Breeding for Sclerotinia Blight Resistance on Peanut in the U.S.: A Review

Abstract

Sclerotinia blight is one of the most widespread and economically damaging diseases of peanut (Arachis hypogaea L.), causing significant crop losses in cooler production areas across the world. In the U.S., Sclerotinia blight caused by Sclerotinia minor has been an issue for producers for over 50 years and remains troublesome with regards to inheritance of resistance, management strategies, and resistant germplasm sources. This review provides an overview of the disease on peanut, progress towards the identification of genomic regions responsible for resistance, and the development of resistant cultivars in the U.S.

1. Introduction

Worldwide peanut (Arachis hypogaea L.) production reached 50.5 metric tons in 2024 [1]. The U.S. ranks fourth in the world in peanut production, and in 2023, the U.S. peanut crop had an estimated value of $1.614 billion dollars [2]. Peanuts are considered an oilseed but are also grown for use in confectionaries and other edible products. Peanuts serve as an excellent source of protein and compounds like resveratrol that block absorption of cholesterol [3]. Peanuts belong to the Leguminosae family and have a symbiotic relationship with Rhizobia, a nitrogen-fixing bacteria. Peanut production practices in the U.S. vary from conventional till, strip-till, or no-till in regions of the country with a calcium-rich, sandy soil and a growing season conducive to the crop. Peanuts are planted in the spring (April–May) when soil temperatures reach approximately 68 °F. Seeds are planted at a depth of about 2 inches at a rate of 4–6 seeds per foot. Row spacing varies depending on the producer. There are four distinct market types of peanuts with different maturity, which is measured in days after planting (DAP): runner (150 DAP), Virginia (135 DAP), Spanish (120 DAP), and Valencia (120 DAP). Upon maturity, peanuts are dug and inverted into windrows, where they are allowed to dry in the field before harvesting 3–7 days later. Crop rotation has been shown to be critical to maintain yields and reduce disease incidence [4].

Challenges to peanut production in the U.S. include a wide array of fungal pathogens including Aspergillus flavus, Aspergillus niger (Aspergillus crown rot), Verticillium dahlia (Verticillium wilt), Pythiium spp. and Rhizoctonia solani (pod rot), Theilaviopsis basicola (black hull), Althelia Rolfsii (white mold), Cylindrocladium parasiticum (Cylindrocladium black rot), and Sclerotinia minor (Sclerotinia blight) [5]. This review focuses on breeding for resistance to Sclerotinia blight in the U.S., where the disease results in significant annual yield losses in the southwestern (SW) and Virginia/Carolina (VC) growing regions.

2. History and Overview of the Pathogen

The first report of Sclerotinia on peanut was from Argentina in 1922 caused by Sclerotinia trifoliorum [6,7]. Over time, other Sclerotinia species, such as S. arachidis, S. minor, S. miyabeana, S. sclerotiorum, and S. trifoliorum, were reported on Arachis hypogaea from all continents except Antarctica [8]. Sclerotinia arachidis has since been moved to the genus Botrytis [9]. Similarly, the taxonomic status of S. miyabeana is uncertain [10], and one early assessment noted no morphological or physiological differences between S. miyabeana and S. sclerotiorum [11]. To date, records of S. trifoliorum on peanut have been restricted to Argentina and Chile [1]. There has not been a comprehensive phylogenetic study of the genus in recent years, but Sclerotinia minor, S. sclerotiorum, and S. trifoliorum appear to be closely related but distinct species [12,13].

By far the most important species of Sclerotinia on peanut are S. minor and S. sclerotiorum. Sclerotinia sclerotiorum and S. minor were first reported on “earthnut” (a colloquialism for peanut) in China in 1936 [7,14]. Another early report of S. minor on peanut was in 1948 from Australia, where it caused a disease outbreak [7,15]. Both species are problematic to peanut production in Argentina, Australia, and South Africa [16,17,18,19,20,21]. In recent reports from China, S. minor is reported on other crop species [22,23], but S. sclerotiorum predominates peanut reports, at least in English [7,24,25].

In the United States, Sclerotinia blight was first found in Virginia and North Carolina in 1971 and 1972, respectively [26]. Porter and Beute [26], following the Sclerotinia classification of Purdy [27], initially reported the pathogen as S. sclerotiorum. However, later examination by Kohn [10] identified the small-sclerotial isolates from Virginia and North Carolina as S. minor. Other early reports of Sclerotinia on peanut in the U.S. were from Oklahoma [28,29]; Wadsworth observed Sclerotinia minor in 1973 [28] and found S. sclerotiorum in 1974 [29]. Sclerotinia minor and/or S. sclerotiorum have since been documented on peanut in Arkansas [30,31], Georgia [32], New Mexico [33], and Texas [34,35]. In the U.S., S. minor is the most problematic species for peanut production [5].

Sclerotinia blight is primarily an issue in peanut production areas with cooler temperatures [5,36], as the optimum temperature for S. minor growth is 18 C [37,38]. Annual disease losses up to 13% are common in years with favorable conditions but can approach 50% in under severe conditions [39,40]. The primary inoculum for the disease is sclerotia, which can remain viable in soil for several years without a host [40]. Sclerotia can spread via infected seed, animals, water, and production machinery [36,41,42,43]. High levels of humidity are required for plant infection [43]. Disease symptoms typically appear after plant canopies have reached maximum size [44], creating humid, shaded microclimates favorable for sclerotial germination. Temperatures later in the growing season also favor disease development as plants approach maturity and when evening temperatures are cooler [43]. Visible symptoms include chlorosis of leaves followed by wilting (flagging) and stem lesions on branches close to the ground [5]. Infection cushions (white, fluffy mycelium) may be observed during cool and damp conditions, and black sclerotia will be seen along the surfaces of stem lesions. Sclerotinia minor is a necrotroph that survives by killing host cells and obtaining nutrients from dying or dead host tissue [5]. Disease lesions can progressively move toward the main stem of infected plants and eventually kill the host. Sclerotia are produced along decaying tissue of lesions and deposit in the soil where they overwinter or germinate when environmental conditions are favorable [45].

Once a field is infested with S. minor, disease management options for Sclerotinia blight are limited. Cultural practices such as crop rotation may not be economically feasible for growers due to long-lived sclerotia and the extensive host range of the pathogen [34,46,47]. Methods to manage plant canopy microclimates may be impractical for growers. Reducing seeding rates to create more open canopies does not appear to significantly reduce disease or yields [48,49]. Efforts should be made to minimize unnecessary damage to peanut vines [50] and excessive irrigation [5].

Fungicides are available for controlling Sclerotinia blight [5]; however, they are expensive and up to three applications per season may be necessary to maintain a healthy crop in years highly favorable for disease development [51]. Guidance on fungicide application timing varies, ranging from regular field scouting to ensure treatments are applied before infection occurs [52] to following a predetermined calendar schedule [53]. The initial fungicide application is typically made at the first detection of the pathogen or disease symptoms in the field, which often occurs 30 to 45 days after planting [54]. Additional applications should follow the guidelines provided on the product label. Protectant fungicides such as fluazinam and boscalid are effective against S. sclerotiorum and S. minor and should be applied before disease onset to achieve better control efficacy [52,53,54,55,56]. The input cost of multiple fungicide applications throughout the growing season to control Sclerotinia blight is a financial burden to most peanut producers and is not preferred from an environmental standpoint.

Host plant resistance offers the most sustainable means of disease control and as with most diseases, planting resistant cultivars is the most economical approach for managing S. minor. If possible, producers should consider planting resistant cultivars or less-susceptible market types in infested fields. Peanut canopy architecture plays a significant role in susceptibility, and upright market types, such as Spanish and Valencia, tend to be less susceptible than those with bunch (Virginia) or prostrate (runner) growth habits [57,58,59]. Upright and/or open growth habits are less conducive to pathogen growth and infection because of the smaller number of branches in close contact with the soil as well as reduced humidity and increased temperature within the canopy [5,48,60,61,62,63].

Although growers primarily use host resistance and fungicides to manage Sclerotinia blight, these strategies focus on limiting disease development rather than directly decreasing the sclerotia population in the soil [64]. Over time, biological control agents have been explored for their potential to parasitize the sclerotia of Sclerotinia minor and other Sclerotinia species, aiming to reduce the number of viable sclerotia in the soil, which serves as the primary source of inoculum during the peanut growing season. An example of microorganism that acts as a mycoparasite of sclerotia includes Coniothyrium minitans Campbell, which readily infects and colonizes the sclerotia of Sclerotinia spp. in the soil [65]. However, in the study by Partridge et al. [64], applying this microorganism to the soil only resulted in a reduction of disease severity approximately 18 months after the initial application of C. minitans, highlighting the need for a long-term integrated management plan to be incorporated into growers’ strategies. Additionally, Penicillium citrinum has been identified as a promising biological control agent for S. minor, as it helps reduce the inoculum density of sclerotia [66]. Despite its potential, biological control of S. minor in peanuts faces several limitations that hinder its widespread adoption by growers. These include the need for a long-term plan for establishing microorganisms in the field, a limited range of available products, high costs, product formulations that are challenging to apply, and unfavorable environmental conditions during application.

3. Sources of Resistance

Developing cultivars with resistance to Sclerotinia blight is difficult because the inheritance of the trait is quantitative and poorly understood [67]. In contrast to Mendelian traits that are controlled by a single gene, quantitative traits are controlled by multiple genes with individual effects that are cumulative and often subject to variable environmental conditions. These traits make it difficult for breeders to identify the contributions of each gene to the overall phenotype. Breeders have been able to track quantitative inheritance by the identification and development of markers associated with quantitative trait loci (QTL) in recombinant inbred line (RIL) mapping populations. RIL populations designed for mapping disease resistance are traditionally developed by crossing a resistant parent with a susceptible parent, followed by repeated selfing past the F₂ generation. To date, only a few QTL associated with resistance to Sclerotinia blight have been found [68,69].

For peanut, few sources of Sclerotinia blight resistance have been identified. Cultivated peanut is tetraploid (2n = 4x = 40), likely derived from a cross between the wild diploid species of A. duranensis and A. ipaënsis, followed by spontaneous chromosome duplication [70,71,72,73]. The tetraploid nature of peanut and the complexity of the genome are factors that contribute to bottlenecks in genetic improvement. One limitation of traditional plant breeding is the lack of available genetic diversity because only genes from within the cultivated species or several closely related wild species can be utilized. Isleib et al. [74] reported that the recycling of lines as parents and exchange of germplasm among breeding programs has resulted in the proliferation of traits from plant introductions (PIs) into many peanut cultivars released since 1960. The PI ancestry of runner and Virginia market-types was estimated at 17.9%, while that of the Spanish market-type was estimated at 50%. Additional sources of genetic traits are needed for cultivar improvement. Norden [75,76] noted that peanut breeders must rely on the use of introductions, hybridization, and pure-line selection to produce new and improved cultivars with value-added traits. However, the narrow genetic base of peanut has created a crop that is vulnerable to many pests and environmental stresses, including Sclerotinia blight.

Peanut breeders utilize the USDA National Plant Germplasm System’s (NPGS) peanut collection, which contains accessions collected worldwide and others introduced from international repositories. NPGS’ collection includes over 9000 entries of cultivated and wild species of Arachis. Geographically and genetically representative subsets of the cultivated Arachis collection are available, such as the U.S. core (N = 831) [77] and the mini core (N = 112) [78] collections. The U.S. core and mini core have been examined for genetic diversity [78,79,80,81,82,83], oil and nutritional composition [84,85], and seed quality traits [86,87]. Several studies have screened the core and mini core in the field against diseases [88,89,90,91,92,93,94,95]. Similar work has been done for other germplasm collections across the globe including Argentina (Instituto Nacional de Technología Agropecuaria and Instituto de Botánica del Nordeste; Brazil (EMBRAPA-CENARGEN and the Instituto Agronômico de Campinas); the Chinese Academy of Agricultural Sciences and Oil Crops Research Institute; Korea (National Agrobiodiversity Center); and the International Crops and Research Institute for the Semi-Arid Tropics (ICRISAT), the Directorate of Groundnut Research, and the National Bureau of Plant Genetic Resources in India. These collections have been characterized genetically as advances in technology have evolved [83,96,97,98,99].

From this work, sources of resistance to Sclerotinia blight have been identified [91,92,93] and some have been incorporated into breeding programs to enable progress in developing cultivars with some level of resistance. A recent cultivar released for Southwest production [100] was developed from a cross with the Sclerotinia-resistant accession PI 274,193 from the U.S. core collection [91] and requires no fungicide sprays to control the disease. To date, cultivars with improved resistance have been released for all four peanut market types, Virginia [101,102,103], Spanish [104], runner [100,105,106,107], and Valencia [108]. Germplasm lines with enhanced resistance have also been released for use by breeders [109,110]. These improved cultivars have enabled sustainable peanut production without excessive fungicide application in areas heavily infested with S. minor. Unfortunately, little work has investigated the underlying mechanisms responsible for the resistance observed in the germplasm collections. It is unknown if these resistant PIs will also be effective against S. sclerotiorum, which is more problematic in other countries. Studies are limited, but there is evidence that host resistance (and susceptibility) to S. minor will also be similar against S. sclerotiorum [20,32].

4. Genomics and Genetic Transformation

Some progress has been made in pinpointing the location of genomic regions responsible. Chenault et al. [111] examined the genetic diversity among a set of well-phenotyped cultivars with pairs of simple sequence repeat (SSR) markers reported by Ferguson et al. [112] and identified a specific primer pair (marker) associated with Sclerotinia bight resistance, located on chromosome A07 [113]. That marker, validated by the work of Bennett et al. [92] was used in later work to screen germplasm collections and identify new possible sources of resistance [65,113,114,115,116]. Liang et al. [68] developed and characterized a recombinant inbred line (RIL) population and identified eight QTLs associated with resistance, located on chromosomes A04, A08, and B14. Rosso et al. [69] examined an interspefic RIL population with introgressed regions from three diploid wild species and identified two QTLs located on chromosomes A04 and B04 associated with resistance to S. minor. The identification of numerous QTLs associated with resistance underscores the complexity of the quantitative inheritance of the resistance trait.

Attempts have been made to genetically engineer peanut with Sclerotinia blight resistance. Transgenic peanut lines expressing a rice chitinase and/or an alfalfa glucanase, enzymes that degrade fungal cell walls [117], were shown to have enhanced resistance to S. minor under greenhouse [118] and field conditions [119,120]. Sclerotinia blight resistance was also achieved by transforming peanut with a barley oxalate oxidase gene [121,122] that, when expressed, detoxifies oxalate produced by the fungus. Although peanut transformed with genes conferring resistance to S. minor has been successful, no genetically modified peanut cultivars have been released for commercial production, largely due to the numerous regulations and the expense involved in human testing for GMO crops as well as the reluctance of consumer and export market acceptance. In the U.S., oversight for GMO crop release falls on multiple government agencies including U.S. Department of Agriculture’s Animal and Plant Health Inspection Service (APHIS) [123], the Environmental Protection Agency (EPA) [124], and the Food and Drug Administration (FDA) [125]. The cost of developing and releasing GMO crops depends on the intended use and can reach millions of dollars due to the number of laboratory and field trials required, regulatory submissions, monitoring and reporting requirements, and commercial launch estimates [126].

Products produced by CRISPR/Cas9 technology are not currently classified as GMO. This method could be used to genetically engineer resistance to Sclerotinia blight in peanut. This technology has been used to transform peanut oil chemistry from normal to high oleic acid content [127,128,129], to examine nodulation receptors [130] and is being considered for use in editing allergen genes [131]. Using CRISPR/Cas9 to engineer Sclerotinia blight resistance in peanut may be challenging due to its quantitative nature and lack of information on the numerous genes involved, but it has been used to engineer quantitative traits in other crops such as tomato [132], rice [133], and many others [134]. If successful, the use of CRISPR techniques to engineer quantitative traits in peanut would greatly reduce the amount of time and resources breeders currently exhaust breeding for resistance to Sclerotinia blight.

5. Summary

Sclerotinia blight remains a widespread and global threat to peanut production. Due to the lack of availability of highly resistant cultivars, timely application of fungicidal sprays throughout the growing season in addition to equipment sanitation remain the best cultural practices for controlling the disease and spread of the pathogen. Further advancements in the development of resistant cultivars in all peanut market types are needed to eliminate the need for expensive fungicide treatment and/or the threat posed by S. minor.