Contributions of the Bean Cowpea CRSP to (1)

Contributions of the Bean/Cowpea CRSP to cultivar and germplasm development in common bean

b c d e J.S. Beaver f , J.C. Rosas , J. Myers , J. Acosta , J.D. Kelly , S. Nchimbi-Msolla ,

a,*

R. Misangu j , J. Bokosi , S. Temple , E. Arnaud-Santana , D.P. Coyne

a Department of Agronomy and Soils, University of Puerto Rico, P.O. Box 9030, Mayaguez, PR 00681, USA b Department of Agricultural Science and Production, Escuela Agrı´cola Panamericana, P.O. Box 93, Tegucigalpa, Honduras c Department of Horticulture, Oregon State University, 4017 Agriculture and Life Sciences, Corvallis, OR 97331, USA d INIFAP, Apartado Postal, C.P. 56230, Chapingo, Edo Mexico, Mexico e Department of Crop and Soil Sciences, Michigan State University, East Lansing, MI 48824, USA f Department of Crop Science and Production, Sokoine University of Agriculture, Morogoro, Tanzania g Bunda College of Agriculture, Lilongwe, Malawi h Department of Agronomy and Range Science, University of California at Davis, Davis, CA 95616, USA i CESIAF, San Juan de la Maguana, Dominican Republic j Department of Horticulture, University of Nebraska, 386 Plant Sciences, East Campus, Lincoln, NE 68583, USA

Abstract Disease and abiotic stress are important factors limiting bean production wherever beans are grown. The development of bean

cultivars having resistance to these stresses is a cost-effective and sustainable means to address these constraints. During the past 20 years, the Bean/Cowpea Collaborative Research Support Project (B/C CRSP) has supported common bean cultivar development and germplasm improvement programs in the USA and developing countries. Plant breeders have developed and released in Central America and the Caribbean bean cultivars and germplasm with one or more of the following traits; resistance to bean golden yellow mosaic virus (BGYMV), bean common mosaic necrotic virus (BCMNV), rust, web blight and common bacterial blight (CBB) and greater tolerance to high temperatures. In the highlands of Mexico and Ecuador bean cultivars with resistance to anthracnose, rust, root rots and bean common mosaic virus (BCMV), greater biological nitrogen fixation and improved adaptation to intermittent drought have been released. The bean breeding programs in East Africa have developed and released bean cultivars and germplasm with resistance to BCMNV, rust and bruchid seed weevils. Participation in the B/C CRSP has permitted USA bean breeding programs to develop and release bean cultivars and germplasm with resistance to BGYMV, BCMNV, anthracnose, rust, CBB, architectural avoidance to white mold and greater yield potential. Numerous plant breeders, plant pathologists and agronomists from developing countries have received advanced degree training in the USA, which has enhanced the capacity to develop improved bean cultivars for Latin America and Africa. The lack of sustainable seed production and delivery systems continues to limit the impact of the release of improved bean cultivars in many parts of Latin America and East Africa. # 2003 Elsevier Science B.V. All rights reserved.

Keywords: Phaseolus vulgaris ; BGYMV; BCMV; Rust; Anthracnose; Yield; Abiotic stress; Drought; Heat tolerance; Bean cultivars

* Corresponding author.

88 J.S. Beaver et al. / Field Crops Research 82 (2003) 87–102

1. Introduction the genetic base of bean cultivars released in the USA and developing countries. B/C CRSP cultivar devel-

Diseases such as anthracnose, bean rust, CBB and opment programs have benefited greatly from the bean common mosaic and abiotic stresses such as

availability of breeding lines developed by the Centro drought and low soil fertility are important constraints

Internacional de Agricultura Tropical (CIAT) in Cali, to bean production wherever the crop is grown

Colombia. CIAT scientists have mostly collaborated ( Schwartz et al., 1996; Van Schoonhoven and Voysest,

with bean breeding programs associated with Minis- 1989; Wortmann et al., 1998 ). Angular leaf spot is a

tries of Agriculture, whereas B/C CRSP projects have serious bean disease in the tropics, whereas white

tended to associate with institutions of higher educa- mold is more important in temperate bean growing

tion including the Escuela Agrı´cola Panamericana regions. Halo blight and root rots are production

(EAP) in Honduras, the University of Costa Rica, constraints in the tropical highlands and temperate

Sokoine University of Agriculture in Tanzania, and bean production zones ( Murillo et al., 1997 ). In the

Bunda College of Agriculture in Malawi. This differ- lowland tropics, BGYMV, web blight and high tem-

ence in focus by CIAT and the B/C CRSP has helped to peratures can threaten bean production.

broaden the base of bean research expertise in devel- Since 1981, the USAID funded Bean/Cowpea Col-

oping countries ( Table 2 ).

laborative Research Support Project (B/C CRSP) has The development of bean cultivars with resistance supported common bean (Phaseolus vulgaris L.) cul-

to the most important abiotic and biotic stresses tivar development and germplasm improvement pro-

represents a cost-effective and sustainable means to grams in Latin America, the Caribbean, East Africa

address these constraints. The following sections con- and the USA. A network for bean research is needed

tain examples where bean breeding programs sup- because no single institution can address all of the

ported by the B/C CRSP have had significant factors constraining bean production and utilization in

impact in developing countries and the USA. each region. Because a number of these stresses affect production in both the USA and developing countries, bean breeders within the B/C CRSP share common

2. Biotic constraints

interests and research results are often mutually ben- eficial ( Table 1 ).

2.1. Bean golden yellow mosaic virus Long-term support by USAID provides continuity of effort, a key to the success of cultivar development

Bean golden yellow mosaic is a whitefly transmitted programs. Bean breeders and plant pathologists, for

geminivirus that threatens dry bean production in example, have been able to identify sources of durable

Central America and the Caribbean and snap bean resistance to BGYMV, rust and anthracnose. The B/C

production in southern Florida ( Blair et al., 1995; CRSP has provided opportunities for bean breeders

Morales, 1994 ). Genetic progress in breeding for from developing countries to obtain advanced degree

BGYMV resistance has been incremental. CIAT bean training and has permitted scientists from Latin Amer-

breeders, working in Guatemala, made significant ica and Africa to have access to laboratories where

advances in the identification of sources of resistance marker-assisted selection, and other advanced techni-

to BGYMV and developed black and small red culti- ques can be conducted.

vars with resistance to the virus ( Beebe, 1994 ). At the Most of the genetic diversity of beans is found in

University of Puerto Rico, a greenhouse screening Latin America ( Gepts and Debouk, 1991 ) where bean

technique was developed that allowed inheritance diseases and pests are often more virulent. This has

studies to be conducted ( Adames-Mora et al., 1996 ). enabled B/C CRSP supported bean breeders to iden-

Velez et al. (1998) identified two recessive genes, tify tropical germplasm with valuable genes for dis-

bgm-1 , in CIAT breeding line A429, and bgm-2, in ease resistance. Key to the B/C CRSP programs has

CIAT breeding line DOR303, that confer resistance to been the use of elite lines from USA bean breeding

chlorosis caused by BGYMV. Molina Castaneda and programs and landrace cultivars from Latin America,

Beaver (1998) identified a dominant gene, Bgp, in the Caribbean and Eastern Africa. This has broadened

CIAT breeding line DOR482, that confers resistance

89 Table 1

J.S. Beaver et al. / Field Crops Research 82 (2003) 87–102

Bean cultivars developed with participation by B/C CRSP scientists Seed type

Name

Countries where the

Traits

cultivar was released

Black Arroyo Loro Negro

Dominican Republic

Web blight and rust resistance and heat tolerance

(DR) and Haiti

Jaguar

USA

Tolerance to white mold, Co-1 and Co-2 genes for anthracnose resistance, I gene resistance to BCMV and Ur-3 resistance to rust

Negro Sahuatoba

Mexico

Anthracnose and rust resistance, I gene resistance to BCMV and tolerance to common bacterial blight and root rot. This is the first opaque black seeded cultivar developed for the Mexican highlands

Negro Altiplano

Mexico

Anthracnose and rust resistance, I gene resistance to BCMV and tolerance to common bacterial blight and root rot

Phantom

USA

Co-1 and Co-2 genes for anthracnose resistance, I gene resistance to BCMV, Ur-3 resistance to rust and tolerant to root rot

Raven

USA

I and bc-3 resistance genes for BCMV and BCMNV, Ur-3 rust resistance genes and resistance to alpha and alpha Brazilian races of anthracnose

Pinto Bayacora

Anthracnose and rust resistance and tolerance to root rots Chase

Mexico

USA

Common bacterial blight, halo blight and brown spot resistance, Ur-3 rust resistance gene and moderate avoidance of white mold

Kodiak

USA

I gene for BCMV resistance, bc-1 2 gene for BCMNV, Ur-3 and Ur-6 rust resistance genes and tolerance to root rot

Pinto Mestizo

Mexico

Resistant to rust and most races of anthracnose and tolerance to common bacterial blight and root rot

Pinto Villa

Mexico

Broad adaptation and yield stability in the semiarid highlands of Mexico partially due to phenotypic plasticity and ability to continue seed fill at low night temperatures. Resistant to anthracnose and tolerant to rust and low soil fertility

Sierra

USA

Upright type II plant, rust resistant, moderate resistance to the alpha race of anthracnose, tolerant to Michigan races of halo blight potato leafhopper and Fusarium wilt

Small red Bribri

BGYMV, anthracnose, web blight resistance and heat tolerance Tio Canela 75

Costa Rica

Honduras, Nicaragua,

bgm-1 gene for BGYMV, I gene for BCMV and CBB resistance

El Salvador and Panama

and heat tolerance

White Anacaona

Common bacterial blight and web blight resistance Arroyo Loro

Dominican Republic

I gene for BCMV resistance and rust resistance Beluga (alubia)

Puerto Rico and the DR

USA

I gene for BCMV resistance, Co-1 anthracnose resistance gene and rust resistance

I gene for BCMV resistance, resistance to alpha race of anthracnose and Ur-3 gene for rust resistance, and excellent canning quality Mackinac (navy)

Huron (navy)

USA

I gene for BCMV resistance, Co-1 gene anthracnose resistance gene and Ur-3 gene rust resistance. Excellent seed and canning quality Mayflower (navy)

USA

I gene BCMV resistance, resistance to beta and gamma anthracnose races, rust resistance and tolerant to ozone pollution Matterhorn (GN)

USA

I gene for BCMV resistance and Ur-3 gene rust resistance and Great northern

USA

tolerance to root rot, and yield stability Morales

Puerto Rico

bgm-1 gene for BGYMV resistance, I gene BCMV resistance and rust resistance

Newport (navy)

USA

I gene for BCMV resistance, Co-1 and Co-2 anthracnose resistance genes and Ur-3 gene rust resistance

Starlight (GN)

Common bacterial blight resistance and seed quality Weihing (GN)

USA

USA

Common bacterial blight, bacterial brown spot and rust resistance

90 J.S. Beaver et al. / Field Crops Research 82 (2003) 87–102

Table 1 (Continued ) Seed type

Name

Countries where the

Traits

cultivar was released

Red mottled CIAS 95

Dominican Republic

Rust and common bacterial blight resistance. Resistant to NY-15 race of BCMV

JB 178

Dominican Republic

Resistance to rust, common bacterial blight and the NY-15 race of BCMV

Je’Ma

Rust resistance and enhanced biological nitrogen fixation PC 50

Ecuador

Ur-4 and Ur-9 rust resistance genes and cooking quality Saladin 97

Dominican Republic

Resistance to common bacterial blight and the NY-15 race of BCMV Pink

Dominican Republic

Rosada Nativa

Puerto Rico and the DR

bgm-1 gene for BGYMV, I gene for BCMV, rust resistance and heat tolerance

Flor de Mayo M38

Mexico

Drought tolerance, I gene for BCMV

I gene resistance to BCMV, erect architecture Red kidney

UC Flor 9623

USA

Chinook 2000

I gene resistance to BCMV, Co-1 and Co-2 anthracnose resistance (light red kidney)

USA

genes, rust and root rot resistance and excellent canning quality Red Hawk

I gene resistance to BCMV, Co-1 and Co-2 anthracnose resistance (dark red kidney)

USA

genes and rust resistance, and excellent processing quality UC Nichols

I gene resistance to BCMV, superior canning quality (dark red kidney)

USA

Yellow UC Canario 707

USA

I gene resistance to BCMV

Snap bean Genuine

USA

Rust and BGYMV resistant pole garden bean with climbing habit

to pod deformation in the presence of BGYMV. pyramid resistance sources (see Kelly et al. (2003) in Identification of a codominant RAPD marker linked

this issue).

to the bgm-1 gene has proved very useful for indirect Rosas et al. (2000a) also reported success in devel- selection for BGYMV resistance ( Urrea et al., 1996 ).

oping BGYMV resistant small red bean cultivars for In addition to the major gene resistance, quantitative

Central America. Tio Canela 75, released in Hon- trait loci (QTL) associated with the BGYMV resis-

duras, Nicaragua and El Salvador, combines BGYMV tance in DOR 364 have also been identified ( Miklas

resistance with a commercially acceptable small red et al., 1996 ). Markers linked to resistance sources have

seed type, heat tolerance and moderate levels of CBB been utilized to breed for resistance to BGYMV and

resistance ( Rosas et al., 1997 ). In 2000, more than

Table 2 Bean germplasm lines developed with participation by B/C CRSP scientists

Seed type Name

Country where germplasm

Traits

was developed

Black MUS-N-8

Web blight resistance White

Dominican Republic

BelMiDak RR 1-12 (navy)

Pyramided rust resistance genes BelMiNeb RR 1-7 (GN)

USA

Pyramided rust resistance genes Red kidney

USA

bgm-2 gene for BGYMV and CBB resistance Pinto

PR9443-4

Puerto Rico

Pyramided rust resistance genes Red mottled

BelDakMi RR 1-18

USA

PR9745-232

bgm-1 gene for BGYMV resistance PR9909-5

Puerto Rico

bgm-1 gene for BGYMV resistance Small red

Puerto Rico

bgm-1 gene for BGYMV and bc-3 gene for BCMV Snap

PR9357-107

Puerto Rico

bgm-1 gene for BGYMV and rust resistance Various

BelDade RGMR 4, 5 and 6

USA

ICB-3, ICB-6, ICB-8 and ICB-10

Puerto Rico

Common blight resistance derived from P. coccineus

J.S. Beaver et al. / Field Crops Research 82 (2003) 87–102

20% of the bean producers in Honduras planted Tio from BCMV ( Mink et al., 1994 ). BCMNV causes Canela 75 (Rosas, pers. commun.). Farmers in Haiti

whole plant systemic top necrosis (black root reaction) have expressed an increased interest in planting small

in bean lines possessing the I gene, independent of red beans based on the yield and adaptation of Tio

temperature, whereas BCMV isolates either do not Canela 75 in on-farm trials (Prophete, pers. commun.).

cause systemic necrosis, or only do so when tempera- ‘Bribri’, a small red bean cultivar that combines

tures exceed 30 8C ( Drijfhout, 1978 ). Greater genetic BGYMV, web blight resistance and tolerance to heat,

diversity in BCMNV is evident in East Africa than was released in Costa Rica in 2000 ( Rosas et al., 2003 ).

in other bean production regions. BCMNV isolates The BGYMV, BCMV and rust resistant white bean

have occasionally been transported to other continents cultivar Morales has become the most popular bean

through the green bean seed trade based in Arusha, cultivar for green-shelled bean production in Puerto

Tanzania.

Rico ( Beaver and Miklas, 1999 ). Rosada Nativa, a pink Most bean cultivars released in Central America bean cultivar that combines BGYMV, BCMV and rust

and the Caribbean carry the dominant I gene for resistance and heat tolerance was released in Puerto

resistance to BCMV and this source of resistance Rico ( Beaver et al., 1999b ). The bgm-1 gene for

has proven to be effective in controlling the virus in BGYMV resistance has also been incorporated into

the region. Unfortunately, the recent arrival of tropically adapted, light red kidney, red mottled and

BCMNV in the Dominican Republic and Haiti will pinto bean lines ( Beaver et al., 1999a ). Collaboration

require that future Caribbean bean breeding lines among researchers at the University of Puerto Rico,

possess additional genes to protect against the necrotic University of Florida and USDA-ARS led to develop-

reaction to BCMNV. Due to similar problems in the ment of BelDade RGMR 4, 5 and 6, which are McCa-

USA, the black bean cultivar ‘Raven’ was developed slan type pole (type IV) beans that combine superior

to resist both viruses by combining I and bc-3 resis- culinary traits with BGYMV and rust resistance ( Sta-

tance genes ( Kelly et al., 1994 ). Marker-assisted vely et al., 2001 ). BelDade RGMR 5 is being marketed

selection was used to incorporate the bgm-1 gene into by a private company in southern Florida as the cultivar

black and white-seeded breeding lines with the reces- Genuine (Shamrock Seed Co., Salinas, CA).

sive bc-3 gene confirmed through inoculation with the Research supported by the B/C CRSP to develop

NL3 strain of BCMNV.

transgenic beans with BGYMV resistance was unsuc- In Central America, bean lines with the I gene are cessful. Although a few transgenic beans were devel-

susceptible to bean severe mosaic, a beetle-trans- oped at great effort and expense, susceptibility of the

mitted comovirus ( Morales and Singh, 1997 ). Bean transgenic lines to BGYMV was attributed to a failure

researchers from the University of Puerto Rico and of the plants to express the viral coat protein ( Azzam

Michigan State University collaborated to eliminate et al., 1996 ). This experience belies the widely held

the I gene from local germplasm and, concurrently assumption ( Victor and Runge, 2002 ) that biotechnol-

incorporate the bgm-1 and bc-3 genes into small red ogy provides a more rapid and efficient approach to

beans. Sequence characterized amplified regions achieve plant breeding objectives.

(SCAR) markers for both the bgm-1 and I genes were multiplexed to simultaneously select for the presence

2.2. Bean common mosaic virus and bean common of bgm-1 and the absence of the dominant I allele mosaic necrotic virus

( Kelly et al., 2003 ). Breeding lines without the I gene were inoculated with the NL3 strain of BCMNV to

Bean common mosaic virus (BCMV) and bean detect the presence of bc-3 gene. This collaboration common mosaic necrotic virus (BCMNV) are aphid-

resulted in the release of the small red bean germplasm transmitted viruses that can cause significant yield loss

line PR9357-107 with resistance to BGYMV and ( Ga´lvez and Morales, 1989 ). The viruses can be seed-

BCMNV ( Beaver et al., 1998 ). borne, allowing long distance spread and compromis-

Because of the widespread occurrence of BCMNV ing bean seed increase and dissemination programs.

in East Africa, the I gene has been considered a major B/C CRSP supported research in East Africa led to

liability in the region. Most landraces are susceptible the discovery of BCMNV as a separate virus species

to BCMV and BCMNV, so breeders have used strain

92 J.S. Beaver et al. / Field Crops Research 82 (2003) 87–102

specific recessive resistance genes alone or in combi-

a very strong root system, and has demonstrated high nation with the I gene. The latter strategy is termed

yields and excellent canning quality. Canario 707, a ‘‘protected I gene resistance’’ ( Kelly et al., 1995b ). By

sulfur yellow bean with high yield, large seed size, and combining one of the recessive resistance genes (pre-

BCMV resistance, represents a new seed type for ferably bc-2 2 or bc-3) with the I gene, the systemic

producers in the USA. Similarly, UC Flor 9623, a necrosis reaction is prevented ( Kelly, 1997 ). The I

representative of the ‘‘Flor de Mayo’’ class popular in gene prevents more virulent virus strains from over-

some areas of Mexico, combines BCMV resistance coming the recessive gene resistance thereby creating

with very erect architecture and high yield ( Temple

a more durable form of resistance than conferred by

et al., 2002 ).

either gene alone. Rojo, released from Sokoine Uni-

A ‘‘protected I gene’’ approach has been increasingly versity of Agriculture in Tanzania in 1997 is an

used in the USA as a resistance strategy with a number example of a cultivar developed using this approach.

of germplasm and cultivar releases such as Kodiak pinto Studies by Martin and Adams (1987) demonstrated

that combine the I gene with either the bc-1 2 , bc-2 2 , or the importance of landraces with distinct seed types and

bc-3 genes ( Kelly et al., 1999a ; Miklas et al., 1997 ; plant characteristics for Malawian bean production and

Myers et al., 2001 ; Pastor-Corrales et al., 2001 ). consumption. Researchers at the University of Califor-

Several rust and BCMV resistant great northern nia at Davis and Malawi’s Bunda College of Agriculture

germplasm (GN) and pinto lines have been released. used successive backcrosses to incorporate bc-3 resis-

GN BelNeb 1 and 2 combines resistance to CBB, halo tance to BCMV and BCMNV into six contrasting land-

blight, bacterial brown spot, rust and I gene BCMV race types. National disease surveys had also confirmed

( Stavely et al., 1992 ). The Ur-5, Ur-6 and Ur-7 genes significant losses due to the foliar pathogen angular leaf

for rust resistance from donor parents B-190, Pinto spot (ALS), caused by the fungus Phaeoisariopsis

Olathe and GN 1140, respectively, were backcrossed griseola . Initial crosses to transfer bc-3 were therefore

into Harris, a GN cultivar developed at the University made as three-way crosses, using CIAT lines A 286 and

of Nebraska. Subsequently, GN BelMiNeb 4 and 5 BAT 477 as sources of ALS resistance. These parents

(Ur-4, Ur-6, Ur-11) and 7 (Ur-3, Ur-4, Ur-11) and were selected based on results from multi-location tests

pinto BelDakMi 18 with resistance (Ur-3, Ur-4, Ur-6, of many potential BCMNVand ALS resistance sources.

Ur-11 ). Germplasm lines from this backcross program Deployment of durable ALS resistance into certain

were released which have resistance to all of the rust Malawian landraces was complicated by the exis-

and BCMV races present in the US ( Pastor-Corrales tence of specific gene pools within P. vulgaris ( Gepts,

et al., 2001 ).

1998 ). Guzman et al. (1995) demonstrated a coevolu- tionary relationship between host resistance genes

2.3. Common bacterial blight and pathogenicity genes identified in Phaeoisariop- sis . A low frequency of offspring that combined

Common bacterial blight caused by Xanthomonas resistance to Andean and Mesoamerican races of

axonopodis pv. phaseoli (Xap) is a serious seed-borne ALS slowed the development of Malawian landrace

bacterial disease of common bean reducing both the types with ALS and BCMNV resistance. Progeny

yield and quality of bean seed ( Saettler, 1989 ). Com- from the third backcross to landrace parental types

mon bacterial blight often infects bean seed produced have been selected for BCMVN and ALS resistances.

in the tropics and the humid regions of the USA. Bean Several lines, currently in multiplication and multi-

germplasm lines ICB-3, ICB-6, ICB-8 and ICB-10 site testing, have grain and plant types nearly identical

derive their resistance to CBB from Phaseolus cocci- to their landrace progenitors.

neus ( Miklas et al., 1999 ). Resistance to CBB in leaves The Malawi/UC Davis breeding and BCMV testing

and pods was identified in red mottled landrace culti- activities have also produced three new varieties for

vars such as Pomjor 17 from the Dominican Republic the USA that carry both the I-gene resistance to

( Beaver et al., 1992 ). In Puerto Rico, the light red BCMV, and significant amounts of subtropical genetic

kidney germplasm line PR9443-4 was found to have background. The Dark Red Kidney variety UC

resistance to three strains of Xap when inoculated in Nichols, released in 2000 ( Temple et al., 1999 ), has

the greenhouse ( Beaver et al., 1999a ). The pinto bean

J.S. Beaver et al. / Field Crops Research 82 (2003) 87–102

Chase (Type II) is the first pinto bean to combine subsistence farmers in the Dominican Republic and resistance to CBB, bacterial brown spot, halo blight and

Haiti. PC-50, a selection from the Dominican Repub- some avoidance of white mold due to a porous canopy

lic landrace Pompadour Checa ( Saladin et al., 2000 ), ( Coyne et al., 1994 ). The cultivar GN Starlight with

possesses specific resistance to rust determined by the excellent seed size and bright white seed coat along

Ur-9 gene, adult plant resistance conditioned by the with moderate resistance to CBB was released in 1991

Ur-12 gene, which is hypostatic to Ur-9, and also a ( Coyne et al., 1991 ). The large, bright, white-seeded

dominant gene Pu-a for dense abaxial leaf pubescence Weihing (Type IIb) is the first GN cultivar to combine

( Bokosi, 1996 ). These three genes are inherited inde- resistance to CBB, halo blight, bacterial brown spot,

pendently ( Bokosi, 1996 ) and were mapped by Jung BCMV (I gene), rust (Ur-3, Ur-6) and architectural

et al. (1998) . Adult plant resistance was also detected avoidance to white mold ( Coyne et al., 2000 ). Efforts

in other landraces in the Dominican Republic by researchers from the University of Nebraska to

( Mmbaga et al., 1992a ) and in Andean germplasm pyramid resistance to CBB using molecular markers

from Malawi ( Bokosi, 1996 ). The genetic merit of are discussed by Kelly et al. (2003) and Miklas et al.

adult plant resistance and pubescence to reduce yield (2000a) . High levels of CBB resistance of VAX lines

losses in rust epidemics when specific resistance developed at CIAT are the result of an effort to pyramid

breaks down needs to be determined. Dense abaxial different sources of resistance ( Singh et al., 2001 ).

leaf pubescence in Caribbean germplasm is thought to contribute to reduced rust infection through trapping

2.4. Bean rust of spores on long dense hairs ( Mmbaga et al., 1992b ). The rust resistant red mottled bean cultivars JB-178

Bean rust caused by Uromyces appendiculatus and CIAS-95 were released in the Dominican Repub- (Pers.) Unger var. appendiculatus is an important

lic ( Arnaud-Santana et al., 2000a,c ). disease in most bean production regions of the world

Pinto Chase was developed in response to a request ( Stavely and Pastor-Corrales, 1989 ). Because Hon-

from the Nebraska Dry Bean Growers Association duras has among the most virulent pathotypes of rust

because of epidemics of rust in southwestern Nebraska in Central America and the Caribbean, it has proven to

and the lack of pinto cultivars with resistance to rust

be an ideal site to screen beans for resistance ( Araya, pathotypes endemic in the region ( Coyne et al., 1994 ). 1996 ). An effective field screening technique for bean

The annual value of the release of Chase, based on rust has been developed at the Escuela Agrı´cola

higher (7–10%) yields and reduced use of fungicides Panamericana where bean lines growing in benches

was estimated to be US$ 5 million ( Perrin et al., 2000 ). are inoculated with a mixture of virulent pathotypes of

Bean rust is a constraint in Africa as well as in the bean rust followed by a frequent moistening of the

New World. Germplasm and cultivars with resistance leaf canopy using micro-irrigation. Twelve navy

to rust races in East Africa have been identified and (BelMiDak), 18 pinto (BelDakMi) and 7 great north-

released. Examples of resistant cultivars include SUA ern (BelMiNeb) bean germplasm lines that pyramid

90 (originally a germplasm accession obtained from specific genes for resistance to bean rust were devel-

CIAT) and Rojo in Tanzania, and Kalima (also ori- oped ( Pastor-Corrales et al., 2001 ). The most recent

ginally obtained from CIAT) released by Bunda Col- germplasm releases such as BelDakMi RMR 18 com-

lege in Malawi. Efforts to systematically identify the bine I and bc-3 gene resistance to BCMVand BCMNV

rust races of importance in East Africa are in early with the Ur-3, Ur-4, Ur-6 and Ur-11 genes for rust

stages, although it appears that the Andean Ur-4 gene resistance. Pinto beans have become popular in the

would not be effective. Ur-3 does provide resistance to Caribbean following the distribution of this seed type

most African races, and when combined with Ur-5, by food assistance programs. Tropically adapted

provides resistance against all known African races. pinto bean lines that combine the Ur-6 and Ur-11 rust resistance genes and the bgm-1 gene for BGYMV

2.5. Anthracnose

resistance have been developed in Puerto Rico. Because pinto beans have a higher yield potential than

Anthracnose, the most serious seed-borne fungal Caribbean red mottled beans, these lines may benefit

disease of common bean, is caused by Colletotrichum

94 J.S. Beaver et al. / Field Crops Research 82 (2003) 87–102

lindemuthianum (Sacc. and Magn.) Scrib. Given the ( Polanco et al., 1996 ) and the inoculation of detached substantial variability in the pathogen ( Balardin et al.,

leaves ( Bautista-Pe´rez and Echa´vez-Badel, 2000 ). 1997 ), bean breeders have to combine multiple resis-

Quantitative inheritance and low to moderate her- tance genes to generate lines with durable resistance.

itabilities have been observed for web blight resistance Two black bean cultivars, Jaguar and Phantom, a navy

( Arnaud-Santana et al., 1998; Montoya et al., 1997; cultivar, Newport, a light red kidney cultivar, Chinook

Takegami and Beaver, 2000 ). Screening for web blight 2000 and a dark red kidney cultivar, Red Hawk, carry

resistance would be more effective evaluating both the Co-1 and Co-2 resistance genes to anthracnose

advanced lines in replicated trials. Jung et al. ( Kelly et al., 1995, 1998a, 1998b, 2000, 2001 ). The

(1996) detected QTLs for resistance to web blight, INIFAP bean breeding program in highland Mexico

rust, and common blight in a population of RILs has also been active in the development of bean

derived from the cross BAC 6/HT 7719. cultivars with anthracnose resistance. The black bean

Isolates of R. solani collected from different bean cultivars Negro Sahuatoba and Negro Altiplano and the

production regions of Central America and the Car- pinto bean cultivars Bayacora, Mestizo and Pinto Villa

ibbean vary in morphological characteristics, anasto- are resistant to most anthracnose pathotypes in Mexico

mosis group and virulence ( Godoy-Lutz et al., 1996, ( Acosta-Gallegos et al., 1995a,b, 2001a,b,c,d ). Balar-

2000 ). Only two lines from the CIAT core germplasm din and Kelly (1998) found the red mottled cultivar PC

collection, Talamanca and BAT 93, had useful levels

50 selected in the Dominican Republic to be among the of resistance to web blight in both Panama and Puerto most anthracnose resistant bean lines of Andean origin.

Rico (Beaver, pers. commun.). Bean breeders at the University of Puerto Rico and the EAP have initiated a

2.6. Web blight recurrent selection program to accumulate alleles for resistance to web blight. The base population con-

Web blight, caused by Thanatephorus cucumeris sisted of sources with moderate levels of web blight (Frank) Donk (anamorph: Rhizoctonia solani Ku¨hn) is

resistance from diverse origins. The lines are being one of the most important bean diseases in the warm

evaluated for web blight reaction in both Honduras and humid tropics, and when climatic conditions favor

and Puerto Rico.

disease development, can significantly reduce both Interspecific crosses may also be used to transfer web seed yield and quality ( Godoy-Lutz et al., 1998 ). Only

blight resistance from scarlet runner bean (P. coccineus) moderate levels of resistance to web blight are avail-

and tepary bean (P. acutifolius). Two accessions of P. able in common bean. The black bean cultivar Arroyo

coccineus from the CIAT core germplasm collection, Loro Negro and the small red cultivar Bribri are

G35066 and G35006, have been identified in Puerto reported to have some resistance to web blight

Rico as potential sources of resistance to web blight ( Arnaud-Santana et al., 2000b; Rosas et al., 2003 ).

( Takegami and Beaver, 2000 ). Climatic conditions in Because erect plant architecture contributes to disease

the natural habitat of P. coccineus can favor the devel- avoidance, it is difficult to separate physiological

opment of web blight. Wild bean plants with web blight resistance and disease avoidance in field trials.

symptoms have been observed at an altitude of 1400 m Further, field evaluations for web blight are limited

near Guinope, Honduras. The USDA core germplasm to seasons when climatic conditions favor disease

collection was also screened in the field in Puerto Rico development. In Puerto Rico, Takegami and Beaver

for web blight resistance. Only three lines (<1%) of the (2001) inoculated field trials with a suspension of

Phaseolus core collection were selected for further mycelia prepared from a virulent isolate of the web

evaluation. One of the lines selected was a tepary bean. blight pathogen, then applied short periods of over- head irrigation early in the morning for 2 weeks after

2.7. Bruchid (bean weevil) resistance inoculation. These practices helped to ensure a uni- form web blight infection in the field. Bean lines have

Two species of bruchids (Zabrotes subfasciatus and also been screened for physiological resistance in a

Acanthoscelides obtectus ) are major pests of dry bean greenhouse by applying droplets of a suspension of

seed around the world. Traditional methods for control mycelia on leaflets followed by frequent misting

of these pests include storing seeds in ash, treating

J.S. Beaver et al. / Field Crops Research 82 (2003) 87–102

with insecticides, tumbling infested bags ( Quentin measured at harvest maturity. Crop cover during the et al., 1991 ) and storing in containers to physically

middle of pod fill, has been found to have intermediate exclude the insects. Physical barriers are less likely to

to high correlations with bean seed yield under both

be effective against A. obtectus because this species stress and non-stress conditions ( Acosta et al., 1999 ). will infest seeds in the field before harvest. Genetic

The most reliable crop cover readings are obtained resistance to Zabrotes, first discovered in wild bean

when bean lines are grouped by similar phenology and accessions from Mexico, has been transferred into

growth habit. Genetic improvement for these dissim- cultivated germplasm by CIAT scientists ( Cardona

ilar types of drought will, in large part, require the et al., 1992; Kornegay et al., 1993 ). Resistance is

selection of different traits.

conferred by lectin proteins known as phytohemag- The collaborative structure of the B/C CRSP has glutinin, conditioned by alleles of the ‘arcelin’ seed

permitted the regional testing of germplasm for the protein present only in wild P. vulgaris ( Osborne et al.,

different types of drought stress present in individual 1988 ) and by the a-amylase inhibitor gene family

countries. Beaver and Rosas (1998) found that selec- proteins. Arcelin 1 (arc1) is particularly effective

tion for earlier flowering, a greater rate of partitioning against Z. subfasciatus, but not against A. obtectus.

and a shorter reproductive period permitted the selec- CIAT transferred arc1 into the RAZ germplasm lines.

tion of small red bean breeding lines having 1 week This resistance gene has been backcrossed at Sokoine

earlier maturity without sacrificing yield potential. University of Agriculture into elite local cultivars and

These combinations of phenological and physiologi- four lines with resistance to Z. subfasciatus have been

cal traits contribute to the genotypic avoidance of developed (Nchimbi-Nsolla, pers. commun.). One or

terminal drought. Researchers in Mexico found that two of these lines should be released after completion

selection for high seed yield potential under irrigation of on-farm testing in 2003. Current studies emphasize

may permit indirect selection for greater tolerance to arc4 , which confers limited resistance to both bruchid

terminal drought (Acosta, pers. commun.). species, and the transfer of this gene into advanced

Bean breeders in Mexico have developed bean breeding lines, as well as interspecific transfer of

cultivars having indeterminate, prostrate growth habits bruchid resistance from tepary bean into common

similar to pinto bean landraces in the semiarid high- bean. When used in conjunction with other storage

lands ( Acosta-Gallegos and Kohashi-Shibata, 1989 ). techniques, genetic resistance should be effective in

Cultivars such as ‘Pinto Villa’ use phenotypic plasti- preventing seed loss due to bruchids.

city to respond to intermittent drought (Acosta et al., 1995a). Pinto Villa, now grown on 90% of acreage planted to pinto beans in Mexico, will mature within

3. Abiotic stress

95 days after planting when rainfall distribution is favorable. Maturity, however, can range from 75 to

3.1. Drought 100 days depending on rainfall distribution patterns. Pinto Villa was found to be better adapted to early

Drought is a common cause of yield loss in beans, planting dates in the less productive rainfed environ- with two types of drought distinguished. Farmers in

ments than other pinto bean cultivars. Other cultivars Central America plant beans toward the end of the

released in Mexico with tolerance to intermittent rainy season in relay intercrops with maize. These

drought are Pinto Bayacora, Pinto Mestizo, Negro bean plantings often suffer yield losses due to terminal

Sahuatoba, Negro Altiplano, and Flor-de Mayo M- drought. In the highlands of Mexico beans are sub-

38 ( Acosta-Gallegos et al., 1995a,b, 2001a,b,c,d ). jected to extended periods of intermittent drought. The

Inter-racial and inter-gene pool crosses have been only traits that have proven to be valuable in both

made in Mexico to combine different drought toler- terminal and intermittent drought are earliness and

ance traits ( Schneider et al., 1997 ) and lines derived partitioning toward reproductive structures, resulting

from crosses between the Nueva Granada and Dur- in greater harvest index ( Acosta-Gallegos and Adams,

ango races appear to have promise based on earliness, 1991; Foster et al., 1994 ). A disadvantage of selection

disease resistance and seed yield in the highlands based on harvest index is that the trait can only be

( Rosales-Serna et al., 2002 ).

96 J.S. Beaver et al. / Field Crops Research 82 (2003) 87–102

Resistance to drought is confounded by root health production at lower altitudes in Central America ( Rosas and vigor and with resistance to soil-borne root rot

et al., 1997, 2000a ). The heat tolerant pink bean cultivar pathogens such as Fusarium spp. and R. solani ( Navar-

Rosada Nativa was released in Puerto Rico and the rete-Maya and Acosta-Gallegos, 1999 ). The lack of

Dominican Republic ( Beaver et al., 1999b ). The small adequate levels of root rot resistance contributes to the

red cultivar Bribri released in Costa Rica combines heat increased susceptibility of bean cultivars to intermit-

tolerance with web blight resistance. Indeterminate tent drought in highland production regions. Likewise,

Jamaica Red, a pink striped bean of Andean origin, tolerance to terminal drought is associated with resis-

was identified in Puerto Rico as a promising source of tance to ashy stem blight caused by Macrophomina

heat tolerance ( Baiges et al., 1996 ). Narrow sense phaseolina (Tassi) Goid. Bean cultivars for the low-

heritabilities of heat tolerance in populations derived lands of Mexico require resistance to ashy stem blight

from Indeterminate Jamaica Red were intermediate in in combination with tolerance to terminal drought and

magnitude (h 2 ranged from 0.4 to 0.6 in Puerto Rico low P soils (Acosta, pers. commun.). It has yet to be

during 1999 and 2000) meaning that breeders will determined how selection for shallow vigorous adven-

probably need to screen advanced generation lines in titious root growth to enhance tolerance to low P soils

replicated trials to identify heat tolerant lines ( Roman- ( Liao et al., 2001 ) might affect drought tolerance. Tio

Avile´s and Beaver, 2001 ). Indeterminate Jamaica Red Canela 75, has been observed to have greater drought

is currently being used to improve the heat tolerance of tolerance than other recently released small red culti-

kidney beans in the USA ( Miklas et al., 2000b ). vars (Rosas, pers. commun.). Ashy stem blight resis- tance of a bean line is often limited to a specific geographic region due to variability in virulence pat-

4. Yield potential and stability terns of the pathogen ( Mayek-Perez et al., 2001 ). Nevertheless, a few cultivars such as the pink bean

A range of different approaches to improve yield in Rosada Nativa and BAT 477 were found to be resistant

common bean have been employed by B/C CRSP in both Puerto Rico and Mexico. Echavez-Badel et al.

scientists. Adams (1982) pioneered the ideotype con- (2000) developed a greenhouse technique for screen-

cept in navy beans ( Kelly et al., 1989 ). This approach ing bean lines for resistance to ashy stem blight. This

was adopted to develop erect, indeterminate growth technique can also be used to screen lines for reaction

habit, medium-sized beans of the race Durango in the to Macrophomina isolates from different geographical

USA ( Kelly and Adams, 1987; Brothers and Kelly, regions. Miklas et al. (1998a) identified tepary bean

1993 ). The pinto bean cultivar Sierra and the great lines with resistance to ashy stem blight and QTL that

northern bean Alpine, which have unique erect plant could be used for indirect selection for resistance

architecture for these market classes, are the first ( Miklas et al., 1998b ).

products of this effort ( Kelly et al., 1990, 1992 ). Erect, indeterminate GN cultivars Starlight and Weihing were

3.2. Heat developed at the University of Nebraska to avoid white mold ( Coyne et al., 1991, 2000 ). The upright plant

In lowland environments, terminal drought stress can habit for Starlight and Weihing were derived from the

be aggravated by high temperatures. In Central Amer- black-seeded cultivar Tacaragua. Current type II great ica and the Caribbean, breeders have focused on heat as

northern cultivars such as Matterhorn ( Kelly et al.,

a constraint to expanding bean production in the low- 1999d ) have outperformed all other great northern land tropics. They have made significant progress in the

entries in the National Variety Trials in the USA over development of bean cultivars with improved levels of

the period 1998–2001. Kelly (2000) recently reviewed heat tolerance ( Rosas et al., 2000b ). Heat tolerance,

the importance of bean plant architecture for adapta- combined with BGYM, CBB and web blight resis-

tion and yield. Different ideotypes need to be devel- tance, would permit increased bean production during

oped for the diverse environmental and climatic non-traditional growing seasons when rainfall distri-

conditions in which beans are grown. Recurrent selec- bution patterns are more favorable. The release of

tion also has been useful for increasing yield of Andean Tio Canela 75 has permitted the expansion of bean

beans for the Caribbean ( Beaver and Kelly, 1994 ). The

J.S. Beaver et al. / Field Crops Research 82 (2003) 87–102

base population included large-seeded determinate in the USA which has more yield potential than check parents of Andean origin and small-seeded Mesoamer-

cultivars because of a greater number of seed per pod ican bean lines with greater yield potential and erect

( Wallace and Shardlow, 2001 ). plant architecture. The progeny were evaluated for

Given the diversity of approaches to improving yield yield in the F 5 generation using replicated hill-plots.

of common bean, Kelly et al. (1998c) proposed a more After two cycles of recurrent selection, several inde-

integrated approach that employed a three-tiered pyr- terminate lines with commercially acceptable seed for

amid where breeding activities differed at each level of the Caribbean were selected that yielded 30% more

the pyramid. The purpose of the breeding pyramid is to than determinate check cultivars. However, the lines

better utilize the genetic diversity present within P. selected for yield were 10 days later in maturity

vulgaris , yet to integrate and optimize ways to improve ( Beaver and Kelly, 1994 ).

yield for bean breeders who must work within the Breeding for physiological efficiency was proposed

constraints of growth habit, maturity and seed class as another approach to improve bean yield ( Wallace

restrictions. The pyramid offers a structured metho- et al., 1993 ). Limited adaptation is the major constraint

dology to exploit genetic variability both within the to breeding for yield, since a cultivar must fit the

cultivated and among the wild members of P. vulgaris. environment in which it will be grown. Days to

Since the domestication of common bean may have maturity is the most important physiological trait

reduced genetic variability, wild bean accessions may affecting that outcome. All bean plants have a specific

be a potential source of novel genes for adaptation and growth rate. Through genetic manipulation, this

yield ( Koinange et al., 1996 ). A BC 4 F 4:7 line derived growth rate can be increased. Increasing growth rate

from a cross between an elite black bean cultivar does not necessarily translate into higher seed yield,

Negro Tacana ( Lopez-Salinas et al., 1997 ) and a wild however, unless greater amounts of the photosynthate

bean accession G24423 from Colombia produced the from biomass are partitioned to the seed. Indirect

highest recorded bean yield in a Michigan State Uni- selection for the three major physiological traits affect-

versity yield trial (5790 kg ha 1 ). The original cross ing yield, namely plant biomass, harvest index (HI),

and backcrosses were made at CIAT and the inbred and days to maturity, should result in improved yield

progeny were evaluated through the B/C CRSP net- ( Wallace et al., 1993 ). Simultaneous selection is

work in Mexico and the USA. The highest yielding required because genetically established interrelation-

BC 4 F 4:7 line outperformed the recurrent parent, Tacana ships occur among these three traits. An increase in

by 27% in this study (Kelly, pers. commun.). days to maturity, which is undesirable in some envir-

Yield stability is a critically important characteristic onments, results in an increase in biomass. An increase

for both subsistence farmers in developing countries in HI results in a decrease in days to maturity and a

and producers in the USA. In Michigan, Kelly et al. decrease in biomass. All three physiological traits and

(1987) , compared the yield stability of determinate and the correlations among them can be quantified by

indeterminate beans, and found erect, short vine inde-

a yield system analysis (YSA) of yield trial data terminate (Type II) cultivars to have greater yield ( Wallace et al., 1993; Wallace and Yan, 1998 ). Selec-

potential and more predictable performance than cul- tion for biomass within the constraints of maturity is

tivars having determinate (Type I) or indeterminate equivalent to actual selection for a higher rate of

Type III growth habits. Beaver et al. (1996) evaluated biomass accumulation. Selection for yield per day

the yield stability characteristics of 15 determinate and should help compensate for the tendency for higher

15 indeterminate red mottled landrace cultivars from biomass to result in longer duration of growth. Selec-

the Dominican Republic. The indeterminate lines gen- tion solely for greater biomass will give later maturity,

erally had greater and more predictable yields. Inde- lower HI and higher yield, whereas selection solely for

terminate bean lines with high yield potential were HI results in early maturity with an accompanying

identified that would be better suited for irrigated reduction in yield. Wallace et al. (1993) noted that

production in the valleys. Other lines were identified selection for yield can result in increased harvest index

that expressed more adaptation to lower yielding envir- with little or no increase in biomass. The use of YSA

onments. Beans in the tropics are often produced in led to the release of RedKanner light red kidney bean

very different soil types and under varying rainfall

98 J.S. Beaver et al. / Field Crops Research 82 (2003) 87–102

distribution patterns. Breeding beans for specific envir- plant breeding (PPB) approaches that involve an active participation of farmers in the development of improved

environment interaction and may reduce the number of varieties, have been used since 1999 by the Zamorano traits that need to be selected for each environment

breeders in two bean producing regions of Honduras ( Beaver, 1999 ). A multiplicative interaction (AMMI)

( Rosas, 2001 ). Although these efforts are still experi- model was used by Macchiavelli and Beaver (1999)

mental, simplified PPB methodologies can help to to identify red mottled lines with greater yield potential

increase the adoption of improved varieties among and stability for lowland tropical regions.

small farmers, especially in communities having lim- ited access to existing extension systems or improved cultivars. Awell-organized PPB program requires train-