Effect of botanical and bioagents against powdery mildew of garden pea: A review

Introduction

Pisum sativum L., a nutritious pea that is grown worldwide and can withstand freezing temperatures, is a member of the Leguminosae family (Kour et al., 2020; Tulbek et al., 20 17) [13,25] . India produces more green peas than any other country in the world, second only to China, and ranks tenth in terms of production among vegetable crops. Globally, over 22 million tons of dried pea seeds and 14.5 million tons of green pea seeds are produced annually (FAOSTAT, 2019; Mondor, 2020; Senapati et al., 2019) [6,17,20] . In addition to having low levels of saturated fat, cholesterol, and sodium, pea seeds are a good source of soluble and insoluble fibers, proteins (tryptophan and lysine), complex carbohydrates, vitamin B, folate, and minerals (calcium, potassium, and iron) (Table 1).There are 17-22 g of carbs, 20-50 g of starch, 14-26 g of dietary fiber, 6.2-6.5 g of protein, 0.4-g of fat, and 1.0-g of ash in 100 g of fresh green pea seeds. Furthermore, by enhancing the nutritional value and techno-functional characteristics of peas and their protein, cutting-edge methods like pulse electric fields and ultrasonication have shown a notable impact on efficiency (Ma et al., 2018; Melchior et al., 2020) [15,16] . Peas are susceptible to a wide range of bacterial, fungal, viral, and nematode diseases. In the best of conditions, these diseases significantly lower yield and quality. Important types of organisms that cause soilborne infections in peas include nematodes, bacteria, and fungi. Seedling diseases are caused by Pythium spp. and Rhizoctonia solani Kühn; root rots are caused by Aphanomyces euteiches Drechs., Fusarium solani f. sp. pisi (Jones) Snyd. & Hans., and Thielaviopsis basicola (Berk. and Broome) Ferraris; wilts are caused by Fusarium oxysporum f. sp. pisi (van Hall) Snyd. & Hans. races 1, 2, 5, and 6. Nematode infections are primarily caused by root knots (Meloidogyne spp.), pea cysts (Heterodera goettingiana (Liebscher)), and root-lesion nematodes (Pratylenchus penetrans (Cobb) Filip. & Schuur.-Stek.). Fungi and bacteria are the main causes of pea foliar diseases. Foliar diseases like pea rust (Uromyces fabae (Grev.) Fuckel), powdery mildew (Erysiphe pisi DC.), downy mildew (Peronospora viciae (Berk.) Casp.), white mold (Sclerotinia sclerotiorum (Lib.) de Bary), and Ascochyta blight (a complex of three fungi) are caused by Ascochyta pisi Lib., Mycosphaerella pinodes (Berk. & Bloxam) Vestergr., and/or Phoma medicaginis var. pinodella (Jones) Boerema. Brown spot, which is caused by Pseudomonas syringae pv. syringae, and bacterial blight, which is caused by Pseudomonas syringae pv. pisi (Sackett) Young, Dye, and Wilkie, are significant bacterial infections. Alfalfa mosaic virus, bean leafroll virus, pea enation mosaic virus, pea streak virus, red clover vein mosaic virus, and pea seedborne mosaic virus are among the major viruses that cause these illnesses (Chen et al., 2004) [10] . [10] .

Pea Powdery Mildew: Pathogen and Impact

Powdery mildew, a widespread airborne illness that is particularly problematic in regions with warm, dry days and cool nights, is caused by the obligate biotrophic fungus Erysiphe pisi DC (Smith et al., 1996) [23] . The disease can reduce yields by 25-50% (Munjal et al., 1963; Warkentin et al., 1996) [18,28] and affect total biomass, pod and seed quantities, plant height, and node count (Gritton and Ebert, 1975). It may also accelerate maturity, which can cause tenderometer readings to spike and the quality of the green pea crop to decline (Falloon and Viljanen-Rollinson, 2001) [4] . Severe infections cause unpleasant off-flavors, discolor seeds, and deteriorate the quality of the seeds and processing. Machine operators may also be at risk for respiratory problems from airborne spores and fungal residues. Late-maturing or late-sowing cultivars are especially susceptible, and the more damage, the earlier the disease development.

Disease Symptoms and Spread

Powdery mildew infects all green tissues of pea plants. Initial symptoms appear as small, diffuse spots on lower leaves and stipules, eventually forming white or pale grey powdery patches that can merge to cover entire surfaces (Falloon and Viljanen-Rollinson, 2001) [4] . Control strategies currently include early sowing, fungicide application, and the use of resistant varieties.

Pathogen Diversity

Erysiphe pisi, previously misidentified as E. communis or E. polygoni, has multiple variants: E. pisi var. pisi affects Pisum, Medicago, Vicia, Lupinus, and Lens, while E. pisi var. cruchetiana targets Lathyrus and Ononis (Braun, 1987) [3] . Other species, like E. baeumleri and E. trifolii, have also been linked to pea powdery mildew in the Czech Republic and the Pacific Northwest USA (Ondřej et al., 2005; Attanayake et al., 2010) [19,1] (Table 2). These species differ genetically (rDNA ITS sequences) and morphologically, particularly in the structure of chasmothecial appendages.

The presence of multiple species may complicate resistance breeding efforts and could explain observed breakdowns in resistance. [19,1]

Cultural Management

Early planting or the use of early-maturing cultivars helps prevent outbreaks of severe mildew since late crops are more susceptible to infection. Phosphorus lowers disease incidence, while high nitrogen increases susceptibility through increased vegetative growth (Jarvis et al., 2002) [12] . Though it is not feasible for producers to artificially stress plants to lessen susceptibility, dense, lush canopies are more vulnerable to infection. Crop rotation is not very beneficial since seed transfer is infrequent (Tiwari et al., 1999a) [24] and the disease spreads quickly over wide areas (Viljanen-Rollinson et al., 1998a) [27] .

Chemical Control

Protective fungicides like sulphur and dinocap have been used successfully (Sharma and Mathur, 1984; Singh and Singh, 1978) [21,22] , but their repeated use is often impractical due to cost and application logistics. Reactive spraying-only when symptoms appear-is more economical. Fungicides are most effective when applied early in infection (<5% plant coverage). Wettable sulphur, though less favoured due to late-stage application challenges, remains viable, especially for organic systems or areas where aerial spraying is restricted. Newer fungicide options include triazoles (e.g., triadimefon,

, and broader-spectrum products like strobilurins and anilinopyrimidines. Spiroxamine and quinoxyfen, both mildew-specific, are also in use. Mixtures like pyraclostrobin + boscalid have recently been tested and approved.

Natural Product-Based Control

Growing resistance and environmental concerns have sparked interest in substitute items such plant extracts, oils, silicon, and salts (Bélanger and Labbé, 2002) [2] . in vitro and field studies have demonstrated the effectiveness of extracts from neem (Azadirachta indica), garlic, ginger, Flueggea microcarpa, and other plants in reducing E. pisi. Methionine-riboflavin formulations have been found to be just as effective as traditional fungicides (Tzeng et al., 1996) [26] . Other substances that have shown potential include phosphorous acid, bicarbonate, and potassium silicate.

Biological Control

Biological control remains a promising yet underdeveloped area. Various antagonists, including bacteria (Bacillus subtilis, B. pumilus), fungi (Ampelomyces quisqualis, Trichoderma harzianum), and yeasts (Pseudozyma flocculosa), have shown potential. Commercial products such as AQ10®, Sporodex®, Serenade®, and Sonata® have been released in some markets. Additional fungal and bacterial agents, including Pseudomonas fluorescens and Paecilomyces fumosoroseus, are under investigation. Some natural antagonists like Acrodontium crateriforme and Ramichloridium apiculatum remain unexplored for practical use.

Induced Resistance

Plants can develop systemic resistance through exposure to certain pathogens or stimuli. This resistance is often broadspectrum and race non-specific (Kuc, 1995) [14] . Chemicals such as salicylic acid, chitosan, and β-aminobutyric acid have shown effectiveness in inducing resistance in peas (Frey and Carver, 1998; Bélanger and Labbé, 2002) [8,2] . Neem products and vermicompost extracts have similarly been linked to resistance induction. Soil amendment with vermicompost boosts phenolic acid production, which correlates with enhanced resistance.

Genetic Resistance

To date, three genes conferring powdery mildew resistance in pea have been identified: two recessive (er1, er2) and one dominant (Er3) (Harland, 1948) [11] . er1, the most widely used, functions via loss-of-function in the PsMLO1 gene (Humphry et al., 2011). er2 confers temperature-dependent resistance, most effective at 25 °C or in mature leaves (Fondevilla et al., 2006) [7] . Er3, from Pisum fulvum, has been successfully introgressed into cultivated lines and shows broad-spectrum resistance.Molecular markers linked to these genes facilitate marker-assisted selection. For instance, SSR and SCAR markers are available for er1 (LG VI), er2 (LG III), and Er3. Besides major resistance genes, several accessions with moderate, uncharacterized resistance have also been identified in P. sativum and wild relatives.

Resistance Mechanisms

In susceptible peas, E. pisi penetrates epidermal cells, forming haustoria that support further fungal development and conidia production (Falloon et al., 1989) [5] . In er1 lines, most conidia germinate but fail to develop secondary hyphae. er2-mediated resistance varies with leaf age and temperature and is linked to hypersensitive responses (Fondevilla et al., 2006) [7] . Proteomic analyses indicate that resistant lines like JI2480 have higher baseline levels of defence-related proteins, possibly contributing to their resistance.

Conclusion

Powdery mildew, primarily caused by Erysiphe pisi, poses a significant threat to pea cultivation worldwide, particularly under conducive climatic conditions. Traditional management through fungicides and cultural practices, while effective, faces challenges due to environmental concerns and fungicide resistance. As a result, there is growing interest in alternative control measures such as botanical extracts, biological agents, and induced resistance. Although several natural products and microbial antagonists show promise, their commercial viability and field-level consistency require further research. Genetic resistance, especially through the er1 gene, remains the most reliable and sustainable approach, though reliance on single-gene resistance could be risky. An integrated disease management strategy combining cultural, chemical, biological, and genetic tools offers the best path forward for durable and eco-friendly control of powdery mildew in peas.

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