostresistance can be attributed to correlation with easilymeasured traits like rate of development, water/drymatter ratio and leaf area (Herzog & Saxena, 1988) .

Eventually however, survivors of low temperaturetests have to experience real winters . Hardiness alsoinvolves the ability to harden in the autumn, largereserves in cotyledons to allow rapid root growth intowarmer layers of the soil, ability to withstand desicca-tion from drying winds, and ability to recover in thespring by tittering rapidly . Cultivars that survived bestfollowing the 1984/85 winter in England were "Box-

er", "Throws MS" and "Webo" . Large seeded typessurvived better than small seeded, and in an F, diallelof four inbreds, F, hybrids were less damaged thantheir mid-parental values (Bond et al ., 1986) ; anotherinstance of heterosis contributing to tolerance of abi-otic stress .

Frost on flowersIn Mediterranean areas early sowing is necessaryto avoid spring and summer drought but this canexpose faba bean flowers to damage with loss of yieldand/or late ripening . Hardiness of northern Europeanseedlings is not related to hardiness at flowering socrosses between these types would not necessarily leadto an improvement but greater general diversity amongparents including some from high altitudes should betried. Flowering at a higher node can easily be bred iffrosting of first flowers is inevitable . In Yunnan, Chi-na, genotypes with greater numbers of flowers per planthad greater ability for self-regulation and maintenanceof yield following low temperatures (Liu et al ., 1987) .

High temperatures

Effect on fertilizationThe upper limit of temperature at which fertilizationcan take place is probably about 30°C ; in one experi-ment there was no ovule fertilization at 35'C and flow-ers of "Outlook" cultivar collected 36 or 48 h afterpollination had better fertilization frequency at 15 ° Cthan at 25 °C (Graff, 1988) . This rather low optimumtemperature is probably another reason, in addition todrought, that at low latitudes faba beans are mainlygrown in the cool season or at high altitudes . Acces-sions from hot countries do not tolerate a higher tem-perature at flowering better than those from temperatecountries. However, there is distinct evidence that at35 ° C pollen from hybrids germinates better than thatfrom inbreds (Table 4A). Also, fertilization is moresuccessful in hybrids than inbreds even at low temper-atures (Table 4B) . It may be concluded that FI hybrids,or synthetic cultivars which have a high proportion ofhybrid plants, would be able to tolerate a wider range oftemperatures than inbreds or open-pollinated cultivars .

Effect on pod dehiscenceThe wrinkled or indehiscent pod is widespread amongcultivars in arid regions (Hanelt, 1972) . These arenormally flowering in the cool season but can toler-ate heat without shattering at harvest. More recently,

1 6 1

162

Table 4. Tolerance of pollen and ovules of inbred and hybridfaba beans to high and low temperatures

(A)

Percent germination of pollen from inbred,hybrid and open pollinated lines after ninehours in vitro incubation at 15°C,25°C and 35°C

(B)

Temperature (°C)Genotype

Inbred AInbred BHybrid ACOutlookChinese

Temperature (°C)Genotype

Inbred 24 hHybrid

Inbred 36 hHybrid

cultivars with indehiscent pods e.g., "Alfred", "Vic-tor" and "Caspar", have been introduced in northwest-ern Europe where they have avoided harvesting lossesin hot dry summers there. The genetic control maynot be the same as the recessive gene described byHanelt (1972), or else there are minor modifying genes,because varying degrees of tendency for dehiscencecan be identified ; e .g., small-seeded long-podded cul-tivars with a wide angle to the stem are particularlysusceptible to shattering .

Salinity

Faba beans are not cultivated much on saline soils butin a few places, especially in Egypt and India, thecrop could be extended if salt tolerance were found .El-Karouri (1979) studied the effect of soil salinityon growth and yield of a local Sudanese cultivar and

Effect of temperature on ovule fertili-zation frequency (%) in inbred andhybred flowers after 24 h and 36 hincubation

found it to have medium tolerance . This disagreed withthe earlier findings of Ayers & Eberhard (1960) whoclassified faba beans as having low salt tolerance . El-Karouri (1979) suggested that this may demonstratedifferences for salt tolerance between genotypes. El-Aal and Waly (1988) tested a 5 x 5 diallel cross for salttolerance at germination and found good general com-bining ability effects for the cvs Somaly and Kobrosy .In Germany, "Felix" and Line 49907 developed moreroot and shoot dry matter in controlled saline con-ditions than the salt-sensitive and less branched cvslike "Herz Freya" (Melesse, 1988) . Dua et al. (1989)found variation among faba bean genotypes in thresh-old salinity in India. There may be a basis for breedingprogress.

15 25 35

54 .5 ± 3 .4 61.0± 2 .8 12 .5 ± 1 .987 .9 ± 2.0 79 .5 ± 2 .6 16 .1 ± 2 .366 .9 ± 3 .1 66.7 ± 3 .1 44.6±2 .921 .6 ± 2 .3 62 .9 ± 3 .0 17 .9 ± 2 .420 .3 ± 2 .7 59 .8 ± 3 .1 17.9 ± 2 .4

5 15 25

6 .1 ± 1 .4 17.6±2 .2 25 .3 ± 2 .52.9 ± 1 .2 45.0±3 .5 35 .8 ± 3 .5

10 .8 ± 1 .8 20.5±2 .2 47.3±2.925 .7 ± 3 .2 46 .3 ± 3 .4 72.7±5.5

Discussion of breeding strategies

Wild relatives

Despite many attempts to overcome interspecific barri-ers (Ramsay et al ., 1984), no crosses of Vcia faba withany other species have yet been successful . This papercannot, therefore, contribute to the theme of "Use ofwild species to improve resistance to stress" except toconfirm that high levels of resistance to Botrytis andto aphids, exist in V narbonensis (Birch, 1985) and toOrobanche in VV dasycarpa (El Moneim et al ., 1990) ;and that resistance to other stresses could also be foundin wild Viciae . There are good reasons for wanting toutilize genetic variation in wild species once the bar-riers to crossing are overcome or advances in biotech-nology allow gene transfer to V faba .

Multiple resistance

Sources of resistance to most of the major pathogensexist and the way forward is clearly to combine asmany individual resistances in one faba bean cultivar .Some genotypes are already resistant to more than onepathogen without deliberate breeding to combine them .For example, the ICARDA line BPL 1179 has resis-tance to chocolate spot, rust, Alternaria (Khalil et al .,1986) and Peronospora (Nassib & Salih, 1983) ; alsoINRA line 29H displays resistance to Ascochyta and tostem nematodes . These examples suggest close link-age of the resistance genes and/or a common resistancemechanism . Some well-established resistances, how-ever, have limited application unless they can be com-bined with others . Resistance to Orobanche in Giza402, for example, could be used more widely if com-bined with resistance to chocolate spot . Extreme resis-tance to frost in Cote d'Or is unlikely to be employedin a new cultivar unless combined with resistance tolodging and chocolate spot or with earlier maturity .

A number of multiple resistances can be found inICARDA Annual Reports, notably combinations ofresistance to aphids with chocolate spot, aphids withstem nematodes and chocolate spot with rust (Table 3) .Bernier (1985) reviewed favorably prospects of multi-ple disease resistance to most of the fungal pathogens .However, chocolate spot resistance seems to dependon genetic background for full expression so may notbe so easy to combine with resistance to other dis-eases, in all types of faba bean, as will resistance torust orAscochyta . Resistances to some viruses (BYMVand PEMV) have also been combined (Schmidt et al .,

1 63

1989). Crosses have already been made with the objec-tive of other combinations particularly resistance toOrobanche with resistance to fungal pathogens .

Durable resistance

None of the resistance genes described in this paper hasbeen used widely enough or over a long enough periodto be described as durable sensu Johnson (1979) . Itis known, however, that some sources of resistanceare race specific, particularly in the case of rust andAscochyta, and are not likely to be of value in thelong term. The fact that most bean cultivars are veryheterogeneous, however, provides the opportunity tohave a population containing a number of resistances .Such a scheme has been proposed for rust using genesfor slow rusting (Bernier & Conner, 1983) .

Effect of breeding methods

Initial diversity is mainly from local populations orgermplasm collections. In general, mutation breedinghas produced new plant architecture rather than toler-ance to stress, but one exception was greater resistanceto chocolate spot and to rust than original cultivars inM2 after use of gamma rays (Abdel-Hak & Mansour,1980) .

After creating new populations by crossing, mostfaba bean breeders use some form of pedigree or recur-rent selection with attempts to preserve identity of theselections in pure lines . But the final cultivar as releasedmay be a pure line, population, Fl hybrid, or compositeof contrasting or of sister lines .

Heterosis of 20% or more is well established in Vfaba . Composites are heavier and more stable in yieldthan their inbred components (Bond, 1986) imply-ing the former are on average better able to tolerateyield-limiting factors (= stress) ; and mixtures of non-inbreds also yield more than their components (Tarhuni& McNeilly, 1990). That greater stability of compos-ites is due to a better tolerance of stresses by the morehybrid plants that they contain is suggested by a num-ber of examples of high yields of hybrids in stressconditions or of inbreeding depression in tolerance ofstress .

Due to their autofertility, F, hybrids can toleratelack of pollinating insects better than inbreds and mostother pollinated cultivars (Link, 1990) . Hybrid flowersfertilized faster at low temperatures and hybrid pollengerminated more at high temperatures (Graff, 1988) .F, s were more resistant than parents to bruchids (Waly

164

et al., 1987); and in winter beans, survival values forhybrids were better than for mid-parents (Bond et al .,1986) . In drought conditions, lowest yields were givenby lines suffering most from inbreeding depression(Milewska et al ., 1988), and Hempel (1983) found nofurther response to selection for Ascochyta resistanceafter a third cycle owing to inbreeding effects .

Producing hybrid or composite cultivars conflictswith the objective of uniformity, for ease of manage-ment and to satisfy registration requirements . Hetero-geneity is necessary to provide heterozygosity and het-erotic tolerance of stress . (Hybrids are not necessarilyuniform because only 3-way crosses are economic inpractice). A balance has to be sought between thesetwo opposing pressures, but it is important that reg-istration procedures be formulated in the light of thespecial case of hybrid tolerance in V faba rather thanon models constructed for inbreeding crop species .

Effect of breeding for quality

Selection for reduced antinutritional factors, e.g .,tannin, trypsin inhibitors, glucopyranosides, mostof which have evolved to protect the plant againstpathogens, might reduce tolerance to stress . For exam-ple, in some near-isogenic pairs of lines that differ intannin, emergence from the soil is worse for the tannin-free than for the tannin-containing line at 5 ° C but notat 15° C (Kantar, 1992) . However, this may not be truefor all isogenic pairs (Van Loon et al ., 1989) or forcurrent tannin-free cultivars because they are showingsatisfactory emergence and resistance to Fusarium in arange of soil conditions . A hypothesis is that alternativeplant defenses are being selected as breeding proceedsin tannin-free types, and that a similar scenario couldbe envisaged for other antinutritional factors . Vicineinhibits in vitro fungal growth (Bjerg et al ., 1984) butother resistance mechanisms could be selected .

Integration with other control measures

Breeding can make a major contribution to reducingthe effect of stress but integration of genetic resis-tance with agronomic measures can be of greater ben-efit than either alone. A good example is resistanceto Orobanche which is likely to allow normal yields ifcombined with early sowing and herbicide (glyphosateor fosamine) treatment . Aphid resistance could reducethe need for insecticides from two to one applicationor to borders of fields only. Moderate resistance tochocolate spot could be combined with a reduced rate

of fungicide or with higher plant density if resistancereduces the risk of aggressive attack .

Concluding remarks

Progress has been made in the last few years, mainly byICARDA coordinated research, though also to a lesserextent in some national programs, in breeding for resis-tance to chocolate spot, Ascochyta, rust, Orobanche,and to some viruses . Resistance to chocolate spot is notso clearly defined or so simply transferred into othergenetic backgrounds as the others but it can be helpedsomewhat by breeding for resistance to pre-disposingfactors. Improved levels of resistance to Orobancheare still required but most can be made of existingsources by integrating them with herbicides and withthe appropriate planting dates and densities .

Further multiple resistances will be pursued withthe long term aim of using recurrent selection, back-crosses, and eventually gene transformation as abuilding-block approach to developing the ideal culti-var. However, this will not be easy. Some lines are resis-tant to one pathogen but very susceptible to another.Also a survey of most of the ICARDA disease-resistantlines showed a skewed distribution toward small seedsand late maturity (Robertson & Saxena, 1993) . In otherwords some linkages may have to be broken .

Another problem is the unknown degree of dura-bility of the present sources of resistance. New racesof pathogens may not appear as often in Vafaba as ininbreeding crops but the trend in faba bean is towardgreater uniformity (e .g ., where quality is required bythe end user or distinctness for Breeders' Rights) sonew sources and strict monitoring will be needed .

There is some hope of improving tolerance of abi-otic stresses, though within the constraints of the fun-damental morphology of the plant. Some cultivars tol-erate drought or frost better than others and this givesthem good local adaptation . Improvements in thesetolerances, in the short term by trials with the stressimposed and in the long term by selection for associat-ed biochemical traits, should allow wider cultivation,but rarely an improved very broad adaptation as in thecase of disease resistance . Hybrid vigor is an importantfactor in allowing faba bean to tolerate various stress-es; thus, breeding methods that allow high levels ofhybridity in a cultivar should be adopted .

Very few of the above possibilities for breedingwould exist if germplasm had not been collected, evalu-ated and maintained . Because tolerance to some stress-

es is still lacking and existing resistances may not bedurable, there is a continuing need for collection, eval-uation, and maintenance of genetic resources in V. faba .

The problems and challenges are now too large to befragmented among national or private companies . Onlyinternational collaboration can tackle requirements likemultiple resistances, differentiation of pathotypes, thedevelopment of strategies to find durable resistance,and the extension of research and breeding needed toimprove tolerance of abiotic stresses .

References

Abdel-Hak, T.M . & K. Mansour, 1980. Agricultural ResearchReview 58 : 57-63 .

Ayers, A .D. & D.L. Eberhard, 1960 . Agronomy Journal 52 : 110-111

Bardner, R ., K.E . Fletcher & D .C . Griffiths, 1982 . RothamstedAnnual Report for 1991 (Part l) pp . 102-103 .

Bernier, C.C ., 1985 . In : M.C. Saxena & S . Varma (Eds.), Fababeans, Kabuli chickpeas, and lentils in the 1980s, pp . 129-136 .ICARDA, Aleppo, Syria .

Bernier, C .C . & R .L. Conner, 1983 . In : F. Lamberti, J .M. Walker &N.A . van der Graaff (Eds.), Durable resistance in crops, pp . 429-431 . Plenum Press, New York .

Birch, N ., 1985 . Annals of Applied Biology 106 : 561-569 .Bishara, S ., G . Defrowy, S. Khalil & S . Weigand, 1989 . Annu-

al report of the Food Legume Improvement Program for 1989,pp. 221-223 . ICARDA, Aleppo, Syria .

Bjerg, B ., M. Heide, J .C.N. Knudsen & H . Sorensen, 1984.Zeitschrift fur Pflanzenkrankheiten and Pflanzenschutz 91 : 483-487 .

Blaszczak, W. & Z . Fiedorow, 1979 . Biuletyn Instytutu Hodowli iAklimatyzacjii Roslin 1979 137 : 11-22 .

Bond, D .A ., 1986. Biologisches Zentralblatt 105 : 129-135 .Bond, D.A ., S .J . Brown, G .J . Jellis, M . Pope, J .A. Hall & M .H .E .

Clarke, 1986 . Annual report of Plant Breeding Institute, pp . 42-46. Cambridge, UK .

Bond, D.A . & H .J .B . Lowe, 1978. Annals of Applied Biology 81 :21-32 .

Caubel, F. & J . Le Guen, 1992 . In : 1st European conference on grainlegumes, pp . 337-338 . 1-3 June 1992 . Angers, France .

Caubel, G . & D . Leclercq, 1989 . FABIS 25 :45-48 .Conner, R .L . & C.C. Bernier, 1982. Phytopathology 72 : 687-689 .Cubero, J .1 ., M .T. Moreno & L . Hernandez, 1992 . In : 1st European

conference on grain legumes, pp. 41-42 . 1-3 June 1992 . Angers,France .

Cubero, J .1., A. Pieterse, A .R . Saghir & S . Borg, 1988 . In : R .J . Sum-merfield (Ed .), World crops : cool season food legumes, pp . 549-563 . Kluwer Academic Publishers, Dordrecht .

Dawkins, T.C .K . & J .C. Brereton, 1984 . World Crops 10 : 113-126 .Dobson, S .C . & N .J . Giltrap, 1991 . Aspects of Applied Biology 27 :

111-116 .Drayner, J.M ., 1959 . Journal of Agricultural Science, Cambridge

53 :387-404 .Dua, R.E, S.K. Sharma & B. Mishara, 1989 . Indian Journal of

Agricultural Science 59 : 729-731 .El-Aal, S .A .A . & E .A . Waly, 1988 . FABIS 22 :9-10 .

165

El-Hady Mohamed, M.M ., 1988 . Diallel analysis of resistance tochocolate spot disease (Botrytisfabae Sard .) and other agronom-ic traits in faba bean (Vicia faba L .). Ph.D . Thesis, Faculty ofAgriculture, Cairo University .

El-Karouri, M.O.H ., 1979 . Experimental Agriculture 15 : 59-63 .El Moneim, A.A ., W. Erskine, K .B . Singh, K .- H . Linke & M .C . Sax-

ena, 1990. Annual report of Food Legume Improvement Program1990, p . 224 . ICARDA, Aleppo, Syria .

El-Shazly, M .S . & I .B . Warboys, 1989 . Experimental Agriculture25: 35-37 .

Gondran, J ., 1975 . In : VII Plant protection congress, pp . 109-123 .Reports and information section VI . Moscow, USSR .

Graff, R ., 1988 . Factors affecting ovule fertilization frequency andseed set in faba bean (Vicia faba L). Ph.D . Thesis, University ofSaskatchewan .

Halila, H., M . Kharrat & S .B . Hanounik, 1990 . In : Annual report for1990 of the Food Legume Improvement Program of ICARDA,pp. 205-206. ICARDA, Aleppo, Syria .

Hanelt, P., 1972 . Kulturpflanze 20 : 75-128 .Hanna, A .S . & D .A . Lawes 1967 . Annals of Applied Biology 59 :

289-295 .Hanounik, S .B ., H . Halila & M . Harrabi, 1986 . FABIS 16 : 37-39 .Hanounik, S.B ., G .J . Jellis & M .M. Hussein, 1993 . In : Breeding

for stress tolerance in cool season food legumes . Edited by K.B.Singh and M .C . Saxena, John Wiley & Sons, Chichester U.K . ;pp . 97-106

Hanounik, S .B . & L .D. Robertson, 1988 . Plant Disease 72 :696-698 .Hanounik, S .B . & L .D. Robertson, 1989 . Plant Disease 73 : 202-205 .Harrewijn T.L. & A . van Novel, 1986 . Veldbonen . Annual report

of Stichting voor Plantenveredeling (SVP) Wageningen for 198541 :74-75 .

Harrison, J .G ., 1981 . Tests of Agrochemicals and Cultivars 2 : 72-73 .Hempel, K ., 1983. Tagungsbericht, Akademie der Land-

wirtschaftswissenschaften der Deutschen DemokratischenRepublik 216 : 11 :579-590 .

Herzog, H . & M .C . Saxena, 1988 . FABIS 21 : 19-25 .Holden, J .H.W. & D.A. Bond, 1960. Heredity 15 : 175-192 .Hussein, H.A.S ., S .S . Youssef, E .H .A. Hussein & B.A. Hus-

sein, 1988 . In : Improvement of grain legume productions usinginduced mutations, pp . 127-144 . IAEA, Vienna, Austria .

Jellis, G .J ., A .S . Plumb & M .H.E. Clarke, 1991 . Aspects of AppliedBiology, Production and Protection of Legumes 27 : 63-66 .

Jellis, G .J ., D .B . Smith & E .S . Scott, 1990 . Mycological Research94:407-409 .

Johnson, R ., 1979 . Phytopathology 69 : 198-199 .Kantar, F, 1992 . Studies on the establishment of white flowered

(zero tannin) Vicia faba . Ph.D. Thesis, University of Nottingham .Karamanos, A .J. & C .E . Avgoulas, 1989. FABIS 25 : 40-45 .Khaled, A.K . & F.I . El-Bastewesy, 1989 . FABIS 25 : 5-9 .Khalil, S.A ., A.M. Nassib & N.M. Abou Zeid, 1986 . Biologisches

Zentralblatt 105 : 155-161 .Kharrat, M ., M .H. Halila, K .H. Linke & T. Haddar, 1992 . In :

2nd international food legume research conference program andabstracts, p . 53 . 12-16 April 1992, Cairo, Egypt .

Kheir, N .F, S .M. Salem, A .H .H. Ahmed & O.M.A . El-Shihy, 1989 .Agriculture University of Cairo 40 : 197-212 .

Klinghauf, FA .J ., 1982 . In : G . Hawkin & C. Webb (Eds .), Fababean improvement, pp . 285-295 . Martinus Nijhoff/Dr, W. JunkPublishers, The Hague, The Netherlands .

Lawes, D.A ., D.A. Bond & M.H. Poulsen, 1983 . In : PD . Hebbleth-waite (Ed .), The faba bean, pp . 23-76 . Butterworths, London .

Lawes, D.A ., L .R . Mytton, M .H . EI-Sherbeeny & F.K . Sorwli, 1978 .Annals Applied Biology 88 : 466-468 .

Liang, X.Y., 1989 . FABIS 25:3-4 .

166

Link, W, . 1990 . Theoretical and Applied Genetics 79 : 713-717 .Link, W. & K . Hempel, 1993, Abstracts of First International Crop

Science Congress, Iowa 1992 ; p 73 .Liu, Z.S ., YZ. Zhao, S.Y Bao & Wen Guang, 1987. FABIS 18:

14-17 .Melesse, T., 1988. Mitteilungen der Gesellschaft fur Pflanzen-

bauwissenschaften 1 : 96.Milewska, J ., E . Januszewicz & 1. Koczowska, 1988 . Biuletyn Insty-

tutu Hodwli i Acklimatiyzacji, Roslin 165 : 107-114.Muller, H .J ., 1968 . Entomologica experimentalis et applicata 11 :

355-371 .Nanda, H.C ., M. Yasin, C .B . Singh & S.K. Rao, 1988 . FABIS 21 :

26-30 .Nassib, A .M ., A.A . Ibrahim & S .A . Khalil, 1982 . In : G . Hawkin &

C. Webb (Eds .), Faba bean improvement, pp . 199-206 . MartinusNijhoff/Dr. W. Junk Publishers, The Hague, The Netherlands .

Nassib, A . & FA. Salih, 1983 . In : M.C. Saxena & R .A . Stewart(Eds .), Faba bean in the Nile Valley, pp . 59-68 . ICARDA, Aleppo,Syria .

Nerkar, YS ., D. Wilson & D.A. Lawes, 1981 . Euphytica 30 : 335-345 .

Ondrej, M., 199 1 . Ochrana Rostlin 27 : 257-264 .Pascual Villalobos, M . & G.J . Jellis, 1990 . Journal of Agricultural

Science 115 : 57-62 .Poulsen, M.H., 1980. Inbreeding and autofertility in Vicia faba L.

Ph.D . Thesis . University of Cambridge .Radwan, M .S ., M.M.F. Abdalla, G . Fisbeck, A .A. Metwally & D .S .

Darwish, 1988. Plant Breeding 101 : 208-216 .Ramsay, G ., B . Pickersgill, J .K . Jones, L. Hammond & M.H . Stew-

art, 1984. In : PD . Hebblethwaite, T.C .K. Dawkins, M .C . Heath& G. Lockwood (Eds .), World crops : production, utilization,and description 10 :201-208 . Martinus Nijhoff, The Hague, TheNetherlands .

Rashid, K .Y., C .C . Bernier & R .L. Conner, 1991 . Plant Disease 75:852-855 .

Rashid, K.Y. & C .C. Bernier, 1986 . Canadian Journal of Plant Pathol-ogy 8 : 317-322 .

Ricciardi, L., 1989a. Agricoltura Mediterranea 119 : 297-308 .Ricciardi, L., 1989b. Agricoltura Mediterranea 119 : 424-434 .Ricciardi, L. & P. Steduto, 1988 . FABIS 20 : 21-24 .Robertson, L.D. & M . El Sherbeeny, 1988 . In : Fababean germplasm

catalog. Pure line collection ICARDA Aleppo Syria, 140 pp .

Robertson, L.D. & S .B . Hanounik, 1987 . In : Annual report for FoodLegume Improvement Program for 1987, pp . 205-212.ICARDA,Aleppo, Syria.

Robertson, L.D. & M .C . Saxena, 1993 . In : K .B. Singh & M.C .Saxena (Eds .) . Breeding for stress tolerance in cool-season foodlegumes . John Wiley & Sons, Chichester, U .K ., pp 37-50 .

Rohloff, H. & R . Stulpnagel, 1984. FABIS 10 : 29 .Salih, S .H. & A .E. Ali, 1989 . FABIS 23 : 8-10.Schmidt, H.E ., 1984 . Nachrichtenblatt fur den Pflanzenschutz in der

DDR 38:157-162 .Schmidt, H .E ., K . Geissler, E. Karl & H.B. Schmidt, 1986 . Archiv

fur Phytopathologie and Pflanzenschutz 22 : 87-99 .Schmidt, H.E., U. Meyer, 1. Haack & E. Karl, 1989 . Archiv fur

Zuchtungforschung 19 : 193-196.Shukkla, R .S ., C.B. Singh & D. Khare, 1986 . FABIS 14 :18.Soja, G ., A .- M . Soja & Z . Reza, 1988 . FABIS 22 :20-24 .Stoddard, FL., 1986 . FABIS 15 : 22-26 .Tarhuni, A.M. & T. McNeilly, 1990 . Journal of Agronomy and Crop

Science 165 : 39-46.Tivoli, B ., P. Berthelem, J . Le Guen & C. Onfroy, 1986 . FABIS 16 :

46-50.Tomashevski, Z. & E. Yanushevich, 1975 . Biuletyn Instytutu

Hodowli i Acklimatyzacjii, Roslin 128/129 : 157-164 .Van der Wal, A.F., 1981 . In : R . Thompson (Ed .), Vicia faba: Physi-

ology and breeding, World Crops 4, pp . 49-54 . Martinus Nijhoff,The Hague, The Netherlands.

Van Loon, J .J .A., A . van Norel & L.M.W. Dellaert, 1989 . In : J . Huis-man, T.FB van der Poel & I .E . Liener (Eds .), Recent advancesof research in antinutritional factors in legume seeds, pp . 23-25.Pudoc, Lanham, Maryland, USA .

Van Noel, A ., 1985 . Zaadbelangen 39 : 157-159.Waly, E.A ., S .A .A. El-Aal & M .H . Hussein, 1987 . FABIS 17 :3-5.Yartiev, A.G ., 1976 . Sel' Skokhozyaistvennaya Akademiya Imeni

Timiryazeva, pp . 65-68 . Moscow, USSR .Yeoman, D.P., D .H. Lapwood & J. McEwen, 1987 . Crop Protection

6 : 90-94 .Zakrzewska, E ., 1986 . In : Proceedings of XI EUCARPIA Congress,

pp. 311-317 . Warsaw, Poland .Zebitz, C.P.W, Bauru & B. Tenhumberg, 1988 . Mitteilungen mans

der Biologischen Bundesanstalt fur Landundforstwirtschaft .Berlin-Dahlem 245 : 313 .