Introduction

Common bean (Phaseolus vulgaris L.) is the most important grain legume, with 28.9 million tonnes produced globally on approximately 33 million hectares (FAOSTAT 2019). In Africa, the common bean is produced on 7.8 million hectares, which is equivalent to approximately 25% of the global area of common bean production (Nadeem et al. 2021). Common bean is consumed by more than 100 million households in Africa (Mukankusi et al. 2019). The top five African countries producing common bean are Tanzania, Uganda, Kenya, Burundi and Ethiopia (FAOSTAT 2019). Common bean contains important nutrients for human health such as carbohydrates (50–60 mg kg^-1), dietary fiber (75–80 mg kg^-1), energy (50–70 mg kg^-1), proteins (18.5–25 mg kg^-1), iron (18.8–82.4 mg kg^-1), magnesium (19–26 mg kg^-1), potassium (43–300 mg kg^-1) and zinc (32.6–70.2 mg kg^-1) (Rubyogo et al. 2019; Punia et al. 2020). Common bean is a healthy food, the consumption of which can reduce incidence of diseases such as cancer and diabetes, due to its low fat content and lack of cholesterol (Robinson 2019).

Fig. 1: Common bean production (tonnes) and area under bean cultivation (hectares) in Africa in 2010–2019

Bean consumption in Africa is high, reaching up to 66 kg person^-1 y^-1, while the global average is 2.51 kg person^-1 y^-1 (Nadeem et al. 2021). This indicates the importance of beans as a food crop in Africa compared with other regions. However, on‐farm productivity remains low (0.8 t ha^-1) (Fig. 1), compared to a potential reported productivity of 2.5–5 t ha^-1 (Muthoni et al. 2017). Low productivity is attributed to both biotic and abiotic factors, including diseases, insect pests, poor seed quality, drought, heat, low soil fertility and poor crop management. Of these factors, disease, particularly anthracnose caused by Colletotrichum lindemuthianum is an important bean yield inhibitor (Padder et al. 2017; Mlemba 2021).

The C. lindemuthianum, first discovered in Lima bean (Phaseolus lunatus) samples from Germany in 1875 by Lindemuth and described by Saccardo (1878). Since then, it has spread and is now distributed worldwide including in Africa, Canada, Europe, Latin America and the USA (Ansari et al. 2004). In Africa, the disease is of particular concern in Burundi, D.R. Congo, Ethiopia, Kenya, Rwanda, Tanzania and Uganda (Farrow and Muthoni 2020). Anthracnose is most serious in temperatures of about 17°C, with relative humidity above 92% and soil pH of 5.8–6.5 (Padder et al. 2017). Bean anthracnose attacks leaves, stems, pods and seeds, causing dark brown necrotic lesions that decrease leaf photosynthetic activity. Reduced photosynthesis results in leaf senescence, stunted bean growth and eventual death. Yield loss of up to 100% due to anthracnose has been reported in Africa (Masunga et al. 2020).

In comparison, angular leaf spot causes yield loss of 80% and bean common mosaic virus causes yield loss of 40% (Mwaipopo et al. 2017) In Africa; some of the commercial bean varieties are susceptible to anthracnose disease (Muthoni et al. 2017), therefore, farmers in major bean-producing regions rely heavily on growing local cultivars. It is not clear whether local cultivars are preferred over commercial varieties based on resistance to anthracnose or due to differences in the ease of disease management.

Anthracnose can be managed by crop rotation, planting resistant varieties, foliar application of plant extracts, seed treatment and foliar application of contact or systemic fungicides. However, common bean production in Africa is vulnerable to anthracnose due to poor management and the prevalence of diverse races of the anthracnose pathogen that render the majority of varieties susceptible. Genes in common bean that confer resistance to anthracnose have been documented (Ferreira et al. 2013). However, common bean breeders are unsure which gene to deploy in resistance breeding programs. Pathogen variability is documented (Munda et al. 2009; Palacıog ̆lu et al. 2021) and marker-assisted selection is used in developing resistant varieties (Meziadi et al. 2016; Padder et al. 2017). Nevertheless, great variability in pathogenicity makes management of anthracnose disease in Africa difficult (Uwera et al. 2021). This is due to extensive diversity and virulence of C. lindemuthianum, where a single gene can affect stability of resistance in the bean plant and a complementary gene conditions pathogen virulence. Information on fungal infection and pathogenicity of C. lindemuthianum is very limited and fragmented. Therefore, the aim of this review is to discuss mechanisms for anthracnose infection and pathogenicity and to design suitable disease management strategies. This information will facilitate stakeholders working on common bean in Africa to better manage anthracnose disease to allow for increased productivity, nutrition and income.

Mechanisms of infection

Infection is the process by which a pathogen establishes contact with and acquires nutrients from susceptible host cells or tissue. The process of anthracnose infection begins when a C. lindemuthianum conidium (spore) lands on the leaf, stem or pod of a bean, adheres to the plant cuticle and germinates (Pellier et al. 2003; Alkemade et al. 2021). Conidia are disseminated by splashes from rain and quickly attach to the aerial parts of a plant to infect it. Under humid conditions, the conidium germinates and develops a spherical structure, the appressorium, which is essential for epidermal cell penetration (Sharma and Kulshrestha 2015). The appressorial surface adhering to the cuticle is flattened and a pore forms on the flat surface. Subsequently, an infection peg emerges through this pore, pierces the bean leaf cuticle and cell wall and directly mediates entry into the host epidermal cell. Oxidase, cutinase and lipases are secreted from the infection peg to degrade the plant cuticle and wax layers (Pawlowski and Hartman 2016).

Fungal spores germinate when they come into contact with the bean plant, then a germ tube elongates to form an appressorium for penetration (Chethana et al. 2021). Germ tube elongation and differentiation occurs in response to environmental signals like surface hardness, hydrophobicity, plant signals and surface topography (Tucker and Talbot 2001). If appropriate environmental signals are not received, the germ tube remains undifferentiated and will eventually stop growth upon nutrient depletion. If appropriate physical and chemical signals are detected by the germ tube, a complex morphogenetic program is induced, causing appressorium formation which results in indentation in the cell wall. The morphogenetic events from spore attachment to appressorium formation are motivated by host plant signals like cutin monomers, ethylene and topographic signals, and environmental factors like temperature and substrate hydrophobicity. Finally, an infection peg protrudes from the appressorium, penetrating through the cell wall where infection hyphae grow and develop into infection vesicles. C. lindemuthianum is considered a hemibiotrophic fungus (Dubrulle et al. 2020), spending part of the infection cycle as a biotroph and the other as a necrotroph.

Phases of infection

Biotrophic phase: The biotrophic phase is the first stage of infection, where broad primary hyphae grow out of the infection vesicle (Padder et al. 2017; Ciofini et al. 2022). During this phase, the fungus grows between the cell wall and the plasma membrane of host cells without causing death. At this stage, the pathogen establishes interactions with the host plant, producing surface proteins that are important for adhesion and invasion. After successful penetration, the infection vesicle and primary hyphae are formed inside the living host’s epidermal cells and invaginate the host cell’s plasma membrane. Biotrophic fungal pathogens contain sophisticated structures like appresoria, infection pegs and haustoria used for nutrient absorption and secretion of effector proteins.

The pathogen’s primary hyphae penetrate through cell walls by mechanical force. The hyphae grow near the infection vesicle and follow the plant cell walls in such a way that half of the hyphal circumference is in connection with the cell wall at all times (Suparman et al. 2018). C. lindemuthianum forms infection structures for successful attachment, host recognition, penetration, pathogenesis and proliferation. The structures are regulated by gene expression and complex regulatory pathways to facilitate compatible interactions between plant tissue and the pathogen (Padder et al. 2017). Lytic enzymes, carbohydrates and proteins are developed for virulence and haustoria for nutrient absorption and metabolism (Gebrie 2016; Pradhan et al. 2021). Once the fungal effector has bypassed the plant’s defense mechanisms, the plant will no longer resist, reducing its production of defense signaling molecules such as salicylic acid. Depending on environmental conditions, the biotrophic phase ends 2–3 days after inoculation (Suparman et al. 2018). Thereafter, the fungus switches to the necrotrophic phase, which corresponds with the onset of anthracnose symptoms.

Necrotrophic phase: The necrotrophic phase is the second stage of infection, comprising many thin hyphae branching off from the primary hyphae and moving freely through the bean plant in all directions, penetrating cell walls and membranes. During the necrotrophic phase, the fungus differentiates secondary hyphae, which are thinner than primary hyphae and grow extensively, leading to the disorganization and death of infected host cells (Suparman et al. 2018; Alkemade et al. 2022). At this stage, the pathogen produces a cell wall-degrading enzyme that kills host cells by hydrolysis. Growth and multiplication of the fungal pathogen is favored by certain weather conditions. If optimal rainfall, temperature and relative humidity occur, the pathogen can invade the bean plant to its maximum potential regardless of plant defense and as a consequence anthracnose develops (Wang and Kerns 2017). The pathogen spreads into the leaves, stem, pods and seeds (Alkemade et al. 2022) by direct growth through cells as intracellular mycelia; subsequently, it invades the xylem. If successful, C. lindemuthianum grows and continues branching within the infected host plant tissue until the plant dies. The necrotrophic phase is completed 6–7 days after the beginning of the infection cycle.

Switching from the biotrophic to the necrotrophic phase is facilitated by the CLTA1 gene. This encodes a protein that coats the hyphae to form a pseudo cell wall to avoid recognition by the common bean plant (Dufresne et al. 2000). Consequently, the pathogen produces phytotoxins which kill the plant cells, preventing them from responding in a synchronized means to resist infection. Toxins cause pores to form in the mitochondria through which small molecules leak, ceasing adenosine triphosphate (ATP) synthesis and causing cell death (Dufresne et al. 2000). Finally, the toxin induces reactive oxygen species in the bean plant which cause membrane breakdown and nutrient leakage.

Mechanisms of pathogenicity

Pathogenicity is the ability of a pathogen to interfere with the essential functions of a host plant or animal, thereby causing a disease. The mechanism of C. lindemuthianum pathogenesis involves the use of: (1) mechanical forces which include the formation of appressoria and penetration of the host cuticle and cell walls; (2) chemical weapons including enzymes like amylases, cellulases, cutinases, hemicellulases, lignases, lipases, pectinases and proteases; (3) non-host specific and host-specific toxins and (4) growth regulators including abscisic acid, auxins, cytokinins, ethylene and gibberellins (Chethana et al. 2021). Moisture is an important environmental factor influencing the formation of appressoria and development of anthracnose. Moisture affects infection, dispersal, spore germination, anthracnose establishment and development. The pathogen is inactive during the dry season, becoming active when favorable conditions are encountered. It detects and responds to host cues like chemical signals, electrical stimuli, pH, host surface chemistry and surface hardness on penetration (Sharma and Gautam 2019).

Anthracnose is common in African farmers’ bean fields and has wide pathogenic and molecular variability. The disease is becoming more noticeable in Africa due to climate change. A total of 160 races of C. lindemuthianum have been described in Africa (Table 1). Common bean cultivars grown in Africa have significant diversity and adaptation to different climatic and agronomic conditions, and many of the several Andean and highly virulent Mesoamerican C. lindemuthianum races have been characterized in Africa.

During infection of common bean, the pathogen secretes extracellular protein and glycoproteins, which contribute to pathogenicity. Nevertheless, the amount of protein and glycoproteins produced is unknown. Extracellular protein establishes a molecular dialogue between the parasite and host. Hydrolytic enzymes, such as cutinase and pectinases, are produced when anthracnose is attached to the common bean plant, during establishment, development and colonization (Oeser et al. 2002; Li et al. 2007). The production of cellulolytic and pectinolytic enzymes is determined by the degree of cell wall penetration during pathogenesis and the level of enzyme inhibition by the host; this eventually interferes with disease development. The mechanism of pathogen–host interaction involves a series of stages from initial attachment of C. lindemuthianum, to infection, disease development and colonization, described in the following sections.

Pathogen attachment to the bean plant: Attachment of C. lindemuthianum to the bean leaf surface is an essential pre-infection event that determines infection success. A conidium is used as the propagule, adhering to the plant surface with the role of host recognition and subsequent fungal development. The propagule contains a mucilaginous substance, a mixture of water-insoluble polysaccharides, glycoproteins lipids and fibers, which when moistened become sticky and facilitate the pathogen’s adherence to the plant (Chethana et al. 2021). Once adhesion to a leaf or stem has occurred, the pathogen can become established. If adhesion is disrupted by nontoxic synthetic compounds, the spore will neither infect leaves nor stem and there will be no disease development. Temperature changes can alter the adhesion properties of conidia (Sela-Buurlage et al. 1991). Fluctuations in temperature influence respiration and metabolic rate, both of which impair adhesion (Mercure et al. 1995), though the mechanism of this influence is unknown. The adhesion of conidia declines beyond 30 days.

High turgor pressure develops on melanized appressoria walls which supports penetration. Penetration hyphae accumulate a cytoskeleton at their tip which secretes degrading enzymes including cellulases, cutinase, lignases and pectinases to facilitate penetration of the cuticle and plant cell wall (Sharma and Gautam 2019). Infection hyphae differentiate within the bean plant and during differentiation, degrading enzymes are synthesized to facilitate successful establishment, which leads to development of disease symptoms.

Pathogen establishment: Once C. lindemuthianum passes through the external protection of the bean plant, it lives within the host for some time, to obtain nutrients and produce toxins that cause disease symptoms. The pathogen completes parasitic colonization of the plant by reprogramming the defense electron structure of host cells through a range of disease effector proteins (Chethana et al. 2021). Apoplastic effectors are secreted in the plant by extracellular targets and surface receptors. Cytoplasmic effectors translocate inside bean plant cells via an infection vesicle that invigilates in the living host. Effectors facilitate infection or activate disease reaction. The pathogen produces cytokinins on the leaf surface, which is the primary site for pathogen infection of the common bean plant (Sharma and Gautam 2019).

Anthracnose development: Seed-borne infection plays a significant role in disease development. Seasonality affects the persistence of anthracnose. Disease development, spread and severity index coincide with frequent heavy rain and moderate temperatures (Table 2). Heavy rain spreads C. lindemuthianum, stimulating and releasing fungal spores embedded in gelatinous acervuli (Mugambi 2013). C. lindemuthianum requires cool temperatures for growth, infection and development. High temperatures do not affect spread of anthracnose disease, but prolonged high temperatures increase disease severity by the disease spreading slowly for long time.

During disease development, a brick red to purplish discoloration is observed on the veins on the lower surface of the leaf (Fig. 2). Anthracnose disease symptoms extend on the upper surface of the leaf and at the base of the stem, progressing upwards and producing dark brown to black lesions along the veins. Disease symptoms are also observed on bean pods, causing dark red sunken spots (Fig. 2) and finally on bean seeds. In severe infections, young pods shrivel and dry prematurely. When many pods are infected, the number of seeds infected increases and grain yield and seed quality decreases (Mohammed 2013).

Anthracnose resistance mechanism: Common bean has a mechanism that may defend against anthracnose. The crop contains phytochemicals such as catechol, polyphenols and salicylic acid which act as proteinase and polygalacturonase inhibitors and antioxidants. These phytochemicals restrict/interfere with pathogen nutrition and retard anthracnose development, contributing to disease resistance. Once these phytochemicals are no longer sufficient to stop infection development, plant cells increase levels of antifungal phenolic compounds, producing fungitoxic quinones at the infection site. These toxins increase active oxygen species, making the bean plant cell an unfavorable medium for further pathogen development (Weidner et al. 2018). The ability to increase phytochemical production differs depending on bean variety and the environment in which the bean is grown (Ghasemzadeh et al. 2018), which leads to differences in anthracnose resistance.

Management of anthracnose disease

Use of resistant varieties: Cultivation of resistant varieties is the most effective and efficient method of anthracnose management (Negera and Dejene 2018; Palacıog ̆lu et al. 2021; Uwera et al. 2021), because the major transmission and survival structure for the anthracnose pathogen is the seed, in which the pathogen can survive for up to five years. Movement of infected seed between sites increases the chance of spreading anthracnose from one location to another. To avoid this, farmers are advised to use improved bean varieties (Table 3).

Use of resistant varieties is the most economical and effective means to control anthracnose (Paulino et al. 2022), as it ensures protection against the disease, saving time, energy and money that would otherwise be spent on other control measures. Resistant varieties are easy to use, completely avoid the disease cycle, are better for the environment as demand for agrochemicals is reduced and ensure production of healthy beans (Mohammed 2013; Negera and Dejene 2018; Prabha et al. 2021). Use of resistant varieties significantly increases grain yield, by 225 kg ha^-1 (Mukankusi et al. 2019). Although anthracnose resistance provides economical control, farmers’ adoption of improved, resistant varieties is limited. Most African farmers use farm-saved bean seed from previous harvests or purchase seed from neighbouring farmers or at local village markets (Sperling et al. 2021). As a consequence, anthracnose levels are high. Responsible authorities (seed regulatory authorities, seed companies and agro-dealers), should ensure timely and local availability of improved bean varieties at an affordable price.

Due to the high degree of genetic and physiological variability of C. lindemuthianum, management using single-gene resistance is not so much effective, as resistance is not controlled by single gene. For instance, four differential cultivars, G2333 (Co-42, Co-52, Co-7=Co-35), Cornell 49-242 (Co-2), Tu (Co-5) and AB136 (Co-6, Co-8), were reported to confer broad-spectrum resistance to anthracnose in Brazil and Uganda, yet succumb to disease caused by some C. lindemuthianum races. With high pathogen diversity and frequent emergence of new pathotypes, researchers should continue identifying new sources of resistance to bean anthracnose disease. In Africa, many common bean farmers work in diverse environments, exposed to different climatic and agronomic conditions. Different agroecosystems can be favourable for different varieties of common beans. To recommend resistant varieties to anthracnose, researchers are encouraged to conduct triadic comparison of technologies (TRICOT) in evaluation of anthracnose-resistant varieties, which will help to evaluate new varieties on a farm level.

Tricot is a simple format that engages many farmers in evaluation, from the initial point of trial establishment onwards, providing feedback on what has been observed from the experiment. Tricot combines farmer-generated trials and preferences with many seasons of data collection on cropping systems and household farming, allowing in-depth analysis at low cost. The tool engages many available management options and involves many farmers. It allows each farmer to evaluate three randomly assigned genotypes from a large set of genotypes. The tool reduces bias and risk, by recording performance data across different growing seasons and locations (Etten et al. 2018, 2019). In addition, the tool allows sharing data through ClimMob software for meta-analysis to validate and improve recommendations based on existing data. Table 1: Races of C. lindemuthianum characterized in Africa from 1991 to 2021

Country	Races of C. lindemuthianum	Total no of races	Abundant race	Highly virulent race	References
Burundi	9, 69, 84, 87, 141, 246, 358, 384, 385, 401, 448, 449, 485,515,576,768	10	401, 485	401, 485	Bigirimana et al. (2000); Kamiri et al. (2021)
Ethiopia	9, 34, 73, 128, 272,321,385,465, 587, 898,1011, 1172, 1250, 2073, 2225, 2255, 2260, 3047	18	9, 272, 1011, 2260	2073, 2225, 2260, 3047	Gezahegn et al. (2021)
Kenya	1, 2, 17, 23, 38, 55, 485	7	38, 55	38	Nunes et al. (2021)
South Africa	3, 6, 7, 49, 65, 80, 81, 83, 89, 263, 323, 390, 593	13	3, 7, 81, 83, 89, 263	7, 81, 83, 89, 263	Koch (1996); Muth and Liebenberg (2009); Nunes et al. (2021)
Tanzania	0, 2, 9, 12, 28, 31, 38, 39, 60, 62, 63, 91, 98, 101, 105, 112, 128, 129, 133, 155, 166, 167, 182, 191, 192, 274, 277, 287, 316,344, 398, 524, 618, 661, 716, 770, 776, 832, 849, 944, 958, 1176, 1271, 1478, 1510, 1515, 1678, 1696, 1805, 1891, 2061, 2434, 2566, 2614, 3068, 3264, 3610	57	0, 2	3610	Mwalyego (1991); Ansari et al. (2004); Masunga et al. (2020)
Uganda	0, 1, 2, 3, 4, 6, 14, 17, 19, 23, 42, 55, 81, 102, 128, 130, 227, 262, 264, 268, 320, 352, 375, 382, 386, 452, 481, 503, 511, 704, 713, 767, 784, 1023, 1024, 1094, 1169, 1175, 1334, 1471, 1527, 1536, 1538, 1791, 1834, 1856, 1857, 1989, 2023, 2039, 2045, 2047, 2079, 2479, 3086, 4033, 4095	57	167, 2047, 4095	1024, 1536, 1538, 1856, 1857, 1989, 2023, 2039, 2045, 2047, 3086, 4033, 4095	Nkalubo 2006; Mwesigwa 2008; Kiryowa et al. (2016)
Zambia	37,39, 53, 65, 73, 84, 207, 247, 255, 342, 382, 407, 485, 510,566	13	247	247	Zulu 2005; Nalupya et al. (2021)

Table 2: Climate variables during the common bean cropping season (meteorological station located at Arusha airport). Source: TARI Selian

Year	Mean rainfall March-June (mm)	Mean temperature (°C) March–June		Mean RH (%) March-June	Yield loss (%)
Year	Mean rainfall March-June (mm)	Max.	Min.	Mean RH (%) March-June	Yield loss (%)
2015	836.1	26.5	15.6	87.1	64
2016	753.4	26.4	15.3	86.5	60
2017	924.7	26.5	15.5	87.4	65
2018	1286.7	26.9	16.1	94.7	95
2019	1132.3	26.6	15.7	91.3	67
2020	1199.9	26.7	15.9	93.1	71
2021	557.9	26.3	15.4	86.6	42

Fig. 2: Symptoms of anthracnose disease at the Tanzania Agricultural Research Institute (TARI), Selian

Tricot has been used in different countries such as Ethiopia, India and Nicaragua, with promising results across various technologies (Etten et al. 2019). Through the tricot approach, many farmers in Tanzania are being engaged to test a wide range of common bean varieties for anthracnose resistance and adaptation to different environments on farms where the disease is prevalent. More than 1500 on-farm tricot trials have been established in an incomplete block design in the northern, southern highland and western zones of Tanzania. The process offers practical learning to farmers, and provides interpretable and meaningful results for real environments on different farms. The The approach works efficiently, and many stakeholders feel it is useful (Etten et al. 2018, 2019).

Table 3: Examples of anthracnose-resistant varieties released in 2011–2020 in Africa (Muthoni et al. 2017).

Country

Variety

Burundi

LM9220492, MLB122-94B, RWR 2091, CODMLB003, IZ0201543, MAC44, MAC70, MUHORO, RWV1129, RWV 1272

DR Congo

ECAPAN 021, G16157, TY 3396 -12, PRELON, K 132, MAHARAGI SOYA, RJB – 1, VCB81013, NUA 99

Eswatini

MASAI – RED, NUA 45, ZEBRA, KAMIESBERG, MN 12685–15, MR 13557–17-7, MR 14215-9, RCB 265, WERNA

Ethiopia

GLP-2, KATB1, Awash-1, SER-119,SER-125, Fedis, Babile, Hirna, BRC-ACC.NO-4, SARI-1

Ghana

G53, G90, ROBA-1, SMR 53

Kenya

KAT-RM-001, KAT-SR 01, KAT-SW-12, KAT-SW-13, KCB 13-02, KCB 13-09, KCB 13-11, MN6

Lesotho

CAL143

Madagascar

RI 5-3, AND 932-B1, EMP 250-5-1, RI 5-5

Malawi

KK03/KK25/68/S-F, KK25/MAL/112/S-F, KK25/MAL/19/S-F, KK25/NAG/184/S-L, MAL/KK25/9/S-F, MAL/KK25/443/S-L, NAG/KK25/168/S-L, BF 13607-9, SER 124, SER 83

Mozambique

VTT 924/4-4, VTTT 925/9-/-2

Rwanda

RWV1348, RWV 2269, RWV 3317, SB - 273

South Africa

KAMIESBERG, PAN 9213, PAN 9216, RS 7

Tanzania

TARIBEAN 1, TARIBEAN 2, TARIBEAN 3, TARIBEAN 4 TARIBEAN 6, Selian 14, Selian 15, Calima Uyole, Fibea, Rosenda, Pasi, Uyole 16, Uyole Nyeupe

Uganda

NABE 4, NABE 10, NABE 15, NABE 16, NABE 18, NABE 19, NABE 20, NABE 21, NABE 26C, NABE 27C, NABE 29C, NAROBEAN 1, NAROBEAN 2, Moore 88002, MAC 44, NYIRAMUHONDO

Zambia

SPS2-4P-24, C30-920

Zimbabwe

Gloria, NUA45, SUG 131, SWEET VIOLET, CHERRY, SC SUPERIOR

Cultural control: Produce bean seeds in areas that are not anthracnose hotspots (Yesuf and Sangchote 2005; Mohammed 2013; Etana 2022). Plant certified disease free seed grown in non-hotspot areas to anthracnose. Plant beans following the recommended planting dates (Girma et al. 2022) to avoid the extraordinary conditions favoring anthracnose development. Plant beans following the recommended spacing of 50 cm between rows and 20 cm between plants with two seeds per hole, or 50 cm between rows and 10 cm between plants with one seed per hole, to avoid foliar drying (Bush 2009). Timely weeding is required to ensure efficient air circulation and to decrease moisture in the bean plant. Over-irrigation should be avoided to reduce wet conditions which promote disease infestation. Weekly field scouting for anthracnose symptoms is encouraged in order to identify anthracnose as soon as it appears and allow the implementation of control measures to avoid spreading the disease (Batureine 2009; Etana 2022). Disinfect seed storage facilities with a 10% bleach solution equivalent to 0.5% sodium hypochlorite and Dettol to prevent contamination (Buruchara et al. 2010). Incoporate bean residues under the soil immediately after harvest to reduce fungus survival during winter (Yousef 2021). Additionally, Rotate common bean field with cereals and solanaceous crops every two to three years to minimize further pathogen survival (Buruchara et al. 2010; Etana 2022).

Use phosphate fertilizer to the bean field to reduce the incidence and severity of anthracnose (Gadaga et al. 2017). In Brazil, spraying potassium phosphate (KI) and manganese phosphate (Mn) reduced area under the disease progress curve (AUDPC) by 78.3 and 77% respectively (Gadaga et al. 2017). Potassium phosphate formulations have also been reported to reduce anthracnose severity by 68% in the USA (Costa et al. 2019). Sodium silicate should be evaluated and promoted for use on common bean fields in Africa to reduce severity of anthracnose. Application of sodium silicate in Brazil increased silicon concentration in bean leaves by 58%, decreased AUDPC by 62% and increased grain yield by 51% (Polanco et al. 2014). Despite these recommendations and implementation of some similar practices by bean farmers in Africa, anthracnose infection continues to threaten farmers’ fields. Future research should investigate the optimum burying depth for bean residues and optimum burying period. Recommended spacing of bean plants and avoidance of mono-cropping should be encouraged and timely weeding in and around the field should be emphasized. Weekly field scouting for disease symptoms should be encouraged. A literature search encountered limited information on the application of phosphate fertilizer and sodium silicate in Africa. Information from other countries including Brazil, evokes the possibility of using phosphate fertilizer and sodium silicate to reduce anthracnose severity on common beans and consequently achieve greater gains in yield. Future research in Africa should explore the potential of phosphate fertilizer and sodium silicate to control common bean anthracnose.

Biological control: Use of plant growth promoting rhizobacteria (PGPR) such as species of Pseudomona and Bacillus (Sharf et al. 2021) and various species of fungi namely Trichoderma spp. (Javaid et al. 2021; Khan et al. 2021), Penicillium spp. and Aspergillus spp. (Khan and Javaid 2022a, b) as biological control agents against many fungal plant pathogens is gaining much importance nowadays. Spore suspension of Trichoderma viride can be applied as a seed dip and soil drench to control C. lindemuthianum (Bankole 1996). Furthermore, bean seeds can be smeared with cultures of Gliocladium virens, T. hamatum or T. harzianum before sowing to inhibit pathogen infection (Padder et al. 2010). Bean seeds can be inoculated with rhizosphere bacteria from genera such as Arthrobacter, Bacillus, Pseudomonas and Serratia to control anthracnose (Duangkaew and Monkhung 2021). Extracellular metabolites like antibiotics, lytic enzymes, siderophores, and volatile compounds produced by rhizobacteria (Bacillus cepacia and Pseudomonas fluorescens) effectively reduce lesions on and damage to common bean plants caused by anthracnose. Biological application of plant extracts such as Alchornea cordifolia, Azadirachta indica, Carica papaya, Cymbopogon citratus, Cymbopogon flexuosus, Lantana camara, Ocimum sanctum, Piper guineense, Piper nigrum, Tabernaemontana pachysiphon, Vernonia polyanthus and Xylopia aethiopica on bean leaves and stems can control anthracnose (Enyiukwu et al. 2021). Foliar application of Cymbopogon flexuosus, V. polyanthus and Carica papaya in Brazil reduced anthracnose severity by 57.2, 37.6 and 34% respectively (Silva et al. 2015). Studies in Nigeria recorded high (83%) anthracnose incidence on untreated cowpea plots compared to 20.4, 27 and 30% incidence when L. camara, Tabernaemontana pachysiphon and Alchornea cordifolia treatments were used, respectively (Enyiukwu et al. 2021). Toxic activity of some plant extracts like X. aethiopica, P. guineense and Azadirachta indica in the form of benomyl, carbendazim and thiophanate-methyl minimize anthracnose in legumes (Awurum and Uchegu 2013). Biological control of anthracnose is an economical and environmentally sound approach, but has received comparatively little attention in Africa due to lack of information available for farmers on how and when to use biological control measures. Common bean farmers in Africa should be trained on biological control methods to control the incidence and severity of anthracnose. Researchers should establish demonstration plots to promote the use of plant extracts to control anthracnose, reducing the negative impacts of synthetic pesticide use.

Chemical control: Seed treatment with Apron Star, benlate, carbendazim, difenoconazole, mancozeb, Seed Plus, Seed Care and thiram increases seed germination, controls mycelial growth of C. lindemuthianum, controls seed-borne infection and increases seed quality and grain yield (Buruchara et al. 2010; Padder et al. 2010; Boersma et al. 2020; Alkemade et al. 2022). Foliar spraying of bean plants with azoxystrobin, benomyl, carbendazim, chlorothalonil, folpan, mancozeb, mancozeb + carbendazim, pyraclostrobin or thiophanate-methyl + chlorothalonil at an early stage of disease development reduces pressure from anthracnose (Mohammed 2013; Hirpa and Selvaraj 2016). For example, economic analysis of fungicide application in Ethiopia revealed that the highest net benefit is obtained from the Awash Melka bean variety when sprayed at one- or two-week intervals (USD 953.50 ha^-1 and USD 889.60 ha^-1) followed by Chercher (USD 848.90 ha^-1 and USD 823.3 ha^-1) (Hirpa and Selvaraj 2016). In Brazil, pyraclostrobin application provided USD 86–181 ha^-1 return on investment due to decreased disease development (Gillard and Ranatunga 2013). Azoxystrobin application in Brazil reduced mean AUDPC by 63% and increased mean yield by 150% (Polanco et al. 2014). In Nigeria, carbendazim and benomyl reduced the development and spread of anthracnose disease on cowpea by 46 and 40% respectively (Emechebe and Florini 1997). The highest marginal rates of return of 3071 and 2568% were observed in Awash-1 without seed treatments, sprayed at flowering and pod setting respectively (Negera and Dejene 2018). Despite these chemical control options, anthracnose disease continues to destroy common bean farmers’ fields in Africa. Identified challenges include a lack of information provision at appropriate times for spraying as well as the economic injury level of anthracnose control. Seed treatment fungicides are usually available only in large lots, which are difficult for small-scale farmers to access locally. Farmers’ knowledge of seed treatment and foliar spraying methods, application rates, time of application and management methods after application is limited. Therefore, researchers should work with designated authorities to advise farmers accordingly. Research on application methods, rates and timings for chemical control measures of anthracnose disease in Africa should continue. Development of resistance to some fungicides by anthracnose has been reported (Gadaga et al. 2017; Kiptoo et al. 2020). Researchers should evaluate the efficacy of new fungicides that provide cost-effective management options that do not damage the environment.

Integrated disease management: Integrated disease management is the recommended option for anthracnose control since the pathogen infects the seed and all growth stages of the crop and has high diversity. Integration of soil solarization, seed treatment and foliar spray with systemic and contact fungicide effectively reduces anthracnose epidemics (Mohammed 2013). Botanicals and bio-pesticides together with synthetic fungicides have also been shown to efficiently control the disease (Fitsum et al. 2014). Management of primary inoculum (crop rotation, use of resistant varieties) and seed treatment with contact or systemic fungicides effectively controls the disease. For instance, seed treatment with mancozeb followed by carbendazim foliar spray and both seed treatment and foliar spraying with carbendazim significantly reduce bean anthracnose severity (Amin et al. 2013). Ethiopia’s Awash-1 variety, without seed treatment and without foliar spray, showed the highest decrease in foliage (-86.0%) and 71.32% pod severity with AUDPC of 2771.19 days for leaves and 1150.25 days for pods compared to Awash-1 variety, with seed treatment and with foliar spray. However, many bean growers in Africa use a single method to control anthracnose and as a result the disease continues to threaten bean fields and reduce grain yield. Common bean farmers lack information on efficient integration, application methods, and timing and rates of application. Training on and promotion of integrated bean anthracnose management is required in Africa.

Conclusion

This review was aimed to assemble information on the mechanism of anthracnose infection in common bean, its pathogenicity and management approaches in Africa. Reviewing the mechanism of anthracnose infection and pathogenicity provides knowledge of host–pathogen interactions between bean plants and C. lindemuthianum. Many details related to successful fungal infection and subsequent disease development have yet to be elucidated. Topics that would benefit from further research include quantification of protein and glycoprotein production by C. lindemuthianum, identification of factors determining whether host penetration results in successful colonization, and exploration of the mechanism by which temperature affects pathogen adhesion to the host. Understanding interactions between pathogen virulence, resistance and host susceptibility is essential. Identification of plant-derived signals and parts of signal transduction chains involved in cellulase, cutinase, lignase and pectinase induction and appressorium formation in C. lindemuthianum is important. Opportunities for research on anthracnose management in Africa include exploring why most African farmers use local rather than commercial varieties, and why farm-saved seed is preferred.

Planting resistant varieties is recommended because the seed is the major source and survival structure for anthracnose disease. Integrated anthracnose disease management is also recommended due to the fact that the pathogen occurs from seed throughout all growth stages of common bean and due to high pathogen diversity. Further research integrating the use of resistant varieties, testing the efficacy of cultural, biological and chemical controls is of great importance to design consolidated integrated common bean anthracnose management approaches in Africa. Tricot is an important approach to control anthracnose and evaluate anthracnose-resistant varieties, but is not widely used in Africa. Future studies in other African countries can complement tricot research already underway on common bean anthracnose in Tanzania, for increased productivity, nutrition and income.

Acknowledgements

The authors would like to thank staff from the Nelson Mandela African Institution of Science and the Tanzania Agricultural Research Institute (TARI) for administration and technical support and staff from the Alliance of Bioversity International and the International Center for Tropical Agriculture (CIAT) for their technical and financial support. The authors also thank Harri Washington, consultant to the Alliance of Bioversity International and CIAT Science Writing Service, for technical and language editing of the manuscript.

Author Contributions

Conceptualization ELK, ERM, validation PV, TMA, JCN, investigation and resources ELK, ERM, PV, JCN, TMA, CMM, JCR, writing review and editing all authors’ visualization ELK and funding JCR. All authors have read and agreed to the published version of the manuscript.

Conflicts of Interest

The authors declare no conflicts of interest.

Data Availability

Information presented in this study will be available uppon request to the corresponding author

Ethics Approval

Not applicable

Funding Source

This review was supported by a tricot PhD scholarship administered by Accelerated Varietal Improvement and Seed delivery of legumes and cereals in Africa (AVISA) under the Bill and Melinda Gates Foundation and Improving Bean Production and Marketing in Africa (IBPMA) under Global Affairs Canada.

References

Alkemade JA, MM Messmer, RT Voegele, MR Finckh, P Hohmann (2021). Genetic diversity of Colletotrichum lupini and its virulence on white and Andean lupin. Sci Rep Article 13547

Alkemade JA, C Arncken, C Hirschvogel, MM Messmer, A Leska, RTVoegele MR Finckh, R Kölliker, SPC Groot, P Hohmann (2022). The potential of alternative seed treatments to control anthracnose disease in white lupin. Crop Prot 158:1‒7

Amin M, A Ayalew, N Dechassa, M Negeri (2013). Effect of integrated management of anthracnose (Colletotrichum lindemuthianum) through soil solarization and fungicide applications on epidemics of the disease and seed health in Hararghe highlands, Ethiopia. J Plant Pathol Microbiol 4:1‒7

Ansari KI, SN Palacios, C Araya, T Longin, D Egan, FM Dookan (2004). Pathogenic and genetic variability among Colletotrichum lindemuthianum isolates of different geographical origin. Plant Pathol 53:635‒642

Awurum AN, PO Uchegu (2013). Effects of duration of contact of Piper guineense, Monodora myristica and Xylopia aethiopica on the germination and incidence of seed-borne fungi of stored cowpea (Vigna unguiculata L. Walp) seeds. J Biol Sci 6:37‒42

Bankole SA (1996). Bio-control of brown blotch of cowpea caused by Colletotrichum truncatum with Trichoderma viride. Crop Prot 15:633‒636

Batureine MJ (2009). Diversity of Colletotrichum lindemuthianum and reaction of common bean germplasm to anthracnose disease. MSc Thesis. Makerere University

Bigirimana J, R Fontaine, M Hofte (2000). Bean anthracnose: virulence of Colletotrichum lindemuthianum isolates from Burundi, Central Africa. Plant Dis 84:491‒497

Boersma SJ, DJ Depuydt, RJ Vyn (2020). Fungicide efficacy for control of anthracnose of dry bean in Ontario. Crop Prot 127:2411‒2502

Buruchara R, C Mukankusi, K Ampofo (2010). Bean Disease Pest Identification and Management, 4^th Edition, International Center for Tropical Agriculture, Kenya

Bush E (2009). Anthracnose on Snap Beans, 450^th Edition. Virginia Cooperative Extension, USA

Chethana KWT, RS Jayawardena, YJ Chen, S Konta, S Tibpromma, PD Abeywicjrama, D Gomdola, A Balasuriya, XU Jianping, S Lumyong, K Hyde (2021). Diversity and function of appressoria. Pathogens 10:746

Ciofini A, F Negrini, R Baroncelli, E Baraldi (2022). Management of post-harvest anthracnose: current approaches and future perspectives. Plants 11:Article 1856

Costa BHG, MLV de Resende, ACA Monterio, MR Junior, DMS Botelho, BM da Silva (2019). Potassium phosphites in the protection of common bean plants against anthracnose and biochemical defence responses. J Phytopathol 166:95‒102

Duangkaew P, S Monkhung (2021). Antifungal activity of Bacillus subtilis subsp. spizizenii BL-59 to control some important postharvest diseases of mango fruits (Mangifera indica L.). Intl J Agric Technol 17:2053‒2066

Dubrulle G, A Picot, S Madec, E Corre, A Pawtowski, R Baroncelli, M Zivy, T Balliau, G Le Floch, F Pensec (2020). Deciphering the infectious process of Colletotrichum lupini in lupin through transcriptomic and proteomic analysis. Microorganisms 8:Article 1621

Dufresne M, S Perfect, AL Pellier, JA Bailey T Langin (2000). A GAL4-like protein is involved in the switch between biotrophic and necrotrophic phases of the infection process of Colletotrichum lindemuthianum on common bean. Plant Cell 12:1579‒1590

Emechebe AM, D Florini (1997). Fungal and bacterial diseases of cowpea. In: Advances in Cowpea Research, pp: 176–183. Singh RS, M Raj, KE Daswell, LE Jackai (Eds.). Red, IITA Nigeria

Enyiukwu DN, AC Amadioha, CC Ononuju (2021). Evaluation of some pesticides of plant origin for control of anthracnose disease (Colletotrichum destructivum) in cowpea. Asian J Agric 5:4‒11

Etana D (2022). Major insect pests and diseases in common bean (Phaseolus vulgaris L.) production in Ethiopia. Frontiers 2:79‒87

FAOSTAT Food and Agricultural Organization (2019). Crop production data. Available at: http://www.fao.org/faostat/en/ (Accessed: 20 February 2022)

Farrow A, RA Muthoni (2020). Atlas of Common Bean Production in Africa 2^ndEdition. Pan-Africa Bean Research Alliance; International Center for Tropical Agriculture, Kenya

Ferreira JJ, A Campa, J Kelly (2013). Organization of Genes Conferring Resistance to Anthracnose in Common Bean. In: Varshney: Translational Genomic for Crop Breeding: Biotic Stress, pp: 151‒182. Tuberosa RK, J Wiley (Eds.), Chichester, UK

Fitsum S, M Amin, T Selvaraj, A Alemayehu (2014). In vitro evaluation of some fungicides and bioagents against common bean anthracnose (Colletotrichum lindemuthianum Sacc. & Magnus) Briosi & Cavara. Afr J Microbiol Res 8:2000‒2005

Gadaga SJC, MS Abreu, ML Resende, PM Junior (2017). Phosphites for the control of anthracnose in common bean. Pesqui Agropecu Bras 52:36‒44

Gebrie A (2016). Biotrophic fungi infection and plant defense mechanism. J Plant Pathol Microbiol 7: Article 378

Gezahegn A, A Chala, G Ayana (2021). Physiological races of Colletotrichum lindemuthianum, the cause of bean anthracnose in major bean growing regions of Southern and Central Ethiopia. East Afr J Sci 15:103‒114

Ghasemzadeh A, M Karbalaei, H Jaafar, A Rahmat (2018). Phytochemical constituents, antioxidant activity, and antiproliferative properties of black, red, and brown rice bran. Chem Cent J 12:1‒23

Gillard CL, NK Ranatunga (2013). Interaction between seed treatments, surfactants and foliar fungicides on controlling dry bean anthracnose (Colletotrichum lindemuthianum). Crop Prot 45:22‒28

Girma F, C Fininsa, H Tefere, B Amsalu (2022). Distribution of common bacterial blight and anthracnose diseases and factors influencing epidemic development in major common bean growing areas in Ethiopia. Soil Plant Sci 72:685‒699

Hirpa K, T Selvaraj (2016). Evaluation of common bean cultivars and fungicide spray frequency for the management of anthracnose (Colletotrichum lindemuthianum) in Ambo, West Shewa Zone, Ethiopia. J Biol Agric Health 6:68‒80

Javaid A, A Ali, A Shoaib, IH Khan (2021). Alleviating stress of Sclertium rolfsii on growth of chickpea var. Bhakkar-2011 by Trichoderma harzianum and T. viride. J Anim Plant Sci 31:1755‒1761

Kamiri AK, EE Arunga, F Rotich, R Otsyula (2021). Response of french bean genotypes to Colletotrichum lindemuthianum and evaluation of their resistance using SCAR markers. Afr J Biotechnol 20:51‒65

Khan IH, A Javaid, D Ahmed (2021). Trichoderma viride controls Macrophomina phaseolina through its DNA disintegration and production of antifungal compounds. Inter J Agric Biol 25:888‒894

Khan IH, A Javaid (2022a). DNA cleavage of the fungal pathogen and production of antifungal compounds are the possible mechanisms of action of biocontrol agent Penicillium italicum against Macrophomina phaseolina. Mycologia 114:24‒34

Khan IH, A Javaid (2022b). Antagonistic activity of Aspergillus versicolor against Macrophomina phaseolina. Braz J Microbiol 53:1613‒1621

Kiptoo GJ, MG Kinyua, OK Kiplagat, LG Matasyoh (2020). Incidence and severity of Anthracnose (Colletotrichum lindemuthianum) on selected common bean (Phaseolus vulgaris L.) genotypes. Afr J Plant Sci 14:45‒56

Kiryowa JM, A Ebinu, V Kyaligonza, S Nkalubo, C Mukankusi, P Tukamuhabwa (2016). Pathogenic variation of Colletotrichum lindemuthianum causing anthracnose of beans (Phaseolus vulgaris) in Uganda. J Plant Patholol 5:89‒98

Koch SH (1996). The identification of races of Colletotrichum lindemuthianum in South Africa. Ph.D. Thesis. University of Pretoria, South Africa

Lemos SJ, EP de Souza, E Alves, JEBP Pinto, SKV Bertoluci, MLO Freitas, CCL de Andrade, MLVResende (2015). Essential oil of Cymbopogon flexuosus, Vernonia polyanthes and potassium phosphite in control of bean anthracnose. J Med Plant Res 9:243‒253

Li D, AM Ashby, K Johnstone (2007). Molecular evidence that the extracellular cutinase Pbc1 is required for pathogenicity of Pyrenopeziza brassicae on oilseed rape. Mol Plant Microb Interact 16:545‒552

Masunga M, MS Nchimbi, M Robert, AC Luseko (2020). Races of Colletotrichum lindemuthianum (Sacc. Magnus) Briosi Cavara in major bean growing regions in Tanzania. Afr J Plant Sci 14:308‒314

Mercure EW, H Kunoh, RL Nicholson (1995). Visualisation of materials released from adhered, ungerminated conidia of Colletotrichum graminicola. Phy Mol Plant Patholol 46:121‒135

Meziadi C, MM Richard, A Derquennes, V Thareau, S Blanchet, A Gratias (2016). Development of molecular markers linked to disease resistance genes in common bean based on whole genome sequence. Plant Sci 242:351‒357

Mlemba SA (2021). Phenotypic and molecular evaluation of lines developed for multiple disease resistance in common bean (Phaseolus vulgaris L.). MSc Thesis. Sokoine University of Agriculture, Kididimo, Morogoro, Tanzania

Mohammed A (2013). An overview of distribution, biology and the management of common bean anthracnose. J Plant Pathol Microbiol 4:Article 1000193

Mugambi IK (2013). Enhanced legume productivity through incorporation of lablab residues and use of legume species tolerant to root rot disease complex. BSc. Thesis. University of Nairobi, Kenya

Mukankusi C, B Raatz, S Nkalubo, F Berhanu, P Binagwa, M Kilango, M Williams, K Enid, R Chirwa, S Beebe (2019). Genomics, genetics and breeding of common bean in Africa: A review of tropical legume project. Plant Breed 138:401‒414

Munda A, S Radisek, J Šuštar-Vozlič, B Jovonic (2009). Genetic variability of Colletotrichum lindemuthianum isolates from Slovenia and resistance of local Phaseolus vulgaris germplasm. J Plant Dis Prot 116:23‒29

Muth P, M Liebenberg (2009). Resistance of dry bean to South African races of Colletotrichum lindemuthianum. Annu Report Bean Improvement Cooperative 52:40‒41

Muthoni R, R Nagadya, D Okii, O Innocent, C Mukankusi, R Chirwa, R Zulu, M Lungaho, C Ruranduma, M Ugen, D Karanja, E Mazuma, A Musoni, L Sefume, T Meshac, M Amane, D Fourie, A Dlamini, H Andriamazaoro, M Kilango, OS Kweka (2017). Common bean variety releases in Africa constraints, growth habit and days to maturity. Harvard Dataverse. https://dataverse.harvard.edu/dataset.xhtml?persistentId=doi:10.7910/DVN/RPATZA

Mwaipopo BM, MS Nchimbi, P Njau, F Tairo, M Willium, P Binagwa, E Kweka, M Kilango, D Mbanzibwa (2017). Viruses infecting common bean (Phaseolus vulgaris L.) in Tanzania: A review on molecular characterization, detection and disease management. Afr J Agric Res 12:1486‒1500

Mwalyego FM (1991). Progress in bean anthracnose research in Tanzania. In. Proceedings of the First Pan-African Working Group Meeting on Anthracnose of Beans, Buruchara R (Eds.). Ambo, Ethiopia

Mwesigwa JB (2008). Diversity of Colletotrichum lindemuthianum and reaction of common bean germplasm to anthracnose disease. MSc. Thesis. Makerere University. Uganda

Nadeem MA, MZ Yeken, MQ Shahid, E Habyarimana, H Yılmaz, A Alsaleh, R Hatipoğlu, Y Çilesiz, KM Khawar, N Ludidi, S Ercişli, M Aasim, T Karakoy, FS Baloch (2021). Common bean as a potential crop for future food security: An overview of past, current and future contributions in genomics, transcriptomics, transgenics and proteomics. Biotechnol Equip 35:758‒786

Nalupya Z, S Hamabwe, C Mukuma, D Lungu, P Gepts, K Kamfwa (2021). Characterization of Colletotrichum lindemuthianum races in Zambia and evaluation of the CIAT Phaseolus core collection for resistance to anthracnose. Plant Dis 105:1‒31

Negera A, M Dejene (2018). Effect of integrating variety, seed treatment, and foliar fungicide spray timing on managing common bean anthracnose at Bako, Western Ethiopia. East Afr J Sci 12:111‒126

Nkalubo ST (2006). Physiological races of dry bean anthracnose (Colletotrichum lindemuthianum) in Uganda. PhD thesis. University of KwaZulu Natal. South Africa

Nunes MPB, MC Gonçalves-Vidiga, VSR Martins, LFS Xavier, G Valentini, M Vaz Bisneta, PSF Vidiga (2021). Relationship of Colletotrichum lindemuthianum races and resistance loci in the Phaseolus vulgaris L. genome. Crop Sci 61:3877‒3893

Oeser B, PM Heidrich, U Muller, P Tudzynski, KB Tenberge (2002). Polygalacturonase is a pathogenicity factor in the Claviceps purpurea/rye interaction. Fungal Genet Biol 36:176‒186

Padder BA, PN Sharma, HE Awale, JD Kelly (2017). Colletotrichum lindemuthianum, the causal agent of bean anthracnose. J Plant Pathol 99:317‒330

Padder BA, PN Sharma, R Kapil, A Pathania, OP Sharma (2010). Evaluation of bioagents and biopesticides against Colletotrichum lindemuthianum and its integrated management in common bean. Notul Sci Biol 2:72‒78

Palacıog ̆lu GM, G Ozer, MZ Yeken, V Ciftci, H Bayraktar (2021). Resistance sources and reactions of common bean (Phaseolus vulgaris L.) cultivars in Turkey to anthracnose disease Genet Resour Crop Evol 68:3373‒3381

Paulino PPS, MC Gonçalves-Vidigal, M Vaz Bisneta, PSV Filho, MPBA Nunes, LFS Xavier, VSR Martins, GF Lacanallo (2022). Occurrence of anthracnose pathogen races and resistance genes in common bean across 30 years in Brazil. Agron Sci Biotechnol 8: Article 121

Pawlowski M, GL Hartman (2016). Infection mechanisms and colonization patterns of fungi associated with soybean. In: Fungal Pathogenisis, Sultan S (Ed.), pp: 25‒43

Pellier AL, R Laugé, CV Fourrey, T Langin (2003). CLNR1, the AREA/NIT2-like global nitrogen regulator of the plant fungal pathogen Colletotrichum lindemuthianum is required for the infection cycle. Mol Biol 48:639‒655

Polanco LR, FA Rodrigues, E Moreira (2014). Management of Anthracnose in common bean by foliar sprays of potassium silicate, sodium molybdate, and fungicide. Plant Dis 98:84‒89

Prabha D, N Chamoli, YK Negi, JS Chauhan (2021). Multiple genes confer anthracnose resistance in French bean accessions of Garhwal Himalayas. Genet Resour Crop Evol 69:809‒821

Pradhan A, S Ghosh, D Sahoo, J Gojaljee (2021). Fungal effectors, the double edge sword of phytopathogens. Curr Genet 67:27–40

Punia S, SB Dhull, KS Sandhu, M Kaur, S Purewal (2020). Kidney bean (Phaseolus vulgaris) starch. Leg Sci 2:1‒7

Robinson JG (2019). All about beans nutrition. Health Benefits, Preparation and Use in Menus, North Dakota, USA

Rubyogo JC, M Lung'aho, J Ochieng, P Binagwa, M Mdachi, E Zakayo, N Shida, J Msaky, E Kadege, B Birachi, M Mutua, F Nyakundi, S Kalemera (2019). Consumer acceptance of and willingness to pay for high-iron beans in northern Tanzania, pp: 1‒60. Study Report, International Center for Tropical Agriculture Arusha Tanzania

Saccardo P (1878). Fungi Veneti novi v. critici auctore PA Sac-cardo. Seriei VIII. Appendic Michel 1:351‒355

Sela-Buurlage MB, L Epstein, RJ Rodriguez (1991). Adhesion of un-germinated Colletotrichum musae conidia. Physiol Mol Plant Pathol 39:345‒352

Sharf W, A Javaid, A Shoaib, IH Khan (2021). Induction of resistance in chili against Sclerotium rolfsii by plant growth promoting rhizobacteria and Anagallis arvensis. Egypt J Biol Pest Contr 31:Article 16

Sharma M, S Kulshrestha (2015). Colletotrichum gloeosporioides: An anthracnose causing pathogen of fruits and vegetables. Biosci Biotechnol Res Asia 12:1233‒1246

Sharma N, AK Gautam (2019). Early Pathogenicity events in plant pathogenic fungi: A comprehensive review. Biol For Intl J 11:24‒34

Sperling L, E Birachi, S Kalemera, M Mutua, N Templer, C Mukankusi, K Radegunda, M William, P Gallagher, E Kadege, JC Rubyogo (2021). The Informal Seed Business: Focus on Yellow Bean in Tanzania. Sustain 13:1‒16

Suparman S, M Rahmiyah, Y Pujiastuti, B Gunawan T Arsi (2018). Cross inoculation of anthracnose pathogens infecting various tropical fruit. Earth Environ Sci 102:26‒27

Tucker SL, NJ Talbot (2001). Surface attachment and pre-penetration stage development by plant pathogenic fungi. Phytopathol 39:385‒417

Uwera A, JN Rusagara, NS Msolla, A Musoni, T Assefa (2021). Molecular marker-assisted backcrossing of anthracnose resistance genes into common beans (Phaseolus vulgaris L.) varieties. Am J Plant 12:771‒781

Van Etten J, K de Sousa, A Aguilar, M Barrios, A Coto, M Dell’Acqua, C Fadda, Y Gebrehawaryat, J van de Gevel, A Gupta, A Kiros, B Madriz, P Mathur, D Mengistu, L Mercado, J Mohammed, A Paliwal, C Pè M Quiros, J Rosas, N Sharma, S Singh, I. Solanki, J Steinkle (2018). Replication data for crop variety management for climate adaptation supported by citizen science. Harvard Dataverse 3

Van Etten J, E Beza, L Calderer, K van Duijvebdijk, C Fadda, B Fantahun, YG Kidane, J van de Gevel, A Gupta, DK Mengistu, D Kiambi, PN Mathur, L Mercado, S Mittra, MJ Mollel, JC Rosas, J Steinke, JG Suchini, KS Zimmerer (2019). First experience with a novel farmer citizen science approach: Crowdsourcing participatory variety selection through on-farm triadic comparisons of technologies (tricot). Exp Agric 55:275‒296

Wang Y, J Kerns (2017). Temperature effects on formation of appressoria and sporulation of Colletotrichum cereale on two turfgrass species. Dis Plant Pathol 13:123‒132

Weidner S, A Krol, M Karmac, R Amarowicz (2018). Phenolic compounds and the antioxidant properties in seeds of green- and yellow-podded bean (Phaseolus vulgaris L.) varieties. J Food 16:373‒380

Yesuf M, S Sangchote (2005). Seed transmission and epidemics Colletotrichum lindemuthianum in the major common bean growing areas of Ethiopia. J Nat Sci 39:34‒45

Yousef S (2021). Bean anthracnose control using different beneficial bacteria. MSc. Thesis. Salahadin University, Erbil, Iraq

Zulu MM (2005). Race identification and distribution of bean anthracnose (Colletotrichum lindemuthianum) in major bean growing areas of Zambia. MSc. Thesis, University of Zambia, Lusaka, Zambia